EphA4 is associated with multiple cell types in the marmoset primary visual cortex throughout the lifespan

European Journal of Neuroscience

Volumn 39, Issue 9, 2014, Pages 1419-1428

  Goldshmit, Yona ^a   Homman Ludiye, Jihane ^a   Bourne, James A ^a  

^a Monash University   (Australia)

Author keywords

Astrocyte; Development; Monkey; Neuron; Visual cortex

Indexed keywords

EPHRIN A4; EPHRIN RECEPTOR A4;

ADULT; ADULTHOOD; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD VESSEL; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CALLITRICHINAE; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EVOLUTION; FEMALE; GLIA CELL; LIFESPAN; MACROGLIA; MALE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRIATE CORTEX; WHITE MATTER; ANIMAL; CALLITHRIX; ENZYMOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; NERVE CELL; VISUAL CORTEX;

ANIMALS; CALLITHRIX; FEMALE; MALE; MICE; NEUROGLIA; NEURONS; RECEPTOR, EPHA4; VISUAL CORTEX;

EID: 84899926435     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12514     Document Type: Article

References (58)

1. Bonanomi, D., Chivatakarn, O., Bai, G., Abdesselem, H., Lettieri, K., Marquardt, T., Pierchala, B.A. & Pfaff, S.L. (2012) Ret is a multifunctional coreceptor that integrates diffusible- and contact-axon guidance signals. Cell, 148, 568-582.
2. Bourne, J.A. (2005) Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). Cereb. Cortex, 16, 405-414.
3. Bourne, J.A. (2010) Unravelling the development of the visual cortex: implications for plasticity and repair. J. Anat., 217, 449-468.
4. Bourne, J.A., Warner, C.E. & Rosa, M.G.P. (2005) Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. Cereb. Cortex, 15, 740-748.
5. Bylund, M., Andersson, E., Novitch, B.G. & Muhr, J. (2003) Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci., 6, 1162-1168.
6. Cang, J., Kaneko, M., Yamada, J., Woods, G., Stryker, M.P. & Feldheim, D.A. (2005) Ephrin-As guide the formation of functional maps in the visual cortex. Neuron, 48, 577-589.
7. Cheng, H.J., Nakamoto, M., Bergemann, A.D. & Flanagan, J.G. (1995) Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell, 82, 371-381.
8. Davy, A. & Soriano, P. (2005) Ephrin signaling in vivo: look both ways. Dev. Dynam., 232, 1-10.
9. Depaepe, V., Suarez-Gonzalez, N., Dufour, A., Passante, L., Gorski, J.A., Jones, K.R., Ledent, C. & Vanderhaeghen, P. (2005) Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature, 435, 1244-1250.
10. Dimidschstein, J., Passante, L., Dufour, A., van den Ameele, J., Tiberi, L., Hrechdakian, T., Adams, R., Klein, R., Lie, D.C., Jossin, Y. & Vanderhaeghen, P. (2013) Ephrin-b1 controls the columnar distribution of cortical pyramidal neurons by restricting their tangential migration. Neuron, 79, 1123-1135.
11. Doetsch, F., Caillé, I., Lim, D.A., García-Verdugo, J.M. & Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703-716.
12. Donoghue, M.J. & Rakic, P. (1999a) Molecular evidence for the early specification of presumptive functional domains in the embryonic primate cerebral cortex. J. Neurosci., 19, 5967-5979.
13. Donoghue, M.J. & Rakic, P. (1999b) Molecular gradients and compartments in the embryonic primate cerebral cortex. Cereb. Cortex, 9, 586-600.
14. Drescher, U., Kremoser, C., Handwerker, 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. Dufour, A., Seibt, J., Passante, L., Depaepe, V., Ciossek, T., Frisén, J., Kullander, K., Flanagan, J.G., Polleux, F. & Vanderhaeghen, P. (2003) Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron, 39, 453-465.
16. Frugier, T., Conquest, A., McLean, C., Currie, P., Moses, D. & Goldshmit, Y. (2012) Expression and activation of EphA4 in the human brain after traumatic injury. J. Neuropath. Exp. Neur., 71, 242-250.
17. Gale, N.W., Flenniken, A., Compton, D.C., Jenkins, N., Copeland, N.G., Gilbert, D.J., Davis, S., Wilkinson, D.G. & Yancopoulos, G.D. (1996) Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene, 13, 1343-1352.
18. Garcia-Moreno, F., Vasistha, N.A., Trevia, N., Bourne, J.A. & Molnar, Z. (2012) Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb. Cortex, 22, 482-492.
19. Goldshmit, Y. & Bourne, J. (2010) Upregulation of EphA4 on astrocytes potentially mediates astrocytic gliosis after cortical lesion in the marmoset monkey. J. Neurotraum., 27, 1321-1332.
20. Goldshmit, Y., Galea, M.P., Wise, G., Bartlett, P.F. & Turnley, A.M. (2004) Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J. Neurosci., 24, 10064-10073.
21. Goldshmit, Y., Galea, M.P., Bartlett, P.F. & Turnley, A.M. (2006a) EphA4 regulates central nervous system vascular formation. J. Comp. Neurol., 497, 864-875.
22. Goldshmit, Y., McLenachan, S. & Turnley, A. (2006b) Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res. Rev., 52, 327-345.
23. Goldshmit, Y., Sztal, T.E., Jusuf, P.R., Hall, T.E., Nguyen-Chi, M. & Currie, P.D. (2012) Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J. Neurosci., 32, 7477-7492.
24. Greferath, U., Canty, A.J., Messenger, J. & Murphy, M. (2002) Developmental expression of EphA4-tyrosine kinase receptor in the mouse brain and spinal cord. Mech. Develop., 119(Suppl 1), S231-S238.
25. Himanen, J.-P., Chumley, M.J., Lackmann, M., Li, C., Barton, W.A., Jeffrey, P.D., Vearing, C., Geleick, D., Feldheim, D.A., Boyd, A.W., Henkemeyer, M. & Nikolov, D.B. (2004) Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci., 7, 501-509.
26. Holland, S.J., Gale, N.W., Mbamalu, G., Yancopoulos, G.D., Henkemeyer, M. & Pawson, T. (1996) Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature, 383, 722-725.
27. Homman-Ludiye, J., Merson, T.D. & Bourne, J.A. (2012) The early postnatal nonhuman primate neocortex contains self-renewing multipotent neural progenitor cells. PLoS ONE, 7, e34383.
28. Kelava, I., Reillo, I., Murayama, A.Y., Kalinka, A.T., Stenzel, D., Tomancak, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J.C., Okano, H., Huttner, W.B. & Borrell, V. (2012) Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex, 22, 469-481.
29. Khodosevich, K., Watanabe, Y. & Monyer, H. (2011) EphA4 preserves postnatal and adult neural stem cells in an undifferentiated state in vivo. J. Cell Sci., 124, 1268-1279.
30. Kriegstein, A., Noctor, S. & Martínez-Cerdeño, V. (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat. Rev. Neurosci., 7, 883-890.
31. Levitt, P. & Rakic, P. (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol., 193, 815-840.
32. Lim, Y.-S., McLaughlin, T., Sung, T.-C., Santiago, A., Lee, K.-F. & O'Leary, D.D.M. (2008) p75(NTR) mediates ephrin-A reverse signaling required for axon repulsion and mapping. Neuron, 59, 746-758.
33. Marler, K.J.M., Becker-Barroso, E., Martínez, A., Llovera, M., Wentzel, C., Poopalasundaram, S., Hindges, R., Soriano, E., Comella, J. & Drescher, U. (2008) A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. J. Neurosci., 28, 12700-12712.
34. Mashiko, H., Yoshida, A.C., Kikuchi, S.S., Niimi, K., Takahashi, E., Aruga, J., Okano, H. & Shimogori, T. (2012) Comparative anatomy of marmoset and mouse cortex from genomic expression. J. Neurosci., 32, 5039-5053.
35. Missler, M., Eins, S., Merker, H.J., Rothe, H. & Wolff, J.R. (1993a) Pre- and postnatal development of the primary visual cortex of the common marmoset. I. A changing space for synaptogenesis. J. Comp. Neurol., 333, 41-52.
36. Missler, M., Wolff, A., Merker, H.J. & Wolff, J.R. (1993b) Pre- and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes. J. Comp. Neurol., 333, 53-67.
37. Missler, M., Eins, S., Böttcher, H. & Wolff, J.R. (1994) Postnatal development of glial fibrillary acidic protein, vimentin and S100 protein in monkey visual cortex: evidence for a transient reduction of GFAP immunoreactivity. Brain Res. Dev. Brain Res., 82, 103-117.
38. Munro, K.M., Perreau, V.M. & Turnley, A.M. (2012) Differential gene expression in the EphA4 knockout spinal cord and analysis of the inflammatory response following spinal cord injury. PLoS ONE, 7, e37635.
39. Noren, N.K. & Pasquale, E.B. (2004) Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell. Signal., 16, 655-666.
40. North, H.A., Zhao, X., Kolk, S.M., Clifford, M.A., Ziskind, D.M. & Donoghue, M.J. (2009) Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. Development, 136, 2467-2476.
41. North, H.A., Clifford, M.A. & Donoghue, M.J. (2013) 'Til Eph do us part': intercellular signaling via Eph receptors and ephrin ligands guides cerebral cortical development from birth through maturation. Cereb. Cortex, 23, 1765-1773.
42. O'Leary, D.D.M., Chou, S.-J. & Sahara, S. (2007) Area patterning of the mammalian cortex. Neuron, 56, 252-269.
43. Palmer, A., Zimmer, M., Erdmann, K.S., Eulenburg, V., Porthin, A., Heumann, R., Deutsch, U. & Klein, R. (2002) EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol. Cell, 9, 725-737.
44. Pasquale, E.B. (2004) Eph-ephrin promiscuity is now crystal clear. Nat. Neurosci., 7, 417-418.
45. Poliakov, A., Cotrina, M. & Wilkinson, D.G. (2004) Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell, 7, 465-480.
46. Rakic, P. (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res., 33, 471-476.
47. Rakic, P. (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol., 145, 61-83.
48. Rashid, T., Upton, A.L., Blentic, A., Ciossek, T., Knöll, B., Thompson, I.D. & Drescher, U. (2005) Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron, 47, 57-69.
49. Reillo, I., de Juan Romero, C., Garcia-Cabezas, M.A. & Borrell, V. (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex, 21, 1674-1694.
50. Rosa, M.G.P. & Tweedale, R. (2005) Brain maps, great and small: lessons from comparative studies of primate visual cortical organization. Philos. T. Roy. Soc. B., 360, 665-691.
51. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods, 9, 676-682.
52. Sestan, N., Rakic, P. & Donoghue, M.J. (2001) Independent parcellation of the embryonic visual cortex and thalamus revealed by combinatorial Eph/ephrin gene expression. Curr. Biol., 11, 39-43.
53. Song, J. (2003) Tyrosine phosphorylation of the well packed ephrinB cytoplasmic beta-hairpin for reverse signaling. Structural consequences and binding properties. J. Biol. Chem., 278, 24714-24720.
54. Teo, L., Homman-Ludiye, J., Rodger, J. & Bourne, J.A. (2012a) Discrete ephrin-B1 expression by specific layers of the primate retinogeniculostriate system continues throughout postnatal and adult life. J. Comp. Neurol., 520, 2941-2956.
55. Teo, L., Rosenfeld, J. & Bourne, J. (2012b) Models of CNS injury in the nonhuman primate: a new era for treatment strategies. Translat. Neurosci., 3, 181-195.
56. Torii, M. & Levitt, P. (2005) Dissociation of corticothalamic and thalamocortical axon targeting by an EphA7-mediated mechanism. Neuron, 48, 563-575.
57. Torii, M., Rakic, P. & Levitt, P. (2013) Role of EphA/ephrin-a signaling in the development of topographic maps in mouse corticothalamic projections. J. Comp. Neurol., 521, 626-637.
58. Zimmer, G., Kästner, B., Weth, F. & Bolz, J. (2007) Multiple effects of ephrin-A5 on cortical neurons are mediated by SRC family kinases. J. Neurosci., 27, 5643-5653.