Inhibitors of trypsin-like serine proteases inhibit processing of the caspase Nedd-2 and protect PC12 cells and sympathetic neurons from death evoked by withdrawal of trophic support

Journal of Neurochemistry

Volumn 69, Issue 4, 1997, Pages 1425-1437

  Stefanis, Leonidas ^a   Troy, Carol M ^a   Qi, Haiqing ^a   Greene, Lloyd A ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

4 (2 Aminoethyl)benzenesulfonyl fluoride; Apoptosis; Cell cycle; N Tosyl L phenylalanine chloromethyl ketone; Neuronal cell death

Indexed keywords

NERVE GROWTH FACTOR; SERINE PROTEINASE; TOSYLLYSYL CHLOROMETHYL KETONE; TRYPSIN; TRYPTASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL STRAIN; CONTROLLED STUDY; ENZYME INHIBITION; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SYMPATHETIC NERVE CELL;

ANIMALIA;

EID: 0030984171     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69041425.x     Document Type: Article

References (58)

1. Batistatou A. and Greens L. A. (1993) Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Biol. 122, 523-532.
2. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
3. Bredesen D. E. (1995) Neural apoptosis. Ann. Neurol. 38, 839-851.
4. Chow S. C., Weis M., Kass G. E. N., Holmstrom T. H., Eriksson J. E., and Orrenius S. (1995) Involvement of multiple proteases during Fas-mediated apoptosis in T lymphocytes. FEBS Lett. 364, 134-138.
5. Darmon A. J., Nicholson D. W., and Bleackley R. C. (1995) Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377, 446-448.
6. Deiss L. P., Galinka H., Berissi H., Cohen O., and Kimchi A. (1996) Cathepsin D protease mediates programmed cell death induced by interferon-γ, Fas/APO-1 and TNF-α. EMBO J. 15, 3861-3870.
7. Dickinson J. L., Bates E. J., Ferrante A., and Antalis T. M. (1995) Plasminogen activator inhibitor type 2 inhibits tumor necrosis factor α-induced apoptosis; evidence for an alternate biological function. J. Biol Chem. 270, 27894-27904.
8. Duan H., Orth K., Chinnaiyan A. M., Poirier G. G., Froelich C. J., He W., and Dixit V. M. (1996) ICE-LAP6, a novel member of the ICE/ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271, 16720-16724.
9. Farinelli S. E. and Greene L. A. (1996) Cell cycle blockers mimosine, ciclopirox and deferoxamine prevent the death of PC12 cells and postmitotic sympathetic neurons after removal of trophic support. J. Neurosci. 16, 1150-1162.
10. Fearnhead H. O., Rivett A. J., Dinsdale D., and Cohen G. M. (1995) A pre-existing protease is a common effector of thymocyte apoptosis mediated by diverse stimuli. FEBS Lett. 357, 242-246.
11. Fenteany G., Standaert R. F., Reichard G. A., Corey E. J., and Schreiber S. L. (1994) A β-lactone related to lactacystin induces neunte outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc. Natl. Acad. Sci. USA 91, 3358-3362.
12. Fernandes-Alnemri T., Litwack G., and Alnemri E. S. (1994) CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein ced-3 and mammalian interleukin-1β-converting enzyme. J. Biol Chem. 269, 30761-30764.
13. Fraser A. and Evan G. (1996) A licence to kill. Cell 85, 781-784.
14. Freeman R. S., Estus S., and Johnson E. M. Jr. (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12, 343-355.
15. Gagliardini V., Fernandez P.-A., Lee R. K. K., Drexler H. C. A., Rotello R. J., Fishman M. C., and Yuan J. (1994) Prevention of vertebrate neuronal death by the crmA gene. Science 263, 824-828.
16. Greene L. A. (1978) Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J. Cell Biol. 78, 747-755.
17. 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.
18. Grimm L. M., Goldberg A. L., Poirier G. G., Schwartz L. M., and Osborne B. A. (1996) Proteasomes play an essential role in thymocyte apoptosis. EMBO J. 15, 3835-3844.
19. Gu Y., Sarnecki C., Aldape R. A., Livingston D. L., and Su M. S.-S. (1995) Cleavage of poly(ADP-ribose) polymerase by interleukin-1β converting enzyme and its homologs TX and Nedd-2. J. Biol. Chem. 270, 18715-18718.
20. Houenou L. J., Turner P. L., Li L., Oppenheim R. W., and Festoff B. W. (1995) A serine protease inhibitor, protease nexin I, rescues motoneurons from naturally occurring and axotomy-induced cell death. Proc. Natl. Acad. Sci. USA 92, 895-899.
21. Kanai H., Tanaka M., and Hirai S. (1991) α1-Antichymotrypsin has a trophic effect on hippocampal neurons in vitro. Neurosci. Lett. 125, 163-165.
22. King R. W., Deshaies R. J., Peters J.-M., and Kirschner M. W. (1996) How proteolysis drives the cell cycle. Science 274, 1652-1659.
23. Kostura M. J., Tocci M. J., Limjuco G., Chin J., Cameron P., Hillman A. G., Chartrain N. A. and Schmidt J. A. (1989) Identification of a monocyte specific pre-interleukin 1β convertase activity. Proc. Natl. Acad. Sci. USA 86, 5227-5231.
24. Kozaki Y., Kubo M., Ariki T., Onishi T., Zhu D., and Muramatu M. (1994) Properties of three proteinases functioning at G1, S and G2 phases in HeLa cells and their inhibition by guanidino- and amidino-acid esters. Biol. Pharm. Bull. 17, 185-191.
25. Ku G. S. B., Quigley J. P., and Sultzer B. M. (1981) Time-dependent inhibition of tuberculin-induced lymphocyte DNA synthesis by a serine protease inhibitor. J. Immunol. 126, 2209-2214.
26. Ku G. S. B., Quigley J. P., and Sultzer B. M. (1983) The inhibition of the mitogenic stimulation of B lymphocytes by a serine protease inhibitor: commitment to proliferation correlates with an enhanced expression of a cell-associated arginine-specific serine enzyme. J. Immunol. 131, 2494-2499.
27. Kumar S. and Baglioni C. (1991) Protection from tumor necrosis factor-mediated cytolysis by overexpression of plasminogen activator inhibitor type-2. J. Biol. Chem. 266, 20960-20964.
28. Kumar S. and Harvey N. L. (1995) Role of multiple cellular proteases in the execution of programmed cell death. FEBS Lett. 375, 169-173.
29. Kumar S., Kinoshita M., Noda M., Copeland N. G., and Jenkins N. A. (1994) Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1β-converting enzyme. Genes Dev. 8, 1613-1626.
30. Lawson W. B., Valenty V. B., Wos J. D., and Lobo A. P. (1982) Studies on the inhibition of human thrombin: effects of plasma and plasma constituents. Folia Haematol. 109, S.52-S.60.
31. Martin D. P., Ito A., Horigome K., Lampe P. A., and Johnson E. M. Jr. (1992) Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23, 1205-1220.
32. Miller D. K., Ayala J. M., Egger L. A., Raju S. M., Yamin T.-T., et al. (1993) Purification and characterization of active human interleukin-1β-converting enzyme from THP.1 monocytic cells. J. Biol. Chem. 268, 18062-18069.
33. Mizuguchi M. and Kim S. U. (1991) α1-Antichymotrypsin supports short-term survival of cerebral neurons in culture. Neurosci. Lett. 124, 166-168.
34. Nicholson D. W., Ali A., Thornberry N. A., Vaillancourt J. P., Ding C. D., Gallant M., Gareau Y., Griffin P. R., Labelle M., Lazebnik Y. A., Munday N. A., Raju S. M., Smulson M. E., Yamin T.-T., Yu V. L., and Miller D.K. (1995) Identification and inhibition of the ICE/ced-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
35. Oppenheim R. W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
36. Park D. S., Farinelli S. E., and Greene L. A. (1996a) Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J. Biol. Chem. 271, 1-9.
37. Park D. S., Stefanis L., Yan C. Y. I., Farinelli S. E., and Greene L. A. (1996b) Ordering the cell death pathway. Differential effects of bcl-2, an interleukin-1β converting enzyme family protease inhibitor, and other survival agents on JNK activation in serum/nerve growth factor-deprived PC12 cells. J. Biol. Chem. 271, 21898-21906.
38. Redelman D. and Hudig D. (1980) The mechanism of cell-mediated cytotoxicity. I. Killing by murine cytotoxic T lymphocytes requires cell surface thiols and activated proteases. J. Immunol. 124, 870-878.
39. Ruggiero V., Johnson S. E., and Baglioni C. 1987) Protection from tumor necrosis factor cytotoxicity by protease inhibitors. Cell. Immunol. 107, 317-325.
40. Rukenstein A., Rydel R. E., and Greene L. A. (1991) Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J. Neurosci. 11, 2552-2563.
41. Rydel R. E. and Greene L. A. (1988) cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of nerve growth factor. Proc. Natl. Acad. Sci. USA 85, 1257-1261.
42. Sadoul R., Fernandez P., Quiquerez A., Martinou I., Maki M., Schroter M., Becherer J. D., Irmler M., Tschopp J., and Martinou J. (1996) Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J. 15, 3845-3852.
43. Sarin A., Adams D. H., and Henkart P. A. (1993) Protease inhibitors selectively block T cell receptor-triggered programmed cell death in a murine T cell hybridoma and activated peripheral T cells. J. Exp. Med. 178, 1693-1700.
44. + donors by cysteine protease inhibitors. J. Immunol. 153, 862-872.
45. Schnebli H. P. (1975) The effects of protease inhibitors on cells in vitro, in Proteases and Biological Control (Reich E., Rifkin D. B., and Shaw E., eds), pp. 785-794. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
46. α-tosyl-L-lysine. Biochemistry 4, 2219-2224.
47. Shi L., Kam C., Powers J. C., Aabersold R., and Greenberg A. H. (1992) Purification of three cytotoxic lymphocyte granule serine proteases that induce apoptosis through distinct substrate and target cell interactions. J. Exp. Med. 176, 1521-1529.
48. Shields P. P., Gonzales T. A., Charles D., Gilligan J. P., and Stern W. (1991) Accumulation of pepstatin in cultured endothelial cells and its effect on endothelial processing. Biochem. Biophys. Res. Commun. 177, 1006-1012.
49. Squier M. K. T., Miller A. C. K., Malkinson A. M., and Cohen J. J. (1994) Calpain activation in apoptosis. J. Cell. Physiol. 159, 229-237.
50. Stefanis L., Park D. S., Van C. Y. I., Farinelli S. E., Troy C. M., Shelanski M. L., and Greene L. A. (1996) Induction of CPP32-like activity in PC12 cells by withdrawal of trophic support; dissociation from apoptosis. J. Biol. Chem. 271, 30663-30671.
51. Steller H. (1995) Mechanisms and genes of cellular suicide. Science 267, 1445-1449.
52. Suffys P., Beyaert R., Van Roy F., and Fiers W. (1988) Involvement of a serine protease in tumour-necrosis-factor-mediated cytotoxicity. Eur. J. Biochem. 178, 257-265.
53. Troy C. M., Stefanis L., Prochiantz A., Greene L. A., and Shelanski M. L. (1996) The contrasting roles of ICE-family proteases and interleukin 1-β in apoptosis induced by trophic factor withdrawal and by copper/zinc superoxide dismutase down-regulation. Proc. Natl. Acad. Sci. USA 93, 5635-5640.
54. Troy C. M., Stefanis L., Greene L. A., and Shelanski M. L. (1997) Nedd2 is required for apoptosis after trophic factor withdrawal, but not superoxide dismutase (SOD1) downregulation, in sympathetic neurons and PC12 cells. J. Neurosci. 17, 1911-1918.
55. Tsirka S. E., Rogove A. D., Bugge T. H., Degen J. D., and Strickland S. (1997) An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J. Neurosci. 17, 543-552.
56. Xue D., Shaham S., and Horvitz H. R. (1996) The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Gene Dev. 10, 1073-1083.
57. Yamin T., Ayala J. M., and Miller D. K. (1996) Activation of the native 45-kDa precursor form of interleukin-1-converting enzyme. J. Biol. Chem. 271, 13273-13282.
58. Yuan J., Shaham S., Ledoux S., Ellis H. M., and Horvitz H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75, 641-652.