Targeting survivin in cancer therapy: Pre-clinical studies

Apoptosome: An Up-and-coming Therapeutical Tool

Volumn 9789048134151, Issue , 2010, Pages 147-168

  Pennati, Marzia ^a   Folini, Marco ^a   Zaffaroni, Nadia ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Apoptosis; Cell cycle; Human cancers; Inhibitors of apoptosis proteins; Survivin

Indexed keywords

EID: 80052476181     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-90-481-3415-1_8     Document Type: Chapter

References (128)

1. Adida, C., Crotty, P. L., McGrath, J., Berrei, D., Diebold, J., and Altieri, D. C. (1998). Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am J Pathol 152, 43-49.
2. Ai, Z., Yin, L., Zhou, X., Zhu, Y., Zhu, D., Yu, Y., and Feng, Y. (2006). Inhibition of survivin reduces cell proliferation and induces apoptosis in human endometrial cancer. Cancer 107, 746-756.
3. Altieri, D C. (2006). The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr Opin Cell Biol 18, 1-7.
4. Altieri, D. C. (2008). New wirings in the survivin networks. Oncogene 27, 6276-6284.
5. Ambrosini, G., Adida, C., and Altieri, D. C. (1997). A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3, 917-921.
6. Andersen, M. H. and Thor, S. P. (2002). Survivin-a universal tumor antigen. Histol Histopathol 17, 669-675.
7. Ansell, S. M., Arendt, B. K., Grote, D. M., Jelinek, D. F., Novak, A. J., Wellik, L. E., Remstein, E. D., Bennett, C. F., and Fielding, A. (2004). Inhibition of survivin expression suppresses the growth of aggressive non-Hodgkin's lymphoma. Leukemia 18, 616-623.
8. Asanuma, K., Moriai, R., and Yajima, T. (2000). Survivin as a radio-resistance factor in pancreatic cancer. Jap J Cancer Res 91, 1204-1209.
9. Beltrami, E., Plescia, J., Wilkinson, J. C., Duckett, C. S., and Altieri, D. C. (2004). Acute ablation of survivin uncovers p53-dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J Biol Chem 279, 2077-2084.
10. Caldas, H., Honsey, L. E., and Altura, R. A. (2005a). Survivin 2alpha: a novel Survivin splice variant expressed in human malignancies. Mol Cancer 4, 11.
11. Caldas, H., Jiang, Y., Holloway, M. P., Fangusaro, J., Mahotka, C., Conway, E. M., and Altura, R. A. (2005b). Survivin splice variants regulate the balance between proliferation and cell death. Oncogene 24, 1994-2007.
12. Cao, C., Mu, Y., Hallahan, D. E., and Lu, B. (2004). XIAP and survivin as therapeutic targets for radiation sensitization in preclinical models of lung cancer. Oncogene 23, 7047-7052.
13. Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W. C., and Wheatley, S. P. (2003). Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116, 2987-2998.
14. Chang, C. C., Heller, J. D., Kuo, J., and Huang, R. C. (2004). Tetra-O-methyl nordihydrogua-iaretic acid induces growth arrest and cellular apoptosis by inhibiting Cdc2 and survivin expression. Proc Natl Acad Sci USA 101, 13239-13244.
15. Choi, K. S., Lee, T. H., and Jung, M. H. (2003). Ribozyme-mediated cleavage of the human survivin mRNA and inhibition of antiapoptotica function of survivin in MCF-7 cells. Cancer Gene Ther 10, 87-95.
16. Coma, S., Noe, V., Lavarino, C., Adán, J., Rivas, M., López-Matas, M., Pagan, R., Mitjans, F., Vilaró, S., Piulats, J., and Ciudad, C. J. (2004). Use of siRNAs and antisense oligonucleotides against survivin RNA to inhibit steps leading to tumor angiogenesis. Oligonucleotides 14, 100-103.
17. Dohi, T., Beltrami, E., Wall, N. R., Plescia, J., and Altieri, D. C. (2004a). Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 114, 1117-1127.
18. Dohi, T., Okada, K., Xia, F., Wilford, C. E., Samuel, T., Welsh, K., Marusawa, H., Zou, H., Armstrong, R., Matsuzawa, S., Salvesen, G. S., Reed, J. C., and Altieri, D. C. (2004b). An IAP-IAP complex inhibits apoptosis. J Biol Chem 279, 34087-34090.
19. Du, Z. X., Zhang, H. Y., Gaoda, X., Wang, H. Q., Li, Y. J., and Liu, G. L. (2006). Antisurvivin oligonucleotides inhibit growth and induce apoptosis in human medullary thyroid carcinoma cells. Exp Mol Med 38, 230-240.
20. Duffy, M. J., O'Donovan, N., Brennan, D. J., Gallagher, W. M., and Ryan, B. M. (2007) Survivin: a promising tumor biomarker. Cancer Lett 249, 49-60.
21. 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 reports 7, 988-994.
22. Endoh, T., Tsuji, N., Asanuma, K., Yagihashi, A., and Watanabe, N. (2005). Survivin enhances telomerase activity via up-regulation of specificity protein 1- and c-Myc-mediated human telomerase reverse transcriptase gene transcription. Exp Cell Res 305, 300-311.
23. Engelsma, D., Rodriguez, J. A., Fish, A., Giaccone, G., and Fornerod, M. (2007). Homodimerization antagonizes nuclear export of survivin. Traffic 8, 1495-1502.
24. Fodde, R. and Brabletz, T. (2007). Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19, 150-158.
25. 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 USA 100, 13791-13796.
26. Fuessel, S., Kueppers, B., Ning, S., Kotzsch, M., Kraemer, K., Schmidt, U., Meye, A., and Wirth, M. P. (2004). Systematic in vitro evaluation of survivin directed antisense oligodeoxynucle-otides in bladder cancer cells. J Urol 171, 2471-2476.
27. Fukuda, S. and Pelus, L. M. (2002). Elevation of survivin levels by hematopoietic growth factors occurs in quiescent CD34 (+) hematopoietic stem and progenitor cells before cell cycle entry. Cell Cycle 1, 322-326.
28. Fukuda, S. and Pelus, L. M. (2004). Activated H-Ras regulates hematopoietic cell survival by modulating Survivin. Biochem Biophys Res Commun 323, 636-644.
29. Fukuda, S. and Pelus, L. M. (2006). Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 5, 1087-1098.
30. Gassmann, R., Carvalho, A., Henzing, A. J., Ruchaud, S., Hudson, D. F., Honda, R., Nigg, E. A., Gerloff, D. L., and Earnshaw, W. C. (2004). Borealin: a novel chromosomal passenger requied for stability of the bipolar mitotic spindle. J Cell Biol 166, 179-191.
31. Giodini, A., Kallio, M. J., Wall, N. R., Gorbsky, G. J., Tognin, S., Marchisio, P. C., and Altieri, D. C. (2002). Regulation of microtubule stability and mitotic progression by survivin. Cancer Res 62, 2462-2467.
32. Gritsko, T., Williams, A., Turkson, J., Kaneko, S., Bowman, T., Huang, M., Nam, S., Eweis, I., Diaz, N., Sullivan, D., Yoder, S., Enkemann, S., Eschrich, S., Lee, J. H., Beam, C. A., Cheng, J., Minton, S., Muro-Cacho, C. A., and Jove, R. (2006). Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin Cancer Res 12, 11-19.
33. Grossman, D., Mcniff, J. M., Li, F., and Altieri, D. C. (1999). Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma. J Invest Dermatol 113, 1076-1081.
34. Grossman, D., Kim, P. J., Schechner, J. S., and Altieri, D. C. (2001). Inhibition of melanoma tumor growth in vivo by survivin targeting. Proc Natl Acad Sci USA 98, 635-640.
35. Gyurkocza, B., Plescia, J., Raskett, C. M., Garlick, D. S., Lowry, P. A., Carter, B. Z., Andreedd, M., Meli, M., Colombo, G., and Altieri, D. C. (2006). Antileukemic activity of shepherdin and molecular diversity of Hsp90 inhibitors. J Natl Cancer Inst 98, 1068-1077.
36. Hansen, J. B., Fisker, N., Westergaard, M., Kjaerulff, L. S., Hansen, H. F., Thrue, C. A., Rosenbohm, C., Wissenbach, M., Orum, H., and Koch, T. (2008). SPC3042: a proapoptotic survivin inhibitor. Mol Cancer Ther 7, 2736-2745.
37. Hinds, M. G., Norton, R. S., Vaux, D. L., and Day, C. L. (1999). Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat. Nat Struct Biol 6, 648-651.
38. Hoffman, W. H., Biade, S., Zilfou, J. T., Chen, J., and Murphy, M. (2002). Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem 277, 3247-3257.
39. Honda, R., Korner, R., and Nigg, E. A. (2004). Exploring the functional interactions between aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14, 3325-3341.
40. Huang, R. C., Chang, C. C., and Mold, D. (2006). Survivin-dependent and -independent pathways and the induction of cancer cell death by tetra-O-methyl nordihydroguaiaretic acid. Semin Oncol 33, 479-485.
41. Hunter, A. M., Lacasse, E. C., and Korneluk, R. G. (2007). The inhibitor of apoptosis (IAPs) as cancer targets. Apoptosis 12, 1543-1568.
42. Iwasa, T., Okamoto, I., Suzuki, M., Nakahara, T., Yamanaka, K., Hatashita, E., Yamada, Y., Fukuoka, M., Ono, K., Nakagawa, K. (2008). Radiosensitizing effect of YM155, a novel small-molecule survivin suppressant, in non-small cell lung cancer cell lines. Clin Cancer Res 14, 6496-6504.
43. Jiang, Y., Saavedra, H. I., Holloway, M. P., Leone, G., and Altura, R. A. (2004). Aberrant regulation of survivin by the RB/E2F family of proteins. J Biol Chem 279, 40511-40520.
44. Jiang, G., Li, J., Zeng, Z., and Xian, L. (2006). Lentivirus-mediated gene therapy by suppressing sur-vivin in BALB/c nude mice bearing oral squamous cell carcinoma. Cancer Biol Ther 5, 435-440.
45. Kappler, M., Rot, S., Taubert, H., Greither, T., Bartel, F., Dellas, K., Hänsgen, G., Trott, K. R., and Bache, M. (2007). The effects of knockdown of wild-type survivin, survivin-2B or survivin-Delta3 on the radiosensitization in a soft tissue sarcoma cells in vitro under different oxygen conditions. Cancer Gene Ther 14, 994-1001.
46. Kim, P. J., Plescia, J., Clevers, H., Fearon, E. R., and Altieri, D. C. (2003). Survivin and molecular pathogenesis of colorectal cancer. Lancet 362, 205-209.
47. Knauer, S. K., Bier, C., Schlag, P., Fritzmann, J., Dietmaier, W., Rödel, F., Klein-Hitpass, L., Kovács, A. F., Döring, C., Hansmann, M. L., Hofmann, W. K., Kunkel, M., Brochhausen, C., Engels, K., Lippert, B. M., Mann, W., and Stauber, R. H. (2007). The survivin isoform survivin-3B is cytoprotective and can function as a chromosomal passenger complex protein. Cell Cycle 6, 1502-1509.
48. Lee, C. W., Raskett, C. M., Prudovsky, I., and Altieri, D. C. (2008). Molecular dependence of estrogen receptor-negative breast cancer on a Notch-survivin signaling axis. Cancer Res 68, 5273-5281.
49. Lens, S. M., Wolthuis, R. M., Klompmaker, R., Kauw, J., Agami, R., Brummelkamp, T., Kops, G., and Medema, R. H. (2003). Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J 22, 2934-2947.
50. Lens, S. M., Vader, G., and Medema, R. H. (2006). The case for Survivin as mitotic regulator. Curr Opin Cell Biol 18, 616-622.
51. Li, F. (2005). Role of survivin and its splice variants in tumorigenesis. Br J Cancer 92, 212-216.
52. Li, F. and Altieri, D. C. (1999). The cancer antiapoptosis mouse survivin gene: characterization of locus and transcriptional requirements of basal and cell cycle-dependent expression. Cancer Res 59, 3143-3151.
53. Li, F. and Ling, X. (2006). Survivin study: an update of "what is the next wave"? J Cell Physiol 208, 476-486.
54. 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.
55. Li, Q. X., Zhao, J., Liu, J. Y., Jia, L. T., Huang, H. Y., Xu, Y. M., Zhang, Y., Zhang, R., Wang, C. J., Yao, L. B., Chen, S. Y., and Yang, A. G. (2006). Survivin stable knockdown by siRNA inhibits tumor cell growth and angiogenesis in breast and cervical cancers. Cancer Biol Ther 5, 860-866.
56. Ling, X., Bernacki, R. J., Brattain, M. G., and Li, F. (2004). Induction of survivin expression by taxol (paclitaxel) is an early event, which is independent of taxol-mediated G2/M arrest. J Biol Chem 279, 15196-15203.
57. Ling, X., Cheng, Q., Black, J. D., and Li, F. (2007). Forced Expression of Survivin-2B Abrogates Mitotic Cells and Induces Mitochondria-dependent Apoptosis by Blockade of Tubulin Polymerization and Modulation of Bcl-2, Bax, and Survivin. J Biol Chem 282, 27204-27214.
58. Liu, H., Guo, S., Roll, R., Li, J., Diao, Z., Shao, N., Riley, M. R., Cole, A. M., Robinson, J. P., Snead, N. M., Shen, G., and Guo, P. (2007). Phi29 pRNA vector for efficient escort of hammerhead ribozyme targeting survivin in multiple cancer cells. Cancer Biol Ther 6, 697-704.
59. Liu, W. S., Yan, H. J., Qin, R. Y., Tian, R., Wang, M., Jiang, J. X., Shen, M., and Shi, C. J. (2008). siRNA Directed Against Survivin Enhances Pancreatic Cancer Cell Gemcitabine Chemosensitivity. Dig Dis Sci, 54, 89-96.
60. Marconi, A., Dallaglio, K., Lotti, R., Vaschieri, C., Truzzi, F., Fantini, F., and Pincelli, C. (2007). Survivin identifies keratinocyte stemcells and it is down-regulated by anti-{beta}1 integrin during anoikis. Stem Cells 25, 149-155.
61. Marusawa, H., Matsuzawa, S., Welsh, K., Zou, H., Armstrong, R., Tamm, I., and Reed, J. C. (2003). HBXIP functions as a cofactor of survivin in apoptosis suppression. EMBO J 22, 2729-2740.
62. Meli, M., Pennati, M., Curto, M., Daidone, M. G., Plescia, J., Toba, S., Altieri, D. C., Zaffaroni, N., and Colombo, G. (2006). Small-molecule targeting of heat shock protein 90 chaperone function: rational identification of a new anticancer lead. J Med Chem 49, 7721-7730.
63. Mesri, M., Wall, N. R., Li, J., Kim, R. W., and Altieri, D. C. (2001). Cancer gene therapy using a survivin mutant adneovirus. J Clin Invest 108, 981-990.
64. Mita, M. M., Mita, A. C., and Tolcher, A. W. (2006). Apoptosis: mechanism and implications for cancer therapeutics. Targ Oncol 1, 197-214.
65. Mitsiades, C. S., Mitsiades, N., Poulaki, V., Schlossman, R., Akiyama, M., Chauhan, D., Hideshima, T., Treon, S. P., Munshi, N. C., Richardson, P. G., and Anderson, K. C. (2002). Activation of NF-kB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 21, 5673-5683.
66. Moriai, R., Tsuji, N., Moriai, M., Kobayashi, D., and Watanabe, N. (2008). Survivin plays as a resistant factor against tamoxifen-induced apoptosis in human breast cancer cells. Breast Cancer Res Treat, 117, 261-271.
67. Muchmore, S. W., Chen, J., Jakob, C., Zakula, D., Matayoshi, E. D., Wu, W., Zhang, H., Li, F., Ng, S. C., and Altieri, D. C. (2000). Crystal structure and mutagenic analysis of the inhibitor-of-apoptosis protein survivin. Mol. Cell 6, 173-182.
68. Nakagawa, K., Satoh, T., Okamoto, I., Miyazaki, M., Morinaga, R., Tsuya, A., Hasegawa, Y., Terashima, M., Ueda, S., and Fukuoka, M. (2007). Phase I study of YM155, a new first-in-class survivin suppressant, in patient with advanced solid tumors in Japan. ASCO 25, 18S (abstract 3536).
69. Nakahara, T., Takeuchi, M., Kinoyama, I., Minematsu, T., Shirasuna, K., Matsuhisa, A., Kita, A., Tominaga, F., Yamanaka, K., Kudoh, M., and Sasamata, M. (2007). YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts. Cancer Res 67, 8014-8021.
70. Nakano, K., Hamasaki, K., Ichikawa, T., Arima, K., Eguchi, K., and Ishii, N. (2006). Survivin downregulation by siRNA sensitizes human hepatoma cells to TRAIL-induced apoptosis. Oncol Rep 16, 389-392.
71. Nomura, T., Yamasaki, M., Nomura, Y., and Mimata, H. (2005). Expression of the inhibitors of apoptosis proteins in cisplatin-resistant prostate cancer cells. Oncol Rep 14, 993-997.
72. O'Connor, D. S., Grossmann, D., Plescia, J., Li, F., Zhang, H., Villa, A., Tognin, S., Marchisio, P. C., and Altieri, D. C. (2000). Regulation of apoptosis at cell division by p34cdc2 phosphoryla-tion of surviving. Proc Natl Acad Sci 97, 13103-13107.
73. O'Connor, D. S., Wall, N. R., Porter, A. C., and Altieri, D. C. (2002). A p34 (cdc2) survival checkpoint in cancer. Cancer Cell 2, 43-54.
74. Okada, H., Bakal, C., Shahinian, A., Elia, A., Wakeham, A., Suh, W. K., Duncan, G. S., Ciofani, M., Rottapel, R., Zúñiga-Pflücker, J. C., and Mak, T. W. (2004). Survivin loss in thymocytes triggers p53-mediated growth arrest and p53-independent cell death. J Exp Med 199, 399-410.
75. Otto, K., Andersen, M. H., Eggert, A., Keikavoussi, P., Pedersen, L. O., Rath, J. C., Bock, M., Brocker, E. B., Straten, P. T., Kampgen, E., and Becker, J. C. (2005). Lack of toxicity of therapy-induced T cell responses against the universal tumour antigen survivin. Vaccine 23, 884-889.
76. Paduano, F., Villa, R., Pennati, M., Folini, M., Binda, M., Daidone, M. G., and Zaffaroni, N. (2006). Silencing of survivin gene by small interfering RNAs produces supra-additive growth suppression in combination with 17-allylamino-17-demethoxygeldanamycin in human prostate cancer cells. Mol Cancer Ther 5, 179-186.
77. Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., Baehner, F. L., Walker, M. G., Watson, D., Park, T., Hiller, W., Fisher, E. R., Wickerham, D. L., Bryant, J., and Wolmark, N. (2004). A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351, 2817-2826.
78. Park, R., Chang, C. C., Liang, Y. C., Chung, Y., Henry, R. A., Lin, E., Mold, D. E., and Huang, R. C. (2005). Systemic treatment with tetra-O-methyl nordihydroguaiaretic acid suppresses the growth of human xenograft tumors. Clin Cancer Res 11, 4601-4609.
79. Pennartz, S., Belvindrah, R., Tomiuk, S., Zimmer, C., Hofmann, K., Conradt, M., Bosio, A., and Cremer, H. (2004). Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol Cell Neurosci 25, 692-706.
80. Pennati, M., Colella, G., Folini, M., Citti, L., Daidone, M. G., and Zaffaroni, N. (2002). Ribozyme-mediated attenuation of survivin expression sensitizes human melanoma cells to cisplatin-induced apoptosis. J Clin Invest 109, 285-286.
81. Pennati, M., Binda, M., Colella, G., Folini, M., Citti, L., Villa, R., Daidone, M. G., and Zaffaroni, N. (2003). Radiosensitization of human melanoma cells by ribozyme-mediated inhibition of survivin expression. J Invest Dermatol 120, 648-654.
82. Pennati, M., Binda, M., Colella, G., Zoppe', M., Folini, M., Vignati, S., Valentini, A., Citti, L., De Cesare, M., Pratesi, G., Giacca, M., Daidone, M. G., and Zaffaroni, N. (2004a). Ribozyme-mediated inhibition of survivin expression increases spontaneous and drug-induced apoptosis and decreases the tumorigenic potential of human prostate cancer cells. Oncogene 23, 386-394.
83. Pennati, M., Binda, M., De Cesare, M., Pratesi, G., Folini, M., Citti, L., Daidone, M. G., Zunino, F., and Zaffaroni, N. (2004b). Ribozyme-mediated down-regulation of survivin expression sensitizes human melanoma cells to topotecan in vitro and in vivo. Carcinogenesis 25, 1129-1136.
84. Pennati, M., Campbell, A. J., Curto, M., Binda, M., Cheng, Y., Wang, L. Z., Curtin, N., Golding, B. T., Griffin, R. J., Hardcastle, I. R., Henderson, A., Zaffaroni, N., and Newell, D. R. (2005). Popentiation of paclitaxel-induced apoptosis by the novel cyclin-dependent kinase inhibitor NU6140: a possible role for survivin down-regulation. Mol Cancer Ther 4, 1328-1337.
85. Pennati, M., Folini, M., and Zaffaroni, N. (2007). Targeting survivin in cancer therapy; fulfilled promises and open questions. Carcinogenesis 28, 1133-1139.
86. Plescia, J., Salz, W., Xia, F., Pennati, M., Zaffaroni, N., Daidone. M. G., Meli, M., Dohi, T., Fortugno, P., Nefedova, Y., Gabrilovich, D. I., Colombo, G., and Altieri, D. C. (2005). Rational design of shepherdin, a novel anticancer agent. Cancer Cell 7, 457-468.
87. Reker, S., Meier, A., Holten-Andersen, L., Svane, I. M., Becker, J. C., Straten, P. T., and Andersen, M. H. (2004). Identification of novel survivin-derived CTL epitopes. Cancer Biol Ther 3, 173-179.
88. Rodel, C., Haas, J., Groth, A., Grabenbauer, G. G., Sauer, R., and Rodel, F. (2003). Spontaneous and radiation-induced apoptosis in colorectal carcinoma cells with different intrinsic radiosen-sitivities: survivin as a radioresistance factor. Int J Radiat Oncol Biol Phys 55, 1341-1347.
89. Rodel, F., Hoffmann, J., Distel, L., Herrmann, M., Noistenig, T., Papadopoulos, T., Sauer, R., and Rodel, C. (2005). Survivin as a radioresistance factor, and prognostic and therapeutic target for radiotherapy in rectal cancer. Cancer Res 65, 4881-4887.
90. Rodel, F., Frey, B., Leitmann, W., Capalbo, G., Weiss, C., and Rodel, C. (2008). Survivin antisense oligonucleotides effectively radiosensitize colorectal cancer cells in both tissue culture and murine xenograft models. Int J Radiat Oncol Biol Phys 71, 247-255.
91. Rohayem, J., Diestelkoetter, P., Weigle, B., Oehmichen, A., Schmitz, M., Mehlhorn, J., Conrad, K., and Rieber, E. P. (2000). Antibody response to the tumor-associated inhibitor of apoptosis protein in cancer patients. Cancer Res 60, 1815-1817.
92. Sah, N. K., Munshi, A., Hobbs, M., Carter, B. Z., Andreeff, M., and Meyn, R. E. (2006). Effect of downregulation of survivin expression on radiosensitivity of human epidermoid carcinoma cells. Int J Radiat Oncol Biol Phys 66, 852-859.
93. Sarthy, A. V., Morgan-Lappe, S. E., Zakula, D., Vernetti, L., Schurdak, M., Packer, J. C., Anderson, M. G., Shirasawa, S., Sasazuki, T., and Fesik, S. W. (2007). Survivin depletion preferentially reduces the survival of activated K-Ras-transformed cells. Mol Cancer Ther 6, 269-276.
94. Schmidt, S. M., Schag, K., Muller, M. R., Weck, M. M., Appel, S., Kanz, L., Grunebach, F., and Brossart, P. (2003). Survivin is a shered tumor-associated antigen expressed in a broad variety of malignancies and recognized by specific cytotoxic T cells. Blood 102, 571-576.
95. Schmitz, M., Diestelkoetter, P., Weigle, B., Schmachtenberg, F., Stevanovic, S., Ockert, D., Rammensee, H. G., and Rieber, E. P. (2000). Generation of survivin-specific CD8+ T effector cells by dendritic cells pulsed with protein or selected peptides. Cancer Res 60, 4845-4849.
96. Sharma, H., Sen, S., Lo Muzio, L., Mariggio, A., and Singh, N. (2005). Antisense-mediated down-regulation of anti-apoptotic proteins induces apoptosis and sensitizes head and neck squamous cell carcinoma cells to chemotherapy. Cancer Biol Ther 4, 720-727.
97. Sommer, K. W., Schamberger, C. J., Schmidt, G. E., Sasgary, S., and Cerni, C. (2003). Inhibitor of apoptosis protein (IAP) survivin is up-regulated by oncogenic c-H-Ras. Oncogene 22, 4266-4280.
98. Song, J., So, T., Cheng, M., Tang, X., and Croft, M. (2005). Sustained survivin expression from OX40 costimulatory signals drives T cell clonal expansion. Immunity 22, 621-631.
99. Span, P. N., Tjan-Heijnen, V. C., Manders, P., van Tienoven, D., Lehr, J., and Sweep, F. C. (2006). High survivin predicts a poor response to endocrine therapy but a good response to chemotherapy in advanced breast cancer. Brest Cancer Res Treat 98, 223-230.
100. Sun, C., Cai, M., Gunasekera, A. H., Meadows, R. P., Wang, H., Chen, J., Zhang, H., Wu, W., Xu, N., Ng, S. C., and Fesik, S. W. (1999). NMR structure and mutagenesis of the inhibitor-ofapoptosis protein XIAP. Nature 401, 818-822.
101. Talbot, D. C., Davies, J., Callies, S., Andre, V., Lahn, M., Ang, J., De Bono, J. S., Ranson, M. (2008). First human dose study evaluating safety and pharmacokinetics of LY2181308, an antisense oligonucleotide designed to inhibit survivin. J Clin Oncol 26, abstr 3518.
102. Taubert, H., Würl, P., Greither, T., Kappler, M., Bache, M., Bartel, F., Kehlen, A., Lautenschläger, C., Harris, L. C., Kaushal, D., Füssel, S., Meye, A., Böhnke, A., Schmidt, H., Holzhausen, H. J., Hauptmann, S. (2007). Stemcell-associated genes are extremely poor prognostic factors for soft-tissue sarcoma patients. Oncogene 26, 7170-7174.
103. Tirro, E., Consoli, M. L., Massimino, M., Manzella, L., Frasca, F., Sciacca, L., Vicari, L., Stassi, G., Messina, L., Messina, A., and Vigneri, P. (2006). Altered expression of c-IAP1, survivin, and Smac contributes to chemotherapy resistance in thyroid cancer cells. Cancer Res 66, 4263-4272.
104. Tolcher, A. W., Mita, A., Lewis, L. D., Garrett, C. R., Till, E., Daud, A. I., Patnaik, A., Papadopoulos, K., Takimoto, C., Bartels, P., Keating, A., Antonia, S. (2008). Phase I and pharmacokinetic study of YM155, a small-molecule inhibitor of survivin. J Clin Oncol 26, 5198-5203.
105. Tran, J., Master, Z., Yu, J. L., Rak, J., Dumont, D. J., and Kerbel, R. S. (2002). A role for survivin in chemoresistance of endothelial cells mediated by VEGF. Proc Natl Acad Sci USA 99, 4349-4354.
106. Tsuruma, T., Hata, F., Torigoe, T., Furuhata, T., Idenoue, S., Kurotaki, T., Yamamoto, M., Yagihashi, A., Ohmura, T., Yamaguchi, K., Katsuramaki, T., Yasoshima, T., Sasaki, K., Mizushima, Y., Minamida, H., Kimura, H., Akiyama, M., Hirohashi, Y., Asanuma, H., Tamura, Y., Shimozawa, K., Sato, N., and Hirata, K. (2004). Phase I clinical study of antiapop-tosis protein, survivin-derived peptide vaccine therapy for patients with advanced or recurrent colorectal cancer. J Transl Med 2, 19.
107. Tu, S. P., Cui, J. T., Liston, P., Huajiang, X., Xu, R., Lin, M. C., Zhu, Y. B., Zou, B., Ng, S. S., Jiang, S. H., Xia, H. H., Wong, W. M., Chan, A. O., Yuen, M. F., Lam, S. K., Kung, H. F., and Wong, B. C. (2005). Gene therapy for colon cancer by adeno-associated viral vector-mediated transfer of survivin Cys84Ala mutant. Gastroenterology 128, 361-375.
108. Vagnarelli, P. and Earnshaw, W. C. (2004). Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 113, 211-222.
109. Vaira, V., Lee, C. W., Goel, H. L., Bosari, S., Languino, L. R., and Altieri, D. C. (2006). Regulation of survivin expression by IGF-1/mTOR signalling. Oncogene 26, 1-7.
110. Van Geelen, C. M., De Vries, E. G., and De Jong, S. (2004). Lessons from TRAIL-resistance mechanisms in colorectal cancer cells: paving the road to patient-tailored therapy. Drug Resist Updat 7, 345-358.
111. Vaux, D. L. and Silke, J. (2005). IAPs-the ubiquitin connection. Cell Death Diff 12, 1205-1207.
112. Velculescu, V. E., Madden, S. L., Zhang, L., Lash, A. E., Yu, J., Rago, C., Lal, A., Wang, C. J., Beaudry, G. A., Ciriello, K. M., Cook, B. P., Dufault, M. R., Ferguson, A. T., Gao, Y., He, T. C., Hermeking, H., Hiraldo, S. K., Hwang, P. M., Lopez, M. A., Luderer, H. F., Mathews, B., Petroziello, J. M., Polyak, K., Zawel, L., and Kinzler, K. W. (1999). Analysis of human transcrip-tomes. Nat Gen 23, 387-388.
113. Vogelstein, B. and Kinzler, K. W. (2004). Cancer genes and the pathways they control. Nat Med 10, 789-799.
114. 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.
115. Wheatley, S. P., Carvalho, A., Vagnarelli, P., and Earnshaw, W. C. (2001). INCENP is required for proper targeting of survivin to the centromeres and the anaphase spindle during mitosis. Curr Biol 11, 886-890.
116. 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.
117. Wuttig, D., Kunze, D., Fuessel, S., Toma, M., Stade, J., Kotzsch, M., Kappler, M., Taubert, H., Schwenzer, B., Baretton, G., Hakenberg, O. W., Meye, A., and Wirth, M. P. (2007). Are over-expressed alternative survivin transcripts in human bladder cancer suitable targets for siRNA-mediated in vitro inhibition? ? Int J Oncol 30, 1317-1324.
118. Xia, F. and Altieri, D. C. (2006). Mitosis-independent survivin gene expression in vivo and regulation by p53. Cancer Res 66, 3392-3395.
119. Yan, H., Thomas, J., Liu, T., Raj, D., London, N., Tandeski, T., Leachman, S. A., Lee, R. M., and Grossman, D. (2006). Induction of melanoma cell apoptosis and inhibition of tumor growth using a cell-permeable Survivin antagonist. Oncogene 25, 6968-6974.
120. Yang, D., Welm, A., and Bishop, J. M. (2004). Cell division and cell survival in the absence of survivin. Proc Natl Acad Sci 101, 15100-15105.
121. Yang, H., Fu, J. H., Hu, Y., Huang, W. Z., Zheng, B., Wang, G., Zhang, X., and Wen, J. (2008). Influence of SiRNA targeting survivin on chemosensitivity of H460/cDDP lung cancer cells. J Int Med Res 36, 734-747.
122. Yonesaka, K., Tamura, K., Kurata, T., Satoh, T., Ikeda, M., Fukuoka, M., and Nakagawa, K. (2006). Small interfering RNA targeting survivin sensitizes lung cancer cell with mutant p53 to adriamycin. Int J Cancer 118, 812-820.
123. Zaffaroni, N., Pennati, M., Coltella, G., Perego, P., Supino, R., Gatti, L., Pilotti, S., Zunino, F., and Daidone, M. G. (2002). Expression of the anti-apoptotic gene survivin correlates with taxol resistance in human ovarian cancer. Cell Mol. Life Sci 59, 1406-1412.
124. Zhang, M., Mukherjee, N., Bermudez, R. S., Latham, D. E., Delaney, M. A., Zietman, A. L., Shipley, W. U., and Chakravarti, A. (2005a) Adenovirus-mediated inhibition of survivin expression sensitizes human prostate cancer cells to paclitaxel in vitro and in vivo. Prostate 64, 293-302.
125. Zhang, M., Latham, D. E., Delaney, M. A., and Chakravarti, A. (2005b). Survivin mediates resistance to antiandrogen therapy in prostate cancer. Oncogene 24, 2474-2482.
126. Zhang, R., Wang, T., Li, K. N., Qin, W. W., Chen, R., Wang, K., Jia, L. T., Zhao, J., Wen, W. H., Meng, Y. L., Yao, L. B., and Yang, A. G. (2008). A survivin double point mutant has potent inhibitory effect on the growth of hepatocellular cancer cells. Cancer Biol Ther 7, 547-554.
127. Zhang, T., Otevrel, T, Gao, Z., Ehrlich, S. M., Fields, J. Z., and Boman, B. M. (2001). Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 61, 8664-8667.
128. Zhou, J., O'Brate, A., Zelnak, A., and Giannakakou, P. (2004). Survivin deregulation in beta-tubulin mutant ovarian cancer cells underlies their compromised mitotic response to taxol. Cancer Res 64, 8708-8714.