A kinase insert isoform of rat TrkA supports nerve growth factor- dependent cell survival but not neurite outgrowth

Journal of Neurochemistry

Volumn 69, Issue 3, 1997, Pages 954-967

  Meakin, Susan O ^a,b   Gryz, Ela A ^a,b   MacDonald, James I S ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Mutagenesis; Nerve growth factor receptor; Neurotrophin; Signaling; Survival; TrkA

Indexed keywords

NERVE GROWTH FACTOR; PHOSPHOTRANSFERASE;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL SURVIVAL; ENZYME ACTIVITY; ENZYME BINDING; GROWTH REGULATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0030836527     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69030954.x     Document Type: Article

References (57)

1. Altin J. G., Kujubu D. A., Raffioni S., Eveleth D. D., Herschman H. R., and Bradshaw R. A. (1991) Differential induction of primary-response (TIS) genes in PC12 pheochromocytoma cells and the unresponsive variant PC12nnr5. J. Biol. Chem. 266, 5401-5406.
2. Barbacid M. (1994) The Trk family of neurotrophin receptors. J. Neurobiol. 25, 1386-1403.
3. Barker P. A., Lomen-Hoerth C., Gensch E. M., Meakin S. O., Glass D. J., and Shooter E. M. (1993) Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J. Biol. Chem. 268, 15150-15157.
4. 125I-nerve growth factor with PC12 pheochromocytoma cells. Evidence for internalization via high-affinity receptors only and for long-term regulation by nerve growth factor of both high- and low-affinity receptors. J. Biol. Chem. 259, 15509-15516.
5. Birren S. J., Lo L., and Anderson D. J. (1993) Sympathetic neuroblasts undergo a developmental switch in trophic dependence. Development 119, 597-610.
6. Burgering B. M. T. and Coffer P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376, 599-602.
7. Canossa M., Rovelli G., and Shooter E. M. (1996) Transphosphorylation of the neurotrophin Trk receptors. J. Biol. Chem. 271, 5812-5818.
8. Chao M. V., Bothwell M. A., Ross A. H., Koprowski H., Lanahan A. A., Buck C. R., and Sehgal A. (1986) Gene transfer and molecular cloning of the human NGF receptor. Science 232, 518-521.
9. Clary D. O. and Reichardt L. F. (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.
10. Cohen G. B., Ren R., and Baltimore D. (1995) Modular binding domains in signal transduction proteins. Cell 80, 237-248.
11. Cordon-Cardo C., Tapley P., Jing S., Nanduri V., O'Rourke E., Lamballe F., Kovary K., Klein R., Jones K. R., Reichardt L. F., and Barbacid M. (1991) The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66, 173-183.
12. Creedon D. J., Johnson E. M. Jr., and Lawrence J. C. Jr. (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J. Biol. Chem. 271, 20713-20718.
13. Curran T., Gordon M. B., Rubino K. L., and Sambucetti L. C. (1987) Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modifications in vitro. Oncogene 2, 79-84.
14. Danielson P. E., Douglass J., Forss-Petter S., Milner R. J., Brow M. A., Sutcliffe J. G., and Calavetta L. (1988) p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7, 261-267.
15. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M., Segal R. A., Kaplan D. R., and Greenberg M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
16. Eide F. F., Vining E. R., Eide B. L., Zang K., Wang X.-Y., and Reichardt L. F. (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J. Neurosci. 16, 3123-3129.
17. Franke T. F., Yang S., Chan T. O., Datta K., Kazlauskas A., Morrison D. K., Kaplan D. R., and Tsichlis P. N. (1985) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81, 727-736.
18. Franke T. F., Kaplan D. R., Cantley L. C., and Toker A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275, 665-668.
19. Glass D. J. and Yancopoulos G. D. (1993) The neurotrophins and their receptors. Trends Cell Biol. 3, 262-268.
20. Green S. H., Rydel R. E., Connolly J. L., and Greene L. A. (1986) PC12 cell mutants that possess low-but not high-affinity nerve growth factor receptors neither respond to nor internalize nerve growth factor. J. Cell Biol. 102, 830-843.
21. Greene L. A. and Tischler A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73, 2424-2428.
22. Guiton M., Gunn-Moore F. J., Stitt T. N., Yancopoulos G. D., and Tavaré J. M. (1994) Identification of in vivo brain-derived neurotrophic factor-stimulated autophosphorylation sites on the TrkB receptor tyrosine kinase by site-directed mutagenesis. J. Biol. Chem. 269, 30370-30377.
23. Guiton M., Gunn-Moore F. J., Glass D. J., Geis D. R., Yancopoulos G. D., and Tavaré J. M. (1995) Naturally occurring tyrosine kinase inserts block high affinity binding of phospholipase Cγ-1 and Shc to TrkC and neurotrophin-3 signaling. J. Biol. Chem. 270, 20384-20390.
24. Hosang M. and Shooter E. M. (1987) The internalization of nerve growth factor by high-affinity receptors of pheochromocytoma PC12 cells. EMBO J. 6, 1197-1202.
25. Hubbard S. R., Wei L., Ellis L., and Hendrickson W. A. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372, 746-754.
26. Ip N. Y., Stitt T. N., Tapley P., Klein R., Glass D. J., Fandl J., Greene L. A., Barbacid M., and Yancopoulos G. D. (1993) Similarities and differences in the way neurotrophins interact with the trk receptors in neuronal and nonneuronal cells. Neuron 10, 137-149.
27. Jing S., Tapley P., and Barbacid M. (1992) Nerve growth factor mediates signal transduction through trk homodinier receptors. Neuron 9, 1067-1079.
28. Kaplan D. R. and Stephens R. M. (1994) Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25, 1404-1417.
29. Kaplan D. R., Hempstead B. L., Martin-Zanca D., Chao M. V., and Parada L. F. (1991) The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252, 554-558.
30. Klein R., Jing S., Nanduri V., O'Rourke E., and Barbacid M. (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65, 189-197.
31. Laemmli U. K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685.
32. Lamballe F., Tapley P., and Barbacid M. (1993) trkC encodes multiple neurotrophin-3 receptors with distinct biological properties and substrate specificities. EMBO J. 12, 3083-3094.
33. Large T. H., Weskamp G., Helder J. C., Radeke M. J., Misko T. P., Shooter E. M., and Reichardt L. F. (1989) Structure and developmental expression of the nerve growth factor receptor in the chicken central nervous system. Neuron 2, 1123-1134.
34. Levi-Montalcini R. (1987) The nerve growth factor 35 years later. Science 237, 1154-1162.
35. Loeb D. M., Maragos J., Martín-Zanca D., Chao M. V., Parada L. F., and Greene L. A. (1991) The trk proto-oncogene rescues NGF responsiveness in mutant NGF-nonresponsive PC12 cell lines. Cell 66, 961-966.
36. MacDonald J. I. S. and Meakin S. O. (1996) Deletions in the extracellular domain of rat TrkA lead to an altered differentiative phenotype in neurotrophin responsive cells. Mol. Cell. Neurosci. 7, 371-390.
37. Meakin S. O. and Shooter E. M. (1991) Tyrosine kinase activity coupled to the high-affinity nerve growth factor-receptor complex. Proc. Natl. Acad. Sci. USA 88, 5862-5866.
38. Meakin S. O., Suter U., Drinkwater C. C., Welcher A. A., and Shooter E. M. (1992) The rat trk protooncogene product exhibits properties characteristic of the slow nerve growth factor receptor. Proc. Natl. Acad. Sci. USA 89, 2374-2378.
39. Millbrandt J. (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238, 797-798.
40. Millbrandt J. (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1, 183-188.
41. Muragaki Y., Chou T. T., Kaplan D. R., Trojanowski J. Q., and Lee V. M. Y. (1997) Nerve growth factor induces apoptosis in human medulloblastoma cell lines that express TrkA receptors. J. Neurosci. 17, 530-542.
42. Niman H. L., Houghten R. A., Walker L. E., Reisfeld R. A., Wilson I. A., Hogle J. M., and Lerner R. A. (1983) Generation of protein-reactive antibodies by short peptides is an event of high frequency: implication for the structural basis of immune recognition. Proc. Natl. Acad. Sci. USA 80, 4949-4953.
43. Obermeier A., Bradshaw R. A., Seedorf K., Choidas A., Schlessinger J., and Ullrich A. (1994) Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLCγ. EMBO J. 13, 1585-1590.
44. Peng X., Greene L. A., Kaplan D. R., and Stephens R. M. (1995) Deletion of a conserved juxtamembrane sequence in Trk abolishes NGF-promoted neuritogenesis. Neuron 15, 395-406.
45. Rabin S. J., Cleghon V., and Kaplan D. R. (1993) SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol. 13, 2203-2213.
46. Radeke M. J., Misko T. P., Hsu C., Herzenberg L. A., and Shooter E. M. (1987) Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325, 593-597.
47. Rodriguez-Tébar A., Dechant G., and Barde Y.-A. (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron 4, 487-492.
48. Rodriguez-Tébar A., Dechant G., Götz R., and Barde Y.-A. (1992) Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO J. 11, 917-922.
49. Rodriguez-Viciana P., Warne P. H., Dhand R., Vanhaesebroeck B., Gout I., Fry M. J., Waterfield M. D., and Downward J. (1994) Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370, 527-532.
50. Shelton D. L., Sutherland J., Gripp J., Camerato T., Armanini M. P., Phillips H. S., Carroll K., Spencer S. D., and Levinson A. D. (1995) Human trks: molecular cloning, tissue distribution and expression of extracellular domain immunoadhesions. J. Neurosci. 15, 477-491.
51. Stephens R. M., Loeb D. M., Copeland T. D., Pawson T., Greene L. A., and Kaplan D. R. (1994) Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 12, 691-705.
52. Tsoulfas P., Soppet D., Escandon E., Tessarollo L., Mendoza-Ramirez J.-L., Rosenthal A., Nicolics K., and Parada L. F. (1993) The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10, 975-990.
53. Tsoulfas P., Stephens R. M., Kaplan D. R., and Parada L. F. (1996) TrkC isoforms with inserts in the kinase domain show impaired signaling responses. J. Biol. Chem. 271, 5691-5697.
54. Vale R. D. and Shooter E. M. (1985) Assaying binding of nerve growth factor to cell surface receptors. Methods Enzymol. 109, 21-39.
55. Valenzuela S. M., Maisonpierre P. C., Glass D. J., Rojas E., Nunez L., Kong Y., Gies D. R., Stitt T. N., Ip N. Y., and Yancopoulos G. D. (1993) Alternative forms of rat trkC with different functional capabilities. Neuron 10, 963-974.
56. Vambutas V., Kaplan D. R., Sells M. A., and Chernoff J. (1995) Nerve growth factor stimulates tyrosine phosphorylation and activation of Src homology-containing protein-tyrosine phosphatase 1 in PC12 cells. J. Biol. Chem. 270, 25629-25633.
57. Yao R. and Cooper G. M. (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267, 2003-2006.