Journal of Molecular Neuroscience

, Volume 56, Issue 4, pp 887–897 | Cite as

The Neural Stem Cell Microenvironment: Focusing on Axon Guidance Molecules and Myelin-Associated Factors

Article

Abstract

Neural stem cells (NSCs) could produce various cell phenotypes in the subventricular zone (SVZ) and dentate gyrus of the hippocampus in the central nervous system (CNS), where neurogenesis has been determined to occur. The extracellular microenvironment also influences the behaviors of NSCs during development and at CNS injury sites. Our previous study indicates that myelin, a component of the CNS, could regulate the differentiation of NSCs in vitro. Recent reports have implicated three myelin-derived inhibitors, NogoA, myelin-associated glycoprotein (MAG), and oligodendrocyte-myelin glycoprotein (OMgp), as well as several axon guidance molecules as regulators of NSC survival, proliferation, migration, and differentiation. However, the molecular mechanisms underlying the behavior of NSCs are not fully understood. In this study, we summarize the current literature on the effects of different extrinsic factors on NSCs and discuss possible mechanisms, as well as future possible clinical applications.

Keywords

Neural stem cell (NSCs) Myelin Axon guidance molecules Differentiation 

References

  1. Ader M, Schachner M, Bartsch U (2001) Transplantation of neural precursor cells into the dysmyelinated CNS of mutant mice deficient in the myelin‐associated glycoprotein and Fyn tyrosine kinase. Eur J Neurosci 14:561–566PubMedGoogle Scholar
  2. Afshari FT, Kappagantula S, Fawcett JW (2009) Extrinsic and intrinsic factors controlling axonal regeneration after spinal cord injury. Expert Rev Mol Med 11:e37PubMedGoogle Scholar
  3. Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686PubMedGoogle Scholar
  4. Andrews W, Barber M, Hernadez-Miranda LR, Xian J, Rakic S, Sundaresan V, Rabbitts TH, Pannell R, Rabbitts P, Thompson H, Erskine L, Murakami F, Parnavelas JG (2008) The role of Slit-Robo signaling in the generation, migration and morphological differentiation of cortical interneurons. Dev Biol 313:648–658PubMedGoogle Scholar
  5. Aoki M, Yamashita T, Tohyama M (2004) EphA receptors direct the differentiation of mammalian neural precursor cells through a mitogen-activated protein kinase-dependent pathway. J Biol Chem 279:32643–32650PubMedGoogle Scholar
  6. Atwal JK, Pinkston-Gosse J, Syken J, Stawicki S, Wu Y, Shatz C, Tessier-Lavigne M (2008) PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322:967–970PubMedGoogle Scholar
  7. Bagnard D, Sainturet N, Meyronet D, Perraut M, Miehe M, Roussel G, Aunis D, Belin MF, Thomasset N (2004) Differential MAP kinases activation during semaphorin3A-induced repulsion or apoptosis of neural progenitor cells. Mol Cell Neurosci 25:722–731PubMedGoogle Scholar
  8. Bloch-Gallego E, Ezan F, Tessier-Lavigne M, Sotelo C (1999) Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J Neurosci 19:4407–4420PubMedGoogle Scholar
  9. Borrell V, Cardenas A, Ciceri G, Galceran J, Flames N, Pla R, Nobrega-Pereira S, Garcia-Frigola C, Peregrin S, Zhao Z, Ma L, Tessier-Lavigne M, Marin O (2012) Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76:338–352PubMedCentralPubMedGoogle Scholar
  10. Busch SA, Silver J (2007) The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17:120–127PubMedGoogle Scholar
  11. Chakravarthy B, Gaudet C, Menard M, Atkinson T, Brown L, Laferla FM, Armato U, Whitfield J (2010) Amyloid-beta peptides stimulate the expression of the p75(NTR) neurotrophin receptor in SHSY5Y human neuroblastoma cells and AD transgenic mice. J Alzheimers Dis 19:915–925PubMedGoogle Scholar
  12. Chilton JK (2006) Molecular mechanisms of axon guidance. Dev Biol 292:13–24PubMedGoogle Scholar
  13. Choi HW, Kim JS, Choi S, Hong YJ, Kim MJ, Seo HG, Do JT (2014) Neural stem cells differentiated from iPS cells spontaneously regain pluripotency. Stem Cells 32:2596–2604PubMedGoogle Scholar
  14. Christian KM, Song H, Ming G-l (2013) Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci 37:243–262Google Scholar
  15. Chumley MJ, Catchpole T, Silvany RE, Kernie SG, Henkemeyer M (2007) EphB receptors regulate stem/progenitor cell proliferation, migration, and polarity during hippocampal neurogenesis. J Neurosci 27:13481–13490PubMedGoogle Scholar
  16. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3:1091–1097PubMedGoogle Scholar
  17. Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW (2007) How does chondroitinase promote functional recovery in the damaged CNS? Exp Neurol 206:159–171PubMedGoogle Scholar
  18. Daadi MM, Davis AS, Arac A, Li Z, Maag A-L, Bhatnagar R, Jiang K, Sun G, Wu JC, Steinberg GK (2010) Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic–ischemic brain injury. Stroke 41:516–523PubMedGoogle Scholar
  19. De Wit J, De Winter F, Klooster J, Verhaagen J (2005) Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol Cell Neurosci 29:40–55PubMedGoogle Scholar
  20. DeBellard ME, Tang S, Mukhopadhyay G, Shen YJ, Filbin MT (1996) Myelin-associated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein. Mol Cell Neurosci 7:89–101PubMedGoogle Scholar
  21. del Valle K, Theus MH, Bethea JR, Liebl DJ, Ricard J (2011) Neural progenitors proliferation is inhibited by EphB3 in the developing subventricular zone. Int J Dev Neurosci 29:9–14PubMedCentralPubMedGoogle Scholar
  22. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, Ledent C, Vanderhaeghen P (2005) Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435:1244–1250PubMedGoogle Scholar
  23. Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz LI, Geller HM, Giger RJ (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15:703–712PubMedCentralPubMedGoogle Scholar
  24. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang KC, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin MT (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35:283–290PubMedGoogle Scholar
  25. Faigle R, Song H (2013) Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta (BBA)-Gen Sub 1830:2435–2448Google Scholar
  26. Fujita Y, Yamashita T (2014) Axon growth inhibition by RhoA/ROCK in the central nervous system. Front Neurosci 8.Google Scholar
  27. Genander M, Halford MM, Xu NJ, Eriksson M, Yu Z, Qiu Z, Martling A, Greicius G, Thakar S, Catchpole T, Chumley MJ, Zdunek S, Wang C, Holm T, Goff SP, Pettersson S, Pestell RG, Henkemeyer M, Frisen J (2009) Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell 139:679–692PubMedCentralPubMedGoogle Scholar
  28. Gervasi NM, Kwok JC, Fawcett JW (2008) Role of extracellular factors in axon regeneration in the CNS: implications for therapy. Regen Med 3:907–923PubMedGoogle Scholar
  29. Goh ELK, Ma D, Ming G-L, Song H (2003) Adult neural stem cells and repair of the adult central nervous system. J Hematother Stem Cell Res 12:671–679PubMedGoogle Scholar
  30. Goldshmit Y, McLenachan S, Turnley A (2006) Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res Rev 52:327–345PubMedGoogle Scholar
  31. Gu WL, Fu SL, Wang YX, Li Y, Lu HZ, Xu XM, Lu PH (2009) Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway. BMC Neurosci 10:128PubMedCentralPubMedGoogle Scholar
  32. Hakanen J, Duprat S, Salminen M (2011) Netrin1 is required for neural and glial precursor migrations into the olfactory bulb. Dev Biol 355:101–114PubMedGoogle Scholar
  33. Hara Y, Nomura T, Yoshizaki K, Frisen J, Osumi N (2010) Impaired hippocampal neurogenesis and vascular formation in ephrin-A5-deficient mice. Stem Cells 28:974–983PubMedGoogle Scholar
  34. Harburg GC, Hinck L (2011) Navigating breast cancer: axon guidance molecules as breast cancer tumor suppressors and oncogenes. J Mammary Gland Biol Neoplasia 16:257–270PubMedCentralPubMedGoogle Scholar
  35. Hayano Y, Sasaki K, Ohmura N, Takemoto M, Maeda Y, Yamashita T, Hata Y, Kitada K, Yamamoto N (2014) Netrin-4 regulates thalamocortical axon branching in an activity-dependent fashion. Proc Natl Acad Sci U S A 111:15226–15231PubMedCentralPubMedGoogle Scholar
  36. He N, Jin WL, Lok KH, Wang Y, Yin M, Wang ZJ (2013) Amyloid-beta(1–42) oligomer accelerates senescence in adult hippocampal neural stem/progenitor cells via formylpeptide receptor 2. Cell Death Dis 4:e924PubMedCentralPubMedGoogle Scholar
  37. Hedgecock EM, Norris CR (1997) Netrins evoke mixed reactions in motile cells. Trends Genet 13:251–253PubMedGoogle Scholar
  38. Hermann DM, Peruzzotti-Jametti L, Schlechter J, Bernstock JD, Doeppner TR, Pluchino S (2014) Neural precursor cells in the ischemic brain - integration, cellular crosstalk, and consequences for stroke recovery. Front Cell Neurosci 8:291PubMedCentralPubMedGoogle Scholar
  39. Holmberg J, Armulik A, Senti KA, Edoff K, Spalding K, Momma S, Cassidy R, Flanagan JG, Frisen J (2005) Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev 19:462–471PubMedCentralPubMedGoogle Scholar
  40. Hou T, Shi Y, Cheng S, Yang X, Li L, Xiao C (2010) Nogo-A expresses on neural stem cell surface. Int J Neurosci 120:201–205PubMedGoogle Scholar
  41. Huang JY, Wang YX, Gu WL, Fu SL, Li Y, Huang LD, Zhao Z, Hang Q, Zhu HQ, Lu PH (2012) Expression and function of myelin-associated proteins and their common receptor NgR on oligodendrocyte progenitor cells. Brain Res 1437:1–15PubMedGoogle Scholar
  42. Itoh T, Satou T, Hashimoto S, Ito H (2005) Isolation of neural stem cells from damaged rat cerebral cortex after traumatic brain injury. NeuroReport 16:1687–1691PubMedGoogle Scholar
  43. Jensen PL (2000) Eph receptors and ephrins. Stem Cells 18:63–64PubMedGoogle Scholar
  44. Jing X, Miwa H, Sawada T, Nakanishi I, Kondo T, Miyajima M, Sakaguchi K (2012) Ephrin-A1-mediated dopaminergic neurogenesis and angiogenesis in a rat model of Parkinson’s disease. PLoS One 7:e32019PubMedCentralPubMedGoogle Scholar
  45. Julian L, Olson MF (2014) Rho-associated coiled-coil containing kinases (ROCK): structure, regulation, and functions. Small GTPases 5:e29846PubMedCentralPubMedGoogle Scholar
  46. Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, Hansen MJ, Flanagan JG, Yamaguchi Y, Sretavan DW, Giger RJ, Kolodkin AL (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44:961–975PubMedGoogle Scholar
  47. Katakowski M, Zhang Z, deCarvalho AC, Chopp M (2005) EphB2 induces proliferation and promotes a neuronal fate in adult subventricular neural precursor cells. Neurosci Lett 385:204–209PubMedGoogle Scholar
  48. Kazanis I, ffrench-Constant, C (2011) Extracellular matrix and the neural stem cell niche. Dev Neurobiol 71:1006–1017PubMedGoogle Scholar
  49. Kearns SM, Laywell ED, Kukekov VK, Steindler DA (2003) Extracellular matrix effects on neurosphere cell motility. Exp Neurol 182:240–244PubMedGoogle Scholar
  50. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier-Lavigne M (1996) Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87:175–185PubMedGoogle Scholar
  51. Ketschek AR, Haas C, Gallo G, Fischer I (2012) The roles of neuronal and glial precursors in overcoming chondroitin sulfate proteoglycan inhibition. Exp Neurol 235:627–637PubMedCentralPubMedGoogle Scholar
  52. Khodosevich K, Watanabe Y, Monyer H (2011) EphA4 preserves postnatal and adult neural stem cells in an undifferentiated state in vivo. J Cell Sci 124:1268–1279PubMedGoogle Scholar
  53. Klagsbrun M, Eichmann A (2005) A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 16:535–548PubMedGoogle Scholar
  54. Koeberle PD, Bahr M (2004) Growth and guidance cues for regenerating axons: where have they gone? J Neurobiol 59:162–180PubMedGoogle Scholar
  55. Kottis V, Thibault P, Mikol D, Xiao ZC, Zhang R, Dergham P, Braun PE (2002) Oligodendrocyte‐myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J Neurochem 82:1566–1569PubMedGoogle Scholar
  56. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033PubMedGoogle Scholar
  57. Kwak YD, Brannen CL, Qu T, Kim HM, Dong X, Soba P, Majumdar A, Kaplan A, Beyreuther K, Sugaya K (2006) Amyloid precursor protein regulates differentiation of human neural stem cells. Stem Cells Dev 15:381–389PubMedGoogle Scholar
  58. Lepore AC, Fischer I (2005) Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp Neurol 194:230–242PubMedGoogle Scholar
  59. Li X, Su H, Fu QL, Guo J, Lee DH, So KF, Wu W (2011) Soluble NgR fusion protein modulates the proliferation of neural progenitor cells via the Notch pathway. Neurochem Res 36:2363–2372PubMedCentralPubMedGoogle Scholar
  60. Liu H, Ng CE, Tang BL (2002) Nogo-A expression in mouse central nervous system neurons. Neurosci Lett 328:257–260PubMedGoogle Scholar
  61. Liu BP, Cafferty WB, Budel SO, Strittmatter SM (2006) Extracellular regulators of axonal growth in the adult central nervous system. Philos Trans R Soc Lond B Biol Sci 361:1593–1610PubMedCentralPubMedGoogle Scholar
  62. Lööv C, Fernqvist M, Walmsley A, Marklund N, Erlandsson A (2012) Neutralization of LINGO-1 during in vitro differentiation of neural stem cells results in proliferation of immature neurons. PLoS One 7:e29771PubMedCentralPubMedGoogle Scholar
  63. Louissaint A Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34:945–960PubMedGoogle Scholar
  64. Lu H, Jiao Q, Wang Y, Yang Z, Feng M, Wang L, Chen X, Jin W, Liu Y (2013) The mental retardation-associated protein srGAP3 regulates survival, proliferation, and differentiation of rat embryonic neural stem/progenitor cells. Stem Cells Dev 22:1709–1716PubMedGoogle Scholar
  65. Ma DK, Kim WR, Ming G, H. S (2009) Activity‐dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann N Y Acad Sci 1170:664–673PubMedCentralPubMedGoogle Scholar
  66. Marcos S, Backer S, Causeret F, Tessier-Lavigne M, Bloch-Gallego E (2009) Differential roles of Netrin-1 and its receptor DCC in inferior olivary neuron migration. Mol Cell Neurosci 41:429–439PubMedGoogle Scholar
  67. Marillat V, Cases O, Nguyen-Ba-Charvet KT, Tessier-Lavigne M, Sotelo C, Chedotal A (2002) Spatiotemporal expression patterns of slit and robo genes in the rat brain. J Comp Neurol 442:130–155PubMedGoogle Scholar
  68. Martin I, Andres CR, Vedrine S, Tabagh R, Michelle C, Jourdan ML, Heuze-Vourc’h N, Corcia P, Duittoz A, Vourc’h P (2009) Effect of the oligodendrocyte myelin glycoprotein (OMgp) on the expansion and neuronal differentiation of rat neural stem cells. Brain Res 1284:22–30PubMedGoogle Scholar
  69. Mathis C, Schröter A, Thallmair M, Schwab ME (2010) Nogo-A regulates neural precursor migration in the embryonic mouse cortex. Cereb Cortex 20:2380–2390PubMedCentralPubMedGoogle Scholar
  70. Mehta B, Bhat KM (2001) Slit signaling promotes the terminal asymmetric division of neural precursor cells in the Drosophila CNS. Development 128:3161–3168PubMedGoogle Scholar
  71. Merlos-Suarez A, Batlle E (2008) Eph-ephrin signalling in adult tissues and cancer. Curr Opin Cell Biol 20:194–200PubMedGoogle Scholar
  72. Mi Y, Gao X, Ma Y, Gao J, Wang Z, JinW (2014) A novel centrosome and microtubules associated subcellular localization of Nogo-A: implications for neuronal development. Int J Biochem Cell Biol 57:1–6. doi:10.1016/j.biocel.2014.09.024
  73. Ming G-l, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250PubMedGoogle Scholar
  74. Murai K, Qiu R, Zhang H, Wang J, Wu C, Neubig RR, Lu Q (2010) Galpha subunit coordinates with ephrin-B to balance self-renewal and differentiation in neural progenitor cells. Stem Cells 28:1581–1589PubMedCentralPubMedGoogle Scholar
  75. Murase S, Horwitz AF (2002) Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J Neurosci 22:3568–3579PubMedGoogle Scholar
  76. Niclou SP, Ehlert EM, Verhaagen J (2006) Chemorepellent axon guidance molecules in spinal cord injury. J Neurotrauma 23:409–421PubMedGoogle Scholar
  77. North HA, Zhao X, Kolk SM, Clifford MA, Ziskind DM, Donoghue MJ (2009) Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. Development 136:2467–2476PubMedCentralPubMedGoogle Scholar
  78. O’Leary CJ, Bradford D, Chen M, White A, Blackmore DG, Cooper HM (2014) The Netrin/RGM receptor, neogenin, controls adult neurogenesis by promoting neuroblast migration and cell cycle exit. Stem Cells. doi:10.1002/stem.1861 Google Scholar
  79. Ottone C, Krusche B, Whitby A, Clements M, Quadrato G, Pitulescu ME, Adams RH, Parrinello S (2014) Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat Cell Biol 16:1045–1056PubMedCentralPubMedGoogle Scholar
  80. Park JH, Strittmatter SM (2007) Nogo receptor interacts with brain APP and Aβ to reduce pathologic changes in Alzheimer’s transgenic mice. Curr Alzheimer Res 4:568PubMedCentralPubMedGoogle Scholar
  81. Parr A, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, Tator C (2008) Transplanted adult spinal cord–derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155:760–770PubMedGoogle Scholar
  82. Phillips W, Michell AW, Barker RA (2006) Neurogenesis in diseases of the central nervous system. Stem Cells Dev 15:359–379PubMedGoogle Scholar
  83. Qiu R, Wang X, Davy A, Wu C, Murai K, Zhang H, Flanagan JG, Soriano P, Lu Q (2008) Regulation of neural progenitor cell state by ephrin-B. J Cell Biol 181:973–983PubMedCentralPubMedGoogle Scholar
  84. Ramasamy S, Yu F, Hong Yu Y, Srivats H, Stewart Dawe G, Ahmed S (2014) NogoR1 and PirB signaling stimulates neural stem cell survival and proliferation. Stem Cells 32:1636–1648PubMedGoogle Scholar
  85. Ricard J, Salinas J, Garcia L, Liebl DJ (2006) EphrinB3 regulates cell proliferation and survival in adult neurogenesis. Mol Cell Neurosci 31:713–722PubMedGoogle Scholar
  86. Riess P, Zhang C, Saatman KE, Laurer HL, Longhi LG, Raghupathi R, Lenzlinger PM, Lifshitz J, Boockvar J, Neugebauer E (2002) Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery 51:1043–1054PubMedGoogle Scholar
  87. Robak LA, Venkatesh K, Lee H, Raiker SJ, Duan Y, Lee-Osbourne J, Hofer T, Mage RG, Rader C, Giger RJ (2009) Molecular basis of the interactions of the Nogo-66 receptor and its homolog NgR2 with myelin-associated glycoprotein: development of NgROMNI-Fc, a novel antagonist of CNS myelin inhibition. J Neurosci 29:5768–5783PubMedCentralPubMedGoogle Scholar
  88. Schachner M, Bartsch U (2000) Multiple functions of the myelin-associated glycoprotein MAG (siglec-4a) in formation and maintenance of myelin. GLIA 29:154–165PubMedGoogle Scholar
  89. Schmandke A, Schmandke A, Schwab ME (2014) Nogo-A: multiple roles in CNS development, maintenance, and disease. Neurosci 20:372–386. doi:10.1177/1073858413516800
  90. See J, Bonner J, Neuhuber B, Fischer I (2010) Neurite outgrowth of neural progenitors in presence of inhibitory proteoglycans. J Neurotrauma 27:951–957PubMedGoogle Scholar
  91. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592–596PubMedCentralPubMedGoogle Scholar
  92. Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A (2007) Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134:2727–2738PubMedGoogle Scholar
  93. Stanco A, Szekeres C, Patel N, Rao S, Campbell K, Kreidberg JA, Polleux F, Anton ES (2009) Netrin-1-alpha3beta1 integrin interactions regulate the migration of interneurons through the cortical marginal zone. Proc Natl Acad Sci U S A 106:7595–7600PubMedCentralPubMedGoogle Scholar
  94. Staquicini FI, Dias-Neto E, Li J, Snyder EY, Sidman RL, Pasqualini R, Arap W (2009) Discovery of a functional protein complex of netrin-4, laminin gamma1 chain, and integrin alpha6beta1 in mouse neural stem cells. Proc Natl Acad Sci U S A 106:2903–2908PubMedCentralPubMedGoogle Scholar
  95. Suehiro K, Nakamura Y, Xu S, Uda Y, Matsumura T, Yamaguchi Y, Okamura H, Yamashita T, Takei Y (2014) Ecto-domain phosphorylation promotes functional recovery from spinal cord injury. Sci Rep 4:4972PubMedCentralPubMedGoogle Scholar
  96. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279–288PubMedGoogle Scholar
  97. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1133PubMedGoogle Scholar
  98. Tham M, Ramasamy S, Gan HT, Ramachandran A, Poonepalli A, Yu YH, Ahmed S (2010) CSPG is a secreted factor that stimulates neural stem cell survival possibly by enhanced EGFR signaling. PLoS One 5:e15341PubMedCentralPubMedGoogle Scholar
  99. Theus MH, Ricard J, Bethea JR, Liebl DJ (2010) EphB3 limits the expansion of neural progenitor cells in the subventricular zone by regulating p53 during homeostasis and following traumatic brain injury. Stem Cells 28:1231–1242PubMedCentralPubMedGoogle Scholar
  100. Uschkureit T, Spörkel O, Stracke J, Büssow H, Stoffel W (2000) Early onset of axonal degeneration in double (plp−/− mag−/−) and hypomyelinosis in triple (plp−/− mbp−/− mag−/−) mutant mice. J Neurosci 20:5225–5233PubMedGoogle Scholar
  101. Venkatesh K, Chivatakarn O, Lee H, Joshi PS, Kantor DB, Newman BA, Mage R, Rader C, Giger RJ (2005) The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J Neurosci 25:808–822PubMedGoogle Scholar
  102. Vourc’h P, Andres C (2004) Oligodendrocyte myelin glycoprotein (OMgp): evolution, structure and function. Brain Res Rev 45:115–124PubMedGoogle Scholar
  103. Wang F, Zhu Y (2008) The interaction of Nogo-66 receptor with Nogo-p4 inhibits the neuronal differentiation of neural stem cells. Neuroscience 151:74–81PubMedGoogle Scholar
  104. Wang B, Xiao Z, Chen B, Han J, Gao Y, Zhang J, Zhao W, Wang X, Dai J (2008) Nogo-66 promotes the differentiation of neural progenitors into astroglial lineage cells through mTOR-STAT3 pathway. PLoS One 3:e1856PubMedCentralPubMedGoogle Scholar
  105. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16:7599–7609PubMedGoogle Scholar
  106. Wilkinson DG (2001) Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2:155–164PubMedGoogle Scholar
  107. Wu H, Fan J, Zhu L, Liu S, Wu Y, Zhao T, Ding X, Fan W, Fan M (2009) Sema4C expression in neural stem/progenitor cells and in adult neurogenesis induced by cerebral ischemia. J Mol Neurosci 39:27–39PubMedGoogle Scholar
  108. Xing S, He Y, Ling L, Hou Q, Yu J, Zeng J, Pei Z (2008) Blockade of EphB2 enhances neurogenesis in the subventricular zone and improves neurological function after cerebral cortical infarction in hypertensive rats. Brain Res 1230:237–246PubMedGoogle Scholar
  109. Xu L, Xu CJ, Lu HZ, Wang YX, Li Y, Lu PH (2010) Long-term fate of allogeneic neural stem cells following transplantation into injured spinal cord. Stem Cell Rev 6:121–136PubMedGoogle Scholar
  110. Xu CJ, Xu L, Huang LD, Li Y, Yu PP, Hang Q, Xu XM, Lu PH (2011) Combined NgR vaccination and neural stem cell transplantation promote functional recovery after spinal cord injury in adult rats. Neuropathol Appl Neurobiol 37:135–155PubMedGoogle Scholar
  111. Xu DE, Zhang WM, Yang ZZ, Zhu HM, Yan K, Li S, Bagnard D, Dawe GS, Ma QH, Xiao ZC (2014a) Amyloid precursor protein at node of Ranvier modulates nodal formation. Cell Adh Migr 8:396–403PubMedGoogle Scholar
  112. Xu K, Wu Z, Renier N, Antipenko A, Tzvetkova-Robev D, Xu Y, Minchenko M, Nardi-Dei V, Rajashankar KR, Himanen J, Tessier-Lavigne M, Nikolov DB (2014b) Neural migration. Structures of netrin-1 bound to two receptors provide insight into its axon guidance mechanism. Science 344:1275–1279PubMedCentralPubMedGoogle Scholar
  113. Yeh ML, Gonda Y, Mommersteeg MT, Barber M, Ypsilanti AR, Hanashima C, Parnavelas JG, Andrews WD (2014) Robo1 modulates proliferation and neurogenesis in the developing neocortex. J Neurosci 34:5717–5731PubMedCentralPubMedGoogle Scholar
  114. Yuan T, Liao W, Feng NH, Lou YL, Niu X, Zhang AJ, Wang Y, Deng ZF (2013) Human induced pluripotent stem cell-derived neural stem cells survive, migrate, differentiate, and improve neurologic function in a rat model of middle cerebral artery occlusion. Stem Cell Res Ther 4:73PubMedCentralPubMedGoogle Scholar
  115. Zhou Y, Gunput RA, Pasterkamp RJ (2008) Semaphorin signaling: progress made and promises ahead. Trends Biochem Sci 33:161–170PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Histology and Embryology, Institute of NeuroscienceWenzhou Medical UniversityCha ShanChina
  2. 2.School of Laboratory Medicine and Life ScienceWenzhou Medical UniversityWenzhouChina
  3. 3.Institute of Nano Biomedicine and Engineering, Department of Instrument Science and Engineering, Key Laboratory for Thin Film and Microfabrication Technology of Ministry of Education, School of Electronic Information and Electronic EngineeringShanghai Jiao Tong UniversityShanghaiChina
  4. 4.School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina

Personalised recommendations