nach oben

25.07.2017 | Review | Ausgabe 6/2017

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

Zeitschrift:: Translational Stroke Research > Ausgabe 6/2017

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

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.

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Jetzt einloggen Kostenlos registrieren

★ PREMIUM-INHALT

e.Med Interdisziplinär

Mit e.Med Interdisziplinär erhalten Sie Zugang zu allen CME-Fortbildungen und Fachzeitschriften auf SpringerMedizin.de. Zusätzlich können Sie eine Zeitschrift Ihrer Wahl in gedruckter Form beziehen – ohne Aufpreis.

Jetzt gratis testen * Jetzt kaufen

Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.

e.Med Innere Medizin

Kombi-Abonnement

Mit e.Med Innere Medizin erhalten Sie Zugang zu CME-Fortbildungen des Fachgebietes Innere Medizin, den Premium-Inhalten der internistischen Fachzeitschriften, inklusive einer gedruckten internistischen Zeitschrift Ihrer Wahl.

Jetzt testen ¹

e.Med Allgemeinmedizin

Kombi-Abonnement

Mit e.Med Allgemeinmedizin erhalten Sie Zugang zu allen CME-Fortbildungen und Premium-Inhalten der allgemeinmedizinischen Zeitschriften, inklusive einer gedruckten Allgemeinmedizin-Zeitschrift Ihrer Wahl.

Jetzt testen ²

e.Med AINS

Kombi-Abonnement

Mit e.Med AINS erhalten Sie Zugang zu CME-Fortbildungen des Fachgebietes AINS, den Premium-Inhalten der AINS-Fachzeitschriften, inklusive einer gedruckten AINS-Zeitschrift Ihrer Wahl.

Jetzt testen ³

e.Med Neurologie & Psychiatrie

Kombi-Abonnement

Mit e.Med Neurologie & Psychiatrie erhalten Sie Zugang zu CME-Fortbildungen der Fachgebiete, den Premium-Inhalten der dazugehörigen Fachzeitschriften, inklusive einer gedruckten Zeitschrift Ihrer Wahl.

Jetzt testen ⁴

e.Med Neurologie

Kombi-Abonnement

Mit e.Med Neurologie erhalten Sie Zugang zu CME-Fortbildungen des Fachgebietes, den Premium-Inhalten der neurologischen Fachzeitschriften, inklusive einer gedruckten Neurologie-Zeitschrift Ihrer Wahl.

Jetzt testen ⁵

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

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

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

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

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

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

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

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

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.

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.

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.

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.

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.

Hutchings M, Weller RO. Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg. 1986;65:316–25. PubMedCrossRef

15.

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

16.

Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009;32:149–84. PubMedPubMedCentralCrossRef

17.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Kondo T, Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 2000;289:1754–7. PubMedCrossRef

34.

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.

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.

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.

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.

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.

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.

Stallcup WB, Beasley L. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci. 1987;7:2737–44. PubMed

41.

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.

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.

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.

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.

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

46.

Nishiyama A, Suzuki R, Zhu X. NG2 cells (polydendrocytes) in brain physiology and repair. Front Neurosci. 2014;8:133. PubMedPubMedCentralCrossRef

47.

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.

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.

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.

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.

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.

Richardson WD, Young KM, Tripathi RB, McKenzie I. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron. 2011;70:661–73. PubMedPubMedCentralCrossRef

53.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Chang Y, Li H, Guo Z. Mesenchymal stem cell-like properties in fibroblasts. Cell Physiol Biochem. 2014;34:703–14. PubMedCrossRef

70.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Vojnits K, Pan H, Mu X, Li Y. Characterization of an injury induced population of muscle-derived stem cell-like cells. Sci Rep. 2015;5:17355. PubMedPubMedCentralCrossRef

82.

Klein D, Hohn HP, Kleff V, Tilki D, Ergun S. Vascular wall-resident stem cells. Histol Histopathol. 2010;25:681–9. PubMed

83.

Bautch VL. Stem cells and the vasculature. Nat Med. 2011;17:1437–43. PubMedCrossRef

84.

Lin CS, Lue TF. Defining vascular stem cells. Stem Cells Dev. 2013;22:1018–26. PubMedPubMedCentralCrossRef

85.

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.

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.

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.

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.

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.

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.

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

92.

Caplan AI. All MSCs are pericytes? Cell Stem Cell. 2008;3:229–30. PubMedCrossRef

93.

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.

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.

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.

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.

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.

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.

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.

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.

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

102.

Simoes-Costa M, Bronner ME. Establishing neural crest identity: a gene regulatory recipe. Development. 2015;142:242–57. PubMedPubMedCentralCrossRef

103.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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. e345 PubMedCrossRef

132.

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.

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.

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.

Baeten KM, Akassoglou K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev Neurobiol. 2011;71:1018–39. PubMedPubMedCentralCrossRef

136.

Kazanis I, ffrench-Constant C. Extracellular matrix and the neural stem cell niche. Dev Neurobiol. 2011;71:1006–17. PubMedPubMedCentralCrossRef

137.

Hurtado-Alvarado G, Cabanas-Morales AM, Gomez-Gonzalez B. Pericytes: brain-immune interface modulators. Front Integr Neurosci. 2014;7:80. PubMedPubMedCentralCrossRef

138.

Rustenhoven J, Jansson D, Smyth LC, Dragunow M. Brain pericytes as mediators of neuroinflammation. Trends Pharmacol Sci. 2017;38:291–304. PubMedCrossRef

139.

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.

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.

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.

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.

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.

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.

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

Titel: Novel Regenerative Therapies Based on Regionally Induced Multipotent Stem Cells in Post-Stroke Brains: Their Origin, Characterization, and Perspective
Autoren:: Toshinori Takagi
Shinichi Yoshimura
Rika Sakuma
Akiko Nakano-Doi
Tomohiro Matsuyama
Takayuki Nakagomi
Publikationsdatum: 25.07.2017
DOI: https://doi.org/10.1007/s12975-017-0556-0
Verlag: Springer US
Zeitschrift: Translational Stroke Research
Ausgabe 6/2017
Print ISSN: 1868-4483
Elektronische ISSN: 1868-601X

Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.
Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.
Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.
Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.
Das kostenlose Testabonnement läuft nach 14 Tagen automatisch und formlos aus. Dieses Abonnement kann nur einmal getestet werden.

Neu in den Fachgebieten Neurologie und Psychiatrie

19.11.2018 | Hirntraumen | Nachrichten

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

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

e.Med Innere Medizin

e.Med Allgemeinmedizin

e.Med AINS

e.Med Neurologie & Psychiatrie

e.Med Neurologie

Suizidrisiko ist selbst nach leichten Hirntraumen erhöht

Antidepressiva belasten städtische Gewässer

Neurofilament eignet sich als früher Demenzmarker

Sind CGRP-Antikörper das Allheilmittel für Migräne?

Neurologie

Komplikationen in der Neurologie

Facharztwissen Psychiatrie, Psychosomatik und Psychotherapie

Kompendium der Psychotherapie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

e.Med Innere Medizin

e.Med Allgemeinmedizin

e.Med AINS

e.Med Neurologie & Psychiatrie

e.Med Neurologie

Weitere Artikel der Ausgabe 6/2017

Rehabilitation and the Neural Network After Stroke

Infections Up to 76 Days After Stroke Increase Disability and Death

Preclinical and Clinical Evidence on Ipsilateral Corticospinal Projections: Implication for Motor Recovery

Early Increased Bradykinin 1 Receptor Contributes to Hemorrhagic Transformation After Ischemic Stroke in Type 1 Diabetic Rats

MicroRNA Changes in Preconditioning-Induced Neuroprotection

A Combination of Three Repurposed Drugs Administered at Reperfusion as a Promising Therapy for Postischemic Brain Injury

Neu in den Fachgebieten Neurologie und Psychiatrie

Suizidrisiko ist selbst nach leichten Hirntraumen erhöht

Antidepressiva belasten städtische Gewässer

Neurofilament eignet sich als früher Demenzmarker

Sind CGRP-Antikörper das Allheilmittel für Migräne?

Meistgelesene Bücher in der Neurologie & Psychiatrie

Neurologie

Komplikationen in der Neurologie

Facharztwissen Psychiatrie, Psychosomatik und Psychotherapie

Kompendium der Psychotherapie