Control of neuronal size homeostasis by trophic factor-mediated coupling of protein degradation to protein synthesis

Journal of Cell Biology

Volumn 142, Issue 5, 1998, Pages 1313-1324

  Franklin, James L ^a   Johnson Jr , Eugene M ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caspase; Growth; Nerve growth factor; Protein turnover; Sympathetic neuron

Indexed keywords

ACTIN; CELL PROTEIN; CYCLOHEXIMIDE; NEUROTROPHIC FACTOR; TUBULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL SIZE; DOSE TIME EFFECT RELATION; FEMALE; GROWTH REGULATION; HOMEOSTASIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; QUANTITATIVE DIAGNOSIS; RAT;

ACTINS; ANIMALS; ANISOMYCIN; APOPTOSIS; CELL DIVISION; CELL SIZE; CELLS, CULTURED; CYCLOHEXIMIDE; DACTINOMYCIN; EMBRYO; GANGLIA; HOMEOSTASIS; KINETICS; MICROSCOPY, PHASE-CONTRAST; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION, GENETIC; TUBULIN;

EID: 0032494166     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.5.1313     Document Type: Article

References (59)

1. Ballard, F.J. 1987. Regulation of intracellular protein breakdown with special reference to cultured cells. In Lysosomes: Their Role in Protein Breakdown. H. Glauman, and F.J. Ballard, editors. Academic Press, New York. 285-318.
2. Ciechanover, A., and A.L. Schwartz. 1998. The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Cell. 95:2727-2730.
3. Clark, W.A., S.J. Rudnick, J.J. LaPres, L.C. Anderson, and M.C. LaPointe. 1993. Regulation of hypertrophy and atrophy in cultured adult heart cells. Circ. Res. 73:1163-1176.
4. Deckwerth, T.L., and E.M. Johnson, Jr. 1993. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 123:1207-1222.
5. Deshaies, R.J. 1995. Make it or break it: the role of ubiquitin-dependent proteolysis in cellular regulation. Trends Cell Biol. 5:428-434.
6. Deshmukh, M., J. Vasilakos, T.L. Deckwerth, P.A. Lampe, B.D. Shivers, and E.M. Johnson, Jr. 1996. Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE-family proteases. J. Cell Biol. 135:1341-1354.
7. Dice, J.F. 1987. Molecular determinants of protein half-lives in eukaryotic cells. FASEB (Fed. Am. Soc. Exp. Biol.) J. 1:349-357.
8. D'Mello, S.R., C. Galli, T. Ciotti, and P. Calissano. 1993. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc. Natl. Acad. Sci. USA. 90:10989-10993.
9. Doyle, D., and J. Tweto. 1975. Measurement of protein turnover in animal cells. Methods Cell Biol. 10:235-260.
10. Epstein, D., S. Elias-Bishko, and A. Hershko. 1975. Requirement for protein synthesis in the regulation of protein breakdown in cultured hepatoma cells. Biochemistry. 14:5199-5204.
11. Estus, S., W.J. Zaks, R.S. Freeman, M. Gruda, R. Bravo, and E.M. Johnson, Jr. 1994. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127: 1717-1727.
12. 2+ influx but not Trk activation. J. Neurosci. 15:643-664.
13. Freeman, R.S., S. Estus, and E.M. Johnson, Jr. 1994. Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed death. Neuron. 12:343-355.
14. Furuno, K., M.N. Goodman, and A.L. Goldberg. 1990. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J. Biol. Chem. 265:8550-8557.
15. Gao, F., and M. Raff. 1997. Cell size control and a cell-intrinsic maturation program in proliferating oligodendrocyte precursor cells. J. Cell Biol. 138:1367-1377.
16. Garcia-Valenzuela, E., S. Shareef, J. Walsh, and S.C. Sharma. 1995. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp. Eye Res. 61:33-14.
17. Glas, R., M. Bogyo, J.S. McMaster, M. Gaczynska, and H.L. Ploegh. 1998. A proteolytic system that compensates for loss of proteasome function. Nature. 392:618-622.
18. Goldberg, A.L., and K.L. Rock. 1992. Proteolysis, proteasomes and antigen presentation. Nature. 357:375-379.
19. Goldberg, A.L., and A.C. St. John. 1976. Intracellular protein degradation in mammalian and bacterial cells: part 2. Annu. Rev. Biochem. 45:747-803.
20. α-acetylated proteins and may be substituted for by bacterial elongation factor EF-Tu. Proc. Natl Acad. Sci. USA. 91:7648-7652.
21. Gottlieb, R.A., J. Nordberg, E. Skowronski, and B.M. Babior. 1996. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc Natl. Acad. Sci. USA. 93:654-658.
22. Grollman, A.P. 1967. Inhibitors of protein biosynthesis: II. Mode of action of anisomycin. J. Biol. Chem. 242:3226-3233.
23. Halliwell, F.J., and J.M.C. Gutteridge. 1989. Free Radicals in Biology and Medicine. Oxford University Press, New York. 543 pp.
24. Hershko, A., and G.M. Tomkins. 1971. Studies on the degradation of tyrosine aminotransferase in hepatoma cells in culture. J. Biol. Chem. 246:710-714.
25. Hershko, A., P. Mamont, R. Shields, and G.M. Tomkins. 1971. Pleiotypic response. Nat. New Biol. 232:206-211.
26. Hochstrasser, M. 1995. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7:215-223.
27. Jacobson, A., and S.W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-739.
28. Jentsch, S., and S. Schlenker. 1995. Selective protein degradation: a journey's end within the proteasome. Cell. 82:881-884.
29. Johnson, M.I., and V. Argiro. 1983. Techniques in the tissue culture of rat sympathetic neurons. Methods Enzymol. 103:334-347.
30. Koh, J., M.B. Wie, B.J. Gwag, S.L. Sensi, L.M.T. Canzoniero, J. Demaro, C. Csernansky, and D.W. Choi. 1995. Staurosporin-induced neuronal apoptosis. Exp. Neurol. 135:153-159.
31. Lewis, J.G., D.O. Adams, and S. Fan. 1995. Selective sensitivity of macrophages to cytotoxicity by inhibitors of macromolecular synthesis: induction of apoptosis. J. Leukoc. Biol. 57:635-642.
32. Lin, T.A., X. Kong, T.A. Haystead, A. Pause, G. Belsham, N. Sonenberg, and J.C. Lawrence, Jr. 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science. 266:653-656.
33. Macknight, A.D.C. 1988. Principles of cell volume regulation. Renal Physiol. Biochem. 11:114-141.
34. Martin, D.P., R.E. Schmidt, P.S. DiStefano, O.H. Lowry, J.G. Carter, and E.M. Johnson, Jr. 1988. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106: 829-844.
35. Martin, D.P., A. Ito, K. Horigome, P.A. Lampe, and E.M. Johnson, Jr. 1992. Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23:1205-1220.
36. Martinou, I., P.A. Fernandez, M. Missotten, E. White, B. Allet, R. Sadoul, and J.C. Martinou. 1995. Viral proteins E1B19K and p35 protect sympathetic neurons from cell death induced by NGF deprivation. J. Cell Biol. 128:201-208.
37. Miura, M., R.M. Friedlander, and J. Yuan. 1995. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl. Acad. Sci. USA. 92:8318-8322.
38. Olson, T.S., and J.F. Dice. 1989. Regulation of protein degradation rates in eukaryotes. Curr. Opin. Cell Biol. 1:1194-1200.
39. Pause, A., G.J. Belsham, A.C. Gingras, O. Donze, T.A. Lin, J.C. Lawrence, Jr., and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature. 371:762-767.
40. Poole, B., and M. Wibo. 1973. Protein degradation in cultured cells. J. Biol. Chem. 248:6221-6226.
41. Raff, M.C. 1996. Size: the regulation of cell numbers in animal development. Cell. 86:173-175.
42. Rasmussen, C.D., and J.D. Berger. 1982. Downward regulation of cell size in Paramecium tetraurelia: effects of increased cell size, with or without increased DNA content, on the cell cycle. J. Cell Sci. 57:315-329.
43. Ratan, R.R., T.H. Murphy, and J.M. Baraban. 1994. Macromolecular synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione. J. Neuro-sci. 14:4385-4392.
44. Reich, E., and I.H. Goldberg. 1964. Molecular basis of action of actinomycin. In Progress in Nucleic Acid Research and Molecular Biology. J. Davidson and W. Cohn, editors. Academic Press, New York. 184-234.
45. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A.L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 78:761-771.
46. Ross, J. 1997. A hypothesis to explain why translational inhibitors stabilize mRNAs in mammalian cells: mRNA stability and mitosis. Bioessays. 19:527-529.
47. Ruit, K.G., J.L. Elliott, P.A. Osborne, Q. Yan, and W.D. Snider. 1992. Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron. 8:573-587.
48. Schmidt, E.E., and U. Schibler. 1995. Cell size regulation, a mechanism that controls cellular RNA accumulation: consequences on regulation of the ubiquitous transcription factors Oct1 and NF-Y and the liver-enriched transcription factor DBP. J. Cell Biol. 128:467-483.
49. Scott, S.A., and A.M. Davies. 1990. Inhibition of protein synthesis prevents cell death in sensory and parasympathetic neurons deprived of neurotrophic factor in vitro. J. Neurobiol. 21:630-638.
50. Seglin, P.O. 1978. Protein turnover in isolated rat hepatocytes. In Protein Turnover and Lysosome Function. H.L. Segal and D.J. Doyle, editors. Academic Press. New York. 431-453.
51. Seglin, P.O. 1987. Regulation of autophagic protein degradation in isolated liver cells. In Lysosomes: Their Role in Protein Breakdown. H. Glauman and F.J. Ballard, editors. Academic Press, New York. 372-414.
52. Stellar, H. 1995. Mechanisms and genes of cellular suicide. Science. 267:1445-1449.
53. Temparis, S., M. Asensi, D. Taillandier, E. Aurousseau, D. Larbaud, A. Obled, D. Béchet, M. Ferrara, J.M. Estrela, and D. Attaix. 1994. Increased ATP-ubiquitin-dependent proteolysis in skeletal muscle of tumor-bearing rats. Cancer Res. 54:5568-5573.
54. Toomey, D., H.P. Redmond, and D. Bouchier-Hayes. 1995. Mechanisms mediating cancer cachexia. Cancer. 76:2418-2426.
55. Troy, C.M., L. Stefanis, A. Prochiantz, L.A. Greene, and M.L. Shelanski. 1996. The contrasting roles of ICE family proteases and interleukin-18 in apoptosis induced by trophic factor withdrawal and by copper/zinc Superoxide dismutase down-regulation. Proc. Natl. Acad. Sci. USA. 93:5635-5640.
56. Udvardy, A. 1996. The role of controlled proteolysis in cell-cycle regulation Eur. J. Biochem. 240:307-313.
57. Wettstein, F.O., H. Noll, and S. Penman. 1964. Effect of cycloheximide on ribosomal aggregates engaged in protein synthesis in vitro. Biochim. Biophys. Acta. 87:525-528.
58. White, E. 1996. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1-15.
59. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.