Cooperative activity of multiple upper layer proteins for thalamocortical axon growth

Developmental Neurobiology

Volumn 68, Issue 3, 2008, Pages 317-331

  Maruyama, Takuro ^a   Matsuura, Masahiro ^b   Suzuki, Kazuhiro ^c   Yamamoto, Nobuhiko ^a  

^a OSAKA UNIVERSITY   (Japan)

^b Riso Kagaku Corporation   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Axon guidance; Cortex; Lamina; Protein printing method; Thalamus

Indexed keywords

EPHRIN A5; SEMAPHORIN; SEMAPHORIN 7A; STEM CELL FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; FUNCTIONAL PROTEOMICS; METHODOLOGY; MOLECULAR DYNAMICS; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SIMPLE TO MAKE MICROPORE PROTEIN PRINTING METHOD; THALAMOCORTICAL TRACT; THALAMUS;

ANIMALS; AXONS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; EPHRIN-A5; GENE EXPRESSION REGULATION; NERVE TISSUE PROTEINS; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SEMAPHORINS; STEM CELL FACTOR; THALAMUS;

EID: 39349085577     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20592     Document Type: Article

References (66)

1. Agmon A, Yang LT, O'Dowd DK, Jones EG. 1993. Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J Neurosci 13:5365-5382.
2. Berridge MJ. 1998. Neuronal calcium signaling. Neuron 21:13-26.
3. Bolz J, Novak N, Staiger V. 1992. Formation of specific afferent connections in organotypic slice cultures from rat visual cortex cocultured with lateral geniculate nucleus. J Neurosci 12:3054-3070.
4. Brantley-Sieders DM, Caughron J, Hicks D, Pozzi A, Ruiz JC, Chen J. 2004. EphA2 receptor tyrosine kinase regulates endothelial cell migration and vascular assembly through phosphoinositide 3-kinase-mediated Rac 1 GTPase activation. J Cell Sci 117:2037-2049.
5. Calof AL, Lander AD. 1991. Relationship between neuronal migration and cell-substratum adhesion: Laminin and merosin promote olfactory neuronal migration but are anti-adhesive. J Cell Biol 115:779-794.
6. Catalano SM, Robertson RT, Killackey HP. 1996. Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol 367:36-53.
7. Ciossek T, Monschau B, Kremoser C, Loschinger J, Lang S, Muller BK, Bonhoeffer F, et al. 1998. Eph receptor-ligand interactions are necessary for guidance of retinal ganglion cell axons in vitro. Eur J Neurosci 10:1574-1580.
8. Diefenbach TJ, Guthrie PB, Kater SB. 2000. Stimulus history alters behavioral responses of neuronal growth cones. J Neurosci 20:1484-1494.
9. Drescher U, Bonhoeffer F, Muller BK. 1997. The Eph family in retinal axon guidance. Curr Opin Neurobiol 7:75-80.
10. Dufour A, Egea J, Kullander K, Klein R, Vanderhaeghen P. 2006. Genetic analysis of EphA-dependent signaling mechanisms controlling topographic mapping in vivo. Development 133:4415-4420.
11. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, Frisen J, Kullander K, et al. 2003. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 39:453-465.
12. Flanagan JG, Vanderhaeghen P. 1998. The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
13. Frost DO, Caviness VS Jr. 1980. Radial organization of thalamic projections to the neocortex in the mouse. J Comp Neurol 194:369-393.
14. Gao PP, Yue Y, Zhang JH, Cerretti DP, Levitt P, Zhou R. 1998. Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: Implications in the development of thalamocortical projections. Proc Natl Acad Sci USA 95:5329-5334.
15. Garey LJ, Powell TP. 1971. An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc R Soc Lond B Biol Sci 179:41-63.
16. Gomez TM, Robles E, Poo M, Spitzer NC. 2001. Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291:1983-1987.
17. Götz M, Bolz J. 1992. Formation and preservation of cortical layers in slice cultures. J Neurobiol 23:783-802.
18. Gu C, Park S. 2001. The EphA8 receptor regulates integrin activity through p110gamma phosphatidylinositol-3 kinase in a tyrosine kinase activity-independent manner. Mol Cell Biol 21:4579-4597.
19. Hansen MJ, Dallal GE, Flanagan JG. 2004. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42:717-730.
20. Hirata T, Morii E, Morimoto M, Kasugai T, Tsujimura T, Hirota S, Kanakura Y, et al. 1993. Stem cell factor induces outgrowth of c-kit-positive neurites and supports the survival of c-kit-positive neurons in dorsal root ganglia of mouse embryos. Development 119:49-56.
21. Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C. 1999. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401:69-73.
22. Huang EJ, Nocka KH, Buck J, Besmer P. 1992. Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol Biol Cell 3:349-362.
23. Hubener M, Götz M, Klostermann S, Bolz J. 1995. Guidance of thalamocortical axons by growth-promoting molecules in developing rat cerebral cortex. Eur J Neurosci 7:1963-1972.
24. Huntley GW, Benson DL. 1999. Neural (N)-cadherin at developing thalamocortical synapses provides an adhesion mechanism for the formation of somatopically organized connections. J Comp Neurol 407:453-471.
25. Inoue T, Tanaka T, Takeichi M, Chisaka O, Nakamura S, Osumi N. 2001. Role of cadherins in maintaining the compartment boundary between the cortex and striatum during development. Development 128:561-569.
26. Kageyama GH, Robertson RT. 1993. Development of geniculocortical projections to visual cortex in rat: Evidence early ingrowth and synaptogenesis. J Comp Neurol 335:123-148.
27. Kater SB, Mattson MP, Cohan C, Connor J. 1988. Calcium regulation of the neuronal growth cone. Trends Neurosci 11:315-321.
28. Kempf M, Clement A, Faissner A, Lee G, Brandt R. 1996. Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J Neurosci 16:5583-5592.
29. Kinnunen A, Niemi M, Kinnunen T, Kaksonen M, Nolo R, Rauvala H. 1999. Heparan sulphate and HB-GAM (heparin-binding growth-associated molecule) in the development of the thalamocortical pathway of rat brain. Eur J Neurosci 11:491-502.
30. López-Bendito G, Molnár Z. 2003. Thalamocortical development: How are we going to get there? Nat Rev Neurosci 4:276-289.
31. Mackarehtschian K, Lau CK, Caras I, McConnell SK. 1999. Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression. Cereb Cortex 9:601-610.
32. Mann F, Peuckert C, Dehner F, Zhou R, Bolz J. 2002. Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections. Development 129:3945-3955.
33. Matsumoto K, Wanaka A, Takatsuji K, Muramatsu H, Muramatsu T, Tohyama M. 1994. A novel family of heparin-binding growth factors, pleiotrophin and midkine, is expressed in the developing rat cerebral cortex. Brain Res Dev Brain Res 79:229-241.
34. Molnár Z, Blakemore C. 1991. Lack of regional specificity for connections formed between thalamus and cortex in coculture. Nature 351:475-477.
35. Molnár Z, Blakemore C. 1999. Development of signals influencing the growth and termination of thalamocortical axons in organotypic culture. Exp Neurol 156:363-393.
36. Nguyen-Ba-Charvet KT, Brose K, Marillat V, Sotelo C, Tessier-Lavigne M, Chedotal A. 2001. Sensory axon response to substrate-bound Slit2 is modulated by laminin and cyclic GMP. Mol Cell Neurosci 17:1048-1058.
37. Pasterkamp RJ, Peschon JJ, Spriggs MK, Kolodkin AL. 2003. Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424:398-405.
38. Poskanzer K, Needleman LA, Bozdagi O, Huntley GW. 2003. N-cadherin regulates ingrowth and laminar targeting of thalamocortical axons. J Neurosci 23:2294-2305.
39. Redies C, Takeichi M. 1993. Expression of N-cadherin mRNA during development of the mouse brain. Dev Dyn 197:26-39.
40. Ribak CE, Peters A. 1975. An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res 92:341-368.
41. Rosenquist AC, Edwards SB, Palmer LA. 1974. An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the cat. Brain Res 80:71-93.
42. Rosoff WJ, Urbach JS, Esrick MA, McAllister RG, Richards LJ, Goodhill GJ. 2004. A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients. Nat Neurosci 7:678-682.
43. Ruthazer ES, Cline HT. 2002. Multiphoton imaging of neurons in living tissue: Acquisition and analysis of time-lapse morphological data. Real-Time Imaging 8:175-188.
44. Sheppard AM, Brunstrom JE, Thornton TN, Gerfen RW, Broekelmann TJ, McDonald JA, Pearlman AL. 1995. Neuronal production of fibronectin in the cerebral cortex during migration and layer formation is unique to specific cortical domains. Dev Biol 172:504-518.
45. Shirasaki R, Katsumata R, Murakami F. 1998. Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 279:105-107.
46. Skaliora I, Singer W, Betz H, Puschel AW. 1998. Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215-1229.
47. Suda T, Nagata S. 1994. Purification and characterization of the Fas-ligand that induces apoptosis. J Exp Med 179:873-879.
48. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
49. Takei K, Shin RM, Inoue T, Kato K, Mikoshiba K. 1998. Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282:1705-1708.
50. Timokhina I, Kissel H, Stella G, Besmer P. 1998. Kit signaling through PI 3-kinase and Src kinase pathways: An essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J 17:6250-6262.
51. Tuttle R, Schlaggar BL, Braisted JE, O'Leary DD. 1995. Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth. J Neurosci 15:3039-3052.
52. Vanderhaeghen P, Lu Q, Prakash N, Frisen J, Walsh CA, Frostig RD, Flanagan JG. 2000. A mapping label required for normal scale of body representation in the cortex. Nat Neurosci 3:358-365.
53. von Philipsborn AC, Lang S, Loeschinger J, Bernard A, David C, Lehnert D, Bonhoeffer F, et al. 2006a. Growth cone navigation in substrate-bound ephrin gradients. Development 133:2487-2495.
54. von Philipsborn AC, Lang S, Bernard A, Loeschinger J, David C, Lehnen D, Bastmeyer M, et al. 2006b. Microcontact printing of axon guidance molecules for generation of graded patterns. Nat Protoc 1:1322-1328.
55. Walter J, Kern-Veits B, Huf J, Stolze B, Bonhoeffer F. 1987. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101:685-696.
56. Weinl C, Drescher U, Lang S, Bonhoeffer F, Loschinger J. 2003. On the turning of Xenopus retinal axons induced by ephrin-A5. Development 130:1635-1643.
57. Xu X, Ng S, Wu ZL, Nguyen D, Homburger S, Seidel-Dugan C, Ebens A, et al. 1998. Human semaphorin K1 is glycosylphosphatidylinositol-linked and defines a new subfamily of viral-related semaphorins. J Biol Chem 273:22428-22434.
58. Yabuta NH, Butler AK, Callaway EM. 2000. Laminar specificity of local circuits in barrel cortex of ephrin-A5 knockout mice. J Neurosci 20:RC88.
59. Yamamoto N, Higashi S, Toyama K. 1997. Stop and branch behaviors of geniculocortical axons: a time-lapse study in organotypic cocultures. J Neurosci 17:3653-3663.
60. Yamamoto N, Kurotani T, Toyama K. 1989. Neural connections between the lateral geniculate nucleus and visual cortex in vitro. Science 245:192-194.
61. Yamamoto N, Yamada K, Kurotani T, Toyama K. 1992. Laminar specificity of extrinsic cortical connections studied in coculture preparations. Neuron 9:217-228.
62. Yamamoto N, Matsuyama Y, Harada A, Inui K, Murakami F, Hanamura K. 2000a. Characterization of factors regulating lamina-specific growth of thalamocortical axons. J Neurobiol 42:56-68.
63. Yamamoto N, Inui K, Matsuyama Y, Harada A, Hanamura K, Murakami F, Ruthazer ES, et al. 2000b. Inhibitory mechanism by polysialic acid for lamina-specific branch formation of thalamocortical axons. J Neurosci 20:9145-9151.
64. Zhang SC, Fedoroff S. 1997. Cellular localization of stem cell factor and c-kit receptor in the mouse nervous system. J Neurosci Res 47:1-15.
65. Zhong Y, Takemoto M, Fukuda T, Hattori Y, Murakami F, Nakajima D, Nakayama M, et al. 2004. Identification of the genes that are expressed in the upper layers of the neocortex. Cereb Cortex 14:1144-1152.
66. Zhou FC. 1990. Four patterns of laminin-immunoreactive structure in developing rat brain. Brain Res Dev Brain Res 55:191-201.