The role of Robo3 in the development of cortical interneurons

Cerebral Cortex

Volumn 19, Issue SUPPL. 1, 2009, Pages

  Barber, Melissa ^a   Di Meglio, Thomas ^b,c   Andrews, William D ^a   Hernández Miranda, Luis R ^a   Murakami, Fujio ^d   Chédotal, Alain ^b,c   Parnavelas, John G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE LA VISION   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

Interneuron; Morphology; Robo

Indexed keywords

MEMBRANE PROTEIN; NERVE PROTEIN; ROBO3 PROTEIN, MOUSE;

ANIMAL; ARTICLE; BRAIN CORTEX; CELL DIFFERENTIATION; CYTOLOGY; FOREBRAIN; INTERNEURON; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CEREBRAL CORTEX; INTERNEURONS; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; PROSENCEPHALON; SIGNAL TRANSDUCTION;

EID: 69449088024     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp041     Document Type: Article

References (65)

1. Alcantara S, Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E. 1998. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci. 18:7779-7799. (Pubitemid 28441019)
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 278:474-476. (Pubitemid 27454433)
3. Andrews W, Liapi A, Plachez C, Camurri L, Zhang J, Mori S, Murakami F, Parnavelas JG, Sundaresan V, Richards LJ. 2006. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development. 133:2243-2252. (Pubitemid 43986134)
4. Andrews WD, Barber M, Parnavelas JG. 2007. Slit-Robo interactions during cortical development. J Anat. 211:188-198. (Pubitemid 47278551)
5. Andrews W, Barber M, Hernandez-Miranda LR, Xian J, Rakic S, Sundaresan V, Rabbitts TH, Pannell R, Rabbitts P, Thompson H, et al. 2008. The role of Slit-Robo signalling in the generation, migration and morphological differentiation of cortical interneruons. Dev Biol. 313:648-658.
6. Anitha A, Nakamura K, Yamada K, Suda S, Thanseem I, Tsujii M, Iwayama Y, Hattori E, Toyota T, Miyachi T, et al. 2008. Genetic analyses of roundabout (ROBO) axon guidance receptors in autism. Am J Med Genet B Neuropsychiatr Genet. 147:1019-1027.
7. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M. 2002. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron. 33:233-248. (Pubitemid 34127756)
8. Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A. 2005. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci. 8:1002-1012. (Pubitemid 41061510)
9. Camurri L, Mambetisaeva E, Sundaresan V. 2004. Rig-1 a new member of Robo family genes exhibits distinct pattern of expression during mouse development. Gene Expr Patterns. 4:99-103. (Pubitemid 37498300)
10. Camurri L, Mambetisaeva E, Davies D, Parnavelas J, Sundaresan V, Andrews W. 2005. Evidence for the existence of two Robo3 isoforms with divergent biochemical properties. Mol Cell Neurosci. 30:485-493. (Pubitemid 41721167)
11. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci. 8:1059-1068. (Pubitemid 41061517)
12. D'Arcangelo G, Miao CG, Chen S-C, Soares HD, Morgan JI, Curran T. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:719-723.
13. Derer P, Derer M. 1990. Cajal-Retzius cell ontogenesis and death in mouse brain, visualised with horseradish peroxidise and electron microscopy. Neuroscience. 36:839-856. (Pubitemid 20282199)
14. Di Cristo G. 2007. Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders. Clin Genet. 72:1-8. (Pubitemid 47010140)
15. Edmunds SM, Parnavelas JG. 1982. Retzius-Cajal cells: an ultrastructural study in the developing visual cortex of the rat. J Neurocytol. 11:427-446. (Pubitemid 12114617)
16. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marin O. 2004. Short-and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron. 44:251-261.
17. Frotscher M. 1997. Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res. 290:315-322. (Pubitemid 27470064)
18. Garcia-Moreno F, Lopez-Mascaraque L, De Carlos JA. 2007. Origins and migratory routes of murine Cajal-Retzius cells. J Comp Neurol. 500:419-432.
19. Hu H. 1999. Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron. 23:703-711. (Pubitemid 29411560)
20. Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R. 2002. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of angiogenesis. Genomics. 79:547-552. (Pubitemid 34274296)
21. Jen JC, Chan WM, Bosley TM, Wan J, Carr JR, Rub U, Shattuck D, Salamon G, Kudo LC, Ou J, et al. 2004. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science. 304:1509-1513. (Pubitemid 38720933)
22. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G. 1998. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 23:205-215. (Pubitemid 28073044)
23. Lavdas A, Grigoriou M, Pachnis V, Parnavelas JG. 1999. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci. 19:7881-7888. (Pubitemid 30225786)
24. Lin L, Isacson O. 2006. Axonal growth regulation of fetal and embryonic stem cell derived dopaminergic neurons by Netrin-1 and Slits. Stem Cells. 24:2504-2513. (Pubitemid 44674311)
25. Liu Z, Patel K, Schmidt H, Andrews W, Pini A, Sundaresan V. 2004. Extracellular Ig domains 1 and 2 of Robo are important for ligand (Slit) binding. Mol Cell Neurosci. 26:232-240. (Pubitemid 38786461)
26. Lopez-Bendito G, Flames N, Ma L, Fouquet C, Di Meglio T, Chedotal A, Tessier-Lavigne M, Marin O. 2007. Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. J Neurosci. 27:3395-3407. (Pubitemid 46515124)
27. Lopez-Bendito G, Sanchez-Alcaniz JA, Pla R, Borrell V, Pico E, Valdeolmillos M, Marin O. 2008. Chemokine signalling controls intracortical migration and final distribution of GABAergic interneurons. J Neurosci. 28:1613-1624. (Pubitemid 351287037)
28. Ma L, Tessier-Lavigne M. 2007. Dual branch-promoting and branchrepelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J Neurosci. 27:6843-6851. (Pubitemid 46983437)
29. Mallet N, Ballion B, Le Moine C, Gonon F. 2006. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci. 26:3875-3884.
30. Mambetisaeva ET, Andrews W, Camurri L, Annan A, Sundaresan V. 2005. Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interactions is required for midline crossing in vertebrate spinal cord. Dev Dyn. 233:41-51. (Pubitemid 40548022)
31. Marin O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL. 2001. Sorting of striatal and cortical interneurons regulated by semaphoring- neuropilin interactions. Science. 293:872-875. (Pubitemid 32743978)
32. Marin O, Plump AS, Flames N, Sanchez-Camacho C, Tessier-Lavigne M, Rubenstein JL. 2003. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development. 130:1889-1901. (Pubitemid 36575915)
33. Marin O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu Rev Neurosci. 26:441-483. (Pubitemid 37064941)
34. 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. 442:130-155.
35. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C, Tessier-Lavigne M, Chedotal A. 2004. The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebella neurons and axons. Neuron. 43:69-79. (Pubitemid 38952820)
36. Marin-Padilla M. 1998. Cajal-Retzius cells and the development of the neocortex. Trends Neurosci. 21:64-71. (Pubitemid 28078907)
37. Metin C, Baudoin JP, Rakic S, Parnavelas JG. 2006. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci. 23:894-900. (Pubitemid 43344684)
38. Meyer G, Soria JM, Martinez-Galan JR, Martin-Clemente B, Fairen A. 1998. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol. 397:493-518. (Pubitemid 28354324)
39. Meyer G, Goffinet AM, Fairen A. 1999. What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex. 9:765-775. (Pubitemid 30004589)
40. Miranda DM, Wigg K, Feng Y, Sandor P, Barr CL. 2008. Association study between Gilles de la Tourette Syndrome and two genes in the Robo-Slit pathway located in the chromosome 11q24 linked/associated region. Am J Med Genet B Neuropsychiatr Genet. 147:68-72.
41. Nakajima K. 2007. Control of tangential/non-radial migration of neurons in the developing cerebral cortex. Neurochem Int. 51:121-131. (Pubitemid 47176706)
42. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamotot H, Mikoshiba K. 1995. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron. 14:899-912.
43. Ozdinler PH, Erzurumlu RS. 2002. Slit2, a branching-arborization factor for sensory axons in the Mammalian CNS. J Neurosci. 22:4540-4549. (Pubitemid 37465670)
44. Park KW, Morrison CM, Sorensen LK, Jones CA, Rao Y, Chien CB, Wu JY, Urness LD, Li DY. 2003. Robo4 is a vascular specific receptor that inhibits endothelial migration. Dev Biol. 261:251-267. (Pubitemid 36993830)
45. Parnavelas JG, Edmunds SM. 1983. Further evidence that Cajal-Retzius cells transform to nonpyramidal neurons in the developing rat visual cortex. J Neurocytol. 12:863-871. (Pubitemid 13022012)
46. Plachez C, Andrews W, Liapi A, Knoell B, Drescher U, Mankoo B, Zhe L, Mambetisaeva E, Annan A, Bannister L, et al. 2008. Robos are required for the correct targeting of retinal ganglion cell axons in the visual pathway of the brain. Mol Cell Neurosci. 37:719-730.
47. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P. 2003. Genetic disruption of cortical interneuron development causes region and GABA cell type-specific deficits, epilepsy, and behavioural dysfunction. J Neurosci. 23:622-631. (Pubitemid 36139561)
48. Sabatier C, Plump AS, Le MA, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M. 2004. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell. 117:157-169. (Pubitemid 38496237)
49. Sang Q, Wu J, Rao Y, Hsueh YP, Tan SS. 2002. Slit promotes branching and elongation of neuritis of interneurons but not projection neurons from the developing telencephalon. Mol Cell Neurosci. 21:250-265. (Pubitemid 35339391)
50. Sang Q, Tan SS. 2003. Contact-associated neurite outgrowth and branching of immature cortical interneurons. Cereb Cortex. 13:677-683. (Pubitemid 36613177)
51. Shu T, Richards LJ. 2001. Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci. 21:2749-2758. (Pubitemid 32298216)
52. Shu T, Sundaresan V, McCarthy MM, Richards LJ. 2003. Slit2 guides both precrossing and postcrossing callosal axons at the midline in vivo. J Neurosci. 23:8176-8184. (Pubitemid 37082472)
53. Siegenthaler JA, Miller MW. 2008. Generation of Cajal-Retzius neurons in mouse forebrain is regulated by transforming growth factor beta-Fox signalling pathways. Dev Biol. 313:35-46. (Pubitemid 350298300)
54. Shinozaki K, Miyagi T, Yoshida M, Miyata T, Ogawa M, Aizawa S, Suda Y. 2002. Absence of Cajal-Retzius cells and subplate neurons associated with defects of tangential cell migration from ganglionic eminence in Emx1/2double mutant cerebral cortex. Development. 129:3479-3492.
55. Sundaresan V, Mambetisaeva E, Andrews W, Annan A, Knoll B, Tear G, Bannister L. 2004. Dynamic expression patterns of Robo (Robo1 and Robo2) in the developing murine central nervous system. J Comp Neurol. 468:467-481. (Pubitemid 38036689)
56. Super H, Del Rio JA, Martinez A, Perez-Sust P, Soriano E. 2000. Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb Cortex. 10:602-613. (Pubitemid 30387839)
57. Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa R, Migishima R, Yokoyama M, Nakanishi S, Tanabe Y. 2004. Generation of reelin positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci. 24:2286-2295. (Pubitemid 38314560)
58. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci. 4:496-505. (Pubitemid 37280170)
59. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS, Henzel W, Tessier-Lavigne M. 1999. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell. 96:771-784. (Pubitemid 29165081)
60. Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M. 2002. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron. 33:47-61. (Pubitemid 34088178)
61. Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, Rao Y. 1999. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature. 400:331-336. (Pubitemid 29344191)
62. Yoshida M, Assimacopoulos S, Jones KR, Grove EA. 2006. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development. 133:537-545. (Pubitemid 43273839)
63. Yuan SS, Cox LA, Dasika GK, Lee EY. 1999. Cloning and functional studies of a novel gene aberrantly expressed in RB-deficient embryos. Dev Biol. 207:62-75. (Pubitemid 29117801)
64. Yuan W, Zhou L, Chen JH, Wu JY, Rao Y, Ornitz DM. 1999. Themouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol. 212:290-306. (Pubitemid 29387937)
65. Zhu Y, Li H, Zhou L, Wu JY, Rao Y. 1999. Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron. 23:473-485. (Pubitemid 29359919)