Okadaic acid-induced lens epithelial cell apoptosis requires inhibition of phosphatase-1 and is associated with induction of gene expression including p53 and bax

European Journal of Biochemistry

Volumn 257, Issue 2, 1998, Pages 351-361

  David Wan Cheng, L I ^a   Fass, Uwe ^a   Huizar, Isham ^a   Spector, Abraham ^a  

^a Columbia University ^*  (United States)

Author keywords

Apoptosis; Bax; Lens; P53; Phosphatase 1

Indexed keywords

CYCLOHEXIMIDE; DNA FRAGMENT; MESSENGER RNA; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN BAX; PROTEIN P53; PROTEIN SYNTHESIS INHIBITOR; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; LENS EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RABBIT; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL SURVIVAL; CYCLOHEXIMIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENES, P53; LENS, CRYSTALLINE; OKADAIC ACID; OXAZOLES; PHOSPHOPROTEIN PHOSPHATASE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RABBITS;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0032532569     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2570351.x     Document Type: Article

References (83)

1. Steller, H. (1995) Mechanisms and genes of cellular suicide, Science 267, 1145-1149.
2. Thompson, C. B. (1995) Apoptosis in the pathogenesis and treatment of disease, Science 267, 1456-1462.
3. Kerr, J. F. R., VVyllie, A. H. & Currrie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics, Br. J. Cancer 26, 239-257.
4. Wyllie, A. H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation, Nature 284, 555-556.
5. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. & Nagata, S. (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD 43, Nature 391, 43-50.
6. Yuan, J. (1995) Molecular control of life and death, Curr. Opin. Cell Biol. 7,211-214.
7. Tewari, M., Quan, L., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S. & Dixit, V. M. (1995) Yama/CCP32/?, a mammalian homolog of CED-3, is a crmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase, Cell 81, 801-809.
8. Nicholson, W. D., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulsom, M. E., Yamin, T.-T., Yu, V. L. & Miller, D. K. (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis, Nature 376, 37-43.
9. Lazebnik, Y. A., Takahashi, A., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H. & Earnshaw, W. C. (1995) Studies of the lamin protease reveal multiple parallel biochemical pathways during apoptotic execution, Proc. Naü Acad. Sei. USA 92, 9042-9046
10. Glucksmann, A. (1951) Cell deaths in normal vertebrate ontogeny, Dial. Rev. 26, 59-86.
11. Jacobson, M. D., Weil, M. & Raff, M. C. (1997) Programmed cell death in animal development, Cell 88, 347-354.
12. Strasser, A., Harris, A. W. & Cory, S. (1991) bcl-2 transgene inhibits T cell death and purturbs thymic self-censorship, Cell 67, 889 899.
13. Williams, G. T., Smith, C. A., Spooncer, E., Dexter, T. M. & Taylor, D. R. (1990) Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis, Nature 343, 76-79.
14. Cowan, W. M., Fawcett, J. W., O'Leary, D. D. M. & Stanfield, B. B. (1984) Regressive events in neurogenesis, Science 225, 1258-1265.
15. Raff, M. C., Barres, B. A., Burne, J. F., Coles, H. S., Ishizaki, Y. & Jacobson, M. D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system, Science 262, 695-700.
16. Kerr, J. F. R., Harmon, B. & Searle, J. (1974) An electron-microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibers, J. Cell Sei. 14, 571-585.
17. Schwanz, L. M., Smith, S. W., Jones, M. E. E. & Osborne, B. A. (1993) Do all programmed cell deaths occur via apoptosis? Proc. NatlAcad. Sei. USA 90, 980-984.
18. Carson, D. A. & Ribeiro, J. M. (1993) Apoptosis and disease, Lancet 341, 1251-1254.
19. Li, C.-J., Friedman, D. J., Wang, C., Metelev, V. & Pardee, A. B. (1995) Induction of apoptosis in uninfected lymphocytes by HIV-1 at protein. Science 268, 429-431.
20. Westendorp, M. O., Frank, R., Ochsenbauer, C., Stricker, K., Dhein, J., Walczak, H., Debatin, K. & Krammer, P. H. (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 tat and gp!20, Nature 375, 497-500.
21. Li, D. W.-C., Kuszak, J. R., Dunn, K., Wang, R.-R., Ma, W.-C., Wang, G.-M., Spector, A., Leib. M., Cotliar, A. M., Weiss, M., Espy, J., Howard, G., Farris, R. L., Auran, J., Donn, A., Hofeldt, A., Mackay, C., Merriam, J., Mini, R. & Smith, T. R. (1995) Lens epithelial cell apoptosis appears to be a common cellular basis for non-congenital cataract formation in humans and animals, J. Cell Biol. 130, 169-181.
22. Li, D. W.-C. & Spector, A. (1996) Lens epithelial cell apoptosis is an early event during UVB induced cataract formation, Free Radie. Biol. Med. 20, 301-311.
23. Li, D. W.-C. (1997) The lens epithelium, apoptosis and cataract formation, Nova Acta Leopoldina, NF 75/299, 75-101.
24. Vogelstein, B. (1990) A deadly inheritance, Nature 348, 681-682.
25. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, E., Kinzler, K. W. & Vogelstein, B. (1993) VVAF1, a potential mediator of p53 tumor suppression, Cell 75, 817-825.
26. Yonish-Rouach, E., Resnitzky, D., Lotem, J., Sachs, L., Kimchi, A. & Oren, M. (1991) Wild-type p53 induces apoptosis of myeloidleukaemic cells that is inhibited by interleukin-6, Nature 352, 345-347.
27. Miyashita, T., Krajewski, S., Krajeska, M., Wang, H. G., Lin, H. K., Huffman, B., Lieberman, D. & Reed, J. C. (1994) Tumor suppressor p53 is a regulator of bcl-2 and box gene expression in vitro and in vivo, Oncogene 9, 1799-1805.
28. Miyashita, T. & Reed, J. C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293299.
29. Man, J. P., Sabbatini, P., Perez, D., Rao, L., Modha, D. & White, E. (1996) The E1B 19 K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10, 461-477.
30. Caelles, C, Helmberg, A. & Karin, M. (1994) p53-dependent apoptosis in the absence of transcriptional activationof p53-target genes, Nature 370, 220-223.
31. Oltvai, Z. N., Milliman, C. L. & Korsmeyer, S. J. (1993) Bd-2 heterodimerizes in vivo with a conserved homology, Box, that accelerates programmed cell death, Cell 74, 609-619.
32. Oltvai, Z. N. & Korsmeyer, S. J. (1994) Checkpoints of dueling dimers foil death wishes, Cell 79, 189-192.
33. Korsmeyer, S. J., Shutter, J. R., Veis, D. J., Merry, D. E. & Oltvai, N. Z. (1993) Bcl-2/Bax: a Rheostat that regulates an anti-oxidant pathway and cell death, Seniin. Cancer Biol. 4, 327-332.
34. Hunter, T. & Karin, M. (1992) The regulation of transcription by phosphorylation, Cell 70, 375-387.
35. Elledge, S. J. (1996) Cell cycle checkponits: preventing an identity crisis, Science 274, 1664-1672.
36. Gjertsen, B. T. & Doskeland, S. O. (1995) Protein phosphorylation in apoptosis, Biocliim. Biopliy. Acta 1269, 187-199.
37. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. & Greenberg, M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis, Science 270, 1326-1331.
38. Ichijo, H., Nishida, E., Irie, K., Dijke, P. T., Saitoh, M., Moriguchi, T., Tatagi, M., Matsumoto, K., Miyazono, K. & Gotoh, Y. (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signalling pathway, Science 275, 90-94.
39. Cohen, P. (1989) The structure and regulation of protein phosphatases, Annu. Rev. Bioclicm. 58, 453-508.
40. Mumby, M. C. & Walter, G. (1993) Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth, Physiol. Rev. 73, 673-699.
41. Shenolikar, S. & Narin, A. C. (1991) Protein phosphatases: recent progress, Adv. Second Messenger Pliospliopmtein Res. 23, 1-121.
42. Schonthal, A. (1992) Differential regulation of thejun family gene expression by the tumor promoter okadaic acid. New Biol. 4, 16-21.
43. Bialojan, C. & Takai, A. (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases, Biochem. J. 256, 283-290.
44. Ishihara, H., Martin, B. L, Brautigan, D. L., Karaki, H., Ozaki, H., Kato, Y., Fusetani, N., Watabe, S., Hashimoto, K., Uemura, D. & Hartshorne, D. J. (1989) Calyculin A and okadaic acid: inhibitors of protein phosphatase activity, Bioclicm. Biophys. Res. Commun. 759,871-877.
45. Cohen, P., Homes, C. F. B. & Tsukitani, Y. (1990) Okadaic acid: a new probe for the study of cellular regulation, Trends Bioclicm. Sei. 75,98-102.
46. Boe, R., Gjertsen, B. T., Vintermyr, O. K., Houge, G., Lanotte, M. & Doskeland, S. O. (1991) The protein phosphatase inhibitor okadaic acid induces morphological changes typical of apoptosis in mammalian cells, Exp. Cell Res. 195, 237-246.
47. Ishida, Y, Furukawa, Y., De Caprio, J. A., Saito, M. & Griffin, J. D. (1992) Treatment of myeloid leukemic cells with the phosphatase inhibitor okadaic acid induces cell cycle arrest at either Gl/S or G2/M depending on dose, J. Cell Pliysiol. 150, 484-492.
48. Mellgren, G., Vintermyr, O. K., Boe, R. & Doskeland, S. O. (1993) Hepatocyte DNA replication is abolished by inhibitors selecting protein phosphatase 2A rather than phosphatase 1, Exp. Cell Res. 205, 293-301.
49. Kiguchi, K., Glesne, D., Chubb, C. H., Fujiki, H. & Huberman, E. (1994) Differential induction of apoptosis in human breast tumor cells by okadaic acid and related inhibitors of protein phosphatases 1 and 2A, Cell Growth Differ. 5, 995-1004.
50. Weller, M., Malipiero, U., Groscurth, P. & Fontana, A. (1995) T cell apoptosis induced by interleukin-2 deprivation or transforming growth factor-b2: modulation by the phosphatase inhibitors okadaic acid and calyculin A, Exp. Cell Res. 221, 395-403.
51. Morana, S. J., Wolf, C. M., Li, J., Reynolds, J. E., Brown, M. K. & Eastman, A. (1996) The involvement of protein phosphatases in the activation of ICE/CED-3 protease, intracellular acidification, DNA digestion and apoptosis, J. Biol. Cliem. 271, 18263-18271.
52. Yan. Y., Shay, J. W, Wright, W. E. & Mumby, M. C. (1997) Inhibition of protein phosphatase activity induces p53-dependent apoptosis in the absence of p53 transactivation, J. Biot. Chcm. 272, 15220-15226.
53. Sheikh, M. S., Garcia, M., Zhan, Q., Liu, Y. & Fornace, A. J. Jr (1996) Cell cycle-independent regulation of p21 wafl/cipl and retinoblastoma protein during okadaic acid-induced apoptosis is coupled with induction of Bax protein in human breast carcinoma cells. Cell Growth Differ. 7, 15699-11607.
54. Fernandez-Sanchez, M., Garcia-Rodriguez, A., Diaz-Trelles, R. & Novelli, A. (1996) Inhibition of protein phosphatases induces IGF-1-blocked neurotrophin-insensitive neuronal apoptosis, FEBS Lett. 398, 106-112.
55. Reddan, J. R., Cheplinsky, A. B., Dziedzic, D. C, Piatigorsky, J. & Goldenberg, E. M. (1986) Retention of lens specificity in longterm cultures of diploid rabbit lens epithelial cells, Differentiation 33, 168-174.
56. Chen, G., Branton, P. E., Yang, E., Korsmeyer, S. J. & Shore, G. C. (1996) Adenovims E1B 19-kDa death suppressor protein interacts with Bax but not with Bad, J. Biol Cliem. 271, 24221-24225.
57. Ormerod, M. G., Sun, X.-M., Snowden, R. T., Davis, R., Fearnhead, H. & Cohen, G. M. (1993) Increased membrane permeability of apoptotic thymocytes: a flow cytometric study, Cytometry 14, 595-602.
58. Paterson, G. L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable, Anal. Biodiem. 83, 346-356.
59. Laiho, M., DeCaprio, J. A., Ludlow, I. \V., Livingston, D. M. & Massague, J. (1990) Growth inhibition by TGF-b linked to suppression of retinablastoma protein phosphorylationl, Cell 62, 175-185.
60. Jenkins, J., Rudge, K., Redmonds, S. & Wade-Evans, A. (1984) Cloning and expression analysis of full length mouse cDNA sequences encoding the transformation associated protein p53, Nucleic Acids Res. 12, 5609-5626.
61. Tso, J. Y, Sun, X. H., Kao, T. H., Recce, K. S. & VVu, R. (1985) Isolation and characterization of rat and human glyceraldehyde3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene, Nucleic Acids Res. 13, 2485 2502.
62. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. E., Smith, J. A. & Strahl, K. (1995) Current protocols in molecular biology, Wiley, New York.
63. Feinberg, A. P. & Vogelstein, B. (1983) A technique for radiolabelling DNA restriction cndonuclease fragments to high specific activity, Anal. Biochem. 132,6-13.
64. Favre, B., Turowski, P. & Hemmings, B. A. (1997) Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin, J. Biol. Chcm. 272, 13856-13863.
65. Li, M., Guo, H. & Damuni, Z. (1995) Purification and characterization of two potent heat-stable protein inhibitiors of protein phosphatase 2A from bovine kidney, Biochemistry 34, 1988-1996.
66. Park, I., Roach, P., Bondor, J., Fox, S. P. & DePaoli-Roach, A. A. (1994) Molecular mechanism of the synergistic phosphorylation of phosphatase inhibitor-2, J. Biol. Chcm. 269, 944-954.
67. Christofferson, J., Smeland, E. B., Stokke, T., Tasken, K., Andersson, K. B. & Blomhoff, H. K. (1994) Retinoblastoma protein is rapidly dephosphorylated by elevated cyclic adenosine monophosphate levels in human B-lymphoid cells, Cancer Res. 54, 2245-2250.
68. Ludlow, J. W., Glendening, C. L., Livingston, D. M. & De Caprio, J. A. (1993) Specific enzymatic dephosphorylation of the retinoblastoma protein. Mol. Cell. Biol. 13, 367-372.
69. Fraser, A. & Evan, G. (1996) A license to kill. Cell 85, 781-784.
70. Obrig, T. G., Gulp, W. J., Mckeehan, W. L. & Hardesty, B. (1971) The mechanism by which cycloheximide and related glutarimide antibiotics inhibit peptide synthesis on reticulocyte ribosomes, J. Biol. Chem.246, 174-181.
71. Li, D. W.-C., Wang, R.-R. & Spector, A. (1995) Lens epithelial cell apoptosis induced by phosphatase inhibitors, Mol. Biol. Cell. 6, 355a.
72. Yatsunami, J., Komori, A., Ohta, T., Suganuma, M. & Fujiki, H. (1993) Hyperphosphorylation of retinoblastoma protein and p53 by okadaic acid, a tumor promoter, Cancer Res. 53, 239-241.
73. Afshari, C. A. & Barrett, J. C. (1994) Disruption of GO-G1 arrest in quiescent and senescent cells treated with phosphatase inhibitors, Cancer Res. 54, 2317-2321.
74. Li, W.-C., Wang, G.-M., Wang, R. R. & Spector, A. (1994) The redox active components H2O2 and N-acetyl-L-cysteine regulate expression of c-jun and c-fos in lens systems, Exp. Eye Res. 59, 179-190.
75. Sabbatini, P., Lin, J., Levine, A. J. & White, E. (1995) Essential role for p53-mediated transcription in apoptosis but not growth suppression. Genes Dev. 9, 2184-2192.
76. Clarke, A. R., Mandag, E. R., van Roon, M., van der Lugt, N. M. T., van der Valk, M., Hooper, M. L., Berns, A. & te Riele, H. (1992) Requirement for a functional Rb-1 gène in murine development, Nature 359, 328-330.
77. Jack, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A. & Weinberg, R. A. (1992) Effects of an Rb mutation in thé mouse, Nature 359, 295-300.
78. Lee, E. Y.-H. P., Chang, C.-Y., Hu, N., Wang, Y.-C. J., Lai, C. C., Herrup, K. & Lee, W.-H. (1992) Mice deficient for Rb are nonvia-ble and show defects in neurogenesis and haematopoiesis, Nature 359, 288-294.
79. Morgenbesser, S. D., Williams, B. O., Jacks, T. & DePinho, R. A. (1994) p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens, Nature 371, 72-74.
80. Haldar, S., Jena, N. & Croce, C. (1995) Inactivation of Bcl-2 by phosphorylation, Proc. Nail Acacl. Sei. USA 92, 4507-4511.
81. Yamashita, K., Yasuda, H., Pines, J., Yasumoto, K., Nishitani, K., Ohtsubo, M., Hunter, T., Sugimura, T. & Nishimoto, T. (1990) Okadaic acid, a potent inhibitor of type 1 and type 2A protein phosphatases, activates cdc2/Hl kinase and transiently induces a premature mitosis-like state in BHK21 cells, EMBO J. 9, 43314338.
82. Meikrantz, W., Gisselbrecht, S., Tarn, S. W. & Schlegel, R. (1994) Activation of cyclin A-dependent protein kinases during apoptosis, Proc. Nntl Acacl. Sei. USA 91, 3754-3759.
83. cdc2 activation required for apoptosis, Science 263, 1143-1145.