Browse > Article
http://dx.doi.org/10.5115/acb.2010.43.4.269

Control of neuronal migration through rostral migratory stream in mice  

Sun, Woong (Department of Anatomy and Division of Brain Korea 21 Biomedical Science, Korea University College of Medicine)
Kim, Hyun (Department of Anatomy and Division of Brain Korea 21 Biomedical Science, Korea University College of Medicine)
Moon, Young-Hye (Department of Anatomy and Division of Brain Korea 21 Biomedical Science, Korea University College of Medicine)
Publication Information
Anatomy and Cell Biology / v.43, no.4, 2010 , pp. 269-279 More about this Journal
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.
Keywords
Neuronal migration; Rostral migratory stream; Neuroblasts; Adult neurogenesis;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Anton ES, Ghashghaei HT, Weber JL, et al. (2004). Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci 7: 1319-1328   DOI   ScienceOn
2 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: 2704-2717   DOI   ScienceOn
3 Saghatelyan A, Roux P, Migliore M, et al. (2005). Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46: 103-116   DOI   ScienceOn
4 Snapyan M, Lemasson M, Brill MS, et al. (2009). Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci 29: 4172-4188   DOI   ScienceOn
5 Kim WR, Kim Y, Eun B, et al. (2007). 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 27: 14392-14403   DOI   ScienceOn
6 Paratcha G, Ibanez CF, Ledda F. (2006). GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream. Mol Cell Neurosci 31: 505-514   DOI   ScienceOn
7 Platel JC, Dave KA, Bordey A. (2008). Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol 586: 3739-3743   DOI   ScienceOn
8 Rice DS, Curran T. (2001). Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24: 1005-1039   DOI   ScienceOn
9 Jung AR, Kim TW, Rhyu IJ, et al. (2008). 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 28: 2941-2948   DOI   ScienceOn
10 Kim HM, Qu T, Kriho V, et al. (2002). Reelin function in neural stem cell biology. Proc Natl Acad Sci U S A 99: 4020-4025   DOI   ScienceOn
11 Kornack DR, Rakic P. (2001). The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A 98: 4752-4757   DOI   ScienceOn
12 Li WL, Yu SP, Ogle ME, Ding XS, Wei L. (2008). Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice. Dev Neurobiol 68: 1474-1486   DOI   ScienceOn
13 Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. (2006). VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371   DOI   ScienceOn
14 Marshall CA, Novitch BG, Goldman JE. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J Neurosci 25: 7289-7298   DOI   ScienceOn
15 Buss RR, Sun W, Oppenheim RW. (2006). Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci 29: 1-35   DOI   ScienceOn
16 Coskun V, Luskin MB. (2002). Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J Neurosci Res 69: 795-802   DOI   ScienceOn
17 Nam SC, Kim Y, Dryanovski D, et al. (2007). Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol 505: 190-208   DOI   ScienceOn
18 Nguyen-Ba-Charvet KT, Picard-Riera N, Tessier-Lavigne M, Baron-Van Evercooren A, Sotelo C, Chedotal A. (2004). Multiple roles for slits in the control of cell migration in the rostral migratory stream. J Neurosci 24: 1497-1506   DOI   ScienceOn
19 Bovetti S, Bovolin P, Perroteau I, Puche AC. (2007). Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur J Neurosci 25: 2021-2033   DOI   ScienceOn
20 Boutin C, Schmitz B, Cremer H, Diestel S. (2009). NCAM expression induces neurogenesis in vivo. Eur J Neurosci 30: 1209-1218   DOI   ScienceOn
21 Murase S, Cho C, White JM, Horwitz AF. (2008). ADAM2 promotes migration of neuroblasts in the rostral migratory stream to the olfactory bulb. Eur J Neurosci 27: 1585-1595   DOI   ScienceOn
22 Miragall F, Albiez P, Bartels H, de Vries U, Dermietzel R. (1997). 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 287: 243-253   DOI   ScienceOn
23 Mizrahi A. (2007). Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10: 444-452   DOI
24 Mouret A, Gheusi G, Gabellec MM, de Chaumont F, Olivo-Marin JC, Lledo PM. (2008). Learning and survival of newly generated neurons: when time matters. J Neurosci 28: 11511-11516   DOI   ScienceOn
25 Bolteus AJ, Bordey A. (2004). GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24: 7623-7631   DOI   ScienceOn
26 Beard A, Parent A. (2004). Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151: 159-168   DOI
27 Mandairon N, Sacquet J, Jourdan F, Didier A. (2006). Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation. Neuroscience 141: 443-451   DOI   ScienceOn
28 Marins M, Xavier AL, Viana NB, Fortes FS, FrOes MM, Menezes JR. (2009). Gap junctions are involved in cell migration in the early postnatal subventricular zone. Dev Neurobiol 69: 715-730   DOI   ScienceOn
29 Mason HA, Ito S, Corfas G. (2001). Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J Neurosci 21: 7654-7663
30 Blake SM, Strasser V, Andrade N, et al. (2008). Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J 27: 3069-3080   DOI   ScienceOn
31 Andrade N, Komnenovic V, Blake SM, et al. (2007). 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 104: 8508-8513   DOI   ScienceOn
32 Angot E, Loulier K, Nguyen-Ba-Charvet KT, Gadeau AP, Ruat M, Traiffort E. (2008). Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 26: 2311-2320   DOI   ScienceOn
33 Balenci L, Saoudi Y, Grunwald D, et al. (2007). IQGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci 27: 4716-4724   DOI   ScienceOn
34 Mackay-Sima A, Chuahb MI. (2000). Neurotrophic factors in the primary olfactory pathway. Prog Neurobiol 62: 527-559   DOI   ScienceOn
35 Merkle FT, Mirzadeh Z, Alvarez-Buylla A. (2007). Mosaic organization of neural stem cells in the adult brain. Science 317: 381-384   DOI   ScienceOn
36 Lois C, Alvarez-Buylla A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148   DOI
37 Lois C, García-Verdugo JM, Alvarez-Buylla A. (1996). Chain migration of neuronal precursors. Science 271: 978-981   DOI   ScienceOn
38 Maina F, Klein R. (1999). Hepatocyte growth factor, a versatile signal for developing neurons. Nat Neurosci 2: 213-217   DOI   ScienceOn
39 Mandairon N, Jourdan F, Didier A. (2003). Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119: 507-516   DOI   ScienceOn
40 Balordi F, Fishell G. (2007). Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons. J Neurosci 27: 5936-5947   DOI   ScienceOn
41 Battista D, Rutishauser U. (2010). Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues. J Neurosci 30: 3995-4003   DOI   ScienceOn
42 Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A. (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25: 6997-7003   DOI   ScienceOn
43 Law AK, Pencea V, Buck CR, Luskin MB. (1999). Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes. Dev Biol 216: 622-634   DOI   ScienceOn
44 Lee SR, Kim HY, Rogowska J, et al. (2006). Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26: 3491-3495   DOI   ScienceOn
45 Liu G, Rao Y. (2003). Neuronal migration from the forebrain to the olfactory bulb requires a new attractant persistent in the olfactory bulb. J Neurosci 23: 6651-6659
46 Zhang SC. (2001). Defining glial cells during CNS development. Nat Rev Neurosci 2: 840-843   DOI   ScienceOn
47 Zigova T, Pencea V, Betarbet R, et al. (1998). Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant 7: 137-156   DOI   ScienceOn
48 Liu Z, Martin LJ. (2003). Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J Comp Neurol 459: 368-391   DOI   ScienceOn
49 Lledo PM, Merkle FT, Alvarez-Buylla A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31: 392-400   DOI   ScienceOn
50 Wittko IM, Schanzer A, Kuzmichev A, et al. (2009). VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neurosci 29: 8704-8714   DOI   ScienceOn
51 Yamaguchi M, Mori K. (2005). 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 102: 9697-9702   DOI   ScienceOn
52 Yamashita T, Ninomiya M, Hernández Acosta P, et al. (2006). Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26: 6627-6636   DOI   ScienceOn
53 Whitman MC, Fan W, Rela L, Rodriguez-Gil DJ, Greer CA. (2009). Blood vessels form a migratory scaffold in the rostral migratory stream. J Comp Neurol 516: 94-104   DOI   ScienceOn
54 Kohwi M, Petryniak MA, Long JE, et al. (2007). A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27: 6878-6891   DOI   ScienceOn
55 Kaneko N, Marin O, Koike M, et al. (2010). New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron 67: 213-223.   DOI   ScienceOn
56 Kessenbrock K, Plaks V, Werb Z. (2010). Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141: 52-67   DOI   ScienceOn
57 Yang H, Jensen P, Goldowitz D. (2002). The community effect and Purkinje cell migration in the cerebellar cortex: analysis of scrambler chimeric mice. J Neurosci 22: 464-470
58 Waclaw RR, Wang B, Pei Z, Ehrman LA, Campbell K. (2009). Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63: 451-465   DOI   ScienceOn
59 Whitman MC, Greer CA. (2009). Adult neurogenesis and the olfactory system. Prog Neurobiol 89: 162-175   DOI   ScienceOn
60 Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG. (2002). Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16: 1681-1689   DOI   ScienceOn
61 Sun W, Funakoshi H, Nakamura T. (2002b). Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. J Neurosci 22: 6537-6548
62 Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A. (1999). Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci 19: 2171-2180
63 Hurtado-Chong A, Yusta-Boyo MJ, Vergano-Vera E, Bulfone A, de Pablo F, Vicario-AbejOn C. (2009). IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci 30: 742-755   DOI   ScienceOn
64 Soria JM, Taglialatela P, Gil-Perotin S, et al. (2004). Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J Neurosci 24: 11171-11181   DOI   ScienceOn
65 Staquicini FI, Dias-Neto E, Li J, et al. (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: 2903-2908   DOI   ScienceOn
66 Sun W, Funakoshi H, Nakamura T. (2002a). 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 103: 36-48   DOI
67 Sawamoto K, Wichterle H, Gonzalez-Perez O, et al. (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311: 629-632   DOI
68 Jablonska B, Aguirre A, Raymond M, et al. (2010). Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 13: 541-550   DOI   ScienceOn
69 Jankovski A, Garcia C, Soriano E, Sotelo C. (1998). Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 10: 3853-3868   DOI   ScienceOn
70 Hack MA, Saghatelyan A, de Chevigny A, et al. (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8: 865-872   DOI   ScienceOn
71 Simo S, Pujadas L, Segura MF, et al. (2007). Reelin induces the detachment of postnatal subventricular zone cells and the expression of the Egr-1 through Erk1/2 activation. Cereb Cortex 17: 294-303   DOI
72 Saino-Saito S, Cave JW, Akiba Y, (2007). ER81 and CaMKIV identify anatomically and phenotypically defined subsets of mouse olfactory bulb interneurons. J Comp Neurol 502: 485-496   DOI   ScienceOn
73 Hatten ME. (1999). Central nervous system neuronal migration. Annu Rev Neurosci 22: 511-539   DOI   ScienceOn
74 Hu H, Tomasiewicz H, Magnuson T, Rutishauser U. (1996). The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16: 735-743   DOI   ScienceOn
75 Gotts JE, Chesselet MF. (2005). Migration and fate of newly born cells after focal cortical ischemia in adult rats. J Neurosci Res 80: 160-171   DOI   ScienceOn
76 Alonso M, Viollet C, Gabellec MM, Meas-Yedid V, Olivo-Marin JC, Lledo PM. (2006). Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci 26: 10508-10513   DOI   ScienceOn
77 Saghatelyan A, de Chevigny A, Schachner M, Lledo PM. (2004). Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci 7: 347-356   DOI   ScienceOn
78 Gritti A, Bonfanti L, Doetsch F, et al. (2002). Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 22: 437-445
79 Grubb MS, Nissant A, Murray K, Lledo PM. (2008). Functional maturation of the first synapse in olfaction: development and adult neurogenesis. J Neurosci 28: 2919-2932   DOI   ScienceOn
80 Hack I, Bancila M, Loulier K, Carroll P, Cremer H. (2002). Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci 5: 939-945   DOI   ScienceOn
81 Russo VC, Gluckman PD, Feldman EL, Werther GA. (2005). The insulin-like growth factor system and its pleiotropic functions in brain. Endocr Rev 26: 916-943   DOI   ScienceOn
82 Petreanu L, Alvarez-Buylla A. (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113
83 Gascon E, Vutskits L, Jenny B, Durbec P, Kiss JZ. (2007). PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development 134: 1181-1190   DOI   ScienceOn
84 Giachino C, Taylor V. (2009). 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 30: 9-24   DOI   ScienceOn
85 Emsley JG, Hagg T. (2003). alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp Neurol 183: 273-285   DOI   ScienceOn
86 Eom TY, Li J, Anton ES. (2010). Going tubular in the rostral migratory stream: neurons remodel astrocyte tubes to promote directional migration in the adult brain. Neuron 67: 173-175   DOI   ScienceOn
87 Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S. (2008). Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci 28: 5901-5909   DOI   ScienceOn
88 Rochefort C, Gheusi G, Vincent JD, Lledo PM. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22: 2679-2689
89 Pencea V, Luskin MB. (2003). Prenatal development of the rodent rostral migratory stream. J Comp Neurol 463: 402-418   DOI   ScienceOn
90 Cremer H, Lange R, Christoph A, et al. (1994). Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367: 455-459   DOI   ScienceOn
91 Curtis MA, Kam M, Nannmark U, et al. (2007). Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249   DOI   ScienceOn
92 Doetsch F. (2003). A niche for adult neural stem cells. Curr Opin Genet Dev 13: 543-550   DOI   ScienceOn
93 Cayre M, Bancila M, Virard I, Borges A, Durbec P. (2006). Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain. Mol Cell Neurosci 31: 748-758   DOI   ScienceOn
94 Powell EM, Mars WM, Levitt P. (2001). Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30: 79-89   DOI   ScienceOn
95 Ono K, Takebayashi H, Ikenaka K. (2009). Olig2 transcription factor in the developing and injured forebrain; cell lineage and glial development. Mol Cells 27: 397-401   DOI   ScienceOn
96 Chiaramello S, Dalmasso G, Bezin L, et al. (2007). BDNF/TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci 26: 1780-1790   DOI   ScienceOn
97 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: 1091-1097   DOI   ScienceOn
98 Panzanelli P, Bardy C, Nissant A, et al. (2009). Early synapse formation in developing interneurons of the adult olfactory bulb. J Neurosci 29: 15039-15052   DOI   ScienceOn
99 Pencea V, Bingaman KD, Freedman LJ, Luskin MB. (2001). Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172: 1-16   DOI   ScienceOn
100 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: 3568-3579
101 Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H. (2000). Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20: 1446-1457