Reelin inhibits migration of sympathetic preganglionic neurons in the spinal cord of the chick

Journal of Comparative Neurology

Volumn 519, Issue 10, 2011, Pages 1970-1978

  Yip, Yee Ping ^a   Zhou, Guangdou ^a   Kubo, Ken Ichiro ^b   Nakajima, Kazunori ^b   Yip, Joseph W ^a  

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

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Autonomic neurons; Neuronal migration; Reelin function; Spinal cord development

Indexed keywords

REELIN;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CHICK; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; MOTONEURON; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL CORD; SPINAL CORD DEVELOPMENT; SYMPATHETIC PREGANGLIONIC NERVE CELL;

ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CHICK EMBRYO; EXTRACELLULAR MATRIX PROTEINS; GANGLIA, SYMPATHETIC; NERVE TISSUE PROTEINS; NEURONS; SERINE ENDOPEPTIDASES; SPINAL CORD;

EID: 79956270022     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22616     Document Type: Article

References (62)

1. Alcántara 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.
2. Ballif BA, Arnaud L, Arthur WT, Guris D, Imamoto A, Cooper JA. 2004. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr Biol 14: 606-610. Erratum in Curr Biol 14:742.
3. Benhayon D, Magdaleno S, Curran T. 2003. Binding of purified Reelin to ApoER2 and VLDLR mediates tyrosine phosphorylation of Disabled-1. Brain Res Mol Brain Res 112: 33-45.
4. Bos JL. 2005. Linking Rap to cell adhesion. Curr Opin Cell Biol 17: 123-128.
5. Cariboni A, Rakic S, Liapi A, Maggi R, Goffinet A, Parnavelas JG. 2005. Reelin provides an inhibitory signal in the migration of gonadotropin-releasing hormone neurons. Development 132: 4709-4718.
6. Caron E. 2003. Cellular functions of the Rap1 GTP-binding protein: a pattern emerges. J Cell Sci 116: 435-440.
7. Caviness VS Jr, Sidman RL. 1973. Retrohippocampal, hippocampal and related structures of the forebrain in the reeler mutant mouse. J Comp Neurol 147: 235-254.
8. Chai X, Förster E, Zhao S, Bock HH, Frotscher M. 2009. Reelin acts as a stop signal for radially migrating neurons by inducing phosphorylation of n-cofilin at the leading edge. Commun Integr Biol 2: 375-377.
9. Ciment G, Weston JA. 1982. Early appearance in neural crest and crest-derived cells of an antigenic determinant present in avian neurons. Dev Biol 93: 355-367.
10. Ciment G, Ressler A, Letourneau PC, Weston JA. 1986. A novel intermediate filament-associated protein, NAPA-73, that binds to different filament types at different stages of nervous system development. J Cell Biol 102: 246-251.
11. Cooper JA. 2008. A mechanism for inside-out lamination in the neocortex. Trends Neurosci 31: 113-119.
12. D'Arcangelo G, Miao GG, 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. D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T. 1997. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 17: 23-31.
14. de Bergeyck V, Naerhuyzen B, Goffinet AM, Lambert de Rouvroit C. 1998. A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Methods 82: 17-24.
15. Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES. 2000. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27: 33-44.
16. Falconer DS. 1951. Two new mutants, trembler and reeler, with neurological actions in the house mouse (Mus musculus L.). J Genet 50: 192-201.
17. Förster E, Jossin Y, Zhao S, Chai X, Frotscher M, Goffinet AM. 2006. Recent progress in understanding the role of Reelin in radial neuronal migration, with specific emphasis on the dentate gyrus. Eur J Neurosci 23: 901-909.
18. Frotscher M. 1997. Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 290: 315-322.
19. Garces A, Haase G, Airaksinen MS, Livet J, Filippi P, deLapeyriere O. 2000. GFR1 is required for development of distinct subpopulations of motoneuron. J Neurosci 20: 4992-5000.
20. Goffinet AM. 1997. Developmental neurobiology. Unscrambling a disabled brain. Nature 389: 668-669.
21. Haas CA, Dudeck O, Kirsch M, Huszka C, Kann G, Pollak S, Zentner J, Frotscher M. 2002. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J Neurosci 22: 5797-5802.
22. 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.
23. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92.
24. Heinrich C, Nitta N, Flubacher A, Müller M, Fahrner A, Kirsch M, Freiman T, Suzuki F, Depaulis A, Frotscher M, Haas CA. 2006. Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J Neurosci 26: 4701-4713.
25. Herz J, Bock HH. 2002. Lipoprotein receptors in the nervous system. Annu Rev Biochem 71: 405-434.
26. Howell BW, Gertler FB, Cooper JA. 1997. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J 16: 121-132.
27. Howell BW, Herrick TM, Hildebrand JD, Zhang Y, Cooper JA. 2000. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr Biol 10: 877-885.
28. Karlsson O, Thor S, Norberg T, Ohlsson H, Edlund T. 1990. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344: 879-882.
29. Kojima T, Nakajima K, Mikoshiba K. 2000. The disabled 1 gene is disrupted by a replacement with L1 fragment in yotari mice. Brain Res Mol Brain Res 75: 121-127.
30. Krull CE. 2004. A primer on using in ovo electroporation to analyze gene function. Dev Dyn 229: 433-439.
31. Kubo K, Honda T, Tomita K, Sekine K, Ishii K, Uto A, Kobayashi K, Tabata H, Nakajima, K. 2010. Ectopic reelin induces neuronal aggregation with a normal birthdate-dependent "inside-out" alignment in the developing neocortex. J Neurosci 18: 10953-10966.
32. 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.
33. Levi-Montalcini R. 1950. The origin and development of the visceral system in the spinal cord of the chick embryo. J. Morphol 86: 253-283.
34. Magdaleno S, Keshvara L, Curran T. 2002. Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 33: 1-20.
35. Miyata T, Nakajima K, Mikoshiba K, Ogawa M. 1997. Regulation of Purkinje cell alignment by Reelin as revealed with CR-50 antibody. J Neurosci 17: 3599-3609.
36. 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.
37. Nakajima K, Mikoshiba K, Miyata T, Kudo C, Ogawa M. 1997. Disruption of hippocampal development in vivo by CR-50 mAb against reelin. Proc Natl Acad Sci U S A 94: 8196-8201.
38. Nakamura H, Funahashi J. 2001. Introduction of DNA into chick embryos by in ovo electroporation. Methods 24: 43-48.
39. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
40. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto 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.
41. Ogura T. 2002. In vivo electroporation: a new frontier for gene delivery and embryology. Differentiation 70: 163-171.
42. Olson EC, Walsh CA. 2008. Reelin/Dab1 signaling in the developing cerebral cortex. In: Fatemi SH, editor. Reelin glycoprotein. New York: Springer. p 89-105.
43. 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.
44. Prasad A, Hollyday M. 1991. Development and migration of avian sympathetic preganglionic neurons. J Comp Neurol 307: 237-258.
45. Rakic P, Caviness VS. 1995. Cortical development: view from neurological mutants two decades later. Neuron 14: 1101-1104.
46. Rice DS, Curran T. 2001. Role of the Reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24: 1005-1039.
47. 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.
48. Schiffmann SN, Bernier B, Goffinet AM. 1997. Reelin mRNA expression during mouse brain development. Eur J Neurosci 9: 1055-1071.
49. Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T. 1997. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389: 730-733.
50. Thor S, Ericson J, Brannstrom T, Edlund T. 1991. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7: 881-889.
51. Tissir F, Goffinet AM. 2003. Reelin and brain development. Nat Rev Neurosci 4: 496-505.
52. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J. 1999. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97: 689-701.
53. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79: 957-970.
54. Yamagata M, Weiner JA, Dulac C, Roth KA, Sanes JR. 2006. Labeled lines in the retinotectal system: markers for retinorecipient sublaminae and the retinal ganglion cell subsets that innervate them. Mol Cell Neurosci 33: 296-310.
55. Yip YP, Capriotti C, Yip JW. 2003. Migratory pathway of sympathetic preganglionic neurons in normal and reeler mutant mice. J Comp Neurol 460: 94-105.
56. Yip YP, Capriotti C, Magdaleno S, Benhayon D, Curran T, Nakajima K, Yip JW. 2004. Components of the Reelin signaling pathway are expressed in the spinal cord. J Comp Neurol 470: 210-219.
57. Yip YP, Kronstadt-O'Brien P, Capriotti C, Cooper JA, Yip JW. 2007. Migration of sympathetic preganglionic neurons in the spinal cord is regulated by Reelin-dependent Dab1 tyrosine phosphorylation and CrkL. J Comp Neurol 502: 635-643.
58. Yip YP, Mehta N, Magdaleno S, Curran T, Yip JW. 2009. Ectopic expression of reelin alters migration of sympathetic preganglionic neurons in the spinal cord. J Comp Neurol 515: 260-268.
59. Yip JW, Yip YP. 1990. Changes in fibronectin distribution in the developing peripheral nervous system of the chick. Brain Res Dev Brain Res 51: 11-18.
60. Yip JW, Yip YP, Capriotti C. 1998. Specific projections of sympathetic preganglionic neurons are not intrinsically determined by segmental origins of their cell bodies. J Neurobiol 35: 371-378.
61. Yip JW, Yip YPL, Nakajima K, Capriotti C. 2000. Reelin controls position of autonomic neurons in the spinal cord. Proc Natl Acad Sci U S A 97: 8612-8616.
62. Yoneshima H, Nagata E, Matsumoto M, Yamada M, Nakajima K, Miyata T, Ogawa M, Mikoshiba K. 1997. A novel neurological mutant mouse, yotari, which exhibits reeler-like phenotype but expresses CR-5antigen/reelin. Neurosci Res 29: 217-223.