The dynamics of neuronal migration

Advances in Experimental Medicine and Biology

Volumn 800, Issue , 2014, Pages 25-36

  Wu, Qian ^a   Liu, Jing ^a   Fang, Ai ^a   Li, Rui ^a   Bai, Ye ^a   Kriegstein, Arnold R ^b   Wang, Xiaoqun ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Lissencephaly; Microtubules; Neural stem cells; Neuronal migration; Neuronal migration disorders; Radial Glia

Indexed keywords

AGYRIA; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL COMMUNICATION; CELL KINETICS; CELL MIGRATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DYNAMICS; GENE MUTATION; HUMAN; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURONAL MIGRATION DISORDER; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; SUBVENTRICULAR ZONE; CELL ADHESION; CELL FUNCTION; CELL POLARITY; CELLULAR DISTRIBUTION; CYTOSKELETON; EXTRACELLULAR MATRIX; INTRACELLULAR SIGNALING; MACROGLIA; MICROTUBULE; NEURAL STEM CELL TRANSPLANTATION; NEUROBLAST; PYRAMIDAL EXCITATORY NERVE CELL; PYRAMIDAL NERVE CELL;

EID: 84959228443     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-7-7687-6_2     Document Type: Article

References (89)

1. Ables JL, Breunig JJ, Eisch AJ, Rakic P (2011) Not(ch) just development: Notch signalling in the adult brain. Nat Rev Neurosci 12(5):269-283. doi:10.1038/nrn3024
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278(5337):474-476
3. Ang ES Jr, Haydar TF, Gluncic V, Rakic P (2003) Fourdimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci 23(13):5805-5815
4. Asensio VC, Campbell IL (1999) Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci 22(11):504-512
5. Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner WB (2008) Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PloS One 3(6):e2388. doi:10.1371/journal.pone.0002388
6. Ayala R, Shu T, Tsai LH (2007) Trekking across the brain: the journey of neuronal migration. Cell 128(1):29-43. doi:10.1016/j.cell.2006.12.021
7. Bantubungi K, Blum D, Cuvelier L, Wislet-Gendebien S, Rogister B, Brouillet E, Schiffmann SN (2008) Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol Cell Neurosci 37(3):454-470. doi:10.1016/j.mcn.2007.11.001
8. Barros CS, Franco SJ, Muller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3(1):a005108. doi:10.1101/cshperspect.a005108
9. Beffert U, Weeber EJ, Morfini G, Ko J, Brady ST, Tsai LH, Sweatt JD, Herz J (2004) Reelin and cyclindependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J Neurosci 24(8):1897-1906. doi:10.1523/JNEUROSCI.4084-03.2004
10. Bellion A, Baudoin JP, Alvarez C, Bornens M, Metin C (2005) Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J Neurosci 25(24):5691-5699. doi:10.1523/JNEUROSCI.1030-05.2005
11. Belvindrah R, Hankel S, Walker J, Patton BL, Muller U (2007) Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci 27(10):2704-2717. doi:10.1523/JNEUROSCI.2991-06.2007
12. Bhide PG (2009) Dopamine, cocaine and the development of cerebral cortical cytoarchitecture: a review of current concepts. Semin Cell Dev Biol 20(4):395-402. doi:10.1016/j.semcdb.2009.01.006
13. Blurton-Jones M, Kitazawa M, Martinez-Coria H, Castello NA, Muller FJ, Loring JF, Yamasaki TR, Poon WW, Green KN, LaFerla FM (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 106(32):13594-13599. doi:10.1073/pnas.0901402106
14. Botella-Lopez A, Burgaya F, Gavin R, Garcia-Ayllon MS, Gomez-Tortosa E, Pena-Casanova J, Urena JM, Del Rio JA, Blesa R, Soriano E, Saez-Valero J (2006) Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc Natl Acad Sci U S A 103(14):5573-5578. doi:10.1073/pnas.0601279103
15. Bradford D, Cole SJ, Cooper HM (2009) Netrin-1: diversity in development. Int J Biochem Cell Biol 41(3):487-493. doi:10.1016/j.biocel.2008.03.014
16. Calabria LK, da Cruz GC, Nascimento R, Carvalho WJ, de Gouveia NM, Alves FV, Furtado FB, Ishikawa-Ankerhold HC, de Sousa MV, Goulart LR, Espindola FS (2011) Overexpression of myosin-IIB in the brain of a rat model of streptozotocin-induced diabetes. J Neurol Sci 303(1-2):43-49. doi:10.1016/j.jns.2011.01.017
17. Chansard M, Hong JH, Park YU, Park SK, Nguyen MD (2011) Ndel1, Nudel (Noodle): flexible in the cell? Cytoskeleton 68(10):540-554. doi:10.1002/cm.20532
18. Chen ZL, Haegeli V, Yu H, Strickland S (2009) Cortical deficiency of laminin gamma1 impairs the AKT/ GSK-3beta signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev Biol 327(1):158-168. doi:10.1016/j.ydbio.2008.12.006
19. Cheung AF, Pollen AA, Tavare A, DeProto J, Molnar Z (2007) Comparative aspects of cortical neurogenesis in vertebrates. J Anat 211(2):164-176. doi:10.1111/j.1469-7580.2007.00769.x
20. Chin J, Massaro CM, Palop JJ, Thwin MT, Yu GQ, Bien-Ly N, Bender A, Mucke L (2007) Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer's disease. J Neurosci 27(11):2727-2733. doi:10.1523/JNEUROSCI.3758-06.2007
21. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24(2):471-479
22. Darsalia V, Kallur T, Kokaia Z (2007) Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur J Neurosci 26(3):605-614. doi:10.1111/j.1460-9568.2007.05702.x
23. de Carlos JA, Lopez-Mascaraque L, Valverde F (1996) Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16(19):6146-6156
24. Elias LA, Wang DD, Kriegstein AR (2007) Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448(7156):901-907. doi:10.1038/nature06063
25. Elias LA, Turmaine M, Parnavelas JG, Kriegstein AR (2010) Connexin 43 mediates the tangential to radial migratory switch in ventrally derived cortical interneurons. J Neurosci 30(20):7072-7077. doi:10.1523/JNEUROSCI.5728-09.2010
26. Falnikar A, Tole S, Baas PW (2011) Kinesin-5, a mitotic microtubule-associated motor protein, modulates neuronal migration. Mol Biol Cell 22(9):1561-1574. doi:10.1091/mbc.E10-11-0905
27. Franco SJ, Muller U (2011) Extracellular matrix functions during neuronal migration and lamination in the mammalian central nervous system. Dev Neurobiol 71(11):889-900. doi:10.1002/dneu.20946
28. Franco SJ, Muller U (2013) Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 77(1):19-34. doi:10.1016/j.neuron. 2012.12.022
29. Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Muller U (2011) Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69(3):482-497. doi:10.1016/j.neuron.2011.01.003
30. Godin JD, Thomas N, Laguesse S, Malinouskaya L, Close P, Malaise O, Purnelle A, Raineteau O, Campbell K, Fero M, Moonen G, Malgrange B, Chariot A, Metin C, Besson A, Nguyen L (2012) p27(Kip1) is a microtubuleassociated protein that promotes microtubule polymerization during neuron migration. Dev Cell 23(4):729-744. doi:10.1016/j.devcel.2012.08.006
31. Gonzalez-Billault C, Del Rio JA, Urena JM, Jimenez-Mateos EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, Torre AL, Gavin R, Wandosell F, Soriano E, Avila J (2005) A role of MAP1B in Reelin-dependent neuronal migration. Cereb Cortex 15(8):1134-1145. doi:10.1093/cercor/bhh213
32. Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6(10):777-788. doi:10.1038/nrm1739
33. Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH (2003) Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci 6(12):1284-1291. doi:10.1038/nn1151
34. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, Radtke F, Gridley T, Sestan N, Rakic P (2008) Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60(2):273-284. doi:10.1016/j.neuron.2008.09.026
35. Hatten ME (2002) New directions in neuronal migration. Science 297(5587):1660-1663. doi:10.1126/science.1074572
36. Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A 101(9):3196-3201. doi:10.1073/pnas. 0308600100
37. Heng JI, Moonen G, Nguyen L (2007) Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 26(3):537-546. doi:10.1111/j.1460-9568.2007.05694.x
38. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24(2):481-489
39. Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO, Martin ND, Walsh CA (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26(1):93-96. doi:10.1038/79246
40. Howell BW, Herrick TM, Hildebrand JD, Zhang Y, Cooper JA (2000) Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr Biol 10(15):877-885
41. Jin K, Mao XO, Sun Y, Xie L, Greenberg DA (2002) Stem cell factor stimulates neurogenesis in vitro and in vivo. J Clin Invest 110(3):311-319. doi:10.1172/JCI15251
42. Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14(6):697-703. doi:10.1038/nn.2816
43. Kelemenova S, Schmidtova E, Ficek A, Celec P, Kubranska A, Ostatnikova D (2010) Polymorphisms of candidate genes in Slovak autistic patients. Psychiatr Genet 20(4):137-139. doi:10.1097/YPG.0b013e32833a1eb3
44. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, Palmer T, Steinberg GK (2004) Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A 101(32):11839-11844. doi:10.1073/pnas. 0404474101
45. Kim SU, Park IH, Kim TH, Kim KS, Choi HB, Hong SH, Bang JH, Lee MA, Joo IS, Lee CS, Kim YS (2006) Brain transplantation of human neural stem cells transduced with tyrosine hydroxylase and GTP cyclohydrolase 1 provides functional improvement in animal models of Parkinson disease. Neuropathology 26(2):129-140
46. Klein SM, Behrstock S, McHugh J, Hoffmann K, Wallace K, Suzuki M, Aebischer P, Svendsen CN (2005) GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum Gene Ther 16(4):509-521. doi:10.1089/hum.2005. 16.509
47. Konno D, Yoshimura S, Hori K, Maruoka H, Sobue K (2005) Involvement of the phosphatidylinositol 3-kinase/rac1 and cdc42 pathways in radial migration of cortical neurons. J Biol Chem 280(6):5082-5088. doi:10.1074/jbc.M408251200
48. Kriegstein AR, Noctor SC (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27(7):392-399. doi:10.1016/j.tins.2004.05.001
49. LaMonica BE, Lui JH, Wang X, Kriegstein AR (2012) OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr Opin Neurobiol 22(5):747-753. doi:10.1016/j.conb.2012.03.006
50. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84(3):359-369
51. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264(5162):1145-1148
52. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978-981
53. Lopez-Bendito G, Lujan R, Shigemoto R, Ganter P, Paulsen O, Molnar Z (2003) Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb Cortex 13(9):932-942
54. Luxton GW, Gomes ER, Folker ES, Worman HJ, Gundersen GG (2011) TAN lines: a novel nuclear envelope structure involved in nuclear positioning. Nucleus 2(3):173-181. doi:10.1073/pnas.1000824108, 10.4161/nucl.2.3.16243
55. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127(24):5253-5263
56. Marin O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26:441-483. doi:10.1146/annurev.neuro.26.041002.131058
57. Martini FJ, Valiente M, Lopez Bendito G, Szabo G, Moya F, Valdeolmillos M, Marin O (2009) Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development 136(1):41-50. doi:10.1242/dev.025502
58. McCarthy D, Lueras P, Bhide PG (2007) Elevated dopamine levels during gestation produce region-specific decreases in neurogenesis and subtle deficits in neuronal numbers. Brain Res 1182:11-25. doi:10.1016/j.brainres.2007.08.088
59. McCarthy DM, Gioioso V, Zhang X, Sharma N, Bhide PG (2012) Neurogenesis and neuronal migration in the forebrain of the TorsinA knockout mouse embryo. Dev Neurosci 34(4):366-378. doi:10.1159/000342260
60. Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31(5):727-741
61. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surfacedividing and non-surface-dividing cortical progenitor cells. Development 131(13):3133-3145. doi:10.1242/dev.01173
62. Mobley AK, Tchaicha JH, Shin J, Hossain MG, McCarty JH (2009) Beta8 integrin regulates neurogenesis and neurovascular homeostasis in the adult brain. J Cell Sci 122(Pt 11):1842-1851. doi:10.1242/jcs.043257
63. Nahin RL, Humphrey E, Hylden JL (1991) Evidence for calcitonin gene-related peptide contacts on a population of lamina I projection neurons. J Chem Neuroanat 4(2):123-129
64. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714-720. doi:10.1038/35055553
65. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7(2):136-144. doi:10.1038/nn1172
66. Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508(1):28-44. doi:10.1002/cne.21669
67. Nowakowski RS, Rakic P (1979) The mode of migration of neurons to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 8(6):697-718
68. Okada T, Keino-Masu K, Masu M (2007) Migration and nucleogenesis of mouse precerebellar neurons visualized by in utero electroporation of a green fluorescent protein gene. Neurosci Res 57(1):40-49. doi:10.1016/j.neures.2006. 09.010
69. Olstorn H, Varghese M, Murrell W, Moe MC, Langmoen IA (2011) Predifferentiated brain-derived adult human progenitor cells migrate toward ischemia after transplantation to the adult rat brain. Neurosurgery 68(1):213-222. doi:10.1227/NEU.0b013e3181fd2c11; discussion 222
70. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3(9):715-727. doi:10.1038/nrn919
71. Persico AM, D'Agruma L, Maiorano N, Totaro A, Militerni R, Bravaccio C, Wassink TH, Schneider C, Melmed R, Trillo S, Montecchi F, Palermo M, Pascucci T, Puglisi-Allegra S, Reichelt KL, Conciatori M, Marino R, Quattrocchi CC, Baldi A, Zelante L, Gasparini P, Keller F, Collaborative Linkage Study of A (2001) Reelin gene alleles and haplotypes as a factor predisposing to autistic disorder. Mol Psychiatr 6(2):150-159. doi:10.1038/sj.mp.4000850
72. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112(4):453-465
73. Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145(1):61-83. doi:10.1002/cne.901450105
74. Rakic P (2007) The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res Rev 55(2):204-219. doi:10.1016/j.brainresrev.2007.02.010
75. Redmond DE Jr, Bjugstad KB, Teng YD, Ourednik V, Ourednik J, Wakeman DR, Parsons XH, Gonzalez R, Blanchard BC, Kim SU, Gu Z, Lipton SA, Markakis EA, Roth RH, Elsworth JD, Sladek JR Jr, Sidman RL, Snyder EY (2007) Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc Natl Acad Sci U S A 104(29):12175-12180. doi:10.1073/pnas.0704091104
76. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302(5651):1704-1709. doi:10.1126/science.1092053
77. Rogers JT, Rusiana I, Trotter J, Zhao L, Donaldson E, Pak DT, Babus LW, Peters M, Banko JL, Chavis P, Rebeck GW, Hoe HS, Weeber EJ (2011) Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density. Learn Mem 18(9):558-564. doi:10.1101/lm.2153511
78. Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A 102(38):13652-13657. doi:10.1073/pnas. 0506008102
79. Shieh JC, Schaar BT, Srinivasan K, Brodsky FM, McConnell SK (2011) Endocytosis regulates cell soma translocation and the distribution of adhesion proteins in migrating neurons. PloS One 6(3):e17802. doi:10.1371/journal.pone. 0017802
80. Solecki DJ, Trivedi N, Govek EE, Kerekes RA, Gleason SS, Hatten ME (2009) Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63(1):63-80. doi:10.1016/j.neuron.2009.05.028
81. 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(18):7595-7600. doi:10.1073/pnas.0811343106
82. Sun L, Lee J, Fine HA (2004) Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury. J Clin Invest 113(9):1364-1374. doi:10.1172/JCI20001
83. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N (2005) Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115(1):102-109. doi:10.1172/JCI21137
84. Tamamaki N, Nakamura K, Okamoto K, Kaneko T (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41(1):51-60
85. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165(5):709-721. doi:10.1083/jcb.200309025
86. Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46(3):383-388. doi:10.1016/j.neuron.2005.04.013
87. Vallee RB, Seale GE, Tsai JW (2009) Emerging roles for myosin II and cytoplasmic dynein in migrating neurons and growth cones. Trends Cell Biol 19(7):347-355. doi:10.1016/j.tcb.2009.03.009
88. Wu Q, Wang X (2012) Neuronal stem cells in the central nervous system and in human diseases. Protein Cell 3(4):262-270. doi:10.1007/s13238-012-2930-8
89. Ypsilanti AR, Zagar Y, Chedotal A (2010) Moving away from the midline: new developments for Slit and Robo. Development 137(12):1939-1952. doi:10.1242/dev.044511