Irod/Ian5: An inhibitor of γ-radiation- and okadaic acid-induced apoptosis

Molecular Biology of the Cell

Volumn 14, Issue 8, 2003, Pages 3292-3304

  Sandal, Tone ^a   Aumo, Linda ^a   Hedin, Lars ^a   Gjertsen, Bjørn T ^b   Døskeland, Stein O ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INHIBITOR; CASPASE 3; FAS ANTIBODY; GUANINE NUCLEOTIDE BINDING PROTEIN; INHIBITOR OF RADIATION AND OKADAIC ACID INDUCED APOPTOSIS PROTEIN; IROD IAN5 PROTEIN; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; STAUROSPORINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL PROTECTION; CENTROSOME; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GAMMA RADIATION; GENE DELETION; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOFLUORESCENCE; LEUKEMIA CELL LINE; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CASPASES; CELLS, CULTURED; CLONING, MOLECULAR; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; GAMMA RAYS; GENE LIBRARY; GOLGI APPARATUS; GTP-BINDING PROTEINS; HUMANS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; MUTATION; OKADAIC ACID; PROTEIN STRUCTURE, TERTIARY;

EID: 0042469596     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-10-0700     Document Type: Article

References (73)

1. Adrian, C., Creagh, E.M., and Martin, S.J. (2001). Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 20, 6627-6636.
2. Benitez-Bribiesca, L., and Sanchez-Suarez, P. (1999). Oxidative damage, bleomycin, and gamma radiation induce different types of DNA strand breaks in normal lymphocytes and thymocytes. A comet assay study. Ann. NY Acad. Sci. 887, 133-149.
3. Beham, A., Marin, M.C., Fernandez, A., Herrmann, J., Brisbay, S., Tari, A.M., Lopez-Berestein, G., Lozano, G., Sarkiss, M., and McDonnell, T.J. (1997). Bcl-2 inhibits p53 nuclear import following DNA damage. Oncogene 15, 2767-2772.
4. Boe, R., Gjertsen, B.T., Vintermyr, O.K., Houge, G., Lanotte, M., and 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.
5. Boesen-de Cock, J.G., Tepper, A.D., de Vries, E., van Blitterswijk, W.J., and Borst, J. (1999). Common regulation of apoptosis signaling induced by CD95 and the DNA-damaging stimuli etoposide and gamma-radiation downstream from caspase-8 activation. J. Biol. Chem. 274, 14255-14261.
6. Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34.
7. Braun, A.P., and Schulman, H. (1995a). The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu. Rev. Physiol. 57, 417-445.
8. Braun, A.P., and Schulman, H. (1995b). A non-selective cation current activated via the multifunctional Ca(2+)-calmodulin-dependent protein kinase in human epithelial cells. J. Physiol. 488, 37-55.
9. Cambot, M., Aresta, S., Kahn-Perles, B., de Gunzburg, J., and Romeo, P.H. (2002). Human immune associated nucleotide 1: a member of a new guanosine triphosphatase family expressed in resting T and B cells. Blood 99, 3293-3301.
10. Cheng, J., and Haas, M. (1990). Frequent mutations in the p53 tumor suppressor gene in human leukemia T-cell lines. Mol. Cell. Biol. 10, 5502-5509.
11. Daheron, L., Zenz, T., Siracusa, L.D., Brenner, C., and Calabretta, B. (2001). Molecular cloning of Ian4: a BCR/ABL-induced gene that encodes an outer membrane mitochondrial protein with GTP-binding activity. Nucleic Acids Res. 29, 1308-1316.
12. Deveraux, Q.L., and Reed, J.C. (1999). IAP family proteins-suppressors of apoptosis. Genes Dev. 13, 239-252.
13. Dilla, T., Romero, J., Sanstisteban, P., and Velasco, J.A. (2002). The mdm2 proto-oncogene sensitizes human medullary thyroid carcinoma cells to ionizing radiation. Oncogene 21, 2376-2386.
14. Døskeland, A.P., Vintermyr, O.K., Flatmark, T., Cotton, R.G., and Doskeland, S.O. (1992). Phenylalanine positively modulates the cAMP-dependent phosphorylation and negatively modulates the vasopressin-induced and okadaic-acid-induced phosphorylation of phenylalanine 4-monooxygenase in intact rat hepatocytes. Eur. J. Biochem. 206, 161-170.
15. Doxsey, S. (2001). Re-evaluating centrosome function. Nat. Rev. Mol. Cell. Biol. 2, 688-698.
16. Evans, S.C., Viswanathan, M., Grier, J.D., Narayana, M., El-Naggar, A.K., and Lozano, G, (2001). An alternatively spliced HDM2 product increases p53 activity by inhibiting HDM2. Oncogene 20, 4041-4049.
17. Fladmark, K.E., Brustugun, O.T., Hovland, R., Boe, R., Gjertsen, B.T., Zhivotovsky, B., and Doskeland, S.O. (1999). Ultrarapid caspase-3 dependent apoptosis induction by serine/threonine phosphatase inhibitors. Cell Death Differ, 6, 1099-1108.
18. Fladmark, K.E., Brustugun, O.T., Mellgren, G., Krakstad, C., Boe, R., Vintermyr, O.K., Schulman, H., and Doskeland, S.O. (2002). Ca2+/ calmodulin-dependent protein kinase II is required for microcystin-induced apoptosis. J. Biol. Chem. 277, 2804-2811.
19. Fry, A.M., Mayor, T., Meraldi, P., Stierhof, Y.D., Tanaka, K., and Nigg, E.A. (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 141, 1563-1574.
20. Fry, A.M., Mayor, T., and Nigg, E.A. (2000). Regulating centrosomes by protein phosphorylation. Curr. Top. Dev. Biol. 49, 291-312.
21. Fujimori, Y., Saheki, K., Itoi, H., Okamamoto, T., and Kakishita, E. (2000). Increased expression of Fas (APO-1, CD95) on CD4+ and CD8+ T lymphocytes during total body irradiation. Acta Haematol. 104, 193-196.
22. Garchon, H.J., Luan, J.J., Eloy, L., Bedossa, P., and Bach, J.F. (1994). Genetic analysis of immune dysfunction in non-obese diabetic (NOD) mice: mapping of a susceptibility locus close to the Bcl-2 gene correlates with increased resistance of NOD T cells to apoptosis induction. Eur. J. Immunol. 24, 380-384.
23. Gergely, F. (2002). Centrosomal TACCtics. Bioessays 24, 915-925.
24. Gjertsen, B.T., Cressey, L.I., Ruchaud, S., Houge, G., Lanotte, M., and Doskeland, S.O. (1994). Multiple apoptotic death types triggered through activation of separate pathways by cAMP and inhibitors of protein phosphatases in one (IPC leukemia) cell line. J. Cell Sci. 107, 3363-3377.
25. Guo, C.Y., Brautigan, D.L., and Larner, J.M. (2002). ATM-dependent dissociation of B55 regulatory subunit from nuclear PP2A in response to ionizing radiation. J. Biol. Chem. 277, 4839-4844.
26. Hanson, P.I., and Schulman, H. (1992). Neuronal Ca2+/ calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61, 559-601.
27. Hornum, L., Romer, J., and Markholst, H. (2002). The diabetes-prone BB rat carries a frameshift mutation in Ian4, a positional candidate of Iddm1. Diabetes 51, 1972-1979.
28. Inagaki, N., Goto, H., Ogawara, M., Nishi, Y., Ando, S., and Inagaki, M. (1997). Spatial patterns of Ca2+ signals define intracellular distribution of a signaling by Ca2+/Calmodulin-dependent protein kinase II. J. Biol. Chem. 272, 25195-25199.
29. Ishida, A., Kameshita, I., Okuno, S., Kitani, T., and Fujisawa, H. (1995). A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun. 212, 806-812.
30. Kasibhatla, S., Beere, H.M., Brunner, T., Echeverri, F., and Green, D.R. (2000). A 'non-canonical' DNA-binding element mediates the response of the Fas-ligand promoter to c-Myc. Curr. Biol. 10, 1205-1208.
31. Kasibhatla, S., Brunner, T., Genestier, L., Echeverri, F., Mahboubi, A., and Green, D.R. (1998). DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell 1, 543-551.
32. Krucken, J., Schmitt-Wrede, H.P., Markmann-Mulisch, U., and Wunderlich, F. (1997). Novel gene expressed in spleen cells mediating acquired testosterone-resistant immunity to Plasmodium chabaudi malaria. Biochem. Biophys. Res. Commun. 230, 167-170.
33. Krucken, J., Stamm, O., Schmitt-Wrede, H.P., Mincheva, A., Lichter, P., and Wunderlich, F. (1999). Spleen-specific expression of the malaria-inducible intronless mouse gene imap38. J. Biol. Chem. 274, 24383-24391.
34. Lakin, N.D., and Jackson, S.P. (1999). Regulation of p53 in response to DNA damage. Oncogene 18, 7644-7655.
35. Lange, B.M. (2002). Integration of the centrosome in cell cycle control, stress response and signal transduction pathways. Curr. Opin. Cell Biol. 14, 35-43.
36. Lorens, J.B., et al. (2000). Retroviral delivery of peptide modulators of cellular functions. Mol. Ther. 1, 438-447.
37. Lorson, M.A., Horvitz, H.R., and van den Heuvel, S. (2000). LIN-5 is a novel component of the spindle apparatus required for chromosome segregation and cleavage plane specification in Caenorhabditis elegans. J. Cell Biol. 148, 73-86.
38. Lu, H., Taya, Y., Ikeda, M., and Levine, AJ. (1998). Ultraviolet radiation, but not gamma radiation or etoposide-induced DNA damage, results in the phosphorylation of the murine p53 protein at serine-389. Proc. Natl. Acad. Sci. USA 95, 6399-6402.
39. Lupas, A. (1996a). Coiled coils: new structures and new functions. Trends Biochem. Sci. 21, 375-382.
40. Lupas, A. (1996b). Prediction and analysis of coiled-coil structures. Methods Enzymol. 266, 513-525.
41. Lupas, A., Van Dyke, M., and Stock, J. (1991). Predicting coiled coils from protein sequences. Science 252, 1162-1164.
42. MacMurray, A.J., et al. (2002). Lymphopenia in the BB rat model of type 1 diabetes is due to a mutation in a novel immune-associated nucleotide (Ian)-related gene. Genome Res. 12, 1029-1039.
43. Mandik-Nayak, L., Nayak, S., Sokol, C., Eaton-Bassiri, A., Madaio, M.P., Caton, A.J., and Erikson, J. (2000). The origin of anti-nuclear antibodies in bcl-2 transgenic mice. Int. Immunol. 12, 353-364.
44. Maro, B., Paintrand, M., Sauron, M.E., Paulin, D., and Bornens, M. (1984). Vimentin filaments and centrosomes. Are they associated? Exp. Cell Res. 150, 452-458.
45. Matsumoto, Y., and Maller, J.L. (2002). Calcium, calmodulin, and CaMKII requirement for initiation of centrosome duplication in Xenopus egg extracts. Science 295, 499-502.
46. Mellgren, G., Vintermyr, O.K., and Doskeland, S.O. (1995). Okadaic acid, cAMP, and selected nutrients inhibit hepatocyte proliferation at different stages in G 1, modulation of the cAMP effect by phosphatase inhibitors and nutrients. J. Cell. Physiol. 163, 232-240.
47. Meraldi, P., and Nigg, E.A. (2001). Centrosome cohesion is regulated by a balance of kinase and phosphatase activities. J. Cell Sci. 114, 3749-3757.
48. Meraldi, P., and Nigg, E.A. (2002). The centrosome cycle. FEBS Lett. 521, 9-13.
49. Moffett, P., Farnham, G., Peart, J., and Baulcombe, D.C. (2002). Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21, 4511-4519.
50. Morimoto, Y., Morimoto, H., Kobayashi, S., Ohba, T., and Haneji, T. (1999). The protein phosphatase inhibitors, okadaic acid and calyculin A, induce apoptosis in human submandibular gland ductal cell line HSG cells. Oral Dis. 5, 104-110.
51. Ogawa, H., Inouye, S., Tsuji, F.I., Yasuda, K., and Umesono, K. (1995). Localization, trafficking, and temperature-dependence of the Aequorea green fluorescent protein in cultured vertebrate cells. Proc. Natl. Acad. Sci. USA 92, 11899-11903.
52. Perry, M.E., Mendrysa, S.M., Saucedo, L.J., Tannous, P., and Holubar, M. (2000). p76(MDM2) inhibits the ability of p90(MDM2) to destabilize p53. J. Biol. Chem. 275, 5733-5738.
53. Pietromonaco, S.F., Seluja, G.A., and Elias, L. (1995). Identification of enzymatically active Ca2+/calmodulin-dependent protein kinase in centrosomes of hemopoietic cells. Blood Cells Mol. Dis. 21, 34-41.
54. Pockwinse, S.M., Krockmalnic, G., Doxsey, S.J., Nickerson, J., Lian, J.B., van Wijnen, A.J., Stein, J.L., Stein, G.S., and Penman, S. (1997). Cell cycle independent interaction of CDC2 with the centrosome, which is associated with the nuclear matrix-intermediate filament scaffold. Proc. Natl. Acad. Sci. USA 94, 3022-3027.
55. Poirier, G.M., Anderson, G., Huvar, A., Wagaman, P.C., Shuttleworth, J., Jenkinson, E., Jackson, M.R., Peterson, P.A., and Erlander, M.G. (1999). Immune-associated nucleotide-1 (IAN-1) is a thymic selection marker and defines a novel gene family conserved in plants. J. Immunol. 163, 4960-4969.
56. Rudner, J., Belka, C., Marini, P., Wagner, R.J., Faltin, H., Lepple-Wienhues, A., Bamberg, M., and Budach, W. (2001). Radiation sensitivity and apoptosis in human lymphoma cells. Int. J. Radiat. Biol. 77, 1-11.
57. Sandal, T., Ahlgren, R., Lillehaug, J., and Doskeland, S.O. (2001). Establishment of okadaic acid resistant cell clones using a cDNA expression library. Cell Death Differ. 8, 754-766.
58. Sandal, T., Stapnes, C., Kleivdal, H., Hedin, L., and Doskeland, S.O. (2002). A novel, extraneuronal role for cyclin-dependent protein kinase 5 (CDK5). Modulation of cAMP-induced apoptosis in rat leukemia cells. J. Biol. Chem. 277, 20783-20793.
59. Sato, N., Mizumoto, K., Nakamura, M., Ueno, H., Minamishima, Y.A., Farber, J.L., and Tanaka, M. (2000). A possible role for centrosome overduplication in radiation-induced cell death. Oncogene 19, 5281-5290.
60. Srinivasan, M., Edman, C.F., and Schulman, H. (1994). Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus. J. Cell Biol. 126, 839-852.
61. Stamm, O., Krucken, J., Schmitt-Wrede, H.P., Benten, W.P., and Wunderlich, F. (2002). Human ortholog to mouse gene imap38 encoding an ER-localizable G-protein belongs to a gene family clustered on chromosome 7q32-36. Gene 282, 159-167.
62. Staskawicz, B.J., Ausubel, F.M., Baker, B.J., Ellis, J.G., and Jones, J.D. (1995). Molecular genetics of plant disease resistance. Science 268, 661-667.
63. Strasser, A., Harris, A.W., Huang, D.C., Krammer, P.H., and Cory, S. (1995). Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14, 6136-6147.
64. Strasser, A., Whittingham, S., Vaux, D.L., Bath, M.L., Adams, J.M., Cory, S., and Harris, A.W. (1991). Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 88, 8661-8665.
65. Takahashi, M., Shibata, H., Shimakawa, M., Miyamoto, M., Mukai, H., and Ono, Y. (1999). Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the Golgi apparatus. J. Biol. Chem. 274, 17267-17274.
66. Tounekti, O., Kenani, A., Foray, N., Orlowski, S., and Mir, L.M. (2001). The ratio of single- to double-strand DNA breaks and their absolute values determine cell death pathway. Br. J. Cancer 84, 1272-1279.
67. Trevor, K.T., McGuire, J.G., and Leonova, E.V. (1995). Association of vimentin intermediate filaments with the centrosome. J. Cell Sci. 108, 343-356.
68. Turowski, P., Myles, T., Hemmings, B.A., Fernandez, A., and Lamb, N.J. (1999). Vimentin dephosphorylation by protein phosphatase 2A is modulated by the targeting subunit B55. Mol. Biol. Cell 10, 1997-2015.
69. Verde, I., Pahlke, G., Salanova, M., Zhang, G., Wang, S., Coletti, D., Onuffer, J., Jin, S.L., and Conti, M. (2001). Myomegalin is a novel protein of the Golgi/centrosome that interacts with a cyclic nucleotide phosphodiesterase. J. Biol. Chem. 276, 11189-11198.
70. Wigley, W.C., Fabunmi, R.P., Lee, M.G., Marino, C.R., Muallem, S., DeMartino, G.N., and Thomas, P.J. (1999). Dynamic association of proteasomal machinery with the centrosome. J. Cell Biol. 145, 481-490.
71. Wright, S.C., Schellenberger, U., Ji, L., Wang, H., and Larrick, J.W. (1997). Calmodulin-dependent protein kinase II mediates signal transduction in apoptosis. FASEB J. 11, 843-849.
72. Wu, J., Yin, M.B., Hapke, G., Toth, K., and Rustum, Y.M. (2002). Induction of biphasic DNA double strand breaks and activation of multiple repair protein complexes by DNA topoisomerase I drug 7-ethyl-10-hydroxy-camptothecin. Mol. Pharmacol. 61, 742-748.
73. Yan, Y., Shay, J.W., Wright, W.E., and Mumby, M.C. (1997). Inhibition of protein phosphatase activity induces p53-dependent apoptosis in the absence of p53 transactivation. J. Biol. Chem. 272, 15220-15226.