Anat Cell Biol.  2010 Dec;43(4):269-279. 10.5115/acb.2010.43.4.269.

Control of neuronal migration through rostral migration stream in mice

• Sun W
• Kim H
• Moon Y

• KMID: 1455340
• DOI: http://doi.org/10.5115/acb.2010.43.4.269

Abstract

During the nervous system development, immature neuroblasts have a strong potential to migrate toward their destination. In the adult brain, new neurons are continuously generated in the neurogenic niche located near the ventricle, and the newly generated cells actively migrate toward their destination, olfactory bulb, via highly specialized migratory route called rostral migratory stream (RMS). Neuroblasts in the RMS form chains by their homophilic interactions, and the neuroblasts in chains continually migrate through the tunnels formed by meshwork of astrocytes, glial tube. This review focuses on the development and structure of RMS and the regulation of neuroblast migration in the RMS. Better understanding of RMS migration may be crucial for improving functional replacement therapy by supplying endogenous neuronal cells to the injury sites more efficiently.

Keyword

Neuronal migration; Rostral migratory stream; Neuroblasts; Adult neurogenesis

MeSH Terms

Adult
Animals
Astrocytes
Brain
Humans
Mice
Nervous System
Neurons
Olfactory Bulb
Rivers

Figure

• 

  Fig. 1 Rostral migratory stream in the adult mouse brain. (A) New neurons born in the subventricular zone (SVZ) of the lateral ventricle (LV) migrate to the olfactory bulb (OB) through rostral migratory stream (RMS). The RMS tract is connected to sebependymal layer (SE), the central part of the OB. In the RMS, migrating the neuroblasts form chains and they are surrounded by glial tube. Within the RMS, parallel-running blood vessels provide additional scaffolds for migrating neuroblasts. (B, C) Double immunufluorescence labeling of migrating neuroblasts (red, DCX labeling) and glial tube (green, GFAP labeling) in the RMS. (B) shows parasagittal, and (C) shows coronal cut image. Abbreviations are: LV, lateral ventricle; CC, corpus callosum; Str, Stratum; A, type A neuroblasts; G, glial tube; V, blood vessels.

• 

  Fig. 2 Factors regulating RMS migration. In the SVZ, newly generated neuroblasts integrate into the cell clusters in chains and begin to migrate along the RMS (Step 1: Initiation). In the RMS, neuroblasts actively migrate to the rostral orientation, which is regulated by several factors including cell-cell/cell-ECM interactions, chemoattractive or chemorepulsive signals, and local environment in the RMS (Step 2: Migration). In the OB, migrated neuroblasts detach from chains, and they transfer to radial glial dependent-radial migration. By detachment from radial fiber, they arrive at their final destination (Step 3: Termination). Abbreviations are; ECM, extracellular matrix; SVZ, subventricular zone; RMS, rostral migratory stream; LV, lateral ventricle; CC, corpus callosum; Str, Stratum; SE, subependymal layer; A, type A neuroblasts; B, type B neural stem cells; C, type C transit-amplifying cells; E, ependymal cells; G, glial tube; V, blood vessels; R, radial fibers.

Reference

1. Alonso M, Viollet C, Gabellec MM, Meas-Yedid V, Olivo-Marin JC, Lledo PM. Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci. 2006. 26:10508–10513.

2. Andrade N, Komnenovic V, Blake SM, et al. ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin. Proc Natl Acad Sci U S A. 2007. 104:8508–8513.

3. Angot E, Loulier K, Nguyen-Ba-Charvet KT, Gadeau AP, Ruat M, Traiffort E. Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells. 2008. 26:2311–2320.

4. Anton ES, Ghashghaei HT, Weber JL, et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci. 2004. 7:1319–1328.

5. Balenci L, Saoudi Y, Grunwald D, et al. IQGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci. 2007. 27:4716–4724.

6. Balordi F, Fishell G. Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J Neurosci. 2007. 27:5936–5947.

7. Battista D, Rutishauser U. Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues. J Neurosci. 2010. 30:3995–4003.

8. Bédard A, Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res. 2004. 151:159–168.

9. Belvindrah R, Hankel S, Walker J, Patton BL, Müller U. Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci. 2007. 27:2704–2717.

10. Blake SM, Strasser V, Andrade N, et al. Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J. 2008. 27:3069–3080.

11. Bolteus AJ, Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci. 2004. 24:7623–7631.

12. Boutin C, Schmitz B, Cremer H, Diestel S. NCAM expression induces neurogenesis in vivo. Eur J Neurosci. 2009. 30:1209–1218.

13. Bovetti S, Bovolin P, Perroteau I, Puche AC. Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur J Neurosci. 2007. 25:2021–2033.

14. Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci. 2006. 29:1–35.

15. Cayre M, Bancila M, Virard I, Borges A, Durbec P. Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain. Mol Cell Neurosci. 2006. 31:748–758.

16. Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H. Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci. 2000. 20:1446–1457.

17. Chiaramello S, Dalmasso G, Bezin L, et al. BDNF/TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci. 2007. 26:1780–1790.

18. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci. 2000. 3:1091–1097.

19. Coskun V, Luskin MB. Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J Neurosci Res. 2002. 69:795–802.

20. Cremer H, Lange R, Christoph A, et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 1994. 367:455–459.

21. Curtis MA, Kam M, Nannmark U, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science. 2007. 315:1243–1249.

22. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev. 2003. 13:543–550.

23. Emsley JG, Hagg T. alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp Neurol. 2003. 183:273–285.

24. Eom TY, Li J, Anton ES. Going tubular in the rostral migratory stream: neurons remodel astrocyte tubes to promote directional migration in the adult brain. Neuron. 2010. 67:173–175.

25. Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S. Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci. 2008. 28:5901–5909.

26. Gascon E, Vutskits L, Jenny B, Durbec P, Kiss JZ. PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development. 2007. 134:1181–1190.

27. Giachino C, Taylor V. Lineage analysis of quiescent regenerative stem cells in the adult brain by genetic labelling reveals spatially restricted neurogenic niches in the olfactory bulb. Eur J Neurosci. 2009. 30:9–24.

28. Gotts JE, Chesselet MF. Migration and fate of newly born cells after focal cortical ischemia in adult rats. J Neurosci Res. 2005. 80:160–171.

29. Gritti A, Bonfanti L, Doetsch F, et al. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci. 2002. 22:437–445.

30. Grubb MS, Nissant A, Murray K, Lledo PM. Functional maturation of the first synapse in olfaction: development and adult neurogenesis. J Neurosci. 2008. 28:2919–2932.

31. Hack I, Bancila M, Loulier K, Carroll P, Cremer H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci. 2002. 5:939–945.

32. Hack MA, Saghatelyan A, de Chevigny A, et al. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci. 2005. 8:865–872.

33. Hatten ME. Central nervous system neuronal migration. Annu Rev Neurosci. 1999. 22:511–539.

34. Hu H, Tomasiewicz H, Magnuson T, Rutishauser U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron. 1996. 16:735–743.

35. Hurtado-Chong A, Yusta-Boyo MJ, Vergaño-Vera E, Bulfone A, de Pablo F, Vicario-Abejón C. IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci. 2009. 30:742–755.

36. Jablonska B, Aguirre A, Raymond M, et al. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci. 2010. 13:541–550.

37. Jankovski A, Garcia C, Soriano E, Sotelo C. Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci. 1998. 10:3853–3868.

38. Jung AR, Kim TW, Rhyu IJ, et al. Misplacement of Purkinje cells during postnatal development in Bax knock-out mice: a novel role for programmed cell death in the nervous system? J Neurosci. 2008. 28:2941–2948.

39. Kaneko N, Marín O, Koike M, et al. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron. 2010. 67:213–223.

40. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010. 141:52–67.

41. Kim HM, Qu T, Kriho V, et al. Reelin function in neural stem cell biology. Proc Natl Acad Sci U S A. 2002. 99:4020–4025.

42. Kim WR, Kim Y, Eun B, et al. Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci. 2007. 27:14392–14403.

43. Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci. 1999. 19:2171–2180.

44. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A. Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci. 2005. 25:6997–7003.

45. Kohwi M, Petryniak MA, Long JE, et al. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci. 2007. 27:6878–6891.

46. Kornack DR, Rakic P. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A. 2001. 98:4752–4757.

47. Law AK, Pencea V, Buck CR, Luskin MB. Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes. Dev Biol. 1999. 216:622–634.

48. Lee SR, Kim HY, Rogowska J, et al. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci. 2006. 26:3491–3495.

49. Li WL, Yu SP, Ogle ME, Ding XS, Wei L. Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice. Dev Neurobiol. 2008. 68:1474–1486.

50. Liu G, Rao Y. Neuronal migration from the forebrain to the olfactory bulb requires a new attractant persistent in the olfactory bulb. J Neurosci. 2003. 23:6651–6659.

51. Liu Z, Martin LJ. Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J Comp Neurol. 2003. 459:368–391.

52. Lledo PM, Merkle FT, Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008. 31:392–400.

53. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 1994. 264:1145–1148.

54. Lois C, García-Verdugo JM, Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 1996. 271:978–981.

55. Mackay-Sima A, Chuahb MI. Neurotrophic factors in the primary olfactory pathway. Prog Neurobiol. 2000. 62:527–559.

56. Maina F, Klein R. Hepatocyte growth factor, a versatile signal for developing neurons. Nat Neurosci. 1999. 2:213–217.

57. Mandairon N, Jourdan F, Didier A. Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience. 2003. 119:507–516.

58. Mandairon N, Sacquet J, Jourdan F, Didier A. Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation. Neuroscience. 2006. 141:443–451.

59. Marins M, Xavier AL, Viana NB, Fortes FS, Fróes MM, Menezes JR. Gap junctions are involved in cell migration in the early postnatal subventricular zone. Dev Neurobiol. 2009. 69:715–730.

60. Marshall CA, Novitch BG, Goldman JE. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J Neurosci. 2005. 25:7289–7298.

61. Mason HA, Ito S, Corfas G. Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J Neurosci. 2001. 21:7654–7663.

62. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science. 2007. 317:381–384.

63. Miragall F, Albiez P, Bartels H, de Vries U, Dermietzel R. Expression of the gap junction protein connexin43 in the subependymal layer and the rostral migratory stream of the mouse: evidence for an inverse correlation between intensity of connexin43 expression and cell proliferation activity. Cell Tissue Res. 1997. 287:243–253.

64. Mizrahi A. Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci. 2007. 10:444–452.

65. Mouret A, Gheusi G, Gabellec MM, de Chaumont F, Olivo-Marin JC, Lledo PM. Learning and survival of newly generated neurons: when time matters. J Neurosci. 2008. 28:11511–11516.

66. Murase S, Cho C, White JM, Horwitz AF. ADAM2 promotes migration of neuroblasts in the rostral migratory stream to the olfactory bulb. Eur J Neurosci. 2008. 27:1585–1595.

67. Murase S, Horwitz AF. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J Neurosci. 2002. 22:3568–3579.

68. Nam SC, Kim Y, Dryanovski D, et al. Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol. 2007. 505:190–208.

69. Nguyen-Ba-Charvet KT, Picard-Riera N, Tessier-Lavigne M, Baron-Van Evercooren A, Sotelo C, Chédotal A. Multiple roles for slits in the control of cell migration in the rostral migratory stream. J Neurosci. 2004. 24:1497–1506.

70. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol. 2006. 7:359–371.

71. Ono K, Takebayashi H, Ikenaka K. Olig2 transcription factor in the developing and injured forebrain; cell lineage and glial development. Mol Cells. 2009. 27:397–401.

72. Panzanelli P, Bardy C, Nissant A, et al. Early synapse formation in developing interneurons of the adult olfactory bulb. J Neurosci. 2009. 29:15039–15052.

73. Paratcha G, Ibáñez CF, Ledda F. GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream. Mol Cell Neurosci. 2006. 31:505–514.

74. Pencea V, Bingaman KD, Freedman LJ, Luskin MB. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol. 2001. 172:1–16.

75. Pencea V, Luskin MB. Prenatal development of the rodent rostral migratory stream. J Comp Neurol. 2003. 463:402–418.

76. Petreanu L, Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 2002. 22:6106–6113.

77. Platel JC, Dave KA, Bordey A. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol. 2008. 586:3739–3743.

78. Powell EM, Mars WM, Levitt P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron. 2001. 30:79–89.

79. Rice DS, Curran T. Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci. 2001. 24:1005–1039.

80. Rochefort C, Gheusi G, Vincent JD, Lledo PM. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci. 2002. 22:2679–2689.

81. Russo VC, Gluckman PD, Feldman EL, Werther GA. The insulin-like growth factor system and its pleiotropic functions in brain. Endocr Rev. 2005. 26:916–943.

82. Saghatelyan A, de Chevigny A, Schachner M, Lledo PM. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci. 2004. 7:347–356.

83. Saghatelyan A, Roux P, Migliore M, et al. Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron. 2005. 46:103–116.

84. Saino-Saito S, Cave JW, Akiba Y. ER81 and CaMKIV identify anatomically and phenotypically defined subsets of mouse olfactory bulb interneurons. J Comp Neurol. 2007. 502:485–496.

85. Sawamoto K, Wichterle H, Gonzalez-Perez O, et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science. 2006. 311:629–632.

86. Simó S, Pujadas L, Segura MF, et al. Reelin induces the detachment of postnatal subventricular zone cells and the expression of the Egr-1 through Erk1/2 activation. Cereb Cortex. 2007. 17:294–303.

87. Snapyan M, Lemasson M, Brill MS, et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci. 2009. 29:4172–4188.

88. Soria JM, Taglialatela P, Gil-Perotin S, et al. Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J Neurosci. 2004. 24:11171–11181.

89. Staquicini FI, Dias-Neto E, Li J, et al. 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. 2009. 106:2903–2908.

90. Sun W, Funakoshi H, Nakamura T. Localization and functional role of hepatocyte growth factor (HGF) and its receptor c-met in the rat developing cerebral cortex. Brain Res Mol Brain Res. 2002a. 103:36–48.

91. Sun W, Funakoshi H, Nakamura T. Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. J Neurosci. 2002b. 22:6537–6548.

92. Waclaw RR, Wang B, Pei Z, Ehrman LA, Campbell K. Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron. 2009. 63:451–465.

93. Whitman MC, Fan W, Rela L, Rodriguez-Gil DJ, Greer CA. Blood vessels form a migratory scaffold in the rostral migratory stream. J Comp Neurol. 2009. 516:94–104.

94. Whitman MC, Greer CA. Adult neurogenesis and the olfactory system. Prog Neurobiol. 2009. 89:162–175.

95. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci. 2002. 16:1681–1689.

96. Wittko IM, Schänzer A, Kuzmichev A, et al. VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neurosci. 2009. 29:8704–8714.

97. Yamaguchi M, Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A. 2005. 102:9697–9702.

98. Yamashita T, Ninomiya M, Hernández Acosta P, et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci. 2006. 26:6627–6636.

99. Yang H, Jensen P, Goldowitz D. The community effect and Purkinje cell migration in the cerebellar cortex: analysis of scrambler chimeric mice. J Neurosci. 2002. 22:464–470.

100. Zhang SC. Defining glial cells during CNS development. Nat Rev Neurosci. 2001. 2:840–843.

101. Zigova T, Pencea V, Betarbet R, et al. Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant. 1998. 7:137–156.