Role of melanoma inhibitor of apoptosis (ML-IAP) protein, a member of the baculoviral IAP repeat (BIR) domain family, in the regulation of C-RAF kinase and cell migration

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28445-28455

  Oberoi Khanuja, Tripat Kaur ^a   Karreman, Christiaan ^b   Larisch, Sarit ^c   Rapp, Ulf R ^d   Rajalingam, Krishnaraj ^a  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c UNIVERSITY OF HAIFA   (Israel)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACULOVIRAL IAP; CELL MIGRATION; INHIBITING CASPASES; INHIBITOR OF APOPTOSIS; MELANOMA CELLS; PROTEIN LEVEL; PROTEIN STABILITY; TUMOR CELL MIGRATION;

CELL DEATH; DERMATOLOGY; ONCOLOGY; PROTEINS;

ENZYME INHIBITION;

LIVIN; RAF PROTEIN; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; BINDING AFFINITY; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME REGULATION; ENZYME STABILITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME STABILITY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MELANOMA; NEOPLASM PROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-RAF;

EID: 84865220499     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.341297     Document Type: Article

References (46)

1. Vucic, D., Stennicke, H. R., Pisabarro, M. T., Salvesen, G. S., and Dixit, V. M. (2000) ML-IAP, a novel inhibitor of apoptosis that is preferentially expressed in human melanomas. Curr. Biol. 10, 1359-1366
2. Srinivasula, S. M., and Ashwell, J. D. (2008) IAPs. What's in a name? Mol. Cell 30, 123-135
3. Vaux, D. L., and Silke, J. (2005) IAPs, RINGs and ubiquitylation. Nat. Rev. Mol. Cell Biol. 6, 287-297
4. Vaux, D. L., and Silke, J. (2005) IAPs. The ubiquitin connection. Cell Death Differ. 12, 1205-1207
5. Silke, J., Kratina, T., Chu, D., Ekert, P. G., Day, C. L., Pakusch, M., Huang, D. C., and Vaux, D. L. (2005) Determination of cell survival by RING-mediated regulation of inhibitor of apoptosis (IAP) protein abundance. Proc. Natl. Acad. Sci. U.S.A. 102, 16182-16187
6. Gyrd-Hansen, M., Darding, M., Miasari, M., Santoro, M. M., Zender, L., Xue, W., Tenev, T., da Fonseca, P. C., Zvelebil, M., Bujnicki, J. M., Lowe, S., Silke, J., and Meier, P. (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-κB as well as cell survival and oncogenesis. Nat. Cell Biol. 10, 1309-1317
7. Blankenship, J. W., Varfolomeev, E., Goncharov, T., Fedorova, A. V., Kirkpatrick, D. S., Izrael-Tomasevic, A., Phu, L., Arnott, D., Aghajan, M., Zobel, K., Bazan, J. F., Fairbrother, W. J., Deshayes, K., and Vucic, D. (2008) Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2(1). Biochem. J. 417, 1-3
8. Augello, C., Caruso, L., Maggioni, M., Donadon, M., Montorsi, M., Santambrogio, R., Torzilli, G., Vaira, V., Pellegrini, C., Roncalli, M., Coggi, G., and Bosari, S. (2009) Inhibitors of apoptosis proteins (IAPs) expression and their prognostic significance in hepatocellular carcinoma. BMC Cancer 9, 125
9. Sun, J. G., Liao, R. X., Zhang, S. X., Duan, Y. Z., Zhuo, W. L., Wang, X. X., Wang, Z. X., Li, D. Z., and Chen, Z. T. (2011) Role of inhibitor of apoptosis protein Livin in radiation resistance in nonsmall cell lung cancer. Cancer Biother. Radiopharm. 26, 585-592
10. Wu, H. H., Wu, J. Y., Cheng, Y. W., Chen, C. Y., Lee, M. C., Goan, Y. G., and Lee, H. (2010) cIAP2 up-regulated by E6 oncoprotein via epidermal growth factor receptor/phosphatidylinositol 3-kinase/AKT pathway confers resistance to cisplatin in human papillomavirus 16/18-infected lung cancer. Clin. Cancer Res. 16, 5200-5210
11. Gyrd-Hansen, M., and Meier, P. (2010) IAPs. From caspase inhibitors to modulators of NF-κB, inflammation and cancer. Nat. Rev. Cancer 10, 561-574
12. Zender, L., Spector, M. S., Xue, W., Flemming, P., Cordon-Cardo, C., Silke, J., Fan, S. T., Luk, J. M., Wigler, M., Hannon, G. J., Mu, D., Lucito, R., Powers, S., and Lowe, S. W. (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125, 1253-1267
13. Wang, X., Xu, J., Ju, S., Ni, H., Zhu, J., and Wang, H. (2010) Livin gene plays a role in drug resistance of colon cancer cells. Clin. Biochem. 43, 655-660
14. Gazzaniga, P., Gradilone, A., Giuliani, L., Gandini, O., Silvestri, I., Nofroni, I., Saccani, G., Frati, L., and Aglianò, A. M. (2003) Expression and prognostic significance of LIVIN, SURVIVIN and other apoptosis-related genes in the progression of superficial bladder cancer. Ann. Oncol. 14, 85-90
15. Crnkovic-Mertens, I., Wagener, N., Semzow, J., Grone, E. F., Haferkamp, A., Hohenfellner, M., Butz, K., and Hoppe-Seyler, F. (2007) Targeted inhibition of Livin resensitizes renal cancer cells towards apoptosis. Cell Mol. Life Sci. 64, 1137-1144
16. Kempkensteffen, C., Hinz, S., Christoph, F., Krause, H., Koellermann, J., Magheli, A., Schrader, M., Schostak, M., Miller, K., and Weikert, S. (2007) Expression of the apoptosis inhibitor livin in renal cell carcinomas. Correlations with pathology and outcome. Tumour Biol. 28, 132-138
17. Tanabe, H., Yagihashi, A., Tsuji, N., Shijubo, Y., Abe, S., and Watanabe, N. (2004) Expression of survivin mRNA and livin mRNA in non-small-cell lung cancer. Lung Cancer 46, 299-304
18. Qiuping, Z., Jei, X., Youxin, J., Wei, J., Chun, L., Jin, W., Qun, W., Yan, L., Chunsong, H., Mingzhen, Y., Qingping, G., Kejian, Z., Zhimin, S., Qun, L., Junyan, L., and Jinquan, T. (2004) CC chemokine ligand 25 enhances resistance to apoptosis in CD4+ T cells from patients with T-cell lineage acute and chronic lymphocytic leukemia by means of livin activation. Cancer Res. 64, 7579-7587
19. Kim, D. K., Alvarado, C. S., Abramowsky, C. R., Gu, L., Zhou, M., Soe, M. M., Sullivan, K., George, B., Schemankewitz, E., and Findley, H. W. (2005) Expression of inhibitor-of-apoptosis protein (IAP) livin by neuroblastoma cells. Correlation with prognostic factors and outcome. Pediatr Dev. Pathol. 8, 621-629
20. Yuan, B., Ran, B., Wang, S., Liu, Z., Zheng, Z., and Chen, H. (2011) siRNA directed against Livin inhibits tumor growth and induces apoptosis in human glioma cells. J. Neurooncol. 107, 81-87
21. Ma, L., Huang, Y., Song, Z., Feng, S., Tian, X., Du, W., Qiu, X., Heese, K., and Wu, M. (2006) Livin promotes Smac/DIABLO degradation by ubiquitin-proteasome pathway. Cell Death Differ. 13, 2079-2088
22. Vucic, D., Franklin, M. C., Wallweber, H. J., Das, K., Eckelman, B. P., Shin, H., Elliott, L. O., Kadkhodayan, S., Deshayes, K., Salvesen, G. S., and Fairbrother, W. J. (2005) Engineering ML-IAP to produce an extraordinarily potent caspase 9 inhibitor. Implications for Smac-dependent anti-apoptotic activity of ML-IAP. Biochem. J. 385, 11-20
23. Vucic, D., Deshayes, K., Ackerly, H., Pisabarro, M. T., Kadkhodayan, S., Fairbrother, W. J., and Dixit, V. M. (2002) SMAC negatively regulates the anti-apoptotic activity of melanoma inhibitor of apoptosis (ML-IAP). J. Biol. Chem. 277, 12275-12279
24. Dynek, J. N., Chan, S. M., Liu, J., Zha, J., Fairbrother, W. J., and Vucic, D. (2008) Microphthalmia-associated transcription factor is a critical transcriptional regulator of melanoma inhibitor of apoptosis in melanomas. Cancer Res. 68, 3124-3132
25. Yuan, D., Liu, L., and Gu, D. (2007) Transcriptional regulation of livin by β-catenin/TCF signaling in human lung cancer cell lines. Mol. Cell Biochem. 306, 171-178
26. Dasgupta, A., Peirce, S. K., and Findley, H. W. (2009) MycN is a transcriptional regulator of livin in neuroblastoma. Oncol. Rep. 22, 831-835
27. Wang, R., Lin, F., Wang, X., Gao, P., Dong, K., Zou, A. M., Cheng, S. Y., Wei, S. H., and Zhang, H. Z. (2008) Silencing Livin gene expression to inhibit proliferation and enhance chemosensitivity in tumor cells. Cancer Gene. Ther. 15, 402-412
28. Wang, H., Tan, S. S., Wang, X. Y., Liu, D. H., Yu, C. S., Bai, Z. L., He, D. L., and Zhao, J. (2007) Silencing livin gene by siRNA leads to apoptosis induction, cell cycle arrest, and proliferation inhibition in malignant melanoma LiBr cells. Acta Pharmacol. Sin. 28, 1968-1974
29. Kyriakis, J. M. (2007) The integration of signaling by multiprotein complexes containing Raf kinases. Biochim. Biophys. Acta 1773, 1238-1247
30. Rajalingam, K., Schreck, R., Rapp, U. R., and Albert, S. (2007) Ras oncogenes and their downstream targets. Biochim. Biophys. Acta 1773, 1177-1195
31. Kyriakis, J. M., App, H., Zhang, X. F., Banerjee, P., Brautigan, D. L., Rapp, U. R., and Avruch, J. (1992) Raf-1 activates MAP kinase-kinase. Nature 358, 417-421
32. Wellbrock, C., Karasarides, M., and Marais, R. (2004) The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5, 875-885
33. Downward, J. (2003) Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22
34. Dogan, T., Harms, G. S., Hekman, M., Karreman, C., Oberoi, T. K., Alnemri, E. S., Rapp, U. R., and Rajalingam, K. (2008) X-linked and cellular IAPs modulate the stability of C-RAF kinase and cell motility. Nat. Cell Biol. 10, 1447-1455
35. Oberoi, T. K., Dogan, T., Hocking, J. C., Scholz, R. P., Mooz, J., Anderson, C. L., Karreman, C., Meyer zu Heringdorf, D., Schmidt, G., Ruonala, M., Namikawa, K., Harms, G. S., Carpy, A., Macek, B., Köster, R. W., and Rajalingam, K. (2012) IAPs regulate the plasticity of cell migration by directly targeting Rac1 for degradation. EMBO J. 31, 14-28
36. Dumaz, N., Hayward, R., Martin, J., Ogilvie, L., Hedley, D., Curtin, J. A., Bastian, B. C., Springer, C., and Marais, R. (2006) In melanoma, RAS mutations are accompanied by switching signaling from BRAF to CRAF and disrupted cyclic AMP signaling. Cancer Res. 66, 9483-9491
37. Light, Y., Paterson, H., and Marais, R. (2002) 14-3-3 antagonizes Ras-mediated Raf-1 recruitment to the plasma membrane to maintain signaling fidelity. Mol. Cell Biol. 22, 4984-4996
38. Dhillon, A. S., Meikle, S., Yazici, Z., Eulitz, M., and Kolch, W. (2002) Regulation of Raf-1 activation and signalling by dephosphorylation. EMBO J. 21, 64-71
39. Noble, C., Mercer, K., Hussain, J., Carragher, L., Giblett, S., Hayward, R., Patterson, C., Marais, R., and Pritchard, C. A. (2008) CRAF autophosphorylation of serine 621 is required to prevent its proteasome-mediated degradation. Mol. Cell 31, 862-872
40. Rajalingam, K., Sharma, M., Paland, N., Hurwitz, R., Thieck, O., Oswald, M., Machuy, N., and Rudel, T. (2006) IAP-IAP complexes required for apoptosis resistance of C. trachomatis-infected cells. PLoS Pathog. 2, e114
41. Dueber, E. C., Schoeffler, A. J., Lingel, A., Elliott, J. M., Fedorova, A. V., Giannetti, A. M., Zobel, K., Maurer, B., Varfolomeev, E., Wu, P., Wallweber, H. J., Hymowitz, S. G., Deshayes, K., Vucic, D., and Fairbrother, W. J. (2011) Antagonists induce a conformational change in cIAP1 that promotes autoubiquitination. Science 334, 376-380
42. Shin, H., Okada, K., Wilkinson, J. C., Solomon, K. M., Duckett, C. S., Reed, J. C., and Salvesen, G. S. (2003) Identification of ubiquitination sites on the X-linked inhibitor of apoptosis protein. Biochem. J. 373, 965-971
43. Kolch, W. (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837
44. von Kriegsheim, A., Pitt, A., Grindlay, G. J., Kolch, W., and Dhillon, A. S. (2006) Regulation of the Raf-MEK-ERK pathway by protein phosphatase 5. Nat. Cell Biol. 8, 1011-1016
45. Conze, D. B., Albert, L., Ferrick, D. A., Goeddel, D. V., Yeh, W. C., Mak, T., and Ashwell, J. D. (2005) Posttranscriptional down-regulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo. Mol. Cell Biol. 25, 3348-3356
46. Didelot, C., Lanneau, D., Brunet, M., Bouchot, A., Cartier, J., Jacquel, A., Ducoroy, P., Cathelin, S., Decologne, N., Chiosis, G., Dubrez-Daloz, L., Solary, E., and Garrido, C. (2008) Interaction of heat-shock protein 90 beta isoform (HSP90 β) with cellular inhibitor of apoptosis 1 (c-IAP1) is requiredfor cell differentiation. Cell Death Differ. 15, 859-866