Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits

Journal of Neuroscience

Volumn 18, Issue 12, 1998, Pages 4663-4672

  Castellani, Valérie ^a   Yue, Yong ^b   Gao, Pan Pan ^b   Zhou, Renping ^b   Bolz, Jürgen ^a  

^a INSERM   (France)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Axonal branching; Axonal guidance; Cortical circuit formation; Cortical development; Eph receptors; Ephrins; In vitro assays; Wiring molecules

Indexed keywords

TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ARTICLE; ASSAY; BRAIN CORTEX; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; LIGAND BINDING; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 0032526731     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-12-04663.1998     Document Type: Article

References (68)

1. Angevine JB, Sidman RL (1961) Autobiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768.
2. Auladell, C, Martinez A, Alcantara S, Supèr H, Soriano E (1995) Migrating neurons in the developing cerebral cortex of the mouse send callosal axons. Neuroscience 64:1091-1103.
3. Bastani MJ, du Lac S, Goodman CS (1986) Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of a specific axonal pathway by the pCC neuron. J Neurosci 6:3518-3531.
4. Baver SA, Altman J (1991) Neocortical development. New York: Raven.
5. Berr M, Eayrs JT (1963) Histogenesis of the cerebral cortex. Nature 197:984-985.
6. Berry M, Rogers AW (1965) The migration of neuroblasts in the developine cerebral cortex. J Anat 99:691-709.
7. Burkhalter A (1989) Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J Comp Neurol 279:171-181.
8. Callaway EM, Katz LC (1990) Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurose, 10:1134-1153.
9. Callaway EM, Lieber JL (1996) Development of axonal arbors of laye 6 pyramidal neurons in ferret primary visual cortex. J Comp Neurol 376:295-305.
10. Castellani, Bolz J (1997) Membrane-associated molecules regulate the formation of layer-specific cortical circuits. Proc Natl Acad Sci USA 94:7030-7035.
11. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan, JG (1995) Complementary gradients in expression and binding of ELF-1 and MEK4 in development of the topographic retinotectal projection map. Cell 82:371-381.
12. Cole GJ McCabe CF (1991) Identification of a developmentally regulated keratan sulfate proteoglycan that inhibits cell adhesion and neurite outgrowth. Neuron 7:1007-1018.
13. Davis S, Gale NW, Aldrich TH, Maisonpierre TC, Lhotak V, Pawson T, Goldarb M, Yancopoulos GD (1994) Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816-819.
14. Drecher U, Kremoser C, Handworker C, Löschinger J, Noda M, Bonhoeffer F (1995) In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
15. Eph Nomenclature Committee (1997) Unified nomenclature for Eph family receptors and their ligands, the ephrins. Cell 90:403-404.
16. Fisken RA, Garey LJ, Powell TPS (1975) The intrinsic, association and commissural connections of area 17 of the visual cortex. Philos Trans R Soc Lond B Biol Sci 272:487-536.
17. Fitzpatrick D (1996) The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. Cereb Cortex 6:329-341.
18. Friedman GC, O'Leary DDM (1996) Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J Neurosci 16:5498-5509.
19. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19.
20. Gao PP, Zhang JH, Yokoyama M, Racey B, Dreyfus CF, Black IB, Zhou R (1996) Regulation of topographic projection in the-brain: Elf- 1 in the hippocamposeptal system. Proc Natl Acad Sci USA 93:11161-11166.
21. Gilbert CD (1992) Horizontal integration and cortical dynamics. Neuron 9:1-13.
22. Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280:120-125.
23. Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116-1133.
24. Gilbert CD, Wiesel TN (19S9) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432-2442.
25. Götz M, Bolz J (1994) Differentiation of transmitter phcnotypes in rat cerebral cortex. Eur J Neurosci 6:18-32.
26. Götz M, Novak N, Bastmeyer M, Bolz J (1992) Membrane bound molecules in rat cerebral cortex regulate thalamic innervation. Development 116:507-519.
27. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R (1996) Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86:35-46.
28. Horton HL, Levitt P (1988) A unique membrane protein is expressed on early developing limbic systems axons and cortical targets. J Neurosci 8:4653-4661.
29. Hübener M, Schwarz C, Bolz J (1990) Morphological types of projection neurons in layer 5 of cat visual cortex. J Comp Neurol 301:655-674.
30. Itasaki N, Nakamura H (1992) Rostrocaudal polarity of the tectum in birds: correlation of en gradients and topographic order in retinotectal projection. Neuron 8:787-798.
31. Itasaki N, Nakamura H (1996) A role for gradient en expression in positional specification on the optic tectum. Neuron 16:55-62.
32. Kageyama GH, Robertson RT (1993) Development of geniculocortical projections to visual cortex in rat: evidence for early ingrowth and synaptogenesis. J Comp Neurol 335:123-148.
33. Katz LC (1991) Specificity in the development of vertical connections in cat striate cortex. Eur J Neurosci 3:1-9.
34. Katz LC, Callaway EM (1992) Development of local circuits in mammalian visual cortex. Annu Rev Neurosci 15:31-56.
35. Kennedy TE, Serafini T, De la Torre JR, Tessier-Lavigne M (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78:425-435.
36. Klämbt C, Goodman CS (1991) The diversity and pattern of glia during axon pathway formation in the Drosophila embryo, Glia 4:205-213.
37. Lillian L (1996) Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 377:158-162.
38. Löwel S, Singer W (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255:209-212.
39. Luhmann HJ, Greuel JM, Singer W (1990) Horizontal interactions in cat striate cortex: III. Ectopic receptive fields and transient exuberance of tangential interactions. Eur J Neurosci 2:369-377.
40. Lund JS, Boothe RG (1975) Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the macaque monkey. J Comp Neurol 159:305-334.
41. Lund JS, Boothe RG, Lund RD (1977) Development of neurons in the visual cortex of the monkey (Macaca memestrina): a Golgi study from fetal day 127 to postnatal maturity. J Comp Neurol 176:149-188.
42. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
43. Luskin MB, Shatz CJ (1985) Neurogenesis of the cat's primary visual cortex. J Comp Neurol 242:611-631.
44. Malach R, Amir Y, Harel M, Grinvald A (1993) Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc Natl Acad Sci USA 90:10469-10473.
45. Martin KAC, Whitteridge D (1984) Form, function and intracortical projections of spiny neurons in the striate cortex of the cat. J Physiol (Lond) 353:463-504.
46. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
47. Meima L, Kljavin IJ, Moran P, Shih A, Winslow JW, Caras IW (1997) AL-1-induced growth cone collapse of rat cortical neurons is correlated with REK7 expression and rearrangement of the actin cytoskeleton. Eur J Neurosci 9:177-188.
48. Messersmith EK, Leonrdo ED, Shatz CJ, Tessier-Lavigne M, Goodman CS, Kolodkin AL (1995) Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14:949-959.
49. Meyer G, Ferres-Torres R (1984) Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat. J Comp Neurol 228:226-244.
50. Miller MW (1988) Development of projection and local circuit neurons in neocortex. In: Cerebral cortex, Vol 7: Development and maturation of cerebral cortex (Peters A, EG Jones, eds), pp 133-175. New York: Plenum.
51. Miller MW, Peters A (1981) Maturation of rat visual cortex. II. A combined Golgi-electron microscopic study of pyramidal neurons. J Comp Neurol 203:555-573.
52. Nakamoto M, Cheng HJ, Friedman GC, McLaughlin T, Hansen MJ, Yoon CH, O'Leary DDM, Fianagan JG (1996) Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86:755-766.
53. Püschel AW, Adams RH, Betz H (1995) Murine semaphoring D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14:941-948.
54. Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey ncocortex. J Comp Neurol 145:61-84.
55. Rétaux S, McNeill L, Harris WA (1996) Engrailed, retinotectal targeting, and axonal patterning in the midbrain during Xenopus development: an antisense study. Neuron 16:63-75.
56. Rockland KS, Lund JS, Humphrey AL (1982) Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). J Comp Neurol 209:41-58.
57. Schwartz ML, Rakic P, Goldman-Rakic PS (1991) Early phenotype expression of cortical neurons: evidence that a subclass of migrating neurons have callosal axons. Proc Natl Acad Sci USA 88:1354-1358.
58. Schwarz C, Bolz J (1991) Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study. J Neurosci 11:2995-3007.
59. Serafini T, Kennedy TE, Galko MJ, Mirzayan C Jessell TM, TessierLavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424.
60. Shigetani Y, Funahashi J-I, Nakamura H (1997) En-2 regulates the expression of the ligands for Eph type tyrosine kinases in chick embryonic tectum. Neurosci Res 27:211-217.
61. Shoukimas GM, Hinds JW (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J Comp Neurol 179:795-830.
62. Snow DM, Steindler DA, Silver J (1990) Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan of the development of an axon barrier. Dev Biol 138:359-376.
63. Ts'o DY, Gilbert CD, Wiesel TN (1986) Relationships between hotizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6:1160-1170.
64. 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.
65. Winslow JW, Moran P, Vaiverde J, Shih A, Yuan JQ, Wong SC, Tsai SP, Goddard A, Henzel WJ, Hefti F, Beck KD, Caras IW (1995) Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14:973-981.
66. Zhang JH, Cerretti DP, Yu T, Flanagan JG, Zhou RP (1996) Detection of ligands in regions anatomically connected to neurons expressing the eph receptor Bsk: potential roles in neuron-target interaction. J Neurosci 16:7182-7192.
67. Zhang J-H, Pimenta AF, Levitt P, Zhou R (1997) Dynamic expression suggests multiple roles of the eph family receptor brain-specific kinase (Bsk) during mouse neurogenesis. Mol Brain Res 47:202-214.
68. Zhou R, Copeland TD, Kromer LF, Schulz NT (1994) Isolation and characterization of Bsk, a growth factor receptor-like kinase associated with the limbic system. J Neurosci Res 37:129-143.