Eph/ephrin expression in the adult rat visual system following localized retinal lesions: Localized and transneuronal up-regulation in the retina and superior colliculus

European Journal of Neuroscience

Volumn 22, Issue 8, 2005, Pages 1840-1852

  Rodger, J ^a,b   Symonds, A C E ^a   Springbett, J ^a   Shen, W Y ^a,c   Barlett, C A ^a   Rakoczy, P E ^a   Beazley, L D ^a,b   Dunlop, S A ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c LIONS EYE INSTITUTE   (Australia)

Author keywords

Axon guidance cues; CNS; Eph Ephrins; Injury; Polysynaptic pathways; PVG hooded rats

Indexed keywords

EPHRIN; EPHRIN A2; EPHRIN A5; EPHRIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KRYPTON LASER; MOLECULAR DYNAMICS; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA DETACHMENT; RETINA DISEASE; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; SUPERIOR COLLICULUS; UPREGULATION; VISUAL SYSTEM;

ANIMALS; CELL COUNT; CHOLERA TOXIN; DENERVATION; EPHRINS; FEMALE; FUNCTIONAL LATERALITY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MODELS, NEUROLOGICAL; RATS; RECEPTORS, EPH FAMILY; RETINA; SUPERIOR COLLICULUS; UP-REGULATION;

EID: 27644483897     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04381.x     Document Type: Article

References (66)

1. Arce, E.A., Rhoades, R.W. & Mooney, R.D. (1995) Effects of neonatal and adult enucleation on the synaptic organisation of the serotoninergic projection to the superficial gray layer of the hamster's superior colliculus. Dev. Brain Res., 90, 168-173.
2. Bach, H., Feldheim, D.A., Flanagan, J.G. & Scalia, F. (2003) Persistence of graded EphA/Ephrin-A expression in the adult frog visual system. J. Comp. Neurol., 467, 549-565.
3. Beazley, L., Springbett, J., Rodger, J., Shen, W.-Y., Symonds, A., Rakoczy, P. & Dunlop, S. (2002) Partial denervation of the superior colliculus induces localised upregulation of ephrin-A2 in the adult rat. Invest. Ophthalmol. Vis. Sci., 43, E-Abstract 4773.
4. Becker, C.G. & Becker, T. (2000) Gradients of ephrin-A2 and ephrin-A5b mRNA during retinotopic regeneration of the optic projection in adult zebrafish. J. Comp. Neurol., 427, 469-483.
5. Bianchi, L.M. & Gale, N.W. (1998) Distribution of Eph-related molecules in the developing and mature cochlea. Hear. Res., 117, 161-172.
6. Bodeutsch, N., Siebert, H., Dermon, C. & Thanos, S. (1999) Unilateral injury to the adult rat optic nerve causes multiple cellular responses in the contralateral site. J. Neurobiol., 38, 116-128.
7. Boulenguez, P., Abdelkefi, J., Pinard, R., Christolomme, A. & Segu, L. (1993) Effects of retinal deafferentation on serotonin receptor types in the superficial grey layer of the superior colliculus of the rat. J. Chem. Neuroanat., 6, 167-175.
8. Braisted, J.E., McLaughlin, T., Wang, H.U., Friedman, G.C., Anderson, D.J. & O'Learly, D.D.M. (1997) Graded and lamina-specific distributions of ligands of EphB receptor tyrosine kinases in the developing retinotectal system. Dev. Biol., 191, 14-28.
9. Brantley, D.M., Cheng, N., Thompson, E.J., Lin, Q., Brekken, R.A., Thorpe, P.E., Muraoka, R.S., Cerretti, D.P., Pozzi, A., Jackson, D., Lin, C. & Chen, J. (2002) Soluble Eph A receptors inhibit tumor angiogenesis and progression in vivo. Oncogene, 21, 7011-7026.
10. Brown, A., Yates, P.A., Burrola, P., Ortuno, D., Vaidya, A., Jessell, T.M., Pfaff, S.L.O., Leary, D.D.M. & Lemke, G. (2000) Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell, 102, 77-88.
11. Connor, R.J., Menzel, P. & Pasquale, E.B. (1998) Expression and tyrosine phosphorylation of Eph receptors suggest multiple mechanisms in patterning the visual system. Dev. Biol., 193, 21-35.
12. Conover, J.C., Doetsch, F., Garcia-Verdugo, J.-M., Gale, N.W., Yancopoulos, G.D. & Alvarez-Buylla, A. (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nature Neurosci., 3, 1091-1097.
13. Cooke, J.E. & Moens, C.B. (2002) Boundary formation in the hindbrain: Eph only it were simple... TINS, 25, 260-267.
14. Cooke, J., Moens, C., Roth, L., Durbin, L., Shiomi, K., Brennan, C., Kimmel, C., Wilson, S. & Holder, N. (2001) Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development, 128, 571-580.
15. Davenport, R., Thies, E., Zhou, R. & Nelson, P. (1998) Cellular localisation of ephrin-A2, ephrin-A5 and other functional guidance cues underlies retinotopic development across species. J. Neurosci., 18, 975-986.
16. Durbin, L., Brennan, C., Shiomi, K., Cooke, J., Barrios, A., Shanmugalingam, S., Guthrie, B., Lindberg, R. & Holder, N. (1998) Eph signaling is required for segmentation and differentiation of the somites. Genes Dev., 12, 3096-3109.
17. Feldheim, D.A., Kim, Y.-I., Bergemann, A.D., Prisen, J., Barbacid, M. & Flanagan, J.G. (2000) Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron, 25, 563-574.
18. Friedman, G.C. & O'Leary, D.D. (1996) Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J. Neurosci., 16, 5498-5509.
19. Fujiyama, F., Hioki, H., Tomioka, R., Taki, K., Tamamaki, N., Nomura, S., Okamoto, K. & Kaneko, T. (2003) Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation. J. Comp. Neurol., 465, 234-249.
20. Fukuda, Y. (1977) A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Res., 119, 327-344.
21. Gao, P.P., Yue, Y., Zhang, J.H., Cerretti, D.P., 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.
22. Giger, R.J., Wolfer, D.P., De Wit, G.M. & Verhaagen, J. (1996) Anatomy of rat semaphorin III/collapsin-1 mRNA expression and relationship to developing nerve tracts during neuroembryogenesis. J. Comp. Neurol., 375, 378-292.
23. Harvey, A.R., Plant, G.W. & Kent, A.P. (1993) The distribution of astrocytes, oligodendroglia and myelin in normal and transplanted rat superior colliculus: an immunohistochemical study. J. Neural Transplant Plast., 4, 1-14.
24. Hattori, M., Osterfield, M. & Flanagan, J.G. (2000) Regulated cleavage of a contact-mediated axon repellent. Science, 289, 1360-1364.
25. Humphrey, M.F. & Beazley, L.D. (1985) Retinal ganglion cell death during optic nerve regeneration in the frog Hyla moorei. J. Comp. Neurol., 236, 382-402.
26. Hyde, P.S. & Knudsen, E.I. (2001) A topographic instructive signal guides the adjustment of the auditory space map in the optic tectum. J. Neurosci., 21, 8586-8593.
27. Itasaki, N. & Nakamura, H. (1996) A role for gradient en expression in positional specification on the optic tectum. Neuron, 16, 55-62.
28. Jen, L.S. & Au, C. (1986) Intercollicular fibres terminating in the superficial layers of the superior colliculus. A WGA-HRP study in the rat. Brain Res., 379, 385-389.
29. King, C.E., Lacey, R., Bartlett, C.A., Rodger, J., Beazley, L.D. & Dunlop, S.A. (2003) Ephrin-A2 is up-regulated in a residential population of tectal neurons during optic nerve regeneration in goldfish. Proc. Am. Neurosci. Soc., 28, 358.2.
30. King, A.J., Schnupp, J.W. & Thompson, I.D. (1998) Signals from the superficial layers of the superior colliculus enable the development of the auditory space map in the deeper layers. J. Neurosci., 18, 9394-9408.
31. King, C.E., Wallace, A.N., Rodger, J., Bartlett, C.A., Beazley, L.D. & Dunlop, S.A. (2004) Expression of EphA3, EphA5 and ephrin-A2 in the retina during optic nerve regeneration in goldfish. Exp. Neurol., 183, 593-599.
32. Knöll, B. & Drescher, U. (2002) Ephrin-As as receptors in topographic projections. TINS, 25, 145-149.
33. Knoll, B., Isenmann, S., Kilic, E., Walkenhorst, J., Engel, S., Wehinger, J., Bahr, M. & Drescher, U. (2001) Graded expression patterns of ephrin-As in the superior colliculus after lesion of the adult mouse optic nerve. Mech. Dev., 106, 119-127.
34. Knudsen, E.I. (1982) Auditory and visual maps of space in the optic tectum of the owl. J. Neurosci., 2, 1177-1194.
35. Kuppner, M.C., Liversidge, J., McKillop-Smith, S., Lumsden, L. & Forrester, J.V. (1993) Adhesion molecule expression in acute and fibrotic sympathetic ophthalmia. Curr. Eye Res., 12, 923-934.
36. Lai, K.-O., Ip, F.C.F., Cheung, J. & Fu, A.K.Y. (2001) Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction. Mol. Cell Neurosci., 17, 1034-1047.
37. Lee, S.K., Danelian, P.S., Fritzsch, B. & McMahon, A.P. (1997) Evidence that FGF8 signalling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development, 124, 959-969.
38. Levkovitch-Verbin, H., Quigley, H.A., Kerrigan-Baumrind, L.A., D'Anna, S.A., Kerrigan, D. & Pease, M.E. (2001) Optic nerve transection in monkeys may result in secondary degeneration of retinal ganglion cells. Invest. Ophthalmol Vis. Sci., 42, 975-982.
39. Levkovitch-Verbin, H., Quigley, H.A., Martin, K.R., Zack, D.J., Pease, M.E. & Valenta, D.F. (2003) A model to study differences between primary and secondary degeneration of retinal ganglion cells in rats by partial optic nerve transection. Invest. Ophthalmol. Vis. Sci., 44, 3388-3393.
40. Linden, R. & Perry, V.H. (1983) Retrograde and anterograde- transneuronal degeneration in the parabigeminal nucleus following tectal lesions in developing rats. J. Comp. Neurol., 218, 270-281.
41. 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.
42. McLaughlin, T., Hindges, T. & O'Leary, D.D.M. (2003) Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol., 13, 57-69.
43. McLoon, S.C. (1986) Response of astrocutes in the visual system to Wallerian degeneration: an immunohistochemical analysis of laminin and glial fibrillary acidic protein (GFAP). Exp. Neurol., 91, 613-621.
44. Milner, A.D. & Taylor, M.J. (1990) Auditory orienting and detection in rats following lesions of the superior colliculus. Behav. Brain Res., 37, 293-296.
45. Moreno-Flores, M.T. & Wandosell, F. (1999) Up-regulation of Eph tyrosine kinase receptors after excitotoxic injury in adult hippocampus. Neuroscience, 91, 193-201.
46. Muller, M. & Hollander, H. (1988) A small population of retinal ganglion cells projecting to the retina of the other eye. An experimental study in the rat and the rabbit. Exp. Brain Res., 71, 611-617.
47. Perry, V.H. (1979) The ganglion cell layer of the retina of the rat: a Golgi study. Proc. R. Soc. Lond. B Biol Sci., 204, 363-375.
48. Ravin, J.G. (2004) Sir Frederick Treves and sympathetic ophthalmia. Arch. Ophthalmol., 122, 99-103.
49. Rodger, J., Bartlett, C.A., Beazley, L.D. & Dunlop, S.A. (2000) Transient up-regulation of the rostro-caudal gradient of ephrin A2 in the tectum coincides with re-establishment of orderly projections during optic nerve regeneration in goldfish. Exp. Neurol., 166, 196-200.
50. Rodger, J., Lindsey, K.A., Leaver, S.G., King, C.E., Dunlop, S.A. & Beazley, L.D. (2001) Expression of ephrin-A2 in the superior colliculus and EphA5 in the retina following optic nerve section in adult rat. Eur. J. Neurosci., 14, 1929-1936.
51. Rodger, J., Vitale, P.N., Tee, L.B.G., King, C.E., Bartlett, C.A., Fall, A., Brennan, C., O'Shea, J.E., Dunlop, S.A. & Beazley, L.D. (2004) EphA/ephrin-A interactions during optic nerve regeneration: restoration of topography and regulation of ephrin-A2 expression. Mol. Cell. Neurosci., 25, 56-68.
52. Rogers, J.H., Ciossek, T., Menzel, P. & Pasquale, E.B. (1999) Eph receptors and ephrins demarcate cerebellar lobules before and during their formation. Mech. Dev., 87, 119-128.
53. Sajjadi, F.G. & Pasquale, E.B. (1993) Five novel avian Eph-related tyrosine kinases are differentially expressed. Oncogene, 8, 1807-1813.
54. 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 hybridisation using digoxigenin-labelled cRNA probes. Histochemistry, 100, 431-440.
55. Schmidt-Kastner, R., Wietasch, K., Wiegel, H. & Eysel, U.T. (1993) Immunohistochemical staining for glial fibrillary acidic protein (GFAP) after deafferentation or ischemic infarction in rat visual system: features of reactive and damaged astroctes. Int. J. Dev. Neurosci., 11, 157-174.
56. Sefton, A.J., Dreher, D. & Harvey, A.R. (2004) Visual system. In Paxinos, G., (Ed), The Rat Nervous System, 3rd Edn. Academic Press, Sydney, pp. 169-221.
57. Smith, B.N., Banfield, B.W., Smeraski, C.A., Wilcox, C.L., Dudek, F.E., Enquist, L.W. & Pickard, G.E. (2000) Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc. Natl Acad. Sci. USA, 97, 9264-9269.
58. Sobieszczuk, D.F. & Wilkinson, D.G. (1999) Masking of Eph receptors and ephrins. Curr. Biol., 9, R469-R470.
59. Symonds, A.C.E., Rodger, J., Tan, M.M.L., Dunlop, S.A., Beazley, L.D. & Harvey, A.R. (2001) Reinnervation of the superior colliculus delays down-regulation of ephrinA2 in neonatal rat. Exp. Neurol., 170, 364-370.
60. Tu, S., Butt, C.M., Pauly, J.R. & Debski, E.A. (2000) Activity-dependent regulation of substance P expression and topographic map maintenance by a cholinergic pathway. J. Neurosci., 20, 5346-5357.
61. Wang, H.U., Chen, Z.F. & Anderson, D.J. (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell, 93, 741-753.
62. Willson, C.A., Irizarry-Ramirez, M., Gaskins, H.E., Cruz-Orengo, L., Figueroa, J.D., Whittemore, S.R. & Miranda, J.D. (2002) Upregulation of EphA receptor expression in the injured adult rat spinal cord. Cell Transplant, 11, 229-239.
63. Willson, C.A., Miranda, J.D., Foster, R.D., Onifer, S.M. & Whittemore, S.R. (2003) Transection of the adult rat spinal cord upregulates EphB3 receptor and ligand expression. Cell Transplant, 12, 279-290.
64. Withington, D.J. & McCrossan, D. (1996) Severing the intercollicular commissure prevents bilateral disruption of the map of auditory space in the superior colliculi following monocular enucleation. Neurosci. Lett., 220, 29-32.
65. Yamasaki, D.S., Krauthamer, G. & Rhoades, R. W. (1984) Organization of the intercollicular pathway in rat. Brain Res., 300, 368-371.
66. Zilles, K., Wree, A., Petrovic-Minic, B., Schleicher, A. & Beck, T. (1989) Different metabolic changes in the lateral geniculate nucleus and the superior colliculus of adult rats after simultaneous or delayed double enucleation. Brain Res., 488, 14-21.