Spatial requirements for TrkA kinase activity in the support of neuronal survival and axon growth in rat sympathetic neurons

Neuropharmacology

Volumn 45, Issue 7, 2003, Pages 995-1010

  MacInnis, Bronwyn L ^a   Senger, Donna L ^b   Campenot, Robert B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Axon growth; K252a; Neuronal apoptosis; Neuronal survival; NGF; Signaling endosome; TrkA

Indexed keywords

ALKALOID; K 252A; NERVE GROWTH FACTOR; PROTEIN TYROSINE KINASE; REAGENT;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; ENDOSOME; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NERVE CELL; NERVE ENDING; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL; TISSUE CULTURE;

EID: 0142090754     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(03)00273-9     Document Type: Article

References (70)

1. Atwal J.K., Massie B., Miller F.D., Kaplan D.R. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron. 27:2000;265-277.
2. Bhattacharyya A., Watson F.L., Bradlee T.A., Pomeroy S.L., Stiles C.D., Segal R.A. Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J. Neurosci. 17:1997;7007-7016.
3. Bhattacharyya A., Watson F.L., Pomeroy S.L., Zhang Y.Z., Stiles C.D., Segal R.A. High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors. J. Neurobiol. 51:2002;302-312.
4. Borasio G.D. Differential effects of the protein kinase inhibitor K-252a on the in vitro survival of chick embryonic neurons. Neurosci. Lett. 108:1990;207-212.
5. Brami-Cherrier K., Valjent E., Garcia M., Pages C., Hipskind R.A., Caboche J. Dopamine induces a PI3-kinase-independent activation of Akt in striatal neurons: a new route to cAMP response element-binding protein phosphorylation. J. Neurosci. 22:2002;8911-8921.
6. Brunet A., Datta S.R., Greenberg M.E. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11:2001;297-305.
7. Campenot R.B. Local control of neurite development by nerve growth factor. Proc. Natl. Acad. Sci. USA. 74:1977;4516-4519.
8. Campenot R.B. Development of sympathetic neurons in compartmentalized cultures. I Local control of neurite growth by nerve growth factor. Dev. Biol. 93:1982;1-12.
9. Campenot R.B. Local control of neurite sprouting in cultured sympathetic neurons by nerve growth factor. Brain Res. 465:1987;293-301.
10. Campenot R.B. Compartmented culture analysis of nerve growth. Stevenson B.R., Gallin W.J., Paul D.L. Cell-Cell Interactions A Practical Approach. 1992;275-298 IRL Press, Oxford.
11. Campenot R.B. NGF and the local control of nerve terminal growth. J. Neurobiol. 25:1994;599-611.
12. Campenot, R.B., MacInnis, B.L., 2003. Retrograde transport of neurotrophins: fact and function. J. Neurobiol. (in press).
13. Campenot R.B., Martin G. Construction and use of compartmented cultures for studies of cell biology of neurons. Federoff S., Richardson A. Protocols for Neural Cell Culture. 2001;49-57 Humana Press, Totowa, New Jersey.
14. Cheng B., Barger S.W., Mattson M.P. Staurosporine, K-252a, and K-252b stabilize calcium homeostasis and promote survival of CNS neurons in the absence of glucose. J. Neurochem. 62:1994;1319-1329.
15. Coulier F., Kumar R., Ernst M., Klein R., Martin-Zanca D., Barbacid M. Human trk oncogenes activated by point mutation, in-frame deletion, and duplication of the tyrosine kinase domain. Mol. Cell Biol. 10:1990;4202-4210.
16. Crowley C., Spencer S.D., Nishimura M.C., Chen K.S., Pitts-Meek S., Armanini M.P., Ling L.H., MacMahon S.B., Shelton D.L., Levinson A.D., et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 76:1994;1001-1011.
17. Cunningham M.E., Stephens R.M., Kaplan D.R., Greene L.A. Autophosphorylation of activation loop tyrosines regulates signaling by the TRK nerve growth factor receptor. J. Biol. Chem. 272:1997;10957-10967.
18. Daniele N., Rajas F., Payrastre B., Mauco G., Zitoun C., Mithieux G. Phosphatidylinositol 3-kinase translocates onto liver endoplasmic reticulum and may account for the inhibition of glucose-6-phosphatase during refeeding. J. Biol. Chem. 274:1999;3597-3601.
19. Doherty P., Walsh F.S. K-252a specifically inhibits the survival and morphological differentiation of NGF-dependent neurons in primary cultures of human dorsal root ganglia. Neurosci. Lett. 96:1989;1-6.
20. Du K., Montminy M. Creb is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:1998;32377-32379.
21. Ehlers M.D., Kaplan D.R., Price D.L., Koliatsos V.E. NGF-stimulated retrograde transport of trkA in the mammalian nervous system. J. Cell. Biol. 130:1995;149-156.
22. Ginty D.D., Segal R.A. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 12:2002;268-274.
23. Glicksman M.A., Forbes M.E., Prantner J.E., Neff N.T. K-252a promotes survival and choline acetyltransferase activity in striatal and basal forebrain neuronal cultures. J. Neurochem. 64:1995;1502-1512.
24. Griffin J.W., Watson D.F. Axonal transport in neurological disease. Ann. Neurol. 23:1988;3-13.
25. Grimes M.L., Beattie E., Mobley W.C. A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc. Natl. Acad. Sci. USA. 94:1997;9909-9914.
26. Hada H., Miyamoto K. Enhancing effects of sound on methamphetamine- induced behavioral aberrations in the rat: a model of relapse of schizophrenia-like symptoms. Jpn. J. Psychiat. Neurol. 44:1990;619-627.
27. Hashimoto S. K-252a, a potent protein kinase inhibitor, blocks nerve growth factor-induced neurite outgrowth and changes in the phosphorylation of proteins in PC12h cells. J. Cell Biol. 107:1988;1531-1539.
28. Hashimoto S., Hagino A. Blockage of nerve growth factor action in PC12h cells by staurosporine, a potent protein kinase inhibitor. J. Neurochem. 53:1989;1675-1685.
29. Hayakawa J., Ohmichi M., Tasaka K., Kanda Y., Adachi K., Nishio Y., Hisamoto K., Mabuchi S., Hinuma S., Murata Y. Regulation of the PRL promoter by Akt through cAMP response element binding protein. Endocrinology. 143:2002;13-22.
30. Heerssen H.M., Segal R.A. Location, location, location: a spatial view of neurotrophin signal transduction. Trends Neurosci. 25:2002;160-165.
31. Hendry I.A., Stockel K., Thoenen H., Iversen L.L. The retrograde axonal transport of nerve growth factor. Brain Res. 68:1974;103-121.
32. Howe C.L., Valletta J.S., Rusnak A.S., Mobley W.C. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron. 32:2001;801-814.
33. 125I] NGF. Brain Res. 150:1978;319-331.
34. Kase H., Iwahashi K., Matsuda Y. K-252a, a potent inhibitor of protein kinase C from microbial origin. J. Antibiot. (Tokyo). 39:1986;1059-1065.
35. Kase H., Iwahashi K., Nakanishi S., Matsuda Y., Yamada K., Takahashi M., Murakata C., Sato A., Kaneko M. K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem. Biophys. Res. Commun. 142:1987;436-440.
36. Koizumi S., Contreras M.L., Matsuda Y., Hama T., Lazarovici P., Guroff G. K-252a: a specific inhibitor of the action of nerve growth factor on PC 12 cells. J. Neurosci. 8:1988;715-721.
37. Korsching S., Thoenen H. Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor. Neurosci. Lett. 39:1983;1-4.
38. Kramer B.M., Van der Zee C.E., Hagg T. P75 nerve growth factor receptor is important for retrograde transport of neurotrophins in adult cholinergic basal forebrain neurons. Neuroscience. 94:1999;1163-1172.
39. Kuruvilla R., Ye H., Ginty D.D. Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron. 27:2000;499-512.
40. Lee F.S., Chao M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. USA. 98:2001;3555-3560.
41. Lee F.S., Rajagopal R., Kim A.H., Chang P.C., Chao M.V. Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J. Biol. Chem. 277:2002;9096-9102.
42. Levi-Montalcini R., Angeletti P.U. Nerve growth factor. Physiol. Rev. 48:1968;534-569.
43. MacInnis B.L., Campenot R.B. Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science. 295:2002;1536-1539.
44. MacPhee I., Barker P.A. Extended ceramide exposure activates the trkA receptor by increasing receptor homodimer formation. J. Neurochem. 72:1999;1423-1430.
45. Maroney A.C., Lipfert L., Forbes M.E., Glicksman M.A., Neff N.T., Siman R., Dionne C.A. K-252a induces tyrosine phosphorylation of the focal adhesion kinase and neurite outgrowth in human neuroblastoma SH-SY5Y cells. J. Neurochem. 64:1995;540-549.
46. Miller F.D., Kaplan D.R. On Trk for retrograde signaling. Neuron. 32:2001;767-770.
47. Miller F.D., Kaplan D.R. Neurobiology. TRK makes the retrograde. Science. 295:2002;1471-1473.
48. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65:1983;55-63.
49. Ohno M., Yamamoto T., Watanabe S. Effect of staurosporine, a protein kinase C inhibitor, on impairment of working memory in rats exposed to cerebral ischemia. Eur. J. Pharmacol. 204:1991;113-116.
50. Orike N., Middleton G., Borthwick E., Buchman V., Cowen T., Davies A.M. Role of PI 3-kinase, Akt and Bcl-2-related proteins in sustaining the survival of neurotrophic factor-independent adult sympathetic neurons. J. Cell Biol. 154:2001;995-1005.
51. Palmatier M.A., Hartman B.K., Johnson E.M. Jr. Demonstration of retrogradely transported endogenous nerve growth factor in axons of sympathetic neurons. J. Neurosci. 4:1984;751-756.
52. Perkinton M.S., Ip J.K., Wood G.L., Crossthwaite A.J., Williams R.J. Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurones. J. Neurochem. 80:2002;239-254.
53. Phung T.L., Roncone A., Jensen K.L., Sparks C.E., Sparks J.D. Phosphoinositide 3-kinase activity is necessary for insulin-dependent inhibition of apolipoprotein B secretion by rat hepatocytes and localizes to the endoplasmic reticulum. J. Biol. Chem. 272:1997;30693-30702.
54. Posse de Chaves E., Bussiere M., MacInnis B., Vance D.E., Campenot R.B., Vance J.E. Ceramide inhibits axonal growth and nerve growth factor uptake without compromising the viability of sympathetic neurons. J. Biol. Chem. 13:2001;13.
55. Posse de Chaves E.I., Rusinol A.E., Vance D.E., Campenot R.B., Vance J.E. Role of lipoproteins in the delivery of lipids to axons during axonal regeneration. J. Biol. Chem. 272:1997;30766-30773.
56. Pugazhenthi S., Nesterova A., Sable C., Heidenreich K.A., Boxer L.M., Heasley L.E., Reusch J.E. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J. Biol. Chem. 275:2000;10761-10766.
57. Riccio A., Pierchala B.A., Ciarallo C.L., Ginty D.D. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons (see comments). Science. 277:1997;1097-1100.
58. Roux P.P., Dorval G., Boudreau M., Angers-Loustau A., Morris S.J., Makkerh J., Barker P.A. K252a and CEP1347 are neuroprotective compounds that inhibit mixed-lineage kinase-3 and induce activation of Akt and ERK. J. Biol. Chem. 277:2002;49473-49480.
59. Segal R.A., Bhattacharyya A., Rua L.A., Alberta J.A., Stephens R.M., Kaplan D.R., Stiles C.D. Differential utilization of Trk autophosphorylation sites. J. Biol. Chem. 271:1996;20175-20181.
60. Senger D.L., Campenot R.B. Rapid retrograde tyrosine phosphorylation of trkA and other proteins in rat sympathetic neurons in compartmented cultures. J. Cell Biol. 138:1997;411-421.
61. Song M., Chivers Q., Posse E.I., Posse De Chaves E.I. Endogenous and exogenous ceramide inhibit sympathetic neurons apoptosis by different mechanisms. Role of P75 in ceramide generation. Soc. Neurosci. Abst. 426:2002;18.
62. Takenawa T., Itoh T. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim. Biophys. Acta. 1533:2001;190-206.
63. Toma J.G., Rogers D., Senger D.L., Campenot R.B., Miller F.D. Spatial regulation of neuronal gene expression in response to nerve growth factor. Dev. Biol. 184:1997;1-9.
64. Tsui-Pierchala B.A., Ginty D.D. Characterization of an NGF-P-TrkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J. Neurosci. 19:1999;8207-8218.
65. 125I-nerve growth factor in rat sympathetic neurons in compartmented cultures. J. Neurosci. 17:1997;1282-1290.
66. Vance J.E., Pan D., Campenot R.B., Bussiere M., Vance D.E. Evidence that the major membrane lipids, except cholesterol, are made in axons of cultured rat sympathetic neurons. J. Neurochem. 62:1994;329-337.
67. Watson F.L., Heerssen H.M., Bhattacharyya A., Klesse L., Lin M.Z., Segal R.A. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat. Neurosci. 4:2001;4.
68. Watson F.L., Heerssen H.M., Moheban D.B., Lin M.Z., Sauvageot C.M., Bhattacharyya A., Pomeroy S.L., Segal R.A. Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 19:1999;7889-7900.
69. Wu C., Lai C.F., Mobley W.C. Nerve growth factor activates persistent Rap1 signaling in endosomes. J. Neurosci. 21:2001;5406-5416.
70. Yeo T.T., Chua-Couzens J., Butcher L.L., Bredesen D.E., Cooper J.D., Valletta J.S., Mobley W.C., Longo F.M. Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J. Neurosci. 17:1997;7594-7605.