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Translational Stroke Research

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29.06.2016 | Original Article

Induction of Perivascular Neural Stem Cells and Possible Contribution to Neurogenesis Following Transient Brain Ischemia/Reperfusion Injury

verfasst von: Masayo Nakata, Takayuki Nakagomi, Mitsuyo Maeda, Akiko Nakano-Doi, Yoshihiro Momota, Tomohiro Matsuyama

Erschienen in: Translational Stroke Research | Ausgabe 2/2017

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Abstract

Recent therapeutic advances have increased the likelihood of recanalizing the obstructed brain arteries in patients with stroke. Therefore, it is important to understand the fate of neural cells under transient ischemia/reperfusion injury. Accumulating evidence shows that neurogenesis occurs in perivascular regions following brain injury, although the precise mechanism and origin of these newborn neurons under transient ischemia/reperfusion injury remain unclear. Using a mouse model of transient brain ischemia/reperfusion injury, we found that neural stem cells (NSCs) develop within injured areas. This induction of NSCs following ischemia/reperfusion injury was observed even in response to nonlethal ischemia, although massive numbers of NSCs were induced by lethal ischemia. Immunohistochemical and immunoelectron microscopic studies indicated that platelet-derived growth factor receptor beta-positive (PDGFRβ⁺) pericytes within injured areas following nonlethal ischemia began to express the NSC marker nestin as early as 3 days after transient ischemia/reperfusion. Some PDGFRβ⁺ pericytes expressed the immature neuronal marker doublecortin at day 7. These findings indicate that brain pericytes are a potential source of the perivascular NSCs that generate neuronal cells under lethal and nonlethal ischemic conditions following transient ischemia/reperfusion. Thus, brain pericytes might be a target for neurogenesis mediation in patients with nonlethal and lethal ischemia following transient ischemia/reperfusion injury.

Mokin M, Kass-Hout T, Kass-Hout O, Dumont TM, Kan P, Snyder KV, et al. Intravenous thrombolysis and endovascular therapy for acute ischemic stroke with internal carotid artery occlusion: a systematic review of clinical outcomes. Stroke. 2012;43(9):2362–8.CrossRefPubMed

Zaidat OO, Suarez JI, Sunshine JL, Tarr RW, Alexander MJ, Smith TP, et al. Thrombolytic therapy of acute ischemic stroke: correlation of angiographic recanalization with clinical outcome. AJNR Am J Neuroradiol. 2005;26(4):880–4.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(7):1292–302.PubMed

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(9):2185–95.CrossRefPubMed

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(1):90–8.CrossRefPubMed

Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci. 2002;22(3):629–34.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(6):2027–33.PubMed

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(9):1842–52.CrossRefPubMed

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(13):2350–4.CrossRefPubMedPubMedCentral

10.

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(12):2037–51.CrossRefPubMed

11.

Nakagomi T, Nakano-Doi A, Matsuyama T. Leptomeninges: a novel stem cell niche harboring ischemia-induced neural progenitors. Histol Histopathol. 2015;30:391–9.PubMed

12.

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(6):1962–74.CrossRefPubMed

13.

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(2):173–9.CrossRefPubMed

14.

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(3):330–8.CrossRefPubMedPubMedCentral

15.

Taguchi A, Wen Z, Myojin K, Yoshihara T, Nakagomi T, Nakayama D, et al. Granulocyte colony-stimulating factor has a negative effect on stroke outcome in a murine model. Eur J Neurosci. 2007;26(1):126–33.CrossRefPubMed

16.

Tamura A, Gotoh O, Sano K. Focal cerebral infarction in the rat: I. Operative technique and physiological monitorings for chronic model. No To Shinkei. 1986;38(8):747–51.PubMed

17.

Kasahara Y, Ihara M, Nakagomi T, Momota Y, Stern DM, Matsuyama T, et al. A highly reproducible model of cerebral ischemia/reperfusion with extended survival in CB-17 mice. Neurosci Res. 2013;76(3):163–8.CrossRefPubMed

18.

Kasahara Y, Nakagomi T, Matsuyama T, Stern D, Taguchi A. Cilostazol reduces the risk of hemorrhagic infarction after administration of tissue-type plasminogen activator in a murine stroke model. Stroke. 2012;43(2):499–506.CrossRefPubMed

19.

Taguchi A, Kasahara Y, Nakagomi T, Stern DM, Fukunaga M, Ishikawa M, et al. A reproducible and simple model of permanent cerebral ischemia in CB-17 and SCID Mice. J Exp Stroke Transl Med. 2010;3(1):28–33.CrossRefPubMedPubMedCentral

20.

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(11):2385–97.PubMed

21.

Zille M, Farr TD, Przesdzing I, Muller J, Sommer C, Dirnagl U, et al. Visualizing cell death in experimental focal cerebral ischemia: promises, problems, and perspectives. J Cereb Blood Flow Metab. 2012;32(2):213–31.CrossRefPubMed

22.

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(9):e552–60.CrossRefPubMedPubMedCentral

23.

Zaidat OO, Suarez JI, Santillan C, Sunshine JL, Tarr RW, Paras VH, et al. Response to intra-arterial and combined intravenous and intra-arterial thrombolytic therapy in patients with distal internal carotid artery occlusion. Stroke. 2002;33(7):1821–6.CrossRefPubMed

24.

Dore-Duffy P, Owen C, Balabanov R, Murphy S, Beaumont T, Rafols JA. Pericyte migration from the vascular wall in response to traumatic brain injury. Microvasc Res. 2000;60(1):55–69.CrossRefPubMed

25.

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 Invest. 2014;94(12):1340–54.CrossRefPubMed

26.

Tsang WP, Shu Y, Kwok PL, Zhang F, Lee KK, Tang MK, et al. CD146+ human umbilical cord perivascular cells maintain stemness under hypoxia and as a cell source for skeletal regeneration. PLoS One. 2013;8(10):e76153.CrossRefPubMedPubMedCentral

27.

Chen CW, Okada M, Proto JD, Gao X, Sekiya N, Beckman SA, et al. Human pericytes for ischemic heart repair. Stem Cells. 2013;31(2):305–16.CrossRefPubMedPubMedCentral

28.

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(5):613–24.CrossRefPubMed

29.

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(1):67–84.CrossRefPubMedPubMedCentral

30.

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(1):87–99.CrossRefPubMed

31.

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(1):57.CrossRefPubMedPubMedCentral

32.

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(4):471–6.CrossRefPubMed

33.

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(15):1730–9.CrossRefPubMed

34.

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.CrossRefPubMedPubMedCentral

35.

Jiao J, Chen DF. Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells. 2008;26(5):1221–30.CrossRefPubMedPubMedCentral

36.

Banerjee S, Bhat MA. Neuron-glial interactions in blood–brain barrier formation. Annu Rev Neurosci. 2007;30:235–58.CrossRefPubMedPubMedCentral

Titel: Induction of Perivascular Neural Stem Cells and Possible Contribution to Neurogenesis Following Transient Brain Ischemia/Reperfusion Injury
verfasst von: Masayo Nakata
Takayuki Nakagomi
Mitsuyo Maeda
Akiko Nakano-Doi
Yoshihiro Momota
Tomohiro Matsuyama
Publikationsdatum: 29.06.2016
Verlag: Springer US
Erschienen in: Translational Stroke Research / Ausgabe 2/2017
Print ISSN: 1868-4483
Elektronische ISSN: 1868-601X
DOI: https://doi.org/10.1007/s12975-016-0479-1

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Induction of Perivascular Neural Stem Cells and Possible Contribution to Neurogenesis Following Transient Brain Ischemia/Reperfusion Injury

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