Characterization of the netrin/RGMa receptor neogenin in neurogenic regions of the mouse and human adult forebrain

Journal of Comparative Neurology

Volumn 518, Issue 16, 2010, Pages 3237-3253

  Bradford, D ^a   Faull, R L M ^b   Curtis, M A ^b   Cooper, H M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

adult neurogenesis; neural migration; neural stem cell; rostral migratory stream; subventricular zone

Indexed keywords

NEOGENIN; NETRIN 1; REPULSIVE GUIDANCE MOLECULE A; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MEMBRANE PROTEIN; NERVE GROWTH FACTOR; NERVE PROTEIN; NETRIN RECEPTORS; NETRIN-1; RGMA PROTEIN, HUMAN; RGMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL POPULATION; CONTROLLED STUDY; EMBRYO; FEMALE; FOREBRAIN; HUMAN; HUMAN TISSUE; HYPOTHESIS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STEM CELL; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MIDDLE AGED; STEM CELL NICHE; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL MOVEMENT; FEMALE; GPI-LINKED PROTEINS; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MIDDLE AGED; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROGENESIS; PROSENCEPHALON; RECEPTORS, CELL SURFACE; STEM CELL NICHE; STEM CELLS; TUMOR SUPPRESSOR PROTEINS; YOUNG ADULT;

EID: 77954572294     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22397     Document Type: Article

References (69)

1. Alvarez-Buylla A, Garcia-Verdugo JM. 2002. Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
2. Arellano JI, DeFelipe J, Munoz A. 2002. PSA-NCAM immunore-activity in chandelier cell axon terminals of the human temporal cortex. Cereb Cortex 12:617-624.
3. Bae GU, Yang YJ, Jiang G, Hong M, Lee HJ, Tessier-Lavigne M, Kang JS, Krauss RS. 2009. Neogenin regulates skeletal myofiber size and focal adhesion kinase and extracellular signal-regulated kinase activities in vivo and in vitro. Mol Biol Cell 20:4920-4931.
4. Baker KA, Moore SW, Jarjour AA, Kennedy TE. 2006. When a diffusible axon guidance cue stops diffusing: roles for netrins in adhesion and morphogenesis. Curr Opin Neuro-biol 16:529-534.
5. 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.
6. Bernier PJ, Vinet J, Cossette M, Parent A. 2000. Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2. Neurosci Res 37: 67-78.
7. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Sudhof TC. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531.
8. Bradford D, Cole SJ, Cooper HM. 2009. Netrin-1: diversity in development. Int J Biochem Cell Biol 41:487-493.
9. Breton-Provencher V, Lemasson M, Peralta MR 3rd, Sagha-telyan A. 2009. Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29:15245-15257.
10. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascon S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner RF, Raineteau O, Gotz M. 2009. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12:1524-1533.
11. Brinks H, Conrad S, Vogt J, Oldekamp J, Sierra A, Deitinghoff L, Bechmann I, Alvarez-Bolado G, Heimrich B, Monnier PP, Mueller BK, Skutella T. 2004. The repulsive guidance molecule RGMa is involved in the formation of afferent connections in the dentate gyrus. J Neurosci 24:3862-3869.
12. Cai Y, Xiong K, Chu Y, Luo DW, Luo XG, Yuan XY, Struble RG, Clough RW, Spencer DD, Williamson A, Kordower JH, Patrylo PR, Yan XX. 2009. Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol 216:342-356.
13. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shupliakov O, Cassidy RM, Lindvall O, Frisen J. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12:259-267.
14. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. 2009. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12:399-408.
15. Cooper HM, Armes P, Britto J, Gad J, Wilks AF. 1995. Cloning of the mouse homologue of the deleted in colorectal cancer gene (mDCC) and its expression in the developing mouse embryo. Oncogene 11:2243-2254. (Pubitemid 26008400)
16. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wik-kelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243-1249.
17. De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Per-etto P, Fasolo A, Puche AC, Rossi F. 2007. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657-664.
18. de Vries M, Cooper HM. 2008. Emerging roles for neogenin and its ligands in CNS development. J Neurochem 106:1483-1492.
19. Debus E, Weber K, Osborn M, 1983. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25:193-203.
20. Dellarole A, Grilli M. 2008. Adult dorsal root ganglia sensory neurons express the early neuronal fate marker doublecor-tin. J Comp Neurol 511:318-328.
21. Dodd J, Morton SB, Karagogeos D, Yamamoto M, Jessell TM. 1988. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1:105-116.
22. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the sub-ventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
23. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
24. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. 2002. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-1034.
25. Fasolo A, Peretto P, Bonfanti L. 2002. Cell migration in the rostral migratory stream. Chem Senses 27:581-582.
26. Fitzgerald DP, Cole SJ, Hammond A, Seaman C, Cooper HM. 2006a. Characterization of neogenin-expressing neural progenitor populations and migrating neuroblasts in the embryonic mouse forebrain. Neuroscience 142:703-716.
27. Fitzgerald DP, Seaman C, Cooper HM. 2006b. Localization of neogenin protein during morphogenesis in the mouse embryo. Dev Dyn 235:1720-1725.
28. Fitzgerald DP, Bradford D, Cooper HM. 2007. Neogenin is expressed on neurogenic and gliogenic progenitors in the embryonic and adult central nervous system. Gene Expr Patterns 7:784-792.
29. Gad JM, Keeling SL, Wilks AF, Tan SS, Cooper HM. 1997. The expression patterns of guidance receptors, DCC and neo-genin, are spatially and temporally distinct throughout mouse embryogenesis. Dev Biol 192:258-273.
30. Gad JM, Keeling SL, Shu T, Richards LJ, Cooper HM. 2000. The spatial and temporal expression patterns of netrin receptors, DCC and neogenin, in the developing mouse retina. Exp Eye Res 70:711-722.
31. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. 1998. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neuro-biol 36:234-248.
32. Gritti A, Bonfanti L. 2007. Neuronal-glial interactions in central nervous system neurogenesis: the neural stem cell perspective. Neuron Glia Biol 3:309-323.
33. Hata K, Kaibuchi K, Inagaki S, Yamashita T. 2009. Unc5B associates with LARG to mediate the action of repulsive guidance molecule. J Cell Biol 184:737-750.
34. Hockfield S, McKay RD. 1985. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
35. Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H. 2008. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA 105:20994-20999.
36. Ji S, Kronenberg G, Balkaya M, Farber K, Gertz K, Kettenmann H, Endres M. 2009. Acute neuroprotection by pioglitazone after mild brain ischemia without effect on long-term outcome. Exp Neurol 216:321-328.
37. Kam M, Curtis MA, McGlashan SR, Connor B, Nannmark U, Faull RL. 2009. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 37:196-205.
38. Kang JS, Yi MJ, Zhang W, Feinleib JL, Cole F, Krauss RS. 2004. Netrins and neogenin promote myotube formation. J Cell Biol 167:493-504.
39. Kee N, Wilson N, de Vries M, Bradford D, Key B, Cooper HM. 2008. Neogenin and RGMa control neural tube closure and neuroepithelial morphology by regulating cell polarity. J Neurosci 28:12643-12653.
40. Keeling SL, Gad JM, Cooper HM. 1997. Mouse Neogenin, a DCC-like molecule, has four splice variants and is expressed widely in the adult mouse and during embryo-genesis. Oncogene 15:691-700.
41. Khodosevich K, Seeburg PH, Monyer H. 2009. Major signaling pathways in migrating neuroblasts. Front Mol Neurosci 2:7.
42. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M. 2001. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410:174-179.
43. 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.
44. Lledo PM, Saghatelyan A. 2005. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 28:248-254.
45. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. 1996. Chain migration of neuronal precursors. Science 271:978-981.
46. Louvi A, Artavanis-Tsakonas S. 2006. Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93-102.
47. Matsunaga E, Chedotal A. 2004. Repulsive guidance molecule/neogenin: a novel ligand-receptor system playing multiple roles in neural development. Dev Growth Differ 46:481-486.
48. Matsunaga E, Nakamura H, Chedotal A. 2006. Repulsive guidance molecule plays multiple roles in neuronal differentiation and axon guidance. J Neurosci 26:6082-6088.
49. Mawdsley DJ, Cooper HM, Hogan BM, Cody SH, Lieschke GJ, Heath JK. 2004. The netrin receptor neogenin is required for neural tube formation and somitogenesis in zebrafish. Dev Biol 269:302-315.
50. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317: 381-384.
51. Meyerhardt JA, Look AT, Bigner SH, Fearon ER. 1997. Identification and characterization of neogenin, a DCC-related gene. Oncogene 14:1129-1136.
52. Monnier PP, Sierra A, Macchi P, Deitinghoff L, Andersen JS, Mann M, Flad M, Hornberger MR, Stahl B, Bonhoeffer F, Mueller BK. 2002. RGM is a repulsive guidance molecule for retinal axons. Nature 419:392-395.
53. 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.
54. 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.
55. Niederkofler V, Salie R, Sigrist M, Arber S. 2004. Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system. J Neurosci 24:808-818.
56. Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM. 2009. Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12:728-730.
57. Oldekamp J, Kramer N, Alvarez-Bolado G, Skutella T. 2004. Expression pattern of the repulsive guidance molecules RGM A, B and C during mouse development. Gene Expr Patterns 4:283-288.
58. Pencea V, Bingaman KD, Freedman LJ, Luskin MB. 2001. Neu-rogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1-16.
59. Quiñones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. 2006. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494:415-434.
60. Rajagopalan S, Deitinghoff L, Davis D, Conrad S, Skutella T, Chedotal A, Mueller BK, Strittmatter SM. 2004. Neogenin mediates the action of repulsive guidance molecule. Nat Cell Biol 6:756-762.
61. Rajasekharan S, Kennedy TE. 2009. The netrin protein family. Genome Biol 10:239.
62. Sanai N, Tramontin AD, Quiñones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-744.
63. Schmidtmer J, Engelkamp D. 2004. Isolation and expression pattern of three mouse homologues of chick Rgm. Gene Expr Patterns 4:105-110.
64. Schubert W, Coskun V, Tahmina M, Rao MS, Luskin MB, Kap-rielian Z. 2000. Characterization and distribution of a new cell surface marker of neuronal precursors. Dev Neurosci 22:154-166.
65. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M. 1996. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
66. Srinivasan K, Strickland P, Valdes A, Shin GC, Hinck L. 2003. Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Dev Cell 4:371-382.
67. Wen Z, Zheng JQ. 2006. Directional guidance of nerve growth cones. Curr Opin Neurobiol 16:52-58.
68. Wilson NH, Key B. 2006. Neogenin interacts with RGMa and netrin-1 to guide axons within the embryonic vertebrate forebrain. Dev Biol 296:485-498.
69. Yamashita T, Mueller BK, Hata K. 2007. Neogenin and repulsive guidance molecule signaling in the central nervous system. Curr Opin Neurobiol 17:29-34.