Steroid receptor coactivator-interacting protein (SIP) inhibits caspase-independent apoptosis by preventing apoptosis-inducing factor (AIF) from being released from mitochondria

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 12612-12621

  Wang, Dandan ^a   Liang, Jing ^a   Zhang, Yu ^a   Gui, Bin ^a   Wang, Feng ^a   Yi, Xia ^a   Sun, Luyang ^a   Yao, Zhi ^b   Shang, Yongfeng ^a,b  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS-INDUCING FACTORS; APOPTOTIC STIMULI; CASPASE-INDEPENDENT; CHROMATIN CONDENSATION; DNA FRAGMENTATION; PRO-APOPTOTIC STIMULI; RAPID DEGRADATION; STEROID RECEPTORS;

INTERNET PROTOCOLS; MITOCHONDRIA;

CELL DEATH;

APOPTOSIS INDUCING FACTOR; APOPTOSIS REGULATORY PROTEIN; CASPASE; STEROID RECEPTOR COACTIVATOR INTERACTING PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; BREAST NEOPLASMS; CASPASES; CELL DIVISION; FEMALE; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MITOCHONDRIA; NUCLEAR RECEPTOR COACTIVATOR 1;

EID: 84859757966     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.334151     Document Type: Article

References (50)

1. Hengartner, M. O. (2000) The biochemistry of apoptosis. Nature 407, 770-776
2. Green, D. R., and Kroemer, G. (2004) The pathophysiology of mitochondrial cell death. Science 305, 626-629 (Pubitemid 39006738)
3. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M., and Kroemer, G. (1999) Molecular characterization of mitochondrial apoptosis- inducing factor. Nature 397, 441-446
4. Ye, H., Cande, C., Stephanou, N. C., Jiang, S., Gurbuxani, S., Larochette, N., Daugas, E., Garrido, C., Kroemer, G., and Wu, H. (2002) DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nat.Struct. Biol. 9, 680-684 (Pubitemid 34977301)
5. Joza, N., Oudit, G. Y., Brown, D., Bénit, P., Kassiri, Z., Vahsen, N., Benoit, L., Patel, M. M., Nowikovsky, K., Vassault, A., Backx, P. H., Wada, T., Kroemer, G., Rustin, P., and Penninger, J. M. (2005) Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol. Cell. Biol. 25, 10261-10272 (Pubitemid 41681953)
6. Klein, J. A., Longo-Guess, C. M., Rossmann, M. P., Seburn, K. L., Hurd, R. E., Frankel, W. N., Bronson, R. T., and Ackerman, S. L. (2002) The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419, 367-374
7. Pospisilik, J. A., Knauf, C., Joza, N., Benit, P., Orthofer, M., Cani, P. D., Ebersberger, I., Nakashima, T., Sarao, R., Neely, G., Esterbauer, H., Kozlov, A., Kahn, C. R., Kroemer, G., Rustin, P., Burcelin, R., and Penninger, J. M. (2007) Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131, 476-491 (Pubitemid 350017761)
8. Vahsen, N., Candé, C., Brière, J. J., Bénit, P., Joza, N., Larochette, N., Mastroberardino, P. G., Pequignot, M. O., Casares, N., Lazar, V., Feraud, O., Debili, N., Wissing, S., Engelhardt, S., Madeo, F., Piacentini, M., Penninger, J. M., Schägger, H., Rustin, P., and Kroemer, G. (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J. 23, 4679-4689 (Pubitemid 39657867)
9. Joza, N., Susin, S. A., Daugas, E., Stanford, W. L., Cho, S. K., Li, C. Y., Sasaki, T., Elia, A. J., Cheng, H. Y., Ravagnan, L., Ferri, K. F., Zamzami, N., Wakeham, A., Hakem, R., Yoshida, H., Kong, Y. Y., Mak, T. W., Zúñiga-Pflücker, J. C., Kroemer, G., and Penninger, J. M. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410, 549-554 (Pubitemid 32267191)
10. Loeffler, M., Daugas, E., Susin, S. A., Zamzami, N., Metivier, D., Nieminen, A. L., Brothers, G., Penninger, J. M., and Kroemer, G. (2001) Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor. FASEB J. 15, 758-767 (Pubitemid 32245994)
11. Daugas, E., Susin, S. A., Zamzami, N., Ferri, K. F., Irinopoulou, T., Larochette, N., Prévost, M. C., Leber, B., Andrews, D., Penninger, J., and Kroemer, G. (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14, 729-739 (Pubitemid 30198571)
12. Artus, C., Boujrad, H., Bouharrour, A., Brunelle, M. N., Hoos, S., Yuste, V. J., Lenormand, P., Rousselle, J. C., Namane, A., England, P., Lorenzo, H. K., and Susin, S. A. (2010) AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J. 29, 1585-1599
13. Yu, S. W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M., and Dawson, V. L. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297, 259-263 (Pubitemid 34761289)
14. Wang, X., Yang, C., Chai, J., Shi, Y., and Xue, D. (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298, 1587-1592 (Pubitemid 35387191)
15. Candé, C., Vahsen, N., Kouranti, I., Schmitt, E., Daugas, E., Spahr, C., Luban, J., Kroemer, R. T., Giordanetto, F., Garrido, C., Penninger, J. M., and Kroemer, G. (2004) AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis. Oncogene 23, 1514-1521 (Pubitemid 38406513)
16. Otera, H., Ohsakaya, S., Nagaura, Z., Ishihara, N., and Mihara, K. (2005) Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 24, 1375-1386 (Pubitemid 40593058)
17. Uren, R. T., Dewson, G., Bonzon, C., Lithgow, T., Newmeyer, D. D., and Kluck, R. M. (2005) Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J. Biol. Chem. 280, 2266-2274
18. Cao, G., Xing, J., Xiao, X., Liou, A. K., Gao, Y., Yin, X. M., Clark, R. S., Graham, S. H., and Chen, J. (2007) Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J. Neurosci. 27, 9278-9293 (Pubitemid 47358221)
19. Polster, B. M., Basañez, G., Etxebarria, A., Hardwick, J. M., and Nicholls, D. G. (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem. 280, 6447-6454 (Pubitemid 40341192)
20. Joshi, A., Bondada, V., and Geddes, J. W. (2009) Mitochondrial micro-calpain is not involved in the processing of apoptosis-inducing factor. Exp. Neurol. 218, 221-227
21. Andrabi, S. A., Kim, N. S., Yu, S. W., Wang, H., Koh, D. W., Sasaki, M., Klaus, J. A., Otsuka, T., Zhang, Z., Koehler, R. C., Hurn, P. D., Poirier, G. G., Dawson, V. L., and Dawson, T. M. (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl. Acad. Sci. U.S.A. 103, 18308-18313 (Pubitemid 44871654)
22. Yu, S. W., Andrabi, S. A., Wang, H., Kim, N. S., Poirier, G. G., Dawson, T. M., and Dawson, V. L. (2006) Apoptosis-inducing factor mediates poly- (ADP-ribose) (PAR) polymer-induced cell death. Proc. Natl. Acad. Sci. U.S.A. 103, 18314-18319 (Pubitemid 44871655)
23. Gurbuxani, S., Schmitt, E., Cande, C., Parcellier, A., Hammann, A., Daugas, E., Kouranti, I., Spahr, C., Pance, A., Kroemer, G., and Garrido, C. (2003) Heat shock protein 70 binding inhibits the nuclear import of apoptosis- inducing factor. Oncogene 22, 6669-6678 (Pubitemid 37372207)
24. Matsumori, Y., Hong, S. M., Aoyama, K., Fan, Y., Kayama, T., Sheldon, R. A., Vexler, Z. S., Ferriero, D. M., Weinstein, P. R., and Liu, J. (2005) Hsp70 overexpression sequesters AIF and reduces neonatal hypoxic/ischemic brain injury. J. Cereb. Blood Flow Metab. 25, 899-910 (Pubitemid 40905617)
25. Ravagnan, L., Gurbuxani, S., Susin, S. A., Maisse, C., Daugas, E., Zamzami, N., Mak, T., Jäättelä, M., Penninger, J. M., Garrido, C., and Kroemer, G. (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol. 3, 839-843 (Pubitemid 32842690)
26. Zhang, Y., Zhang, H., Liang, J., Yu, W., and Shang, Y. (2007) SIP, a novel ankyrin repeat containing protein, sequesters steroid receptor coactivators in the cytoplasm. EMBO J. 26, 2645-2657 (Pubitemid 46884279)
27. Zhang, H., Yi, X., Sun, X., Yin, N., Shi, B., Wu, H., Wang, D., Wu, G., and Shang, Y. (2004) Differential gene regulation by the SRC family of coactivators. Genes Dev. 18, 1753-1765 (Pubitemid 38938190)
28. Wu, H., Chen, Y., Liang, J., Shi, B., Wu, G., Zhang, Y., Wang, D., Li, R., Yi, X., Zhang, H., Sun, L., and Shang, Y. (2005) Hypomethylation-linked activation of PAX2 mediates tamoxifen-stimulated endometrial carcinogenesis. Nature 438, 981-987 (Pubitemid 43093965)
29. Zhang, H., Sun, L., Liang, J., Yu, W., Zhang, Y., Wang, Y., Chen, Y., Li, R., Sun, X., and Shang, Y. (2006) The catalytic subunit of the proteasome is engaged in the entire process of estrogen receptor-regulated transcription. EMBO J. 25, 4223-4233 (Pubitemid 44435220)
30. Shi, B., Liang, J., Yang, X., Wang, Y., Zhao, Y., Wu, H., Sun, L., Zhang, Y., Chen, Y., Li, R., Zhang, Y., Hong, M., and Shang, Y. (2007) Integration of estrogen and Wnt signaling circuits by the polycomb group protein EZH2 in breast cancer cells. Mol. Cell. Biol. 27, 5105-5119 (Pubitemid 47068285)
31. Li, R., Zhang, H., Yu, W., Chen, Y., Gui, B., Liang, J., Wang, Y., Sun, L., Yang, X., Zhang, Y., Shi, L., Li, Y., and Shang, Y. (2009) ZIP. A novel transcription repressor, represses EGFR oncogene and suppresses breast carcinogenesis. EMBO J. 28, 2763-2776
32. Sun, L., Shi, L., Li, W., Yu, W., Liang, J., Zhang, H., Yang, X., Wang, Y., Li, R., Yao, X., Yi, X., and Shang, Y. (2009) JFK, a Kelch domain-containing F-box protein, links the SCF complex to p53 regulation. Proc. Natl. Acad. Sci. U.S.A. 106, 10195-10200
33. Li, Y., Sun, L., Zhang, Y., Wang, D., Wang, F., Liang, J., Gui, B., and Shang, Y. (2011) The histone modifications governing TFF1 transcription mediated by estrogen receptor. J. Biol. Chem. 286, 13925-13936
34. Shi, L., Sun, L., Li, Q., Liang, J., Yu, W., Yi, X., Yang, X., Li, Y., Han, X., Zhang, Y., Xuan, C., Yao, Z., and Shang, Y. (2011) Histone demethylase JMJD2B coordinates H3K4/H3K9 methylation and promotes hormonally responsive breast carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 7541-7546
35. Sun, L., Shi, L., Wang, F., Huangyang, P., Si, W., Yang, J., Yao, Z., and Shang, Y. (2011) Substrate phosphorylation and feedback regulation in JFK-promoted p53 destabilization. J. Biol. Chem. 286, 4226-4235
36. Wang, Y., Zhang, H., Chen, Y., Sun, Y., Yang, F., Yu, W., Liang, J., Sun, L., Yang, X., Shi, L., Li, R., Li, Y., Zhang, Y., Li, Q., Yi, X., and Shang, Y. (2009) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660-672
37. Yang, X., Yu, W., Shi, L., Sun, L., Liang, J., Yi, X., Li, Q., Zhang, Y., Yang, F., Han, X., Zhang, D., Yang, J., Yao, Z., and Shang, Y. (2011) HAT4, a Golgi apparatus-anchored B-type histone acetyltransferase, acetylates free histone H4 and facilitates chromatin assembly. Mol. Cell 44, 39-50
38. Belmokhtar, C. A., Hillion, J., and Ségal-Bendirdjian, E. (2001) Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene 20, 3354-3362 (Pubitemid 32588984)
39. Yuste, V. J., Moubarak, R. S., Delettre, C., Bras, M., Sancho, P., Robert, N., d'Alayer, J., and Susin, S. A. (2005) Cysteine protease inhibition prevents mitochondrial apoptosis-inducing factor (AIF) release. Cell Death Differ. 12, 1445-1448 (Pubitemid 41521936)
40. Susin, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M., and Kroemer, G. (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184, 1331-1341 (Pubitemid 26354689)
41. Kroemer, G. (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3, 614-620
42. Zhu, C., Wang, X., Deinum, J., Huang, Z., Gao, J., Modjtahedi, N., Neagu, M. R., Nilsson, M., Eriksson, P. S., Hagberg, H., Luban, J., Kroemer, G., and Blomgren, K. (2007) Cyclophilin A participates in the nuclear translocation of apoptosis-inducing factor in neurons after cerebral hypoxia-ischemia. J. Exp. Med. 204, 1741-1748 (Pubitemid 47236312)
43. Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Tailor, P., Morimoto, R. I., Cohen, G. M., and Green, D. R. (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2, 469-475
44. Saleh, A., Srinivasula, S. M., Balkir, L., Robbins, P. D., and Alnemri, E. S. (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2, 476-483
45. Rogers, S., Wells, R., and Rechsteiner, M. (1986) Amino acid sequences common to rapidly degraded proteins. The PEST hypothesis. Science 234, 364-368 (Pubitemid 17181385)
46. Spencer, M. L., Theodosiou, M., and Noonan, D. J. (2004) NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J. Biol. Chem. 279, 37069-37078 (Pubitemid 39129057)
47. Harada, J. N., Bower, K. E., Orth, A. P., Callaway, S., Nelson, C. G., Laris, C., Hogenesch, J. B., Vogt, P. K., and Chanda, S. K. (2005) Identification of novel mammalian growth regulatory factors by genome-scale quantitative image analysis. Genome Res. 15, 1136-1144 (Pubitemid 41126869)
48. Urbano, A., Lakshmanan, U., Choo, P. H., Kwan, J. C., Ng, P. Y., Guo, K., Dhakshinamoorthy, S., and Porter, A. (2005) AIF suppresses chemical stress-induced apoptosis and maintains the transformed state of tumor cells. EMBO J. 24, 2815-2826 (Pubitemid 41170030)
49. Miramar, M. D., Costantini, P., Ravagnan, L., Saraiva, L. M., Haouzi, D., Brothers, G., Penninger, J. M., Peleato, M. L., Kroemer, G., and Susin, S. A. (2001) NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem. 276, 16391-16398
50. Bénit, P., Goncalves, S., Dassa, E. P., Brière, J. J., and Rustin, P. (2008) The variability of the harlequin mouse phenotype resembles that of human mitochondrial-complex I-deficiency syndromes. PLoS One 3, e3208