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Erschienen in: Translational Stroke Research 6/2017

25.07.2017 | Review

Novel Regenerative Therapies Based on Regionally Induced Multipotent Stem Cells in Post-Stroke Brains: Their Origin, Characterization, and Perspective

verfasst von: Toshinori Takagi, Shinichi Yoshimura, Rika Sakuma, Akiko Nakano-Doi, Tomohiro Matsuyama, Takayuki Nakagomi

Erschienen in: Translational Stroke Research | Ausgabe 6/2017

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Abstract

Brain injuries such as ischemic stroke cause severe neural loss. Until recently, it was believed that post-ischemic areas mainly contain necrotic tissue and inflammatory cells. However, using a mouse model of cerebral infarction, we demonstrated that stem cells develop within ischemic areas. Ischemia-induced stem cells can function as neural progenitors; thus, we initially named them injury/ischemia-induced neural stem/progenitor cells (iNSPCs). However, because they differentiate into more than neural lineages, we now refer to them as ischemia-induced multipotent stem cells (iSCs). Very recently, we showed that putative iNSPCs/iSCs are present within post-stroke areas in human brains. Because iNSPCs/iSCs isolated from mouse and human ischemic tissues can differentiate into neuronal lineages in vitro, it is possible that a clearer understanding of iNSPC/iSC profiles and the molecules that regulate iNSPC/iSC fate (e.g., proliferation, differentiation, and survival) would make it possible to perform neural regeneration/repair in patients following stroke. In this article, we introduce the origin and traits of iNSPCs/iSCs based on our reports and recent viewpoints. We also discuss their possible contribution to neurogenesis through endogenous and exogenous iNSPC/iSC therapies following ischemic stroke.
Literatur
1.
Zurück zum Zitat Nakata M, Nakagomi T, Maeda M, Nakano-Doi A, Momota Y, Matsuyama T. Induction of perivascular neural stem cells and possible contribution to neurogenesis following transient brain ischemia/reperfusion injury. Transl Stroke Res. 2017;8:131–43.PubMedCrossRef Nakata M, Nakagomi T, Maeda M, Nakano-Doi A, Momota Y, Matsuyama T. Induction of perivascular neural stem cells and possible contribution to neurogenesis following transient brain ischemia/reperfusion injury. Transl Stroke Res. 2017;8:131–43.PubMedCrossRef
2.
Zurück zum Zitat Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol. 2004;469:311–24.PubMedCrossRef Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol. 2004;469:311–24.PubMedCrossRef
3.
Zurück zum Zitat Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703–16.PubMedCrossRef Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703–16.PubMedCrossRef
4.
Zurück zum Zitat Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 1996;16:2027–33.PubMed Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 1996;16:2027–33.PubMed
5.
Zurück zum Zitat Goings GE, Sahni V, Szele FG. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res. 2004;996:213–26.PubMedCrossRef Goings GE, Sahni V, Szele FG. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res. 2004;996:213–26.PubMedCrossRef
6.
Zurück zum Zitat Nakagomi T, Taguchi A, Fujimori Y, Saino O, Nakano-Doi A, Kubo S, et al. Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur J Neurosci. 2009;29:1842–52.PubMedCrossRef Nakagomi T, Taguchi A, Fujimori Y, Saino O, Nakano-Doi A, Kubo S, et al. Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur J Neurosci. 2009;29:1842–52.PubMedCrossRef
7.
Zurück zum Zitat Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, et al. Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci. 2010;13:173–9.PubMedCrossRef Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, et al. Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci. 2010;13:173–9.PubMedCrossRef
8.
Zurück zum Zitat Sirko S, Neitz A, Mittmann T, Horvat-Brocker A, von Holst A, Eysel UT, et al. Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain. 2009;132:2252–64.PubMedCrossRef Sirko S, Neitz A, Mittmann T, Horvat-Brocker A, von Holst A, Eysel UT, et al. Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain. 2009;132:2252–64.PubMedCrossRef
9.
Zurück zum Zitat Xue JH, Yanamoto H, Nakajo Y, Tohnai N, Nakano Y, Hori T, et al. Induced spreading depression evokes cell division of astrocytes in the subpial zone, generating neural precursor-like cells and new immature neurons in the adult cerebral cortex. Stroke. 2009;40:e606–13.PubMedCrossRef Xue JH, Yanamoto H, Nakajo Y, Tohnai N, Nakano Y, Hori T, et al. Induced spreading depression evokes cell division of astrocytes in the subpial zone, generating neural precursor-like cells and new immature neurons in the adult cerebral cortex. Stroke. 2009;40:e606–13.PubMedCrossRef
10.
Zurück zum Zitat Ninomiya S, Esumi S, Ohta K, Fukuda T, Ito T, Imayoshi I, et al. Amygdala kindling induces nestin expression in the leptomeninges of the neocortex. Neurosci Res. 2013;75:121–9.PubMedCrossRef Ninomiya S, Esumi S, Ohta K, Fukuda T, Ito T, Imayoshi I, et al. Amygdala kindling induces nestin expression in the leptomeninges of the neocortex. Neurosci Res. 2013;75:121–9.PubMedCrossRef
11.
Zurück zum Zitat Decimo I, Bifari F, Rodriguez FJ, Malpeli G, Dolci S, Lavarini V, et al. Nestin- and doublecortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction. Stem Cells. 2011;29:2062–76.PubMedPubMedCentralCrossRef Decimo I, Bifari F, Rodriguez FJ, Malpeli G, Dolci S, Lavarini V, et al. Nestin- and doublecortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction. Stem Cells. 2011;29:2062–76.PubMedPubMedCentralCrossRef
12.
Zurück zum Zitat Nakagomi T, Molnar Z, Taguchi A, Nakano-Doi A, Lu S, Kasahara Y, et al. Leptomeningeal-derived doublecortin-expressing cells in poststroke brain. Stem Cells Dev. 2012;21:2350–4.PubMedPubMedCentralCrossRef Nakagomi T, Molnar Z, Taguchi A, Nakano-Doi A, Lu S, Kasahara Y, et al. Leptomeningeal-derived doublecortin-expressing cells in poststroke brain. Stem Cells Dev. 2012;21:2350–4.PubMedPubMedCentralCrossRef
13.
Zurück zum Zitat Nakagomi T, Molnar Z, Nakano-Doi A, Taguchi A, Saino O, Kubo S, et al. Ischemia-induced neural stem/progenitor cells in the pia mater following cortical infarction. Stem Cells Dev. 2011;20:2037–51.PubMedCrossRef Nakagomi T, Molnar Z, Nakano-Doi A, Taguchi A, Saino O, Kubo S, et al. Ischemia-induced neural stem/progenitor cells in the pia mater following cortical infarction. Stem Cells Dev. 2011;20:2037–51.PubMedCrossRef
14.
Zurück zum Zitat Hutchings M, Weller RO. Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg. 1986;65:316–25.PubMedCrossRef Hutchings M, Weller RO. Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg. 1986;65:316–25.PubMedCrossRef
15.
Zurück zum Zitat Nakagomi T, Kubo S, Nakano-Doi A, Sakuma R, Lu S, Narita A, et al. Brain vascular pericytes following ischemia have multipotential stem cell activity to differntiate into neural and vascular lineage cells. Stem Cells. 2015;33:1962–74.PubMedCrossRef Nakagomi T, Kubo S, Nakano-Doi A, Sakuma R, Lu S, Narita A, et al. Brain vascular pericytes following ischemia have multipotential stem cell activity to differntiate into neural and vascular lineage cells. Stem Cells. 2015;33:1962–74.PubMedCrossRef
17.
Zurück zum Zitat Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008;3:279–88.PubMedCrossRef Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008;3:279–88.PubMedCrossRef
18.
Zurück zum Zitat Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, et al. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells. 2010;28:545–54.PubMed Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, et al. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells. 2010;28:545–54.PubMed
19.
Zurück zum Zitat Obernier K, Tong CK, Alvarez-Buylla A. Restricted nature of adult neural stem cells: re-evaluation of their potential for brain repair. Front Neurosci. 2014;8:162.PubMedPubMedCentralCrossRef Obernier K, Tong CK, Alvarez-Buylla A. Restricted nature of adult neural stem cells: re-evaluation of their potential for brain repair. Front Neurosci. 2014;8:162.PubMedPubMedCentralCrossRef
20.
Zurück zum Zitat Shimada IS, Peterson BM, Spees JL. Isolation of locally derived stem/progenitor cells from the peri-infarct area that do not migrate from the lateral ventricle after cortical stroke. Stroke. 2010;41:e552–60.PubMedPubMedCentralCrossRef Shimada IS, Peterson BM, Spees JL. Isolation of locally derived stem/progenitor cells from the peri-infarct area that do not migrate from the lateral ventricle after cortical stroke. Stroke. 2010;41:e552–60.PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Shimada IS, LeComte MD, Granger JC, Quinlan NJ, Spees JL. Self-renewal and differentiation of reactive astrocyte-derived neural stem/progenitor cells isolated from the cortical peri-infarct area after stroke. J Neurosci. 2012;32:7926–40.PubMedPubMedCentralCrossRef Shimada IS, LeComte MD, Granger JC, Quinlan NJ, Spees JL. Self-renewal and differentiation of reactive astrocyte-derived neural stem/progenitor cells isolated from the cortical peri-infarct area after stroke. J Neurosci. 2012;32:7926–40.PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Gotz M, Sirko S, Beckers J, Irmler M. Reactive astrocytes as neural stem or progenitor cells: in vivo lineage, in vitro potential, and genome-wide expression analysis. Glia. 2015;63:1452–68.PubMedPubMedCentralCrossRef Gotz M, Sirko S, Beckers J, Irmler M. Reactive astrocytes as neural stem or progenitor cells: in vivo lineage, in vitro potential, and genome-wide expression analysis. Glia. 2015;63:1452–68.PubMedPubMedCentralCrossRef
23.
Zurück zum Zitat Faiz M, Sachewsky N, Gascon S, Bang KW, Morshead CM, Nagy A. Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell. 2015;17:624–34.PubMedCrossRef Faiz M, Sachewsky N, Gascon S, Bang KW, Morshead CM, Nagy A. Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell. 2015;17:624–34.PubMedCrossRef
24.
Zurück zum Zitat Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci U S A. 2008;105:1026–31.PubMedPubMedCentralCrossRef Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci U S A. 2008;105:1026–31.PubMedPubMedCentralCrossRef
25.
Zurück zum Zitat Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, et al. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007;67:5727–36.PubMedCrossRef Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, et al. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007;67:5727–36.PubMedCrossRef
26.
Zurück zum Zitat Chojnacki AK, Mak GK, Weiss S. Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci. 2009;10:153–63.PubMedCrossRef Chojnacki AK, Mak GK, Weiss S. Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci. 2009;10:153–63.PubMedCrossRef
27.
Zurück zum Zitat Moreno-Manzano V, Rodriguez-Jimenez FJ, Garcia-Rosello M, Lainez S, Erceg S, Calvo MT, et al. Activated spinal cord ependymal stem cells rescue neurological function. Stem Cells. 2009;27:733–43.PubMedCrossRef Moreno-Manzano V, Rodriguez-Jimenez FJ, Garcia-Rosello M, Lainez S, Erceg S, Calvo MT, et al. Activated spinal cord ependymal stem cells rescue neurological function. Stem Cells. 2009;27:733–43.PubMedCrossRef
28.
Zurück zum Zitat Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, et al. Forebrain ependymal cells are notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci. 2009;12:259–67.PubMedCrossRef Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, et al. Forebrain ependymal cells are notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci. 2009;12:259–67.PubMedCrossRef
29.
Zurück zum Zitat Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell. 2009;139:597–609.PubMedPubMedCentralCrossRef Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, et al. Retinoic acid from the meninges regulates cortical neuron generation. Cell. 2009;139:597–609.PubMedPubMedCentralCrossRef
30.
Zurück zum Zitat Danilov AI, Gomes-Leal W, Ahlenius H, Kokaia Z, Carlemalm E, Lindvall O. Ultrastructural and antigenic properties of neural stem cells and their progeny in adult rat subventricular zone. Glia. 2009;57:136–52.PubMedCrossRef Danilov AI, Gomes-Leal W, Ahlenius H, Kokaia Z, Carlemalm E, Lindvall O. Ultrastructural and antigenic properties of neural stem cells and their progeny in adult rat subventricular zone. Glia. 2009;57:136–52.PubMedCrossRef
31.
Zurück zum Zitat Bifari F, Decimo I, Pino A, Llorens-Bobadilla E, Zhao S, Lange C, et al. Neurogenic radial glia-like cells in meninges migrate and differentiate into functionally integrated neurons in the neonatal cortex. Cell Stem Cell. 2017;20:360–373.e7.PubMedCrossRef Bifari F, Decimo I, Pino A, Llorens-Bobadilla E, Zhao S, Lange C, et al. Neurogenic radial glia-like cells in meninges migrate and differentiate into functionally integrated neurons in the neonatal cortex. Cell Stem Cell. 2017;20:360–373.e7.PubMedCrossRef
32.
Zurück zum Zitat Moss J, Gebara E, Bushong EA, Sanchez-Pascual I, O'Laoi R, El M'Ghari I, et al. Fine processes of Nestin-GFP-positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature. Proc Natl Acad Sci U S A. 2016;113:E2536–45.PubMedPubMedCentralCrossRef Moss J, Gebara E, Bushong EA, Sanchez-Pascual I, O'Laoi R, El M'Ghari I, et al. Fine processes of Nestin-GFP-positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature. Proc Natl Acad Sci U S A. 2016;113:E2536–45.PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Kondo T, Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 2000;289:1754–7.PubMedCrossRef Kondo T, Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 2000;289:1754–7.PubMedCrossRef
34.
Zurück zum Zitat Gaughwin PM, Caldwell MA, Anderson JM, Schwiening CJ, Fawcett JW, Compston DA, et al. Astrocytes promote neurogenesis from oligodendrocyte precursor cells. Eur J Neurosci. 2006;23:945–56.PubMedCrossRef Gaughwin PM, Caldwell MA, Anderson JM, Schwiening CJ, Fawcett JW, Compston DA, et al. Astrocytes promote neurogenesis from oligodendrocyte precursor cells. Eur J Neurosci. 2006;23:945–56.PubMedCrossRef
35.
Zurück zum Zitat Maki T, Maeda M, Uemura M, Lo EK, Terasaki Y, Liang AC, et al. Potential interactions between pericytes and oligodendrocyte precursor cells in perivascular regions of cerebral white matter. Neurosci Lett. 2015;597:164–9.PubMedPubMedCentralCrossRef Maki T, Maeda M, Uemura M, Lo EK, Terasaki Y, Liang AC, et al. Potential interactions between pericytes and oligodendrocyte precursor cells in perivascular regions of cerebral white matter. Neurosci Lett. 2015;597:164–9.PubMedPubMedCentralCrossRef
36.
Zurück zum Zitat Seo JH, Maki T, Maeda M, Miyamoto N, Liang AC, Hayakawa K, et al. Oligodendrocyte precursor cells support blood-brain barrier integrity via TGF-beta signaling. PLoS One. 2014;9:e103174.PubMedPubMedCentralCrossRef Seo JH, Maki T, Maeda M, Miyamoto N, Liang AC, Hayakawa K, et al. Oligodendrocyte precursor cells support blood-brain barrier integrity via TGF-beta signaling. PLoS One. 2014;9:e103174.PubMedPubMedCentralCrossRef
37.
Zurück zum Zitat Sundberg M, Skottman H, Suuronen R, Narkilahti S. Production and isolation of NG2+ oligodendrocyte precursors from human embryonic stem cells in defined serum-free medium. Stem Cell Res. 2010;5:91–103.PubMedCrossRef Sundberg M, Skottman H, Suuronen R, Narkilahti S. Production and isolation of NG2+ oligodendrocyte precursors from human embryonic stem cells in defined serum-free medium. Stem Cell Res. 2010;5:91–103.PubMedCrossRef
38.
Zurück zum Zitat Ulrich R, Seeliger F, Kreutzer M, Germann PG, Baumgartner W. Limited remyelination in Theiler’s murine encephalomyelitis due to insufficient oligodendroglial differentiation of nerve/glial antigen 2 (NG2)-positive putative oligodendroglial progenitor cells. Neuropathol Appl Neurobiol. 2008;34:603–20.PubMedCrossRef Ulrich R, Seeliger F, Kreutzer M, Germann PG, Baumgartner W. Limited remyelination in Theiler’s murine encephalomyelitis due to insufficient oligodendroglial differentiation of nerve/glial antigen 2 (NG2)-positive putative oligodendroglial progenitor cells. Neuropathol Appl Neurobiol. 2008;34:603–20.PubMedCrossRef
39.
Zurück zum Zitat Song FE, Huang JL, Lin SH, Wang S, Ma GF, Tong XP. Roles of NG2-glia in ischemic stroke. CNS Neurosci Ther. 2017;23:547–53.PubMedCrossRef Song FE, Huang JL, Lin SH, Wang S, Ma GF, Tong XP. Roles of NG2-glia in ischemic stroke. CNS Neurosci Ther. 2017;23:547–53.PubMedCrossRef
40.
Zurück zum Zitat Stallcup WB, Beasley L. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci. 1987;7:2737–44.PubMed Stallcup WB, Beasley L. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci. 1987;7:2737–44.PubMed
41.
Zurück zum Zitat Birbrair A, Zhang T, Wang ZM, Messi ML, Olson JD, Mintz A, et al. Type-2 pericytes participate in normal and tumoral angiogenesis. Am J Physiol Cell Physiol. 2014;307:C25–38.PubMedPubMedCentralCrossRef Birbrair A, Zhang T, Wang ZM, Messi ML, Olson JD, Mintz A, et al. Type-2 pericytes participate in normal and tumoral angiogenesis. Am J Physiol Cell Physiol. 2014;307:C25–38.PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev. 2013;22:2298–314.PubMedPubMedCentralCrossRef Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev. 2013;22:2298–314.PubMedPubMedCentralCrossRef
43.
Zurück zum Zitat Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Res. 2012;10:67–84.PubMedPubMedCentralCrossRef Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Res. 2012;10:67–84.PubMedPubMedCentralCrossRef
44.
Zurück zum Zitat Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab. 2006;26:613–24.PubMedCrossRef Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab. 2006;26:613–24.PubMedCrossRef
45.
Zurück zum Zitat Milesi S, Boussadia B, Plaud C, Catteau M, Rousset MC, De Bock F, et al. Redistribution of PDGFRbeta cells and NG2DsRed pericytes at the cerebrovasculature after status epilepticus. Neurobiol Dis. 2014;71:151–8.PubMedCrossRef Milesi S, Boussadia B, Plaud C, Catteau M, Rousset MC, De Bock F, et al. Redistribution of PDGFRbeta cells and NG2DsRed pericytes at the cerebrovasculature after status epilepticus. Neurobiol Dis. 2014;71:151–8.PubMedCrossRef
47.
Zurück zum Zitat Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol. 2003;161:169–86.PubMedPubMedCentralCrossRef Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol. 2003;161:169–86.PubMedPubMedCentralCrossRef
48.
Zurück zum Zitat Aguirre A, Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci. 2004;24:10530–41.PubMedCrossRef Aguirre A, Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci. 2004;24:10530–41.PubMedCrossRef
49.
Zurück zum Zitat Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell. 2010;6:578–90.PubMedCrossRef Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell. 2010;6:578–90.PubMedCrossRef
50.
Zurück zum Zitat Yokoyama A, Sakamoto A, Kameda K, Imai Y, Tanaka J. NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia. 2006;53:754–68.PubMedCrossRef Yokoyama A, Sakamoto A, Kameda K, Imai Y, Tanaka J. NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia. 2006;53:754–68.PubMedCrossRef
51.
Zurück zum Zitat Nakagomi T, Nakano-Doi A, Kawamura M, Matsuyama T. Do vascular Pericytes contribute to neurovasculogenesis in the central nervous system as multipotent vascular stem cells? Stem Cells Dev. 2015;24:1730–9.PubMedCrossRef Nakagomi T, Nakano-Doi A, Kawamura M, Matsuyama T. Do vascular Pericytes contribute to neurovasculogenesis in the central nervous system as multipotent vascular stem cells? Stem Cells Dev. 2015;24:1730–9.PubMedCrossRef
52.
53.
Zurück zum Zitat Zhang J, Takahashi HK, Liu K, Wake H, Liu R, Maruo T, et al. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke. 2011;42:1420–8.PubMedCrossRef Zhang J, Takahashi HK, Liu K, Wake H, Liu R, Maruo T, et al. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke. 2011;42:1420–8.PubMedCrossRef
54.
Zurück zum Zitat Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557–61.PubMedCrossRef Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557–61.PubMedCrossRef
55.
Zurück zum Zitat Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68:409–27.PubMedPubMedCentralCrossRef Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68:409–27.PubMedPubMedCentralCrossRef
56.
Zurück zum Zitat Crisan M, Chen CW, Corselli M, Andriolo G, Lazzari L, Peault B. Perivascular multipotent progenitor cells in human organs. Ann N Y Acad Sci. 2009;1176:118–23.PubMedCrossRef Crisan M, Chen CW, Corselli M, Andriolo G, Lazzari L, Peault B. Perivascular multipotent progenitor cells in human organs. Ann N Y Acad Sci. 2009;1176:118–23.PubMedCrossRef
57.
Zurück zum Zitat Kabara M, Kawabe J, Matsuki M, Hira Y, Minoshima A, Shimamura K, et al. Immortalized multipotent pericytes derived from the vasa vasorum in the injured vasculature. A cellular tool for studies of vascular remodeling and regeneration. Lab Investig. 2014;94:1340–54.PubMedCrossRef Kabara M, Kawabe J, Matsuki M, Hira Y, Minoshima A, Shimamura K, et al. Immortalized multipotent pericytes derived from the vasa vasorum in the injured vasculature. A cellular tool for studies of vascular remodeling and regeneration. Lab Investig. 2014;94:1340–54.PubMedCrossRef
58.
Zurück zum Zitat Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Pericytes: multitasking cells in the regeneration of injured, diseased, and aged skeletal muscle. Front Aging Neurosci. 2014;6:245.PubMedPubMedCentralCrossRef Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Pericytes: multitasking cells in the regeneration of injured, diseased, and aged skeletal muscle. Front Aging Neurosci. 2014;6:245.PubMedPubMedCentralCrossRef
59.
Zurück zum Zitat Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation. 2004;110:2226–32.PubMedCrossRef Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation. 2004;110:2226–32.PubMedCrossRef
60.
Zurück zum Zitat Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, et al. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation. 2012;125:87–99.PubMedCrossRef Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, et al. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation. 2012;125:87–99.PubMedCrossRef
61.
Zurück zum Zitat Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE. Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res. 1998;13:828–38.PubMedCrossRef Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE. Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res. 1998;13:828–38.PubMedCrossRef
62.
Zurück zum Zitat Sakuma R, Kawahara M, Nakano-Doi A, Takahashi A, Tanaka Y, Narita A, et al. Brain pericytes serve as microglia-generating multipotent vascular stem cells following ischemic stroke. J Neuroinflammation. 2016;13:57.PubMedPubMedCentralCrossRef Sakuma R, Kawahara M, Nakano-Doi A, Takahashi A, Tanaka Y, Narita A, et al. Brain pericytes serve as microglia-generating multipotent vascular stem cells following ischemic stroke. J Neuroinflammation. 2016;13:57.PubMedPubMedCentralCrossRef
63.
Zurück zum Zitat Nakano-Doi A, Nakagomi T, Sakuma R, Takahashi A, Tanaka Y, Kawamura M, et al. Expression patterns and phenotypic changes regarding stemness in brain pericytes in health and disease. J Stem Cell Res Ther. 2016;6:332.CrossRef Nakano-Doi A, Nakagomi T, Sakuma R, Takahashi A, Tanaka Y, Kawamura M, et al. Expression patterns and phenotypic changes regarding stemness in brain pericytes in health and disease. J Stem Cell Res Ther. 2016;6:332.CrossRef
64.
Zurück zum Zitat An SJ, Liu P, Shao TM, Wang ZJ, Lu HG, Jiao Z, et al. Characterization and functions of vascular adventitial fibroblast subpopulations. Cell Physiol Biochem. 2015;35:1137–50.PubMedCrossRef An SJ, Liu P, Shao TM, Wang ZJ, Lu HG, Jiao Z, et al. Characterization and functions of vascular adventitial fibroblast subpopulations. Cell Physiol Biochem. 2015;35:1137–50.PubMedCrossRef
65.
Zurück zum Zitat Park TI, Monzo H, Mee EW, Bergin PS, Teoh HH, Montgomery JM, et al. Adult human brain neural progenitor cells (NPCs) and fibroblast-like cells have similar properties in vitro but only NPCs differentiate into neurons. PLoS One. 2012;7:e37742.PubMedPubMedCentralCrossRef Park TI, Monzo H, Mee EW, Bergin PS, Teoh HH, Montgomery JM, et al. Adult human brain neural progenitor cells (NPCs) and fibroblast-like cells have similar properties in vitro but only NPCs differentiate into neurons. PLoS One. 2012;7:e37742.PubMedPubMedCentralCrossRef
66.
Zurück zum Zitat Makihara N, Arimura K, Ago T, Tachibana M, Nishimura A, Nakamura K, et al. Involvement of platelet-derived growth factor receptor beta in fibrosis through extracellular matrix protein production after ischemic stroke. Exp Neurol. 2015;264:127–34.PubMedCrossRef Makihara N, Arimura K, Ago T, Tachibana M, Nishimura A, Nakamura K, et al. Involvement of platelet-derived growth factor receptor beta in fibrosis through extracellular matrix protein production after ischemic stroke. Exp Neurol. 2015;264:127–34.PubMedCrossRef
67.
Zurück zum Zitat Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMedCrossRef Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMedCrossRef
68.
Zurück zum Zitat Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.PubMedCrossRef Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.PubMedCrossRef
69.
Zurück zum Zitat Chang Y, Li H, Guo Z. Mesenchymal stem cell-like properties in fibroblasts. Cell Physiol Biochem. 2014;34:703–14.PubMedCrossRef Chang Y, Li H, Guo Z. Mesenchymal stem cell-like properties in fibroblasts. Cell Physiol Biochem. 2014;34:703–14.PubMedCrossRef
70.
Zurück zum Zitat Kuroda Y, Wakao S, Kitada M, Murakami T, Nojima M, Dezawa M. Isolation, culture and evaluation of multilineage-differentiating stress-enduring (Muse) cells. Nat Protoc. 2013;8:1391–415.PubMedCrossRef Kuroda Y, Wakao S, Kitada M, Murakami T, Nojima M, Dezawa M. Isolation, culture and evaluation of multilineage-differentiating stress-enduring (Muse) cells. Nat Protoc. 2013;8:1391–415.PubMedCrossRef
71.
Zurück zum Zitat Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A. 2010;107:8639–43.PubMedPubMedCentralCrossRef Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A. 2010;107:8639–43.PubMedPubMedCentralCrossRef
72.
Zurück zum Zitat Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, Akashi H, et al. Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc Natl Acad Sci U S A. 2011;108:9875–80.PubMedPubMedCentralCrossRef Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, Akashi H, et al. Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc Natl Acad Sci U S A. 2011;108:9875–80.PubMedPubMedCentralCrossRef
73.
Zurück zum Zitat Tatebayashi K, Tanaka Y, Nakano-Doi A, Sakuma R, Kamachi S, Shirakawa M, et al. Identification of multipotent stem cells in human brain tissue following stroke. Stem Cells Dev. 2017;26:787–97.PubMedPubMedCentralCrossRef Tatebayashi K, Tanaka Y, Nakano-Doi A, Sakuma R, Kamachi S, Shirakawa M, et al. Identification of multipotent stem cells in human brain tissue following stroke. Stem Cells Dev. 2017;26:787–97.PubMedPubMedCentralCrossRef
74.
Zurück zum Zitat Thier M, Worsdorfer P, Lakes YB, Gorris R, Herms S, Opitz T, et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell. 2012;10:473–9.PubMedCrossRef Thier M, Worsdorfer P, Lakes YB, Gorris R, Herms S, Opitz T, et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell. 2012;10:473–9.PubMedCrossRef
75.
Zurück zum Zitat Karow M, Sanchez R, Schichor C, Masserdotti G, Ortega F, Heinrich C, et al. Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell. 2012;11:471–6.PubMedCrossRef Karow M, Sanchez R, Schichor C, Masserdotti G, Ortega F, Heinrich C, et al. Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell. 2012;11:471–6.PubMedCrossRef
76.
Zurück zum Zitat Yanger K, Zong Y, Maggs LR, Shapira SN, Maddipati R, Aiello NM, et al. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev. 2013;27:719–24.PubMedPubMedCentralCrossRef Yanger K, Zong Y, Maggs LR, Shapira SN, Maddipati R, Aiello NM, et al. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev. 2013;27:719–24.PubMedPubMedCentralCrossRef
77.
Zurück zum Zitat Luz-Madrigal A, Grajales-Esquivel E, McCorkle A, DiLorenzo AM, Barbosa-Sabanero K, Tsonis PA, et al. Reprogramming of the chick retinal pigmented epithelium after retinal injury. BMC Biol. 2014;12:28.PubMedPubMedCentralCrossRef Luz-Madrigal A, Grajales-Esquivel E, McCorkle A, DiLorenzo AM, Barbosa-Sabanero K, Tsonis PA, et al. Reprogramming of the chick retinal pigmented epithelium after retinal injury. BMC Biol. 2014;12:28.PubMedPubMedCentralCrossRef
78.
Zurück zum Zitat Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150–61.PubMedCrossRef Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150–61.PubMedCrossRef
79.
Zurück zum Zitat Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell. 2009;5:237–41.PubMedCrossRef Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell. 2009;5:237–41.PubMedCrossRef
80.
Zurück zum Zitat Nakagomi T, Nakano-Doi A, Narita A, Matsuyama T. Concise review: are stimulated somatic cells truly reprogrammed into an ES/iPS-like pluripotent state? Better understanding by ischemia-induced multipotent stem cells in a mouse model of cerebral infarction. Stem Cells Int. 2015;2015:630693.PubMedPubMedCentralCrossRef Nakagomi T, Nakano-Doi A, Narita A, Matsuyama T. Concise review: are stimulated somatic cells truly reprogrammed into an ES/iPS-like pluripotent state? Better understanding by ischemia-induced multipotent stem cells in a mouse model of cerebral infarction. Stem Cells Int. 2015;2015:630693.PubMedPubMedCentralCrossRef
81.
82.
Zurück zum Zitat Klein D, Hohn HP, Kleff V, Tilki D, Ergun S. Vascular wall-resident stem cells. Histol Histopathol. 2010;25:681–9.PubMed Klein D, Hohn HP, Kleff V, Tilki D, Ergun S. Vascular wall-resident stem cells. Histol Histopathol. 2010;25:681–9.PubMed
85.
Zurück zum Zitat Paul G, Ozen I, Christophersen NS, Reinbothe T, Bengzon J, Visse E, et al. The adult human brain harbors multipotent perivascular mesenchymal stem cells. PLoS One. 2012;7:e35577.PubMedPubMedCentralCrossRef Paul G, Ozen I, Christophersen NS, Reinbothe T, Bengzon J, Visse E, et al. The adult human brain harbors multipotent perivascular mesenchymal stem cells. PLoS One. 2012;7:e35577.PubMedPubMedCentralCrossRef
86.
Zurück zum Zitat Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMedCrossRef Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMedCrossRef
87.
Zurück zum Zitat Esteves CL, Sheldrake TA, Dawson L, Menghini T, Rink BE, Amilon K, et al. Equine mesenchymal stromal cells retain a pericyte-like phenotype. Stem Cells Dev. 2017;26:964–72.PubMedPubMedCentralCrossRef Esteves CL, Sheldrake TA, Dawson L, Menghini T, Rink BE, Amilon K, et al. Equine mesenchymal stromal cells retain a pericyte-like phenotype. Stem Cells Dev. 2017;26:964–72.PubMedPubMedCentralCrossRef
88.
Zurück zum Zitat Ozen I, Boix J, Paul G. Perivascular mesenchymal stem cells in the adult human brain: a future target for neuroregeneration? Clin Transl Med. 2012;1:30.PubMedPubMedCentralCrossRef Ozen I, Boix J, Paul G. Perivascular mesenchymal stem cells in the adult human brain: a future target for neuroregeneration? Clin Transl Med. 2012;1:30.PubMedPubMedCentralCrossRef
89.
Zurück zum Zitat Vezzani B, E Pierantozzi, Sorrentino V. Not all pericytes are born equal: pericytes from human adult tissues present different differentiation properties. Stem Cells Dev. 2016;25(20):1549–58. Vezzani B, E Pierantozzi, Sorrentino V. Not all pericytes are born equal: pericytes from human adult tissues present different differentiation properties. Stem Cells Dev. 2016;25(20):1549–58.
90.
Zurück zum Zitat Bouacida A, Rosset P, Trichet V, Guilloton F, Espagnolle N, Cordonier T, et al. Pericyte-like progenitors show high immaturity and engraftment potential as compared with mesenchymal stem cells. PLoS One. 2012;7:e48648.PubMedPubMedCentralCrossRef Bouacida A, Rosset P, Trichet V, Guilloton F, Espagnolle N, Cordonier T, et al. Pericyte-like progenitors show high immaturity and engraftment potential as compared with mesenchymal stem cells. PLoS One. 2012;7:e48648.PubMedPubMedCentralCrossRef
91.
Zurück zum Zitat Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT. Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A. 2011;108:6503–8.PubMedPubMedCentralCrossRef Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT. Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A. 2011;108:6503–8.PubMedPubMedCentralCrossRef
93.
Zurück zum Zitat Corselli M, Chen CW, Crisan M, Lazzari L, Peault B. Perivascular ancestors of adult multipotent stem cells. Arterioscler Thromb Vasc Biol. 2010;30:1104–9.PubMedCrossRef Corselli M, Chen CW, Crisan M, Lazzari L, Peault B. Perivascular ancestors of adult multipotent stem cells. Arterioscler Thromb Vasc Biol. 2010;30:1104–9.PubMedCrossRef
94.
Zurück zum Zitat Appaix F, Nissou MF, van der Sanden B, Dreyfus M, Berger F, Issartel JP, et al. Brain mesenchymal stem cells: the other stem cells of the brain? World J Stem Cells. 2014;6:134–43.PubMedPubMedCentralCrossRef Appaix F, Nissou MF, van der Sanden B, Dreyfus M, Berger F, Issartel JP, et al. Brain mesenchymal stem cells: the other stem cells of the brain? World J Stem Cells. 2014;6:134–43.PubMedPubMedCentralCrossRef
95.
Zurück zum Zitat Tropel P, Noel D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res. 2004;295:395–406.PubMedCrossRef Tropel P, Noel D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res. 2004;295:395–406.PubMedCrossRef
96.
Zurück zum Zitat Kubota Y, Takubo K, Hirashima M, Nagoshi N, Kishi K, Okuno Y, et al. Isolation and function of mouse tissue resident vascular precursors marked by myelin protein zero. J Exp Med. 2011;208:949–60.PubMedPubMedCentralCrossRef Kubota Y, Takubo K, Hirashima M, Nagoshi N, Kishi K, Okuno Y, et al. Isolation and function of mouse tissue resident vascular precursors marked by myelin protein zero. J Exp Med. 2011;208:949–60.PubMedPubMedCentralCrossRef
97.
Zurück zum Zitat Nagoshi N, Shibata S, Nakamura M, Matsuzaki Y, Toyama Y, Okano H. Neural crest-derived stem cells display a wide variety of characteristics. J Cell Biochem. 2009;107:1046–52.PubMedCrossRef Nagoshi N, Shibata S, Nakamura M, Matsuzaki Y, Toyama Y, Okano H. Neural crest-derived stem cells display a wide variety of characteristics. J Cell Biochem. 2009;107:1046–52.PubMedCrossRef
98.
Zurück zum Zitat Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, et al. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell. 2008;2:392–403.PubMedCrossRef Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, et al. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell. 2008;2:392–403.PubMedCrossRef
99.
Zurück zum Zitat Calloni GW, Le Douarin NM, Dupin E. High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci U S A. 2009;106:8947–52.PubMedPubMedCentralCrossRef Calloni GW, Le Douarin NM, Dupin E. High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci U S A. 2009;106:8947–52.PubMedPubMedCentralCrossRef
100.
Zurück zum Zitat Calloni GW, Glavieux-Pardanaud C, Le Douarin NM, Dupin E. Sonic hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci U S A. 2007;104:19879–84.PubMedPubMedCentralCrossRef Calloni GW, Glavieux-Pardanaud C, Le Douarin NM, Dupin E. Sonic hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci U S A. 2007;104:19879–84.PubMedPubMedCentralCrossRef
101.
Zurück zum Zitat Wislet-Gendebien S, Laudet E, Neirinckx V, Alix P, Leprince P, Glejzer A, et al. Mesenchymal stem cells and neural crest stem cells from adult bone marrow: characterization of their surprising similarities and differences. Cell Mol Life Sci. 2012;69:2593–608.PubMedCrossRef Wislet-Gendebien S, Laudet E, Neirinckx V, Alix P, Leprince P, Glejzer A, et al. Mesenchymal stem cells and neural crest stem cells from adult bone marrow: characterization of their surprising similarities and differences. Cell Mol Life Sci. 2012;69:2593–608.PubMedCrossRef
103.
Zurück zum Zitat Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development. 2001;128:1059–68.PubMed Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development. 2001;128:1059–68.PubMed
104.
Zurück zum Zitat Korn J, Christ B, Kurz H. Neuroectodermal origin of brain pericytes and vascular smooth muscle cells. J Comp Neurol. 2002;442:78–88.PubMedCrossRef Korn J, Christ B, Kurz H. Neuroectodermal origin of brain pericytes and vascular smooth muscle cells. J Comp Neurol. 2002;442:78–88.PubMedCrossRef
105.
Zurück zum Zitat Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, et al. A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci U S A. 2008;105:9349–54.PubMedPubMedCentralCrossRef Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, et al. A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci U S A. 2008;105:9349–54.PubMedPubMedCentralCrossRef
106.
Zurück zum Zitat Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest. 2004;113:1258–65.PubMedPubMedCentralCrossRef Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest. 2004;113:1258–65.PubMedPubMedCentralCrossRef
107.
Zurück zum Zitat Klein D, Meissner N, Kleff V, Jastrow H, Yamaguchi M, Ergun S, et al. Nestin(+) tissue-resident multipotent stem cells contribute to tumor progression by differentiating into pericytes and smooth muscle cells resulting in blood vessel remodeling. Front Oncol. 2014;4:169.PubMedPubMedCentralCrossRef Klein D, Meissner N, Kleff V, Jastrow H, Yamaguchi M, Ergun S, et al. Nestin(+) tissue-resident multipotent stem cells contribute to tumor progression by differentiating into pericytes and smooth muscle cells resulting in blood vessel remodeling. Front Oncol. 2014;4:169.PubMedPubMedCentralCrossRef
108.
Zurück zum Zitat Chen Y, Wong MM, Campagnolo P, Simpson R, Winkler B, Margariti A, et al. Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler Thromb Vasc Biol. 2013;33:1844–51.PubMedCrossRef Chen Y, Wong MM, Campagnolo P, Simpson R, Winkler B, Margariti A, et al. Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler Thromb Vasc Biol. 2013;33:1844–51.PubMedCrossRef
109.
Zurück zum Zitat Yamashima T, Tonchev AB, Vachkov IH, Popivanova BK, Seki T, Sawamoto K, et al. Vascular adventitia generates neuronal progenitors in the monkey hippocampus after ischemia. Hippocampus. 2004;14:861–75.PubMedCrossRef Yamashima T, Tonchev AB, Vachkov IH, Popivanova BK, Seki T, Sawamoto K, et al. Vascular adventitia generates neuronal progenitors in the monkey hippocampus after ischemia. Hippocampus. 2004;14:861–75.PubMedCrossRef
110.
Zurück zum Zitat Kramann R, Goettsch C, Wongboonsin J, Iwata H, Schneider RK, Kuppe C, et al. Adventitial MSC-like cells are progenitors of vascular smooth muscle cells and drive vascular calcification in chronic kidney disease. Cell Stem Cell. 2016;19:628–42.PubMedCrossRef Kramann R, Goettsch C, Wongboonsin J, Iwata H, Schneider RK, Kuppe C, et al. Adventitial MSC-like cells are progenitors of vascular smooth muscle cells and drive vascular calcification in chronic kidney disease. Cell Stem Cell. 2016;19:628–42.PubMedCrossRef
111.
Zurück zum Zitat Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Skeletal muscle neural progenitor cells exhibit properties of NG2-glia. Exp Cell Res. 2013;319:45–63.PubMedCrossRef Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, et al. Skeletal muscle neural progenitor cells exhibit properties of NG2-glia. Exp Cell Res. 2013;319:45–63.PubMedCrossRef
112.
Zurück zum Zitat Zujovic V, Thibaud J, Bachelin C, Vidal M, Deboux C, Coulpier F, et al. Boundary cap cells are peripheral nervous system stem cells that can be redirected into central nervous system lineages. Proc Natl Acad Sci U S A. 2011;108:10714–9.PubMedPubMedCentralCrossRef Zujovic V, Thibaud J, Bachelin C, Vidal M, Deboux C, Coulpier F, et al. Boundary cap cells are peripheral nervous system stem cells that can be redirected into central nervous system lineages. Proc Natl Acad Sci U S A. 2011;108:10714–9.PubMedPubMedCentralCrossRef
113.
Zurück zum Zitat Weber M, Apostolova G, Widera D, Mittelbronn M, Dechant G, Kaltschmidt B, et al. Alternative generation of CNS neural stem cells and PNS derivatives from neural crest-derived peripheral stem cells. Stem Cells. 2015;33:574–88.PubMedCrossRef Weber M, Apostolova G, Widera D, Mittelbronn M, Dechant G, Kaltschmidt B, et al. Alternative generation of CNS neural stem cells and PNS derivatives from neural crest-derived peripheral stem cells. Stem Cells. 2015;33:574–88.PubMedCrossRef
114.
Zurück zum Zitat Cimadamore F, Fishwick K, Giusto E, Gnedeva K, Cattarossi G, Miller A, et al. Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell. 2011;8:538–51.PubMedPubMedCentralCrossRef Cimadamore F, Fishwick K, Giusto E, Gnedeva K, Cattarossi G, Miller A, et al. Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell. 2011;8:538–51.PubMedPubMedCentralCrossRef
115.
Zurück zum Zitat Isern J, A Garcia-Garcia, AM Martin, L Arranz, D Martin-Perez, C Torroja, F Sanchez-Cabo and S Mendez-Ferrer. (2014). The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. Elife 3:e03696. Isern J, A Garcia-Garcia, AM Martin, L Arranz, D Martin-Perez, C Torroja, F Sanchez-Cabo and S Mendez-Ferrer. (2014). The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. Elife 3:e03696.
116.
Zurück zum Zitat Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell. 2007;129:1377–88.PubMedCrossRef Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell. 2007;129:1377–88.PubMedCrossRef
117.
Zurück zum Zitat John N, Cinelli P, Wegner M, Sommer L. Transforming growth factor beta-mediated Sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells. Stem Cells. 2011;29:689–99.PubMedCrossRef John N, Cinelli P, Wegner M, Sommer L. Transforming growth factor beta-mediated Sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells. Stem Cells. 2011;29:689–99.PubMedCrossRef
118.
Zurück zum Zitat Nakayama D, Matsuyama T, Ishibashi-Ueda H, Nakagomi T, Kasahara Y, Hirose H, et al. Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur J Neurosci. 2010;31:90–8.PubMedCrossRef Nakayama D, Matsuyama T, Ishibashi-Ueda H, Nakagomi T, Kasahara Y, Hirose H, et al. Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur J Neurosci. 2010;31:90–8.PubMedCrossRef
119.
Zurück zum Zitat Nakano-Doi A, Nakagomi T, Fujikawa M, Nakagomi N, Kubo S, Lu S, et al. Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells. 2010;28:1292–302.PubMed Nakano-Doi A, Nakagomi T, Fujikawa M, Nakagomi N, Kubo S, Lu S, et al. Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells. 2010;28:1292–302.PubMed
120.
Zurück zum Zitat Takata M, Nakagomi T, Kashiwamura S, Nakano-Doi A, Saino O, Nakagomi N, et al. Glucocorticoid-induced TNF receptor-triggered T cells are key modulators for survival/death of neural stem/progenitor cells induced by ischemic stroke. Cell Death Differ. 2012;19:756–67.PubMedCrossRef Takata M, Nakagomi T, Kashiwamura S, Nakano-Doi A, Saino O, Nakagomi N, et al. Glucocorticoid-induced TNF receptor-triggered T cells are key modulators for survival/death of neural stem/progenitor cells induced by ischemic stroke. Cell Death Differ. 2012;19:756–67.PubMedCrossRef
121.
Zurück zum Zitat Saino O, Taguchi A, Nakagomi T, Nakano-Doi A, Kashiwamura S, Doe N, et al. Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res. 2010;88:2385–97.PubMed Saino O, Taguchi A, Nakagomi T, Nakano-Doi A, Kashiwamura S, Doe N, et al. Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res. 2010;88:2385–97.PubMed
122.
Zurück zum Zitat Nakagomi N, Nakagomi T, Kubo S, Nakano-Doi A, Saino O, Takata M, et al. Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction. Stem Cells. 2009;27:2185–95.PubMedCrossRef Nakagomi N, Nakagomi T, Kubo S, Nakano-Doi A, Saino O, Takata M, et al. Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction. Stem Cells. 2009;27:2185–95.PubMedCrossRef
123.
Zurück zum Zitat Hicks AU, Hewlett K, Windle V, Chernenko G, Ploughman M, Jolkkonen J, et al. Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke. Neuroscience. 2007;146:31–40.PubMedCrossRef Hicks AU, Hewlett K, Windle V, Chernenko G, Ploughman M, Jolkkonen J, et al. Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke. Neuroscience. 2007;146:31–40.PubMedCrossRef
124.
Zurück zum Zitat Kameda M, Shingo T, Takahashi K, Muraoka K, Kurozumi K, Yasuhara T, et al. Adult neural stem and progenitor cells modified to secrete GDNF can protect, migrate and integrate after intracerebral transplantation in rats with transient forebrain ischemia. Eur J Neurosci. 2007;26:1462–78.PubMedCrossRef Kameda M, Shingo T, Takahashi K, Muraoka K, Kurozumi K, Yasuhara T, et al. Adult neural stem and progenitor cells modified to secrete GDNF can protect, migrate and integrate after intracerebral transplantation in rats with transient forebrain ischemia. Eur J Neurosci. 2007;26:1462–78.PubMedCrossRef
125.
Zurück zum Zitat Honma T, Honmou O, Iihoshi S, Harada K, Houkin K, Hamada H, et al. Intravenous infusion of immortalized human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Exp Neurol. 2006;199:56–66.PubMedCrossRef Honma T, Honmou O, Iihoshi S, Harada K, Houkin K, Hamada H, et al. Intravenous infusion of immortalized human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Exp Neurol. 2006;199:56–66.PubMedCrossRef
126.
Zurück zum Zitat Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H, et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest. 2004;114:330–8.PubMedPubMedCentralCrossRef Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H, et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest. 2004;114:330–8.PubMedPubMedCentralCrossRef
127.
Zurück zum Zitat Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue H, Savitz SI, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 2009;18:683–92.PubMedCrossRef Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue H, Savitz SI, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 2009;18:683–92.PubMedCrossRef
128.
Zurück zum Zitat Argibay B, Trekker J, Himmelreich U, Beiras A, Topete A, Taboada P, et al. Intraarterial route increases the risk of cerebral lesions after mesenchymal cell administration in animal model of ischemia. Sci Rep. 2017;7:40758.PubMedPubMedCentralCrossRef Argibay B, Trekker J, Himmelreich U, Beiras A, Topete A, Taboada P, et al. Intraarterial route increases the risk of cerebral lesions after mesenchymal cell administration in animal model of ischemia. Sci Rep. 2017;7:40758.PubMedPubMedCentralCrossRef
129.
Zurück zum Zitat Cai W, Liu H, Zhao J, Chen LY, Chen J, Lu Z, et al. Pericytes in brain injury and repair after ischemic stroke. Transl Stroke Res. 2017;8:107–21.PubMedCrossRef Cai W, Liu H, Zhao J, Chen LY, Chen J, Lu Z, et al. Pericytes in brain injury and repair after ischemic stroke. Transl Stroke Res. 2017;8:107–21.PubMedCrossRef
130.
Zurück zum Zitat Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J. A pericyte origin of spinal cord scar tissue. Science. 2011;333:238–42.PubMedCrossRef Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J. A pericyte origin of spinal cord scar tissue. Science. 2011;333:238–42.PubMedCrossRef
131.
Zurück zum Zitat Guimaraes-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton ND, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell. 2017;20:345–59. e345PubMedCrossRef Guimaraes-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton ND, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell. 2017;20:345–59. e345PubMedCrossRef
132.
Zurück zum Zitat Birbrair A, Borges IDT, Gilson Sena IF, Almeida GG, da Silva Meirelles L, Goncalves R, et al. How plastic are pericytes? Stem Cells Dev. 2017;26:1013–9.PubMedCrossRef Birbrair A, Borges IDT, Gilson Sena IF, Almeida GG, da Silva Meirelles L, Goncalves R, et al. How plastic are pericytes? Stem Cells Dev. 2017;26:1013–9.PubMedCrossRef
133.
Zurück zum Zitat Kubota Y, Hirashima M, Kishi K, Stewart CL, Suda T. Leukemia inhibitory factor regulates microvessel density by modulating oxygen-dependent VEGF expression in mice. J Clin Invest. 2008;118:2393–403.PubMedPubMedCentral Kubota Y, Hirashima M, Kishi K, Stewart CL, Suda T. Leukemia inhibitory factor regulates microvessel density by modulating oxygen-dependent VEGF expression in mice. J Clin Invest. 2008;118:2393–403.PubMedPubMedCentral
134.
Zurück zum Zitat Luo J, Qiao F, Yin X. Hypoxia induces FGF2 production by vascular endothelial cells and alters MMP9 and TIMP1 expression in extravillous trophoblasts and their invasiveness in a cocultured model. J Reprod Dev. 2011;57:84–91.PubMedCrossRef Luo J, Qiao F, Yin X. Hypoxia induces FGF2 production by vascular endothelial cells and alters MMP9 and TIMP1 expression in extravillous trophoblasts and their invasiveness in a cocultured model. J Reprod Dev. 2011;57:84–91.PubMedCrossRef
135.
Zurück zum Zitat Baeten KM, Akassoglou K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev Neurobiol. 2011;71:1018–39.PubMedPubMedCentralCrossRef Baeten KM, Akassoglou K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev Neurobiol. 2011;71:1018–39.PubMedPubMedCentralCrossRef
137.
138.
Zurück zum Zitat Rustenhoven J, Jansson D, Smyth LC, Dragunow M. Brain pericytes as mediators of neuroinflammation. Trends Pharmacol Sci. 2017;38:291–304.PubMedCrossRef Rustenhoven J, Jansson D, Smyth LC, Dragunow M. Brain pericytes as mediators of neuroinflammation. Trends Pharmacol Sci. 2017;38:291–304.PubMedCrossRef
139.
Zurück zum Zitat Kokaia Z, Martino G, Schwartz M, Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair? Nat Neurosci. 2012;15:1078–87.PubMedCrossRef Kokaia Z, Martino G, Schwartz M, Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair? Nat Neurosci. 2012;15:1078–87.PubMedCrossRef
140.
Zurück zum Zitat Dizon ML, Maa T, Kessler JA. The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia-ischemia. Neurobiol Dis. 2011;42:318–26.PubMedPubMedCentralCrossRef Dizon ML, Maa T, Kessler JA. The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia-ischemia. Neurobiol Dis. 2011;42:318–26.PubMedPubMedCentralCrossRef
141.
Zurück zum Zitat Lei ZN, Liu F, Zhang LM, Huang YL, Sun FY. Bcl-2 increases stroke-induced striatal neurogenesis in adult brains by inhibiting BMP-4 function via activation of beta-catenin signaling. Neurochem Int. 2012;61:34–42.PubMedCrossRef Lei ZN, Liu F, Zhang LM, Huang YL, Sun FY. Bcl-2 increases stroke-induced striatal neurogenesis in adult brains by inhibiting BMP-4 function via activation of beta-catenin signaling. Neurochem Int. 2012;61:34–42.PubMedCrossRef
142.
Zurück zum Zitat Kimura H, Yoshikawa M, Matsuda R, Toriumi H, Nishimura F, Hirabayashi H, et al. Transplantation of embryonic stem cell-derived neural stem cells for spinal cord injury in adult mice. Neurol Res. 2005;27:812–9.PubMedCrossRef Kimura H, Yoshikawa M, Matsuda R, Toriumi H, Nishimura F, Hirabayashi H, et al. Transplantation of embryonic stem cell-derived neural stem cells for spinal cord injury in adult mice. Neurol Res. 2005;27:812–9.PubMedCrossRef
143.
Zurück zum Zitat Salewski RP, Mitchell RA, Li L, Shen C, Milekovskaia M, Nagy A, et al. Transplantation of induced pluripotent stem cell-derived neural stem cells mediate functional recovery following thoracic spinal cord injury through remyelination of axons. Stem Cells Transl Med. 2015;4:743–54.PubMedPubMedCentralCrossRef Salewski RP, Mitchell RA, Li L, Shen C, Milekovskaia M, Nagy A, et al. Transplantation of induced pluripotent stem cell-derived neural stem cells mediate functional recovery following thoracic spinal cord injury through remyelination of axons. Stem Cells Transl Med. 2015;4:743–54.PubMedPubMedCentralCrossRef
144.
Zurück zum Zitat Darsalia V, Kallur T, Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur J Neurosci. 2007;26:605–14.PubMedCrossRef Darsalia V, Kallur T, Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur J Neurosci. 2007;26:605–14.PubMedCrossRef
145.
Zurück zum Zitat Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A. 2004;101:11839–44.PubMedPubMedCentralCrossRef Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A. 2004;101:11839–44.PubMedPubMedCentralCrossRef
Metadaten
Titel
Novel Regenerative Therapies Based on Regionally Induced Multipotent Stem Cells in Post-Stroke Brains: Their Origin, Characterization, and Perspective
verfasst von
Toshinori Takagi
Shinichi Yoshimura
Rika Sakuma
Akiko Nakano-Doi
Tomohiro Matsuyama
Takayuki Nakagomi
Publikationsdatum
25.07.2017
Verlag
Springer US
Erschienen in
Translational Stroke Research / Ausgabe 6/2017
Print ISSN: 1868-4483
Elektronische ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-017-0556-0

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