Expression of TrkB receptor isoforms in the developing avian visual system

Journal of Neuroscience

Volumn 16, Issue 5, 1996, Pages 1740-1752

  Garner, Andrew S ^a   Menegay, Harry J ^a   Boeshore, Kristen L ^a   Xie, Xiao Yi ^a   Voci, James M ^a   Johnson, James E ^b   Large, Thomas H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

alternative splicing; chicken; retina; tectum; TrkB receptor; visual system

Indexed keywords

ARTICLE; CHICK EMBRYO; EMBRYO; EYE DEVELOPMENT; MOLECULAR CLONING; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VISUAL SYSTEM;

EID: 0029966646     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-05-01740.1996     Document Type: Article

References (91)

1. Acheson A, Conover JC, Fandl JP, DeChiara TM, Russell MP, Thadani A, Squinto SP, Yancopoulos GD, Lindsay RM (1995) A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450-453.
2. Allendoerfer KL, Cabelli RJ, Escandon E, Kaplan DR, Nikolics K, Shatz CJ (1994) Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J Neurosci 14:1795-1811.
3. Barbacid M (1994) The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
4. Benedetti M, Levi A, Chao MV (1993) Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc Natl Acad Sci USA 90:7859-7863.
5. Biffo S, Carter B, Offenhauser N, Barde Y-A (1995) Truncated TrkB restricts BDNF availability during development: expression pattern and biochemical properties. Soc Neurosci Abstr 21:1060.
6. Birren SJ, Verdi JM, Anderson DJ (1992) Membrane depolarization induces p140trk and NGF responsiveness, but not p75 LNGFR, in MAH cells. Science 257:395-397.
7. Cabelli RJ, Hohn A, Shatz CJ (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267:1662-1666.
8. Cantino D, Sisto-Daneo L (1973) Synaptic junctions in the developing chick optic tectum. Experientia 29:85-87.
9. Catsicas M, Pequignot Y, Clarke PGH (1992) Rapid onset of neuronal death induced by blockade of either axoplasmic transport or action potentials in afferent fibers during brain development. J Neurosci 12:4642-4650.
10. Chomczynski P (1992) One hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal Biochem 201:134-139.
11. Clarke PGH, Rogers LA, Cowan WM (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.
12. Clarke PGH (1985) Neuronal death during development in the isthmo-optic nucleus of the chick: sustaining role of afferents from the tectum. J Comp Neurol 234:365-379.
13. Clarke PGH (1992) Neuron death in the developing avian isthmo-optic nucleus, and its relation to the establishment of functional circuitry. J Neurobiol 23:1140-1158.
14. Clary DO, Reichardt LF (1994) An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response to neurotrophin 3. Proc Natl Acad Sci USA 91:11133-11137.
15. Cohen-Cory S, Fraser SE (1994) BDNF in the development of the visual system of Xenopus. Neuron 12:747-761.
16. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
17. Dechant G, Biffo S, Okazawa H, Kolbeck R, Pottgiesser J, Barde Y-A (1993) Expression and binding characteristics of the BDNF receptor chick TrkB. Development 119:545-558.
18. Drescher U, Kremoser C, Handwerker C, Loschinger 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 kinase. Cell 82:359-370.
19. Dugich-Djordjevic MM, Ohsawa F, Okazaki T, Mori N, Day JR, Beck KD, Hefti F (1995) Differential regulation of catalytic and non-catalytic trkB mRNA in the rat hippocampus following seizures induced by systemic administration of kainate. Neuroscience 66:861-877.
20. Ehrlich D, Mark R (1984) An atlas of the primary visual projections in the brain of the chick Gallus gallus. J Comp Neurol 223:592-610.
21. Escandon E, Soppet D, Rosenthal A, Mendoza-Ramirez J-L, Szonyi E, Burton LE, Henderson CE, Parada LF, Nikolics K (1994) Regulation of neurotrophin receptor expression during embryonic and postnatal development. J Neurosci 14:2054-2068.
22. Garner AS, Large TH (1993) Alternate splicing of the trkC tyrosine kinase dissociates process outgrowth from survival. Soc Neurosci Abstr 19:1477.
23. Garner AS, Large TH (1994) Isoforms of the avian TrkC receptor: a novel kinase insertion dissociates transformation and process outgrowth from survival. Neuron 13:457-472.
24. Ghosh A, Camahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618-1623.
25. Golde TE, Estus S, Usiak M, Younkin LH, Younkin SG (1990) Expression of β-amyloid protein precursor mRNAs: recognition of a novel alternatively spliced form and quantitation in Alzheimer's Disease using PCR. Neuron 4:253-267.
26. Goldschmidt-Clermont PJ, Kim JW, Machesky LM, Rhee SG, Pollard TD (1991) Regulation of phospholipase Cγ by profilm and tyrosine phosphorylation. Science 251:1231-1233.
27. Guillemot F, Cepko CL (1992) Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an in vitro assay of early retinal development. Development 114:743-754.
28. Hamburger V, Hamilton H (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
29. Herzog K-H, Barde Y-A (1994) BDNF mRNA levels in the chick optic tectum are regulated by neurotransmitters during synaptogenesis. Soc Neurosci Abstr 20:1304.
30. Herzog K-H, Bailey K, Barde Y-A (1994) Expression of the BDNF gene in the developing visual system of the chick. Development 120:1643-1649.
31. Holtzman DM, Li Y, Parada LF, Kinsman S, Chen CK, Valletta JS, Zhou J, Long JB, Mobley WC (1992) p140trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron 9:465-478.
32. Horikoshi T, Danenberg KD, Stadlbauer THW, Volkenandt M, Shea LC, Aigner K, Gustavsson B, Leichman L, Frosing R, Ray M, Gibson NW, Spears CP, Danenberg PV (1992) Quantitation of thymidylate synthase, dihydrofolate reductase, and DT-diaphorase gene expression in human tumors using the polymerase chain reaction. Cancer Res 52:108-116.
33. Hughes WF, McLoon SC (1979) Ganglion cell death during normal retinal development in the chick: comparisons with cell death induced by early target field destruction. Exp Neurol 66:587-601.
34. Hunt SP, Kunzle H (1976) Observations on the projections and intrinsic organization of the pigeon optic tectum: an autoradiographic study based on anterograde and retrograde axonal and dendritic flow. J Comp Neurol 170:153-172.
35. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993) Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
36. Jelsma TN, Friedman HH, Berkelaar M, Bray GM, Aguayo AJ (1993) Different forms of the neurotrophin receptor TrkB mRNA predominate in rat retina and optic nerve. J Neurobiol 24:1207-1214.
37. Johnson JE, Barde Y-A, Schwab M, Thoenen H (1986) Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J Neurosci 6:3031-3038.
38. Kahn AJ (1973) Ganglion cell formation in the chick neural retina. Brain Res 63:285-290.
39. Kang H, Schuman EM (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
40. Kelly JP, Cowan WM (1972) Studies on the development of the chick optic tectum. III. Effects of early eye removal. Brain Res 42:263-288.
41. Kirkwood A, Lee H-K, Bear MF (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375:328-331.
42. Klein R, Conway D, Parada LF, Barbacid M (1990) The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647-656.
43. Knusel B, Rabin SJ, Hefti F, Kaplan DR (1994) Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J Neurosci 14:1542-1554.
44. Kokaia Z, Bengzon J, Metsis M, Kokaia M, Persson H, Lindvall O (1993) Coexpression of neurotrophins and their receptors in neurons of the central nervous system. Proc Natl Acad Sci USA 90:6711-6715.
45. Lamballe F, Tapley P, Barbacid M (1993) TrkC encodes multiple neurotrophin-3 receptors with distinct biological properties and substrate specificities. EMBO J 12:3083-3094.
46. Large TH, Rauh JJ, DeMello FG, Klein WL (1985) Two molecular weight forms of muscarinic acetylcholine receptors in the avian central nervous system: switch in predominant form during differentiation of synapses. Proc Natl Acad Sci USA 82:8785-8789.
47. Large TH, Weskamp G, Helder JC, Radeke MJ, Misko TP, Shooter EM, Reichardt LF (1989) Structure and developmental expression of the nerve growth factor receptor in the chicken central nervous system. Neuron 2:1123-1134.
48. LaVail JH, Cowan WM (1971) The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res 28:391-419.
49. Lohof AM, Ip NY, Poo MM (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350-353.
50. Mansour-Robaey S, Clarke DB, Wang Y-C, Bray GM, Aguayo AJ (1994) Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc Natl Acad Sci USA 91:1632-1636.
51. Meakin SO, Suter U, Drinkwater CC, Welcher AA, Shooter EM (1992) The rat trk protooncogene product exhibits properties characteristic of the slow nerve growth factor receptor. Proc Natl Acad Sci USA 89:2374-2378.
52. Mey J, Thanos S (1992) Development of the visual system of the chick - a review. J Hirnforsch 33:673-702.
53. Mey J, Thanos S (1993) Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res 602:304-317.
54. Middlemas DS, Lindberg RA, Hunter T (1991) TrkB, a neural receptor prorein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 11:143-153.
55. Nishio T, Furukawa S, Akiguchi I, Oka N, Ohnishi K, Tomimoto H, Nakamura S, Kimura J (1994) Cellular localization of nerve growth factor-like immunoreactivity in adult rat brain: quantitative and immunohistochcmical study. Neuroscience 60:67-84.
56. Okazawa H, Nishiyama K, Kamei M, Washizaki K, Murayama S, Kwak S, Kanazawa I (1994a) Trk immunoreactivity at neuronal dendrite and cell body. Biochem Biophys Res Commun 194:683-690.
57. Okazawa H, Kamei M, Imafuku I, Kanazawa I (1994b) Gene regulation of TrkB and TrkC in the chick retina by light/darkness exposure. Oncogene 9:1813-1818.
58. Page TP, Jaboro NG, Crossland WJ (1993) Retrograde transneuronal degeneration in a basal ganglia target, the lateral spiriform nucleus, induced by anterograde transneuronal degeneration following eye removal in the chicken. Exp Neurol 119:120-127.
59. Peng X, Greene LA, Kaplan DR, Stephens RM (1995) Deletion of a conserved juxtamembrane sequence in trk abolishes NGF-promoted neuritogenesis. Neuron 15:395-406.
60. Perez P, Coll PM, Hempstead BL, Martin-Zanca D, Chao MV (1995) NGF binding to the trk tyrosine kinase receptor requires the extracellular immunoglobulin-like domains. Mol Cell Neurosci 6:97-105.
61. Pollard TD, Almo S, Quirk S, Vinson V, Lattman EE (1994) Structure of actin binding proteins: insights about function at atomic resolution. Annu Rev Cell Biol 10:207-249.
62. Radeke MJ, Baxter G, Kuo R, Medina-Selby A, Coit D, Valenzuela P. Feinstein SC (1994) Signal transduction by the truncated TrkB isoform T1. Soc Neurosci Abstr 20:37.
63. Rager GH (1976) Morphogenesis and physiogenesis of the retino-tectal connection in the chicken. II. The retino-tectal synapses. Proc R Soc Lond [Biol] 192:353-370.
64. Rager GH, Rager U (1978) Systems-matching by degeneration. I. A quantitative electron microscopic study of the generation and degeneration of retinal ganglion cells in the chicken. Exp Brain Res 33:65-78.
65. Rager GH, von Oeynhausen B (1979) Ingrowth and ramification of retinal fibers in the developing optic tectum of the chick embryo. Exp Brain Res 35:213-227.
66. Rager GH (1980) Development of the retinotectal projection in the chicken. Adv Anat Embryol Cell Biol 63:1-92.
67. Rch TA, Tully T (1986) Regulation of tyrosine hydroxylase-containing amacrine cell number in larval frog retina. Dev Biol 114:463-469.
68. Reiner A, Brecha NC, Karten HJ (1982) Basal ganglia pathways to the tectum: the afferent and efferent connections of the lateral spiriform nucleus of pigeon. J Comp Neurol 208.16-36.
69. Rodriguez-Tebar A, Jeffrey PL, Thoenen H, Barde Y-A (1989) The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor depends on their embryonic age. Dev Biol 136:296-303.
70. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487-491.
71. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissues and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochem J 100:431-440.
72. Schechter AL, Bothwell MA (1981) Nerve growth factor receptors on PC12 cells: evidence for two receptor classes with differing cytoskeleton association. Cell 24:867-874.
73. Schecterson LC, Bothwell M (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
74. Schutt CE, Myslik JC, Rozycki MD, Goonsekere NC, Lindberg U (1993) The structure of crystalline profilin-β-actin. Nature 365:810-816.
75. Shelton DL, Sutherland J, Gripp J, Camerato T, Armanini MP, Phillips HS, Carroll K, Spencer SD, Levinson AD (1995) Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J Neurosci 15:477-491.
76. Takahashi JB, Hoshimaru M, Kikuchi H, Hatanaka M (1993) Developmental expression of trkB and low-affinity NGF receptor in the rat retina. Neurosci Lett 151:174-177.
77. Thanos S, Bonhoeffer F (1983) Investigations on the development and topographic order of retinotectal axons: anterograde and retrograde staining of axons and perikarya with rhodamine in vivo. J Comp Neurol 219:420-430.
78. Thanos S, Bonhoeffer F (1987) Axonal arborization in the developing chick retinotectal system. J Comp Neurol 261:155-164.
79. Theriot JA, Mitchison TJ (1993) The three faces of profilin. Cell 75:835-838.
80. Tsoulfas P, Soppet D, Escandon E, Tessarollo L, Mendoza-Ramirez J-L, Rosenthal A, Nikolics K, Parada LF (1993) The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10:975-990.
81. Turner DL, Snyder EY, Cepko CL (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4:833-845.
82. Urfer R, Tsoulfas P, O'Connell L, Shelton DL, Parada LF, Presta CG (1995) An immunoglobulin-like domain determines the specificity of neurotrophin receptor. EMBO J 14:2795-2805.
83. Valenzuela DM, Maisonpierre PC, Glass DJ, Rojas E, Nunez L, Kong Y, Gies DR, Stitt TN, Ip NY, Yancopoulos GD (1993) Alternative forms of rat TrkC with different functional capabilities. Neuron 10:963-974.
84. Voci JM, McKeon RJ, Large TH (1993) Retroviral delivery of neurotrophin genes into embryonic chick retina. Soc Neurosci Abstr 19:722.
85. von Bartheld CS, Schecterson LC, Bothwell M (1993) Retrograde and anterograde transport of neurotrophins from the eye to the brain in chick embryos. Soc Neurosci Abstr 19:1101.
86. von Banheld CS, Kinoshita Y, Prevette D, Yin Q-W, Oppenheim RW, Bothwell M (1994) Positive and negative effects of neurotrophins on the isthmo-optic nucleus in chick embryos. Neuron 12:639-654.
87. von Bartheld CS, Byers MR, Williams R, Bothwell M (1995) Anterograde transport and axo-dendritic transfer of neurotrophins in the developing visual system. Soc Neurosci Abstr 21:1300.
88. Wetmore C, Olson L, Bean AJ (1994) Regulation of BDNF expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J Neurosci 14:1688-1700.
89. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types in the frog retina. Science 239:1142-1145.
90. Wong ROL, Chernjavsky A, Smith SJ, Shatz CJ (1995) Early functional neural networks in the developing retina. Nature 374:716-718.
91. Xie X-Y, Garner AS, Voci JM, Large TH (1992) Neurotrophin expression in the developing chick retina. Soc Neurosci Abstr 18:1289.