Survivin and IAP proteins in cell-death mechanisms

Biochemical Journal

Volumn 430, Issue 2, 2010, Pages 199-205

  Altieri, Dario C ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Cancer therapy; Inhibitor of apoptosis (IAP); Mitochondrion; Nuclear factor B (NF B); Survivin

Indexed keywords

BODY FLUIDS; CELL PROLIFERATION; ONCOLOGY;

CANCER THERAPY; CASPASE INHIBITORS; CELL DIVISIONS; CELL NUMBER; CELL SURVIVAL; CELL-FATE; CELLULAR ADAPTATION; CELLULAR RESPONSE; COMPLEX SIGNALLING; GENE FAMILIES; HOMOEOSTASIS; HUMAN DISEASE; IN-CELL; INHIBITOR OF APOPTOSIS; INTRACELLULAR SIGNALLING; NUCLEAR FACTORS; REASONABLE ACCURACY; SURVIVIN;

CELL DEATH;

CASPASE INHIBITOR; INHIBITOR OF APOPTOSIS PROTEIN; SURVIVIN; MICROTUBULE ASSOCIATED PROTEIN;

CELL DEATH; CELL DIVISION; CELL PROTECTION; CELL STRESS; ENZYME INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; ANIMAL; APOPTOSIS; GENETICS; HUMAN; METABOLISM; NEOPLASM; PATHOPHYSIOLOGY;

METAZOA;

ANIMALS; APOPTOSIS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASMS;

EID: 77956680686     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100814     Document Type: Review

References (105)

1. Kerr, J. F., Wyllie, A. H. and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257
2. Meier, P., Finch, A. and Evan, G. I. (2000) Apoptosis in development. Nature 407, 796-801
3. Danial, N. N. and Korsmeyer, S. J. (2004) Cell death: critical control points. Cell 116, 205-219
4. Hanahan, D. and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70
5. Hengartner, M. O. (2000) The biochemistry of apoptosis. Nature 407, 770-776
6. Krammer, P. H. (2000) CD95's deadly mission in the immune system. Nature 407, 789-795
7. Bouchier-Hayes, L., Lartigue, L. and Newmeyer, D. D. (2005) Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest. 115, 2640-2647
8. Green, D. R. and Kroemer, G. (2004) The pathophysiology of mitochondrial cell death. Science 305, 626-629
9. Shi, Y. (2001) A structural view of mitochondria-mediated apoptosis. Nat. Struct. Biol. 8, 394-401
10. Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J. and Green, D. R. (2010) The BCL-2 family reunion. Mol. Cell 37, 299-310
11. Salvesen, G. S. and Duckett, C. S. (2002) Apoptosis: IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 3, 401-410
12. Eckelman, B. P., Salvesen, G. S. and Scott, F. L. (2006) Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 7, 988-994
13. Srinivasula, S. M. and Ashwell, J. D. (2008) IAPs: what's in a name? Mol. Cell 30, 123-135
14. Li, J. and Yuan, J. (2008) Caspases in apoptosis and beyond. Oncogene 27, 6194-6206
15. Verdecia, M. A., Huang, H., Dutil, E., Kaiser, D. A., Hunter, T. and Noel, J. P. (2000) Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat. Struct. Biol. 7, 602-608
16. Engelsma, D., Rodriguez, J. A., Fish, A., Giaccone, G. and Fornerod, M. (2007) Homodimerization antagonizes nuclear export of survivin. Traffic 8, 1495-1502 (Pubitemid 47578356)
17. Bourhis, E., Hymowitz, S. G. and Cochran, A. G. (2007) The mitotic regulator Survivin binds as a monomer to its functional interactor Borealin. J. Biol. Chem. 282, 35018-35023
18. Jeyaprakash, A. A., Klein, U. R., Lindner, D., Ebert, J., Nigg, E. A. and Conti, E. (2007) Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together. Cell 131, 271-285 (Pubitemid 47576137)
19. Pop, C. and Salvesen, G. S. (2009) Human caspases: activation, specificity, and regulation. J. Biol. Chem. 284, 21777-21781
20. Liu, Z., Sun, C., Olejniczak, E. T., Meadows, R. P., Betz, S. F., Oost, T., Herrmann, J., Wu, J. C. and Fesik, S. W. (2000) Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 408, 1004-1008
21. Lin, S. C., Huang, Y., Lo, Y. C., Lu, M. and Wu, H. (2007) Crystal structure of the BIR1 domain of XIAP in two crystal forms. J. Mol. Biol. 372, 847-854
22. Lu, M., Lin, S. C., Huang, Y., Kang, Y. J., Rich, R., Lo, Y. C., Myszka, D., Han, J. and Wu, H. (2007) XIAP induces NF-κB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol. Cell 26, 689-702
23. Rothe, M., Pan, M. G., Henzel, W. J., Ayres, T. M. and Goeddel, D. V. (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83, 1243-1252
24. Song, Z., Yao, X. and Wu, M. (2003) Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J. Biol. Chem. 278, 23130-23140
25. Sun, C., Nettesheim, D., Liu, Z. and Olejniczak, E. T. (2005) Solution structure of human survivin and its binding interface with Smac/Diablo. Biochemistry 44, 11-17
26. Deveraux, Q. L. and Reed, J. C. (1999) IAP family proteins-suppressors of apoptosis. Genes Dev. 13, 239-252
27. Clem, R. J. and Miller, L. K. (1994) Control of programmed cell death by the baculovirus genes p35 and IAP. Mol. Cell. Biol. 14, 5212-5222
28. Huang, Y., Park, Y. C., Rich, R. L., Segal, D., Myszka, D. G. and Wu, H. (2001) Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain. Cell 104, 781-790 (Pubitemid 32241027)
29. Chai, J., Shiozaki, E., Srinivasula, S. M., Wu, Q., Datta, P., Alnemri, E. S. and Shi, Y. (2001) Structural basis of caspase-7 inhibition by XIAP. Cell 104, 769-780
30. Riedl, S. J., Renatus, M., Schwarzenbacher, R., Zhou, Q., Sun, C., Fesik, S. W., Liddington, R. C. and Salvesen, G. S. (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104, 791-800 (Pubitemid 32241028)
31. Scott, F. L., Denault, J. B., Riedl, S. J., Shin, H., Renatus, M. and Salvesen, G. S. (2005) XIAP inhibits caspase-3 and -7 using two binding sites: evolutionarily conserved mechanism of IAPs. EMBO J. 24, 645-655 (Pubitemid 40343265)
32. Shiozaki, E. N., Chai, J., Rigotti, D. J., Riedl, S. J., Li, P., Srinivasula, S. M., Alnemri, E. S., Fairman, R. and Shi, Y. (2003) Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell 11, 519-527
33. Wilson, R., Goyal, L., Ditzel, M., Zachariou, A., Baker, D. A., Agapite, J., Steller, H. and Meier, P. (2002) The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 4, 445-450
34. Ditzel, M., Broemer, M., Tenev, T., Bolduc, C., Lee, T. V., Rigbolt, K. T., Elliott, R., Zvelebil, M., Blagoev, B., Bergmann, A. and Meier, P. (2008) Inactivation of effector caspases through nondegradative polyubiquitylation. Mol. Cell 32, 540-553
35. Suzuki, Y., Nakabayashi, Y. and Takahashi, R. (2001) Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc. Natl. Acad. Sci. U.S.A. 98, 8662-8667
36. Schile, A. J., Garcia-Fernandez, M. and Steller, H. (2008) Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev. 22, 2256-2266
37. Dohi, T., Okada, K., Xia, F., Wilford, C. E., Samuel, T., Welsh, K., Marusawa, H., Zou, H., Armstrong, R., Matsuzawa, S. et al. (2004) An IAP-IAP complex inhibits apoptosis. J. Biol. Chem. 279, 34087-34090
38. Dohi, T., Xia, F. and Altieri, D. C. (2007) Compartmentalized phosphorylation of IAP by protein kinase A regulates cytoprotection. Mol. Cell 27, 17-28
39. Pohl, C. and Jentsch, S. (2008) Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832-845
40. Samuel, T., Okada, K., Hyer, M., Welsh, K., Zapata, J. M. and Reed, J. C. (2005) cIAP1 Localizes to the nuclear compartment and modulates the cell cycle. Cancer Res. 65, 210-218
41. Dohi, T., Beltrami, E., Wall, N. R., Plescia, J. and Altieri, D. C. (2004) Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J. Clin. Invest. 114, 1117-1127
42. Mehrotra, S., Languino, L. R., Raskett, C. M., Mercurio, A. M., Dohi, T. and Altieri, D. C. (2010) IAP regulation of metastasis. Cancer Cell 17, 53-64
43. Arora, V., Cheung, H. H., Plenchette, S., Micali, O. C., Liston, P. and Korneluk, R. G. (2007) Degradation of survivin by the XIAP-XAF1 complex. J. Biol. Chem. 282, 26202-26209
44. Ceballos-Cancino, G., Espinosa, M., Maldonado, V. and Melendez-Zajgla, J. (2007) Regulation of mitochondrial Smac/DIABLO-selective release by survivin. Oncogene 26, 7569-7575 (Pubitemid 350207708)
45. McNeish, I. A., Lopes, R., Bell, S. J., McKay, T. R., Fernandez, M., Lockley, M., Wheatley, S. P. and Lemoine, N. R. (2005) Survivin interacts with Smac/DIABLO in ovarian carcinoma cells but is redundant in Smac-mediated apoptosis. Exp. Cell Res. 302, 69-82
46. Altieri, D. C. (2003) Validating survivin as a cancer therapeutic target. Nat. Rev. Cancer 3, 46-54
47. Li, F., Ambrosini, G., Chu, E. Y., Plescia, J., Tognin, S., Marchisio, P. C. and Altieri, D. C. (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396, 580-584.
48. Altieri, D. C. (2006) The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr. Opin. Cell Biol. 18, 609-615
49. Lens, S. M., Vader, G. and Medema, R. H. (2006) The case for Survivin as mitotic regulator. Curr. Opin. Cell Biol. 18, 616-622
50. Uren, A. G., Wong, L., Pakusch, M., Fowler, K. J., Burrows, F. J., Vaux, D. L. and Choo, K. H. (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol. 10, 1319-1328.
51. Okada, H. and Mak, T. W. (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer 4, 592-603
52. Gurbuxani, S., Xu, Y., Keerthivasan, G., Wickrema, A. and Crispino, J. D. (2005) Differential requirements for survivin in hematopoietic cell development. Proc. Natl. Acad. Sci. U.S.A. 102, 11480-11485
53. Fraser, A. G., James, C., Evan, G. I. and Hengartner, M. O. (1999) Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr. Biol. 9, 292-301
54. Speliotes, E. K., Uren, A., Vaux, D. and Horvitz, H. R. (2000) The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. Mol. Cell 6, 211-223.
55. Huang, H. K., Bailis, J. M., Leverson, J. D., Gomez, E. B., Forsburg, S. L. and Hunter, T. (2005) Suppressors of Bir1p (Survivin) identify roles for the chromosomal passenger protein Pic1p (INCENP) and the replication initiation factor Psf2p in chromosome segregation. Mol. Cell. Biol. 25, 9000-9015
56. Ruchaud, S., Carmena, M. and Earnshaw, W. C. (2007) The chromosomal passenger complex: one for all and all for one. Cell 131, 230-231
57. Giodini, A., Kallio, M. J., Wall, N. R., Gorbsky, G. J., Tognin, S., Marchisio, P. C., Symons, M. and Altieri, D. C. (2002) Regulation of microtubule stability and mitotic progression by survivin. Cancer Res. 62, 2462-2467
58. Rosa, J., Canovas, P., Islam, A., Altieri, D. C. and Doxsey, S. J. (2006) Survivin modulates microtubule dynamics and nucleation throughout the cell cycle. Mol. Biol. Cell 17, 1483-1493
59. Vong, Q. P., Cao, K., Li, H. Y., Iglesias, P. A. and Zheng, Y. (2005) Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 310, 1499-1504
60. cdc2 phosphorylation of survivin. Proc. Natl. Acad. Sci. U.S.A. 97, 13103-13107.
61. Barrett, R. M., Osborne, T. P. and Wheatley, S. P. (2009) Phosphorylation of survivin at threonine 34 inhibits its mitotic function and enhances its cytoprotective activity. Cell Cycle 8, 278-283
62. Wheatley, S. P., Barrett, R. M., Andrews, P. D., Medema, R. H., Morley, S. J., Swedlow, J. R. and Lens, S. M. (2007) Phosphorylation by Aurora-B negatively regulates survivin function during mitosis. Cell Cycle 6, 1220-1230
63. Wheatley, S. P., Henzing, A. J., Dodson, H., Khaled, W. and Earnshaw, W. C. (2004) Aurora-B phosphorylation in vitro identifies a residue of survivin that is essential for its localization and binding to inner centromere protein (INCENP) in vivo. J. Biol. Chem. 279, 5655-5660
64. Colnaghi, R. and Wheatley, S. P. (2010) Liaisons between survivin and PLK1 during cell division and cell death. J. Biol. Chem. 285, 22592-22604
65. Fortugno, P., Beltrami, E., Plescia, J., Fontana, J., Pradhan, D., Marchisio, P. C., Sessa, W. C. and Altieri, D. C. (2003) Regulation of survivin function by Hsp90. Proc. Natl. Acad. Sci. U.S.A. 100, 13791-13796
66. Ghosh, J. C., Dohi, T., Kang, B. H. and Altieri, D. C. (2008) Hsp60 regulation of tumor cell apoptosis. J. Biol. Chem. 283, 5188-5194
67. Kang, B. H. and Altieri, D. C. (2006) Regulation of survivin stability by the aryl hydrocarbon receptor-interacting protein. J. Biol. Chem. 281, 24721-24727
68. Yano, M., Terada, K. and Mori, M. (2003) AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins. J. Cell Biol. 163, 45-56 (Pubitemid 37271433)
69. Young, J. C., Hoogenraad, N. J. and Hartl, F. U. (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50
70. Lewis, J., Burstein, E., Reffey, S. B., Bratton, S. B., Roberts, A. B. and Duckett, C. S. (2004) Uncoupling of the signaling and caspase-inhibitory properties of X-linked inhibitor of apoptosis. J. Biol. Chem. 279, 9023-9029
71. Sanna, M. G., Duckett, C. S., Richter, B. W., Thompson, C. B. and Ulevitch, R. J. (1998) Selective activation of JNK1 is necessary for the anti-apoptotic activity of hILP. Proc. Natl. Acad. Sci. U.S.A. 95, 6015-6020
72. O'Riordan, M. X., Bauler, L. D., Scott, F. L. and Duckett, C. S. (2008) Inhibitor of apoptosis proteins in eukaryotic evolution and development: a model of thematic conservation. Dev. Cell 15, 497-508
73. Bianchi, K. and Meier, P. (2009) A tangled web of ubiquitin chains: breaking news in TNF-R1 signaling. Mol. Cell 36, 736-742
74. Karin, M. and Greten, F. R. (2005) NF-κB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5, 749-759
75. Perkins, N. D. (2007) Integrating cell-signalling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8, 49-62
76. Leulier, F., Lhocine, N., Lemaitre, B. and Meier, P. (2006) The Drosophila inhibitor of apoptosis protein DIAP2 functions in innate immunity and is essential to resist Gram-negative bacterial infection. Mol. Cell. Biol. 26, 7821-7831
77. Jin, H. S., Lee, D. H., Kim, D. H., Chung, J. H., Lee, S. J. and Lee, T. H. (2009) cIAP1, cIAP2, and XIAP act cooperatively via nonredundant pathways to regulate genotoxic stress-induced nuclear factor-κB activation. Cancer Res. 69, 1782-1791
78. Guha, M., Xia, F., Raskett, C. M. and Altieri, D. C. (2010) Caspase 2-mediated tumor suppression involves survivin gene silencing. Oncogene 29, 1280-1292
79. Baud, V. and Karin, M. (2009) Is NF-κB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discovery 8, 33-40
80. Grivennikov, S. I., Greten, F. R. and Karin, M. (2010) Immunity, inflammation, and cancer. Cell 140, 883-899
81. Bertrand, M. J., Milutinovic, S., Dickson, K. M., Ho, W. C., Boudreault, A., Durkin, J., Gillard, J. W., Jaquith, J. B., Morris, S. J. and Barker, P. A. (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700
82. Varfolomeev, E., Goncharov, T., Fedorova, A. V., Dynek, J. N., Zobel, K., Deshayes, K., Fairbrother, W. J. and Vucic, D. (2008) c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor α (TNFα)-induced NF-κB activation. J. Biol. Chem. 283, 24295-24299
83. Mahoney, D. J., Cheung, H. H., Mrad, R. L., Plenchette, S., Simard, C., Enwere, E., Arora, V., Mak, T. W., Lacasse, E. C., Waring, J. and Korneluk, R. G. (2008) Both cIAP1 and cIAP2 regulate TNFα-mediated NF-κB activation. Proc. Natl. Acad. Sci. U.S.A. 105, 11778-11783
84. Wang, L., Du, F. and Wang, X. (2008) TNF-α induces two distinct caspase-8 activation pathways. Cell 133, 693-703
85. Wu, G., Chai, J., Suber, T. L., Wu, J. W., Du, C., Wang, X. and Shi, Y. (2000) Structural basis of IAP recognition by Smac/DIABLO. Nature 408, 1008-1012
86. Varfolomeev, E., Blankenship, J. W., Wayson, S. M., Fedorova, A. V., Kayagaki, N., Garg, P., Zobel, K., Dynek, J. N., Elliott, L. O., Wallweber, H. J. et al. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681
87. Vince, J. E., Wong, W. W., Khan, N., Feltham, R., Chau, D., Ahmed, A. U., Benetatos, C. A., Chunduru, S. K., Condon, S. M., McKinlay, M. et al. (2007) IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693
88. Zarnegar, B. J., Wang, Y., Mahoney, D. J., Dempsey, P. W., Cheung, H. H., He, J., Shiba, T., Yang, X., Yeh, W. C., Mak, T. W. et al. (2008) Noncanonical NF-κB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat. Immunol. 9, 1371-1378
89. Petersen, S. L., Wang, L., Yalcin-Chin, A., Li, L., Peyton, M., Minna, J., Harran, P. and Wang, X. (2007) Autocrine TNFα signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12, 445-456 (Pubitemid 350064365)
90. Bown, N. (2001) Neuroblastoma tumour genetics: clinical and biological aspects. J Clin Pathol. 54, 897-910 (Pubitemid 34032883)
91. Ma, O., Cai, W. W., Zender, L., Dayaram, T., Shen, J., Herron, A. J., Lowe, S. W., Man, T. K., Lau, C. C. and Donehower, L. A. (2009) MMP13, Birc2 (cIAP1), and Birc3 (cIAP2), amplified on chromosome 9, collaborate with p53 deficiency in mouse osteosarcoma progression. Cancer Res. 69, 2559-2567
92. Guha, M. and Altieri, D. C. (2009) Survivin as a global target of intrinsic tumor suppression networks. Cell Cycle 8, 2708-2710
93. Vaira, V., Lee, C. W., Goel, H. L., Bosari, S., Languino, L. R. and Altieri, D. C. (2007) Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene 26, 2678-2684
94. Nguyen, H. G. and Ravid, K. (2006) Tetraploidy/aneuploidy and stem cells in cancer promotion: the role of chromosome passenger proteins. J. Cell. Physiol. 208, 12-22
95. Vogel, C., Hager, C. and Bastians, H. (2007) Mechanisms of mitotic cell death induced by chemotherapy-mediated G2 checkpoint abrogation. Cancer Res. 67, 339-345 (Pubitemid 46142793)
96. Lu, J., Tan, M., Huang, W. C., Li, P., Guo, H., Tseng, L. M., Su, X. H., Yang, W. T., Treekitkarnmongkol, W., Andreeff, M. et al. (2009) Mitotic deregulation by survivin in ErbB2-overexpressing breast cancer cells contributes to Taxol resistance. Clin. Cancer Res. 15, 1326-1334
97. Goga, A., Yang, D., Tward, A. D., Morgan, D. O. and Bishop, J. M. (2007) Inhibition of CDK1 as a potential therapy for tumors over-expressing MYC. Nat. Med. 13, 820-827
98. Whitesell, L. and Lindquist, S. L. (2005) HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5, 761-772
99. Kang, B. H., Plescia, J., Dohi, T., Rosa, J., Doxsey, S. J. and Altieri, D. C. (2007) Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 131, 257-270
100. Xia, F. and Altieri, D. C. (2006) Mitosis-independent survivin gene expression in vivo and regulation by p53. Cancer Res. 66, 3392-3395
101. Li, F., Cheng, Q., Ling, X., Stablewski, A., Tang, L., Foster, B. A., Johnson, C. S., Rustum, Y. M. and Porter, C. W. (2010) Generation of a novel transgenic mouse model for bioluminescent monitoring of survivin gene activity in vivo at various pathophysiological processes: survivin expression overlaps with stem cell markers. Am. J. Pathol. 176, 1629-1638
102. Keats, J. J., Fonseca, R., Chesi, M., Schop, R., Baker, A., Chng, W. J., Van Wier, S., Tiedemann, R., Shi, C. X., Sebag, M. et al. (2007) Promiscuous mutations activate the noncanonical NF-κB pathway in multiple myeloma. Cancer Cell 12, 131-144
103. Wharry, C. E., Haines, K. M., Carroll, R. G. and May, M. J. (2009) Constitutive non-canonical NFκB signaling in pancreatic cancer cells. Cancer Biol. Ther. 8, 1567-1576
104. Altieri, D. C. (2008) Survivin, cancer networks and pathway-directed drug discovery. Nat. Rev. Cancer 8, 61-70
105. LaCasse, E. C., Mahoney, D. J., Cheung, H. H., Plenchette, S., Baird, S. and Korneluk, R. G. (2008) IAP-targeted therapies for cancer. Oncogene 27, 6252-6275