Lrp12/Mig 13a reveals changing patterns of preplate neuronal polarity during corticogenesis that are absent in reeler mutant mice

Cerebral Cortex

Volumn 21, Issue 1, 2011, Pages 134-144

  Schneider, Stephanie ^a,b   Gulacsi, Alexandra ^a   Hatten, Mary E ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Corticocortical connections; Lrp12 Mig 13a; Neuronal polarity; Preplate development; Reeler

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CONTROLLED STUDY; EMBRYO; FEMALE; GENE SILENCING; IN SITU HYBRIDIZATION; MOUSE; NEOCORTEX; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BRAIN CORTEX; CELL DIFFERENTIATION; CELL MOTION; CELL STRAIN HEK293; CONGENITAL MALFORMATION; DISEASE MODEL; GENETICS; HUMAN; MALE; METABOLISM; MOUSE MUTANT; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM MALFORMATION; PATHOLOGY; TELENCEPHALON; TRANSGENIC MOUSE;

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LRP12 PROTEIN, HUMAN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL MOVEMENT; CELL POLARITY; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HEK293 CELLS; HUMANS; LDL-RECEPTOR RELATED PROTEIN 1; MALE; MICE; MICE, NEUROLOGIC MUTANTS; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NERVOUS SYSTEM MALFORMATIONS; NEUROGENESIS; SERINE ENDOPEPTIDASES; TELENCEPHALON;

EID: 78651337539     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq070     Document Type: Article

References (53)

1. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Ann Rev Neurosci. 17:185-218.
2. Arnaud L, Ballif BA, Forster E, Cooper JA. 2003. Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr Biol. 13:9-17.
3. Blelloch R, Newman C, Kimble J. 1999. Control of cell migration during Caenorhabditis elegans development. Curr Opin Cell Biol. 11:608-613.
4. Bock HH, Herz J. 2003. Reelin activates SRC family tyrosine kinases in neurons. Curr Biol. 13:18-26.
5. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 9:110-122.
6. Caviness VS, Jr. 1982. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 256:293-302.
7. Caviness VS, Jr., Rakic P. 1978. Mechanisms of cortical development: a view from mutations in mice. Ann Rev Neurosci. 1:297-326.
8. Caviness VS, Jr., Sidman RL. 1973. Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol. 148:141-151.
9. Chun JJ, Nakamura MJ, Shatz CJ. 1987. Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons. Nature. 325:617-620.
10. Crandall JE, Jacobson M, Kosik KS. 1986. Ontogenesis of microtubuleassociated protein 2 (MAP2) in embryonic mouse cortex. Brain Res. 393:127-133.
11. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:719-723.
12. D'Arcangelo G, Miao GG, Curran T. 1996. Detection of the reelin breakpoint in reeler mice. Brain Res. 39:234-236.
13. De Carlos JA, O'Leary DD. 1992. Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci. 12:1194-1211.
14. Del Rio JA, Martinez A, Auladell C, Soriano E. 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.
15. Denaxa M, Chan CH, Schachner M, Parnavelas JG, Karagogeos D. 2001. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development. 128:4635-4644.
16. Fukuda T, Kawano H, Ohyama K, Li HP, Takeda Y, Oohira A, Kawamura K. 1997. Immunohistochemical localization of neurocan and L1 in the formation of thalamocortical pathway of developing rats. J Comp Neurol. 382:141-152.
17. Goffinet AM. 1984. Events governing organization of postmigratory neurons: studies on brain development in normal and reeler mice. Brain Res. 319:261-296.
18. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, et al. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature. 425:917-925.
19. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem. 271:695-701.
20. Herz J, Bock HH. 2002. Lipoprotein receptors in the nervous system. Annu Rev Biochem. 71:405-434.
21. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C. 2003. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci. 25:139-151.
22. Howell BW, Hawkes R, Soriano P, Cooper JA. 1997. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature. 389:733-737.
23. Jones L, Lopez-Bendito G, Gruss P, Stoykova A, Molnar Z. 2002. Pax6 is required for the normal development of the forebrain axonal connections. Development. 129:5041-5052.
24. Jossin Y, Goffinet AM. 2007. Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol Cell Biol. 27:7113-7124.
25. Jossin Y, Ogawa M, Metin C, Tissir F, Goffinet AM. 2003. Inhibition of SRC family kinases and non-classical protein kinases C induce a reeler-like malformation of cortical plate development. J Neurosci. 23:9953-9959.
26. Kee Y, Hwang BJ, Sternberg PW, Bronner-Fraser M. 2007. Evolutionary conservation of cell migration genes: from nematode neurons to vertebrate neural crest. Genes Dev. 21:391-396.
27. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol. 297:441-470.
28. Kuo G, Arnaud L, Kronstad-O'Brien P, Cooper JA. 2005. Absence of Fyn and Src causes a reeler-like phenotype. J Neurosci. 25:8578-8586.
29. McConnell SK, Ghosh A, Shatz CJ. 1994. Subplate pioneers and the formation of descending connections from cerebral cortex. J Neurosci. 14:1892-1907.
30. Meyer G, Goffinet AM. 1998. Prenatal development of reelinimmunoreactive neurons in the human neocortex. J Comp Neurol. 397:29-40.
31. Molnar Z, Metin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, Dehay C, Kennedy H. 2006. Comparative aspects of cerebral cortical development. Eur J Neurosci. 23:921-934.
32. Morante-Oria J, Carleton A, Ortino B, Kremer EJ, Fairen A, Lledo PM. 2003. Subpallial origin of a population of projecting pioneer neurons during corticogenesis. Proc Natl Acad Sci U S A. 100:12468-12473.
33. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL. 2001. Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci. 4:143-150.
34. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. 1995. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol. 131:1715-1726.
35. Pinto-Lord MC, Evrard P, Caviness VS, Jr. 1982. Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res. 256:379-393.
36. Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, Ghosh A. 2002. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development. 129:3147-3160.
37. Price DJ, Kennedy H, Dehay C, Zhou L, Mercier M, Jossin Y, Goffinet AM, Tissir F, Blakey D, Molnar Z. 2006. The development of cortical connections. Eur J Neurosci. 23:910-920.
38. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey cortex. J Comp Neurol. 145:61-84.
39. Richards LJ, Plachez C, Ren T. 2004. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet. 66:276-289.
40. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry. 100:431-440.
41. Shakir MA, Lundquist EA. 2005. Analysis of cell migration in Caenorhabditis elegans. Methods Mol Biol. 294:159-173.
42. Shi SH, Cheng T, Jan LY, Jan YN. 2004. APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr Biol. 14:2025-2032.
43. Solecki D, Govek EE, Tomoda T, Hatten ME. 2006. Neuronal polarity in CNS development. Genes Dev. 20:2639-2647.
44. Solecki DJ, Model L, Gaetz J, Kapoor TM, Hatten ME. 2004. Par6alpha signaling controls glial-guided neuronal migration. Nature neuroscience. 7:1195-1203.
45. Sym M, Robinson N, Kenyon C. 1999. MIG-13 positions migrating cells along the anteroposterior body axis of C. elegans. Cell. 98:25-36.
46. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci. 4:496-505.
47. Tomioka N, Osumi N, Sato Y, Inoue T, Nakamura S, Fujisawa H, Hirata T. 2000. Neocortical origin and tangential migration of guidepost neurons in the lateral olfactory tract. J Neurosci. 20:5802-5812.
48. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J. 1999. Reeler/disabledlike disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell. 97:689-701.
49. Wang Y, Du D, Fang L, Yang G, Zhang C, Zeng R, Ullrich A, Lottspeich F, Chen Z. 2006. Tyrosine phosphorylated Par3 regulates epithelial tight junction assembly promoted by EGFR signaling. EMBO J. 25:5058-5070.
50. Wood J, Martin S, Price DJ. 1992. Evidence that the earliest generated cells of the murine cerebral cortex form a transient population in the subplate and marginal zone. Dev Brain Res. 66:137-140.
51. Xie Y, Skinner E, Landry C, Handley V, Schonmann V, Jacobs E, Fisher R, Campagnoni A. 2002. Influence of the embryonic preplate on the organization of the cerebral cortex: a targeted ablation model. J Neurosci. 22:8981-8991.
52. Zecevic N, Milosevic A, Rakic S, Marin-Padilla M. 1999. Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J Comp Neurol. 412:241-254.
53. Zecevic N, Rakic P. 2001. Development of layer I neurons in the primate cerebral cortex. J Neurosci. 21:5607-5619.