Expression of neurotrophins and Trk receptors in the avian retina

Journal of Comparative Neurology

Volumn 364, Issue 4, 1996, Pages 664-676

  Hallböök, Finn ^a,c   Bäckström, Anders ^a   Kullander, Klas ^a   Ebendal, Ted ^a   Carri, Nestor G ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b Instituto Multidisciplinario de Biologia Celular   (Argentina)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

embryonic development; horizontal cells; mRNA regulation; retinal ganglion cells; visual system

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CELL SURFACE RECEPTOR; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPHIN RECEPTOR; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CHICK EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RETINA DEVELOPMENT; RETINA GANGLION CELL; RETINA HORIZONTAL NERVE CELL; VISUAL SYSTEM;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CHICK EMBRYO; DARKNESS; IN SITU HYBRIDIZATION; LIGHT; NERVE FIBERS; NERVE GROWTH FACTORS; NEUROTROPHIN 3; RECEPTOR PROTEIN-TYROSINE KINASES; RETINA; RETINAL GANGLION CELLS; RIBONUCLEASES; RNA; RNA, MESSENGER; UP-REGULATION;

EID: 0030041588     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19960122)364:4<664::aid-cne5>3.3.co;2-e     Document Type: Article

References (85)

1. Adler, R., and D. Farber (1986) The retina: A model for cell biology studies. In R. Alder and D. Farber (eds.): Cellular Neurobiology. Orlando, FL: Academic Press, p. 365.
2. Barde, Y.-A., D. Edgar, and H. Thoenen (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1:549-553.
3. Berkemeier, L.R., J.W. Winslow, D.R. Kaplan, K. Nikolics, D.V. Goeddel, and A. Rosenthal (1991) Neurotrophin-5: A novel neurotrophic factor that activates trk and trkB. Neuron 7:857-866.
4. Buchmann, V.L., and A.M. Davies (1993) Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118:989-1001.
5. Carri, N.G., and T. Ebendal (1983) Organotypic cultures of neural retina: Neunte growth stimulated by brain extracts. Dev. Brain Res. 6:219-229.
6. Carri, N.G., and T. Ebendal (1987) Target-field specificity in the induction of retinal neurite outgrowth. Dev. Brain Res. 31:83-90.
7. Case, C.P., and C.J. Plummer (1993) Changing the light intensity of the visual environment results in large differences in numbers of synapses and in photoreceptor size in the retina of the young adult rat. Neuroscience 55:653-666.
8. Castrén, E., F. Zafra, H. Thoenen, and D. Lindholm (1992) Light regulates expression of brain-derived neuronotrophic factor in rat visual cortex. Proc. Natl. Acad. Sci. USA 89:9444-9448.
9. Catsicas, S., and P.G.H. Clarke (1987) Abrupt loss of dependence of retinopetal neurons on their target cells, as shown by intraocular injections of kainate in chick embryos. J. Comp. Neurol. 262:523-534.
10. Clarke, P.G.H., L.A. Rogers, and W.M. Cowan (1976) The time of origin and the pattern of survival of neurons in the isthmo-optic nucleus of the chick. J. Comp. Neurol. 167:125-141.
11. Cohen-Cory, S., and S.E. Fraser (1994) BDNF in the development of the visual system of Xenopus. Neuron 22:747-761.
12. Crowly, C., S.D. Spencer, M.C. Nishimura, K.S. Chen, S. Pitts-Meek, M.P. Armanini, L.H. Ling, S.B. McMahon, D.L. Shelton, A.D. Levinson, and H.P. Phillips (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011.
13. Cui, Q., and A.R. Harvey (1994) NT4/5 reduces naturally occurring retinal ganglion cell death in neonatal rats. Neuroreport 5:1882-1884.
14. Davies, A.M., C. Bandtlow, R. Heumann, S. Korsching, H. Rohrer, and H. Thoenen (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353-358.
15. de Araujo, E.G., and R. Linden (1993) Trophic factors produced by retinal cells increase the survival of retinal ganglion cells in vitro. Eur. J. Neurosci. 5:1181-1188.
16. De la Rosa, E.J., A. Arribas, J.M. Frade, and A. Rodríguez-Tebár (1994) Role of neurotrophins in the control of neural development and survival of cultured chick retinal cells. Neuroscience 55:347-352.
17. Dechant, G., S. Biffo, H. Okazawa, R. Kolbeck, J. Pottgiesser, and Y. Barde (1993) Expression and binding characteristics of the BDNF receptor chick trkB. Development 119:545-558.
18. Ebendal, T., and H. Persson (1988) Detection of nerve growth factor mRNA in the developing chicken embryo. Development 102:101-106.
19. Ebendal, T., D. Larhammar, and H. Persson (1986) Structure and expression of the chicken β nerve growth factor. EMBO J. 5:1483-1487.
20. Ernfors, P., and H. Persson (1991) Developmentally regulated expression of HDNF/NT-3 mRNA in rat spinal cord motoneurons and detection of BDNF mRNA in embryonic dorsal root ganglia. Eur. J. Neurosci. 3:953-961.
21. Ernfors, P., C.F. Ibán̄ez, T. Ebendal, L. Olson, and H. Persson (1990) Molecular cloning and neurotrophic activities of a protein with structural similarities to β-nerve growth factor: Developmental and topographical expression in the brain. Proc. Natl. Acad. Sci. USA 87:5454-5458.
22. Ernfors, P., J. Merliot, and H. Persson (1992) Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 4:1140-1158.
23. Ernfors, P., K.-F. Lee, and R. Jaenisch (1994) Mice lacking BDNF develop with sensory deficits. Nature 368:147-150.
24. Farber, D., and R. Adler (1986) Issues and questions in cell biology of the retina. In R. Adler and D. Farber (eds.): The Retina: A Model for Cell Biology Studies. Orlando, FL: Academic Press, pp. 2-16.
25. Hallböök, F., T. Ebendal, and H. Persson (1988) Production and expression of biologically active recombinant beta nerve growth factor. Mol. Cell. Biol. 8:452-456.
26. Hallböök, F., C. Ibàn̄ez, and H. Persson (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6:845-858.
27. Hallböök, F., C.F. Ibán̄ez, T. Ebendal, and H. Persson (1993) Cellular localization of brain-derived neurotrophic factor and neurotrophin-3 mRNA in the early chicken embryo. Eur. J. Neurosci. 5:1-14.
28. Hallöök, F., T. Ebendal, and N. Carri (1995) Neutrophins in the developing avian visual system. In C. F. Iban̄ez, T. Hökfelt, H. Jörnvall, L. Olson, K. Fuxe, and D. Ottoson (eds.): Life and death in the nervous system; role of neurotrophins and their receptors. Wenner-Greene international series vol 67 Oxford: Elsevier Science Limited, pp. 143-153.
29. Hammang, J.P., R.R. Behringer, E.E. Baetge, R.D. Palmiter, R.L. Brinster, and A. Messing (1993) Oncogene expression in retinal horizontal cells of transgenic mice results in a cascade of neurodegeneration. Neuron 10:1197-1209.
30. Herzog, K.-H., K. Bailey, and Y.-A. Barde (1994) Expression of the BDNF gene in the developing visual system of the chick. Development 120:324-331.
31. Heyes, B.P., and A.L. Holden (1983) The distribution of centrifugal terminals in the pigeon retina. Exp. Brain Res. 49:189-197.
32. Hohn, A., J. Leibrock, K. Bailey, and Y.-A. Barde (1990) Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 344:339-341.
33. Hughes, W.F., and A. LaVelle (1974) On synaptogenic sequence in the chick retina. Anat. Rec. 179:297-302.
34. Hughes, W.F., and A. LaVelle (1975) The effects of early tectal lesions on development in the retinal ganglion cell layer of chicken embryos. J. Comp. Neurol. 163:256-284.
35. Hughes, W.F., and S.C. McLoon (1979) Ganglion cell death during normal retinal development in the chick: Comparisons with cell death induced by early target destruction. Exp. Neurol. 66:587-601.
36. Ibán̄ez, C.F., F. Hallböök, S. Söderström, T. Ebendal, and H. Persson (1991) Biological and immunological properties of recombinant human, rat and chicken nerve growth factors: A comparative study. J. Neurochem. 57:1033-1041.
37. Ibán̄ez. C.F., P. Ernfors, T. Timmusk, N.Y. Ip, E. Arenas, G.D. Yancopoulos, and H. Persson (1993) Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development 117:1345-1353.
38. Isackson, P.J., M.D. Towner, and M.M. Huntsman (1991) Comparison of mammalian, chicken and Xenopus brain-derived neurotrophic factor coding sequences. FEBS Lett. 285:260-264.
39. Jelsma, T.N., H.H. Friedman, M. Berkelaar, G.M. Bray, and A.J. Aguayo (1993) Different forms of neurotrophin receptor trkB mRNA predominate in rat retina and optic nerve. J. Neurobiol. 24:1207-1214.
40. Johnson, J.E., Y.-A. Barde, M. Schwab, and H. Thoenen (1986) Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J. Neurosci. 6:3031-3038.
41. Jones, K.R., I. Farinas, C. Backus, and L.F. Reichardt (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
42. Kaisho, Y., K. Yoshimura, and K. Nakahama (1990) Cloning and expression of a cDNA encoding a novel human neurotropic factor. FEBS Lett. 266:187-191.
43. Kalcheim, C., C. Carmeli, and A. Rosenthal (1992) Neurotrophin-3 is a mitogen for cultured neural crest cells. Proc. Natl. Acad. Sci. USA 89:1661-1665.
44. Kaplan, D.R., B.L. Hempsted, D. Martin-Zanca, M.V. Chao, and L.F. Parada (1991) The trk proto-oncogene product: A signal transducing receptor for nerve growth factor. Science 252:554-558.
45. Karten, H.J., L.F. Reichardt, D.O. Clary, and K.T. Keyser (1995) TRK A receptors reveal a new class of non-GABAergic horizontal cells in the avian retina. ARVO Abstr. Invest. Ophtalmol. Vis. Sci. 36:S256.
46. Klein, R., F. Lamballe, S. Bryant, and M. Barbacid (1992) The trkB tyrosine protein kinase is a receptor for neurotrophin-4. Neuron 8:947-956.
47. Kullander, K., and T. Ebendal (1994) Neurotrophin-3 acquires NGF-like activity after exchange to five NGF amino acid residues: Molecular analysis of the sites in NGF mediating the specific interaction with the NGF high affinity receptor. J. Neurosci. Res. 39:195-210.
48. Lamballe, F., R. Klein, and M. Barbacid (1991) TrkC, a new member of the trk family of tyrosin protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979.
49. Lamballe, F., P. Tapley, and M. Barbacid (1993) trkC Encodes multiple neurotrophin-3 receptors with distinct biological properties and substrate specificities. EMBO J. 12:3083-3094.
50. Levi-Montalcini, R., and V. Hamburger (1951) Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J. Exp. Zool. 116:321-361.
51. Linden, R. (1993) Dendritic competition in the developing retina: Ganglion cell density gradients and laterally displaced dendrites. Vis. Neurosci. 70:313-324.
52. Linden, R., and V.H. Perry (1982) Evidence for dendritic competition in the developing retina. Nature 297:683-684.
53. Lindvall, O., P. Ernfors, J. Bengzon, Z. Kokaia, M.L. Smith, B.K. Siesjö, and H. Persson (1992) Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. Natl. Acad. Sci. USA 89:648-652.
54. Maisonpierre, P.C., L. Belluscio, S. Squinto, N.Y. Ip, M.E. Furth, R.M. Lindsay, and G.D. Yancopoulos (1990) Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247:1446-1451.
55. Marc, R.E. (1986) The development of retinal networks. In R. Adler and D. Farber (eds.): The Retina: A Model for Cell Biology Studies. Orlando, FL: Academic Press, pp. 17-59.
56. Martin-Zanca, D., R. Oskam, G. Mitra, T. Copeland, and M. Barbacid (1989) Molecular and biochemical characterization of the human trk protooncogene. Mol. Cell Biol. 9:24-33.
57. Maturana, H.R., and S. Frenk (1965) Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150:359-361.
58. McCaffery, C.A., M.R. Bennet, and B. Dreher (1982) The survival of rat retinal ganglion cells in vitro is enhanced in the presence of appropriate part of the brain. Exp. Brain Res. 48:377-386.
59. Merlio, J.P., P. Ernfors, Z. Kokaia, D.S. Middlemas, J. Bengzon, M. Kokaia, M.L. Smith, B.K. Siesjö, T. Hunter, and O. Lindvall, and H. Persson (1993) Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron 10:151-64.
60. Mey, J., and S. Thanos (1992a) Development of the visual system of the chick - A review. J. Hirnforsch 33:673-702.
61. Mey, J., and S. Thanos (1992b) Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res. 602:304-317.
62. O'Leary, D.D.M., and W.M. Cowan (1984) Survival of isthmo-optic neurons after early removal of one eye. Dev. Brain Res. 12:293-310.
63. Okazawa, H., M. Kamei, and I. Kanazawa (1993) Molecular cloning and expression of a novel truncated form of chicken trkC. FEBS Lett. 329:171-177.
64. Okazawa, H., M. Kamei, I. Imafuku, and I. Kanazawa (1994) Gene regulation of trkB and trkC in the chick retina by light/darkness exposure. Oncogene 9:1813-1818.
65. Panabières, F., M. Piechacsyk, B. Rainer, C. Dani, P. Fort, S. Riaad, L. Marty, J.L. Imbach, P. Jeanteur, and J.M. Blanchard (1984) Complete nucleotide sequence of the messenger RNA coding for chicken muscle glyceraldehyde-3-phosphate dehydrogenase. Biochem. Biophys. Res. Commun. 118:767-773.
66. Rager, G., and U. Rager (1976) Generation and degeneration of retinal ganglion cells in the chick. Exp. Brain Res. 25:551-553.
67. Reiner, A., N. Brecha, and H.J. Karten (1979) A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4:1679-1688.
68. Rodriguez-Tébar, A., and Y.A. Barde (1988) Binding characteristics of brain-derived neurotrophic factor to its receptors on neurons from the chick embryo. J. Neurosci. 8:3337-3342.
69. Rodriguez-Tébar, A., P.L. Jafferey, H. Thoenen, and Y. Barde (1989) The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor on their embryonic age. Dev. Biol. 136:296-303.
70. Rodriguez-Tébar, A., E.J. Rosa, and A. Arribas (1993) Neurotrophin receptors in the developing chicken retina. Eur. J. Biochem. 211:789-794.
71. Rosenthal, A., D.V. Goeddel, T. Nguyen, M. Lewis, A. Shih, G.R. Laramee, K. Nikolics, and J.W. Winslow (1990) Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4:767-773.
72. Schecterson, L.C., and M. Bothwell (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
73. Sieber-Blum, M. (1992) Role of the neurotrophic factors BDNF and NGF in the commitment of pluripotent neural crest cells. Neuron 6:949-955.
74. Söderström, S., F. Hallböök, C.F. Ibán̈ez, H. Persson, and T. Ebendal (1990) Recombinant human beta-nerve growth factor (NGF): Biological activities and properties in an enzyme immuno assay. J. Neurosci. Res. 27:665-677.
75. Soppet, D., E. Escandon, J. Maragos, D.S. Middlemas, S.W. Reid, J. Blair, L.E. Burton, B.R. Stanton, D.R. Kaplan, T. Hunter, K. Nikolics, and L.F. Parada (1991) The neurotrophic factors brain-derived neurotrophic factors and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
76. Spence, S.G., and J.A. Robson (1989) An autoradiographic analysis of neurogenesis in the chick retina in vitro and in vivo. Neuroscience 32:801-812.
77. Takahashi, J.B., M. Hoshimaru, H. Kikuchi, and M. Hatanaka (1993) Developmental expression of trkB and low-affinity receptor in the rat retina. Neurosci. Lett. 151:174-177.
78. Tsoulfas, P., D. Soppet, E. Escandon, L. Tessarollo, R.J. Mendoza, A. Rosenthal, K. Nikolics, and L.F. Parada (1993) The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10:975-990.
79. Valenzuela, D.M., P.C. Maisonpierre, D.J. Glass, E. Rojas, L. Nunez, Y. Kong, D.R. Gies, T.N. Stitt, N.Y. Ip, and G.D. Yancopoulos (1993) Alternative forms of rat TrkC with different functional capabilities. Neuron 10:963-974.
80. Vogel, K.S., and A.M. Davies (1991) The duration of neurotrophic factor independence in early sensory neurons is matched to the time course of target field innervation. Neuron 7:819-830.
81. von Bartheld, C.S., Y. Kinoshita, D. Prevette, Q.-W. Yin, R.W. Oppenheim, and M. Bothwell (1993) Positive and negative effects of neurotrophins on the isthmo-optic nucleus in the chick embryo. Neuron 12:639-654.
82. Williams, R., A. Bäckström, T. Ebendal, and F. Hallböök (1993) Molecular cloning and cellular localization of trkC in the chicken embryo. Dev. Brain Res. 75:235-252.
83. Wright, E.M., K.S. Vogel, and A.M. Davies (1992) Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival. Neuron 9:139-150.
84. Zafra, F., B. Hengerer, J. Leibrock, H. Thoenen, and D. Lindholm (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9:3545-3550.
85. Zanellato, A., M.C. Comelli, R.D. Toso, and G. Carmignoto (1993) Developing rat retinal ganglion cells express the functional NGF receptor p140trkA. Dev. Biol. 159:105-113.