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Cell and Tissue Banking

, Volume 13, Issue 4, pp 623–629 | Cite as

Neural stem cells in the ischemic and injured brain: endogenous and transplanted

  • Jing DongEmail author
  • Baohua Liu
  • Lei Song
  • Lei Lu
  • Haitao Xu
  • Yue Gu
Article

Abstract

Neural stem cells functions as the pool of new neurons in adult brain, and plays important roles in normal brain function. Additionally, this pool reacts to brain ischemia, hemorrhage, trauma and many kinds of diseases, serving as endogenous repair mechanisms. The present manuscript discussed the responses of adult neurogenesis to brain ischemia and other insults, then the potential of neural stem cell transplantation therapy to treat such brain injury conditions.

Keywords

Neurogenesis Ischemia Inflammation Autologous transplantation Neural stem cell 

References

  1. Amrein I, Lipp HP (2009) Adult hippocampal neurogenesis of mammals: evolution and life history. Biol Lett 5:141–144PubMedCrossRefGoogle Scholar
  2. Arias-Carrion O, Yuan TF (2009) Autologous neural stem cell transplantation: a new treatment option for Parkinson’s disease? Med Hypotheses 73:757–759PubMedCrossRefGoogle Scholar
  3. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99:11464–11469PubMedCrossRefGoogle Scholar
  4. Booth BW, Mack DL, Androutsellis-Theotokis A, McKay RD, Boulanger CA, Smith GH (2008) The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proc Natl Acad Sci USA 105:14891–14896PubMedCrossRefGoogle Scholar
  5. Burns TC, Verfaillie CM, Low WC (2009) Stem cells for ischemic brain injury: a critical review. J Comp Neurol 515:125–144PubMedCrossRefGoogle Scholar
  6. Cho KO, Kim SY (2010) Effects of brain insults and pharmacological manipulations on the adult hippocampal neurogenesis. Arch Pharm Res 33:1475–1488PubMedCrossRefGoogle Scholar
  7. Das S, Basu A (2008) Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res 86:1199–1208PubMedCrossRefGoogle Scholar
  8. Ekdahl CT, Kokaia Z, Lindvall O (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158:1021–1029PubMedCrossRefGoogle Scholar
  9. Epp JR, Barker JM, Galea LA (2009) Running wild: neurogenesis in the hippocampus across the lifespan in wild and laboratory-bred Norway rats. Hippocampus 19:1040–1049PubMedCrossRefGoogle Scholar
  10. Feng K, Xu YW, Ye FG, Xiao L, Ma XH et al (2011) Autologous peripherial blood hematopoietic stem cell transplantation in the treatment of type 1 diabetic mellitus: a report of 16 cases. Zhonghua Yi Xue Za Zhi 91:1966–1969PubMedGoogle Scholar
  11. Fike JR, Rola R, Limoli CL (2007) Radiation response of neural precursor cells. Neurosurg Clin N Am 18:115–127, xGoogle Scholar
  12. Fowler CD, Liu Y, Ouimet C, Wang Z (2002) The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115–128PubMedCrossRefGoogle Scholar
  13. Garzon-Muvdi T, Quinones-Hinojosa A (2009) Neural stem cell niches and homing: recruitment and integration into functional tissues. ILAR J 51:3–23PubMedGoogle Scholar
  14. Goncalves MB, Williams EJ, Yip P, Yanez-Munoz RJ, Williams G, Doherty P (2010) The COX-2 inhibitors, meloxicam and nimesulide, suppress neurogenesis in the adult mouse brain. Br J Pharmacol 159:1118–1125PubMedCrossRefGoogle Scholar
  15. Grigoriadis N, Lourbopoulos A, Lagoudaki R, Frischer JM, Polyzoidou E et al (2011) Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis. Exp Neurol 230:78–89PubMedCrossRefGoogle Scholar
  16. Gross CG (2009) Three before their time: neuroscientists whose ideas were ignored by their contemporaries. Exp Brain Res 192:321–334PubMedCrossRefGoogle Scholar
  17. Hess DC, Borlongan CV (2008) Stem cells and neurological diseases. Cell Prolif 41 Suppl 1:94–114Google Scholar
  18. Honmou O, Houkin K, Matsunaga T, Niitsu Y, Ishiai S et al (2011) Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain 134:1790–1807PubMedCrossRefGoogle Scholar
  19. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD (2006) Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat. J Neurosci Res 84:1495–1504PubMedCrossRefGoogle Scholar
  20. Hugnot JP, Franzen R (2011) The spinal cord ependymal region: a stem cell niche in the caudal central nervous system. Front Biosci 16:1044–1059PubMedCrossRefGoogle Scholar
  21. Jiao J, Chen DF (2008) Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells 26:1221–1230PubMedCrossRefGoogle Scholar
  22. Joels M, Karst H, Alfarez D, Heine VM, Qin Y et al (2004) Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7:221–231PubMedCrossRefGoogle Scholar
  23. Kaeser M, Brunet JF, Wyss A, Belhaj-Saif A, Liu Y, et al (2011) Autologous adult cortical cell transplantation enhances functional recovery following unilateral lesion of motor cortex in primates: a pilot study. Neurosurgery 68(5):1405–1416Google Scholar
  24. Kalluri HS, Dempsey RJ (2011) IGFBP-3 inhibits the proliferation of neural progenitor cells. Neurochem Res 36:406–411PubMedCrossRefGoogle Scholar
  25. Kang SK, Shin MJ, Jung JS, Kim YG, Kim CH (2006) Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury. Stem Cells Dev 15:583–594PubMedCrossRefGoogle Scholar
  26. Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363:101–122PubMedCrossRefGoogle Scholar
  27. Kaul M (2008) HIV’s double strike at the brain: neuronal toxicity and compromised neurogenesis. Front Biosci 13:2484–2494PubMedCrossRefGoogle Scholar
  28. Kernie SG, Parent JM (2010) Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol Dis 37:267–274PubMedCrossRefGoogle Scholar
  29. Kim SJ, Chung YG, Lee YK, Oh IW, Kim YS, Moon YS (2011) Comparison of the osteogenic potentials of autologous cultured osteoblasts and mesenchymal stem cells loaded onto allogeneic cancellous bone granules. Cell Tissue Res. [Epub ahead of print]Google Scholar
  30. Kulbatski I (2010) Stem/precursor cell-based CNS therapy: the importance of circumventing immune suppression by transplanting autologous cells. Stem Cell Rev 6:405–410PubMedCrossRefGoogle Scholar
  31. Kulcsar I, Szanto A, Varoczy L, Mehes G, Zeher M (2011) Hodgkin’s lymphoma developed after autologous stem cell transplantation for multiple myeloma: transformation or coincidental appearance? Pathol Oncol Res. [Epub ahead of print]Google Scholar
  32. Lee IS, Jung K, Kim M, Park KI (2010) Neural stem cells: properties and therapeutic potentials for hypoxic-ischemic brain injury in newborn infants. Pediatr Int 52:855–865PubMedCrossRefGoogle Scholar
  33. Leker RR, Lasri V, Chernoguz D (2009) Growth factors improve neurogenesis and outcome after focal cerebral ischemia. J Neural Transm 116:1397–1402PubMedCrossRefGoogle Scholar
  34. Li Q, Ford MC, Lavik EB, Madri JA (2006) Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between neural stem cells and endothelial cells: an in vitro study. J Neurosci Res 84:1656–1668PubMedCrossRefGoogle Scholar
  35. Li M, Nishimura H, Sekiguchi H, Kamei N, Yokoyama A et al (2009) Concurrent vasculogenesis and neurogenesis from adult neural stem cells. Circ Res 105:860–868CrossRefGoogle Scholar
  36. Liu CY, Westerlund U, Svensson M, Moe MC, Varghese M et al (2003) Artificial niches for human adult neural stem cells: possibility for autologous transplantation therapy. J Hematother Stem Cell Res 12:689–699PubMedCrossRefGoogle Scholar
  37. Liu YP, Lang BT, Baskaya MK, Dempsey RJ, Vemuganti R (2009) The potential of neural stem cells to repair stroke-induced brain damage. Acta Neuropathol 117:469–480PubMedCrossRefGoogle Scholar
  38. Locatelli F, Bersano A, Ballabio E, Lanfranconi S, Papadimitriou D et al (2009) Stem cell therapy in stroke. Cell Mol Life Sci 66:757–772PubMedCrossRefGoogle Scholar
  39. Luo CX, Jiang J, Zhou QG, Zhu XJ, Wang W et al (2007) Voluntary exercise-induced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. J Neurosci Res 85:1637–1646PubMedCrossRefGoogle Scholar
  40. Mackowiak M, Chocyk A, Markowicz-Kula K, Wedzony K (2004) Neurogenesis in the adult brain. Pol J Pharmacol 56:673–687PubMedGoogle Scholar
  41. Madri JA (2009) Modeling the neurovascular niche: implications for recovery from CNS injury. J Physiol Pharmacol 60 Suppl 4:95–104Google Scholar
  42. Miljan EA, Sinden JD (2009) Stem cell treatment of ischemic brain injury. Curr Opin Mol Ther 11:394–403PubMedGoogle Scholar
  43. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3:265–278PubMedCrossRefGoogle Scholar
  44. Murrell W, Wetzig A, Donnellan M, Feron F, Burne T et al (2008) Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson’s disease. Stem Cells 26:2183–2192PubMedCrossRefGoogle Scholar
  45. Namiecinska M, Marciniak K, Nowak JZ (2005) VEGF as an angiogenic, neurotrophic, and neuroprotective factor. Postepy Hig Med Dosw (Online) 59:573–583Google Scholar
  46. Naylor AS, Bull C, Nilsson MK, Zhu C, Bjork-Eriksson T et al (2008) Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proc Natl Acad Sci USA 105:14632–14637PubMedCrossRefGoogle Scholar
  47. Ohab JJ, Carmichael ST (2008) Poststroke neurogenesis: emerging principles of migration and localization of immature neurons. Neuroscientist 14:369–380PubMedCrossRefGoogle Scholar
  48. Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26:13007–13016PubMedCrossRefGoogle Scholar
  49. Ohira K (2011) Injury-induced neurogenesis in the mammalian forebrain. Cell Mol Life Sci 68:1645–1656PubMedCrossRefGoogle Scholar
  50. Ooboshi H (2011) Gene therapy as a novel pharmaceutical intervention for stroke. Curr Pharm Des 17:424–433PubMedCrossRefGoogle Scholar
  51. Osredkar D, Sall JW, Bickler PE, Ferriero DM (2010) Erythropoietin promotes hippocampal neurogenesis in in vitro models of neonatal stroke. Neurobiol Dis 38:259–265PubMedCrossRefGoogle Scholar
  52. Pai M, Spalding D, Xi F, Habib N (2012) Autologous bone marrow stem cells in the treatment of chronic liver disease. Int J Hepatol 2012:307165PubMedGoogle Scholar
  53. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494PubMedCrossRefGoogle Scholar
  54. Parent JM (2007) Adult neurogenesis in the intact and epileptic dentate gyrus. Prog Brain Res 163:529–540PubMedCrossRefGoogle Scholar
  55. Park BW, Kang DH, Kang EJ, Byun JH, Lee JS, et al (2011) Peripheral nerve regeneration using autologous porcine skin-derived mesenchymal stem cells. J Tissue Eng Regen Med. doi: 10.1002/term.404
  56. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706–6717PubMedGoogle Scholar
  57. Pfeifer K, Vroemen M, Caioni M, Aigner L, Bogdahn U, Weidner N (2006) Autologous adult rodent neural progenitor cell transplantation represents a feasible strategy to promote structural repair in the chronically injured spinal cord. Regen Med 1:255–266PubMedCrossRefGoogle Scholar
  58. Pumiglia K, Temple S (2006) PEDF: bridging neurovascular interactions in the stem cell niche. Nat Neurosci 9:299–300PubMedCrossRefGoogle Scholar
  59. Qureshi IA, Mehler MF (2011) The emerging role of epigenetics in stroke: III. Neural stem cell biology and regenerative medicine. Arch Neurol 68:294–302PubMedCrossRefGoogle Scholar
  60. Robel S, Berninger B, Gotz M (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12:88–104PubMedCrossRefGoogle Scholar
  61. Rodriguez JJ, Noristani HN, Olabarria M, Fletcher J, Somerville TD, et al (2011) Voluntary running and environmental enrichment restores impaired hippocampal neurogenesis in a triple transgenic mouse model of Alzheimer’s disease. Curr Alzheimer Res. [Epub ahead of print]Google Scholar
  62. Saino O, Taguchi A, Nakagomi T, Nakano-Doi A, Kashiwamura S et al (2010) Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res 88:2385–2397PubMedGoogle Scholar
  63. Sasaki T, Kitagawa K, Sugiura S, Omura-Matsuoka E, Tanaka S et al (2003) Implication of cyclooxygenase-2 on enhanced proliferation of neural progenitor cells in the adult mouse hippocampus after ischemia. J Neurosci Res 72:461–471PubMedCrossRefGoogle Scholar
  64. Schmidt NO, Koeder D, Messing M, Mueller FJ, Aboody KS et al (2009) Vascular endothelial growth factor-stimulated cerebral microvascular endothelial cells mediate the recruitment of neural stem cells to the neurovascular niche. Brain Res 1268:24–37PubMedCrossRefGoogle Scholar
  65. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM et al (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell–cell interactions. Cell Stem Cell 3:289–300PubMedCrossRefGoogle Scholar
  66. Shingo T, Yasuhara T, Muraoka K, Kameda M, Date I (2007) Autologous transplantation of adult derived neural stem cells. No Shinkei Geka 35:823–829PubMedGoogle Scholar
  67. Shioda N, Han F, Fukunaga K (2009) Role of Akt and ERK signaling in the neurogenesis following brain ischemia. Int Rev Neurobiol 85:375–387PubMedCrossRefGoogle Scholar
  68. Slevin M, Krupinski J (2009) Cyclin-dependent kinase-5 targeting for ischaemic stroke. Curr Opin Pharmacol 9:119–124PubMedCrossRefGoogle Scholar
  69. Taupin P (2006) Autologous transplantation in the central nervous system. Indian J Med Res 124:613–618PubMedGoogle Scholar
  70. Teng FY, Hor CH, Tang BL (2009) Emerging cues mediating astroglia lineage restriction of progenitor cells in the injured/diseased adult CNS. Differentiation 77:121–127PubMedCrossRefGoogle Scholar
  71. Tonchev AB, Yamashima T, Guo J, Chaldakov GN, Takakura N (2007) Expression of angiogenic and neurotrophic factors in the progenitor cell niche of adult monkey subventricular zone. Neuroscience 144:1425–1435PubMedCrossRefGoogle Scholar
  72. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427–13431PubMedCrossRefGoogle Scholar
  73. van Praag H, Kempermann G, Gage FH (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270PubMedCrossRefGoogle Scholar
  74. Wang C, Zhang M, Sun C, Cai Y, You Y et al (2011) Sustained increase in adult neurogenesis in the rat hippocampal dentate gyrus after transient brain ischemia. Neurosci Lett 488:70–75PubMedCrossRefGoogle Scholar
  75. Whitman MC, Greer CA (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89:162–175PubMedCrossRefGoogle Scholar
  76. Xiong Y, Mahmood A, Chopp M (2010) Angiogenesis, neurogenesis and brain recovery of function following injury. Curr Opin Investig Drugs 11:298–308PubMedGoogle Scholar
  77. Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y et al (2005) Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192:251–264PubMedCrossRefGoogle Scholar
  78. Yagita Y, Kitagawa K, Sasaki T, Terasaki Y, Todo K et al (2006) Postischemic exercise decreases neurogenesis in the adult rat dentate gyrus. Neurosci Lett 409:24–29PubMedCrossRefGoogle Scholar
  79. Yamashima T, Tonchev AB, Yukie M (2007) Adult hippocampal neurogenesis in rodents and primates: endogenous, enhanced, and engrafted. Rev Neurosci 18:67–82PubMedGoogle Scholar
  80. Yang XT, Bi YY, Feng DF (2011) From the vascular microenvironment to neurogenesis. Brain Res Bull 84:1–7PubMedCrossRefGoogle Scholar
  81. Yuan TF (2010) Smell with new neurons. Cell Tissue Res 340:211–214PubMedCrossRefGoogle Scholar
  82. Yuan TF, Arias-Carrion O (2011) Adult neurogenesis in the hypothalamus: evidence, functions, and implications. CNS Neurol Disord Drug Targets 10:433–439PubMedCrossRefGoogle Scholar
  83. Zhang Y, Klassen HJ, Tucker BA, Perez MT, Young MJ (2007) CNS progenitor cells promote a permissive environment for neurite outgrowth via a matrix metalloproteinase-2-dependent mechanism. J Neurosci 27:4499–4506PubMedCrossRefGoogle Scholar
  84. Zhang RL, Chopp M, Roberts C, Jia L, Wei M et al (2011) Ascl1 lineage cells contribute to ischemia-induced neurogenesis and oligodendrogenesis. J Cereb Blood Flow Metab 31:614–625PubMedCrossRefGoogle Scholar
  85. Zheng GQ, Cheng W, Wang Y, Wang XM, Zhao SZ et al (2011) Ginseng total saponins enhance neurogenesis after focal cerebral ischemia. J Ethnopharmacol 133:724–728PubMedCrossRefGoogle Scholar
  86. Zhou J, Cheng G, Kong R, Gao DK, Zhang X (2011) The selective ablation of inflammation in an acute stage of ischemic stroke may be a new strategy to promote neurogenesis. Med Hypotheses 76:1–3PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jing Dong
    • 1
    Email author
  • Baohua Liu
    • 2
  • Lei Song
    • 2
  • Lei Lu
    • 2
  • Haitao Xu
    • 3
  • Yue Gu
    • 4
  1. 1.Neurology Department, General HospitalJiHa Group Company, JilinJilinChina
  2. 2.Neurology Department, First HospitalJilin UniversityChangchunChina
  3. 3.Ophthalmology Department, Second HospitalJilin UniversityChangchunChina
  4. 4.Respiratory Department, First HospitalJilin UniversityChangchunChina

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