The protocadherin gene Celsr3 is required for interneuron migration in the mouse forebrain

Molecular and Cellular Biology

Volumn 29, Issue 11, 2009, Pages 3045-3061

  Ying, Guoxin ^a   Wu, Sen ^b   Hou, Ruiqing ^c   Huang, Wei ^a   Capecchi, Mario R ^a,b   Wu, Qiang ^a,c  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Shanghai Jiao Tong University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CALBINDIN; CALRETININ; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GREEN FLUORESCENT PROTEIN; NEU DIFFERENTIATION FACTOR; PROTOCADHERIN CELSR 3; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CELSR3 PROTEIN, MOUSE; ENHANCED GREEN FLUORESCENT PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 4;

ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL MIGRATION; CONTROLLED STUDY; FOREBRAIN; GENE DELETION; GENETIC VARIABILITY; GERMINAL CENTER; INTERNEURON; MOUSE; NEOCORTEX; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ALLELE; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; METABOLISM; MUTATION; NEOSTRIATUM; PRENATAL DEVELOPMENT; REPORTER GENE; TIME;

MAMMALIA; MURINAE; MUS;

ALLELES; ANIMALS; CADHERINS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCK-IN TECHNIQUES; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; INTERNEURONS; MICE; MUTATION; NEOCORTEX; NEOSTRIATUM; NEUREGULIN-1; PROSENCEPHALON; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CELL SURFACE; TIME FACTORS;

EID: 66349090461     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00011-09     Document Type: Article

References (66)

1. Alcántara, S., E. Pozas, C. F. Ibañez, and E. Soriano. 2006. BDNF-modulated spatial organization of Cajal-Retzius and GABAergic neurons in the marginal zone plays a role in the development of cortical organization. Cereb. Cortex 16:487-499.
2. Anderson, S. A., D. D. Eisenstat, L. Shi, and J. L. Rubenstein. 1997. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476. (Pubitemid 27454433)
3. Anderson, S. A., O. Marín, C. Horn, K. Jennings, and J. L. Rubenstein. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363. (Pubitemid 32184376)
4. Ang, E. S., Jr., T. F. Haydar, V. Gluncic, and P. Rakic. 2003. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J. Neurosci. 23:5805-5815. (Pubitemid 36807860)
5. Ayala, R., T. Shu, and L. H. Tsai. 2007. Trekking across the brain: the journey of neuronal migration. Cell 128:29-43. (Pubitemid 46055273)
6. Benson, D. L., D. R. Colman, and G. W. Huntley. 2001. Molecules, maps and synapse specificity. Nat. Rev. Neurosci. 2:899-909.
7. Butt, S. J., M. Fuccillo, S. Nery, S. Noctor, A. Kriegstein, J. G. Corbin, and G. Fishell. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591-604. (Pubitemid 41654681)
8. Carney, R. S., T. B. Alfonso, D. Cohen, H. Dai, S. Nery, B. Stoica, J. Slotkin, B. S. Bregman, G. Fishell, and J. G. Corbin. 2006. Cell migration along the lateral cortical stream to the developing basal telencephalic limbic system. J. Neurosci. 26:11562-11574. (Pubitemid 44772127)
9. Corbin, J. G., N. Gaiano, R. P. Machold, A. Langston, and G. Fishell. 2000. The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development 127:5007-5020.
10. Corbin, J. G., S. Nery, and G. Fishell. 2001. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat. Neurosci. 4(Suppl.):1177-1182.
11. Curtin, J. A., E. Quint, V. Tsipouri, R. M. Arkell, B. Cattanach, A. J. Copp, D. J. Henderson, N. Spurr, P. Stanier, E. M. Fisher, P. M. Nolan, K. P. Steel, S. D. Brown, I. C. Gray, and J. N. Murdoch. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13:1129-1133.
12. Del Río, J. A., A. Martínez, C. Auladell, and E. Soriano. 2000. Developmental history of the subplate and developing white matter in the murine neocortex. Neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb. Cortex 10:784-801.
13. Flames, N., J. E. Long, A. N. Garratt, T. M. Fischer, M. Gassmann, C. Birchmeier, C. Lai, J. L. Rubenstein, and O. Marín. 2004. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44:251-261. (Pubitemid 39346250)
14. Force, A., M. Lynch, F. B. Pickett, A. Amores, Y. L. Yan, and J. Postlethwait. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545. (Pubitemid 29177561)
15. Formstone, C. J., and P. F. Little. 2001. The flamingo-related mouse Celsr family (Celsr1-3) genes exhibit distinct patterns of expression during embryonic development. Mech. Dev. 109:91-94.
16. Formstone, C. J., and I. Mason. 2005. Combinatorial activity of Flamingo proteins directs convergence and extension within the early zebrafish embryo via the planar cell polarity pathway. Dev. Biol. 282:320-335.
17. Friocourt, G., J. S. Liu, M. Antypa, S. Rakić, C. A. Walsh, and J. G. Parnavelas. 2007. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J. Neurosci. 27:3875-3883. (Pubitemid 46557665)
18. Gao, F. B., M. Kohwi, J. E. Brenman, L. Y. Jan, and Y. N. Jan. 2000. Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 28:91-101.
19. Gonchar, Y., and A. Burkhalter. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7:347-358. (Pubitemid 27231311)
20. Hadjantonakis, A. K., W. J. Sheward, A. J. Harmar, L. de Galan, J. M. Hoovers, and P. F. Little. 1997. Celsr1, a neural-specific gene encoding an unusual seven-pass transmembrane receptor, maps to mouse chromosome 15 and human chromosome 22qter. Genomics 45:97-104.
21. Halbleib, J. M., and W. J. Nelson. 2006. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20:3199-3214. (Pubitemid 44904842)
22. Hammond, V., E. So, J. Gunnersen, H. Valcanis, M. Kalloniatis, and S. S. Tan. 2006. Layer positioning of late-born cortical interneurons is dependent on Reelin but not p35 signaling. J. Neurosci. 26:1646-1655. (Pubitemid 43237035)
23. Kohwi, M., M. A. Petryniak, J. E. Long, M. Ekker, K. Obata, Y. Yanagawa, J. L. Rubenstein, and A. Alvarez-Buylla. 2007. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J. Neurosci. 27:6878-6891.
24. Lavdas, A. A., M. Grigoriou, V. Pachnis, and J. G. Parnavelas. 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)
25. López-Bendito, G., A. Cautinat, J. A. Sánchez, F. Bielle, N. Flames, A. N. Garratt, D. A. Talmage, L. W. Role, P. Charnay, O. Marín, and S. Garel. 2006. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125:127-142.
26. López-Bendito, G., K. Sturgess, F. Erdélyi, G. Szabó, Z. Molnár, and O. Paulsen. 2004. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb. Cortex 14:1122-1133. (Pubitemid 39258167)
27. Marín, O., S. A. Anderson, and J. L. Rubenstein. 2000. Origin and molecular specification of striatal interneurons. J. Neurosci. 20:6063-6076. (Pubitemid 30658400)
28. Marín, O., and J. L. Rubenstein. 2003. Cell migration in the forebrain. Annu. Rev. Neurosci. 26:441-483.
29. Marín, O., A. Yaron, A. Bagri, M. Tessier-Lavigne, and J. L. Rubenstein. 2001. Sorting of striatal and cortical interneurons regulated by semaphorinneuropilin interactions. Science 293:872-875. (Pubitemid 32743978)
30. Mei, L., and W. C. Xiong. 2008. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9:437-452.
31. Molnár, Z., and A. B. Butler. 2002. The corticostriatal junction: a crucial region for forebrain development and evolution. Bioessays 24:530-541. (Pubitemid 34629873)
32. Nery, S., G. Fishell, and J. G. Corbin. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5:1279-1287.
33. Pla, R., V. Borrell, N. Flames, and O. Marín. 2006. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26:6924-6934. (Pubitemid 44309860)
34. Pleasure, S. J., S. Anderson, R. Hevner, A. Bagri, O. Marín, D. H. Lowenstein, and J. L. Rubenstein. 2000. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740. (Pubitemid 32038067)
35. Polleux, F., K. L. Whitford, P. A. Dijkhuizen, T. Vitalis, and A. Ghosh. 2002. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129:3147-3160. (Pubitemid 34874289)
36. Poluch, S., and S. L. Juliano. 2007. A normal radial glial scaffold is necessary for migration of interneurons during neocortical development. Glia 55:822-830. (Pubitemid 46787193)
37. Price, S. R., N. V. De Marco Garcia, B. Ranscht, and T. M. Jessell. 2002. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205-216. (Pubitemid 34518259)
38. Shima, Y., N. G. Copeland, D. J. Gilbert, N. A. Jenkins, O. Chisaka, M. Takeichi, and T. Uemura. 2002. Differential expression of the seven-pass transmembrane cadherin genes Celsr1-3 and distribution of the Celsr2 protein during mouse development. Dev. Dyn. 223:321-332.
39. Shima, Y., S. Y. Kawaguchi, K. Kosaka, M. Nakayama, M. Hoshino, Y. Nabeshima, T. Hirano, and T. Uemura. 2007. Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat. Neurosci. 10:963-969.
40. Shima, Y., M. Kengaku, T. Hirano, M. Takeichi, and T. Uemura. 2004. Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev. Cell 7:205-216. (Pubitemid 39145025)
41. Stenman, J., H. Toresson, and K. Campbell. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23:167-174. (Pubitemid 36050416)
42. Takeichi, M. 2007. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8:11-20.
43. Tamamaki, N., K. Fujimori, Y. Nojyo, T. Kaneko, and R. Takauji. 2003. Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J. Comp. Neurol. 455:238-248.
44. Tamamaki, N., K. Nakamura, and T. Kaneko. 2001. Cell migration from the corticostriatal angle to the basal telencephalon in rat embryos. Neuroreport 12:775-780. (Pubitemid 32222716)
45. Tanaka, D., Y. Nakaya, Y. Yanagawa, K. Obata, and F. Murakami. 2003. Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development 130:5803-5813. (Pubitemid 37540853)
46. Taniguchi, H., D. Kawauchi, K. Nishida, and F. Murakami. 2006. Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain. Development 133:1923-1931. (Pubitemid 43881258)
47. Tissir, F., I. Bar, Y. Jossin, O. De Backer, and A. M. Goffinet. 2005. Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8:451-457.
48. Tissir, F., O. De-Backer, A. M. Goffinet, and C. Lambert de Rouvroit. 2002. Developmental expression profiles of Celsr (Flamingo) genes in the mouse. Mech. Dev. 112:157-160.
49. Tissir, F., and A. M. Goffinet. 2006. Expression of planar cell polarity genes during development of the mouse CNS. Eur. J. Neurosci. 23:597-607.
50. Tuttle, R., Y. Nakagawa, J. E. Johnson, and D. D. O'Leary. 1999. Defects in thalamocortical axon pathfinding correlate with altered cell domains in Mash-1-deficient mice. Development 126:1903-1916.
51. Usui, T., Y. Shima, Y. Shimada, S. Hirano, R. W. Burgess, T. L. Schwarz, M. Takeichi, and T. Uemura. 1999. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98:585-595. (Pubitemid 29418950)
52. Valcanis, H., and S. S. Tan. 2003. Layer specification of transplanted interneurons in developing mouse neocortex. J. Neurosci. 23:5113-5122. (Pubitemid 36793239)
53. Waclaw, R. R., Z. J. Allen II, S. M. Bell, F. Erdélyi, G. Szabó, S. S. Potter, and K. Campbell. 2006. The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49:503-516.
54. Wada, H., H. Tanaka, S. Nakayama, M. Iwasaki, and H. Okamoto. 2006. Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 133:4749-4759.
55. Wang, X., J. A. Weiner, S. Levi, A. M. Craig, A. Bradley, and J. R. Sanes. 2002. Gamma protocadherins are required for survival of spinal interneurons. Neuron 36:843-854. (Pubitemid 35447856)
56. Wichterle, H., J. M. Garcia-Verdugo, D. G. Herrera, and A. Alvarez-Buylla. 1999. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2:461-466.
57. Wichterle, H., D. H. Turnbull, S. Nery, G. Fishell, and A. Alvarez-Buylla. 2001. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
58. Wonders, C. P., and S. A. Anderson. 2006. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7:687-696.
59. Wonders, C. P., L. Taylor, J. Welagen, I. C. Mbata, J. Z. Xiang, and S. A. Anderson. 2008. A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev. Biol. 314:127-136.
60. Wu, Q., and T. Maniatis. 2000. Large exons encoding multiple ectodomains are a characteristic feature of protocadherin genes. Proc. Natl. Acad. Sci. USA 97:3124-3129.
61. Wu, Q., and T. Maniatis. 1999. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97:779-790. (Pubitemid 29278051)
62. Wu, S., G. Ying, Q. Wu, and M. R. Capecchi. 2008. A protocol for constructing gene targeting vectors: generating knockout mice for the cadherin family and beyond. Nat. Protoc. 3:1056-1076.
63. Xu, Q., I. Cobos, E. De La Cruz, J. L. Rubenstein, and S. A. Anderson. 2004. Origins of cortical interneuron subtypes. J. Neurosci. 24:2612-2622. (Pubitemid 38380937)
64. Yagi, T., and M. Takeichi. 2000. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev. 14:1169-1180. (Pubitemid 30327498)
65. Zhou, L., I. Bar, Y. Achouri, K. Campbell, O. De Backer, J. M. Hebert, K. Jones, N. Kessaris, C. L. de Rouvroit, D. O'Leary, W. D. Richardson, A. M. Goffinet, and F. Tissir. 2008. Early forebrain wiring: genetic dissection using conditional Celsr3 mutant mice. Science 320:946-949.
66. Zou, C., W. Huang, G. Ying, and Q. Wu. 2007. Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires. Neuroscience 144:579-603.