RNA interference-mediated validation of survivin and Apollon/BRUCE as new therapeutic targets for cancer therapy

Current Topics in Medicinal Chemistry

Volumn 12, Issue 2, 2012, Pages 69-78

  Pennati, Marzia ^a   Millo, Enrico ^b   Gandellini, Paolo ^a   Folini, Marco ^a   Zaffaroni, Nadia ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Apollon BRUCE; Apoptosis; Chemosensitivity; Human tumors; Inhibitors of apoptosis proteins; Radiosensitivity; Survivin

Indexed keywords

CASPASE; CISPLATIN; DEATH RECEPTOR; DOUBLE STRANDED RNA; DOXORUBICIN; DULANERMIN; GEMCITABINE; GENISTEIN; INHIBITOR OF APOPTOSIS PROTEIN; PACLITAXEL; PROTEIN APOLLON; PROTEIN BRUCE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; SURVIVIN; TAMOXIFEN; TANESPIMYCIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VINCRISTINE;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CANCER CELL CULTURE; CANCER GENE THERAPY; CANCER GROWTH; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; DRUG POTENTIATION; GENE TARGETING; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN STRUCTURE; RADIOSENSITIVITY; REVIEW; RNA INTERFERENCE; VALIDATION STUDY;

ANIMALS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MODELS, BIOLOGICAL; NEOPLASMS; RNA INTERFERENCE;

EID: 84855841415     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802612798919169     Document Type: Review

References (88)

1. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer. Cell, 2000, 100, 57-70.
2. Green, D. R.; Evan, G. I. A Matter of life and death. Cancer Cell, 2002, 1, 19-30.
3. Yuan, J. Transducing signals of life and death. Curr. Opin. Cell Biol., 1997, 9, 247-251.
4. Cryns, V; Yuan, Y. Proteases to die for. Genes Develop., 1999, 12, 1551-1570.
5. Billen, L. P; Shamas-Din, A.; Andrews, D. W. Bid: a bax-like BH3 protein. Oncogene, 2008, 27, S93-104.
6. Deveraux, Q.; Reed, J. IAP family proteins: suppressors of apoptosis. Genes Dev., 1999, 13, 239-252.
7. Hunter, A.; LaCasse, E. C.; Korneluk, R. G. The inhibitors of apoptosis (IAPs) as cancer targets. Apoptosis, 2007, 12, 1543-1568.
8. Hinds, M. G.; Norton, R. S.; Vaux, D. L.; Day, C. L. Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat. Nat. Struct. Biol., 1999, 6, 648-651.
9. Sun, C.; Cai, M.; Gunasekera, A. H.; Meadows, R. P.; Wang, H.; Chen, J.; Zhang, H.; Wu, W.; Xu, N.; Ng, S. C.; Fesik, S. W. NMR structure and mutagenesis of the inhibitor-of apoptosis protein XIAP. Nature, 1999, 401, 818-822.
10. Eckelman, B. P.; Salvesen, G. S.; Scott, F. L. Human inhibitor of apoptosis proteins; why XIAP is the black sheep of the family. EMBO Reports, 2006, 7, 988-994.
11. Vaux, D. L.; Silke, J. IAPs-the ubiquitin connection. Cell Death Diff., 2005, 12, 1205-1207.
12. Marusawa, H.; Matsuzawa, S.; Welsh, K.; Zou, H.; Armstrong, R.; Tamm, I.; Reed, J. C. HBXIP functions as a cofactor of survivin in apoptosis suppression. EMBO J., 2003, 22, 2729-2740.
13. Okada, H.; Bakal, C.; Shahinian, A.; Elia, A.; Wakeham, A.; Suh, W. K.; Duncan, G. S.; Ciofani, M.; Rottapel, R.; Zúñiga-Pflücker, J. C.; Mak, T. W. Survivin loss in thymocytes triggers p53-mediated growth arrest and p53-independent cell death. J. Exp. Med., 2004, 199, 399-410.
14. Lotz, K.; Pyrowolakis, G.; Jentsch, S. BRUCE, a giant E2/E3 ubiquitin ligase and inhibitor of apoptosis protein of the trans-golgi network, is required for normal placenta development and mouse survival. Mol. Cell Biol., 2004, 24, 9339-9350.
15. Ambrosini, G.; Adida, C.; Altieri, D. C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med., 1997, 3, 917-921.
16. Muchmore, S. W.; Chen, J.; Jakob, C.; Zakula, D.; Matayoshi, E. D.; Wu, W.; Zhang, H.; Li, F.; Ng, S. C.; Altieri, D. C. Crystal structure and mutagenic analysis of the inhibitor-of-apoptosis protein survivin. Mol. Cell, 2000, 6, 173-182.
17. Yang, D.; Welm, A.; Bishop, J. M. Cell division and cell survival in the absence of survivin. Proc. Natl. Acad. Sci. USA, 2004, 101, 15100-15105.
18. Altieri, D. C. The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr. Opin. Cell. Biol., 2006, 18, 1-7.
19. Vagnarelli, P.; Earnshaw, W. C. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma, 2004, 113, 211-222.
20. Altieri, D. C. Survivin, cancer networks and pathway-directed drug discovery. Nat. Rev. Cancer, 2008, 8, 61-70.
21. Li, F.; Ambrosini, G.; Chu, E. Y.; Plescia, J.; Tognin, S.; Marchisio, P. C.; Altieri, D. C. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature, 1998, 396, 580-584.
22. Li, F.; Altieri, D. C. The cancer antiapoptosis mouse survivin gene: characterization of locus and transcriptional requirements of basal and cell cycle-dependent expression. Cancer Res., 1999, 59, 3143-3151.
23. Xia, F.; Altieri, D. C. Mitosis-independent survivin gene expression in vivo and regulation by p53. Cancer Res., 2006, 66, 3392-3395.
24. 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.; Altieri, D. C. An IAP-IAP complex inhibits apoptosis. J. Biol. Chem., 2004, 279, 34087-34090.
25. Dohi, T.; Beltrami, E.; Wall, N. R.; Plescia, J.; Altieri, D. C. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J. Clin. Invest, 2004, 114, 1117-1127.
26. Fortugno, P.; Beltrami, E.; Plescia, J.; Fontana, J.; Pradhan, D.; Marchisio, P. C.; Sessa, W. C.; Altieri, D. C. Regulation of survivin function by Hsp90. Proc. Natl. Acad. Sci. USA, 2003, 100, 13791-13796.
27. Khan, S.; Aspe, J. R.; Asumen, M. G.; Almaguel, F.; Odumosu, O.; Acevedo-Martinez, S.; De Leon, M.; Langridge, W. H.; Wall, N. R. Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. Br. J. Cancer, 2009, 100, 1073-1086.
28. Khan, S.; Jutzy, J. M.; Aspe, J. R.; McGregor, D. W.; Neidigh, J. W.; Wall, N. R. Survivin is released from cancer cells via exosomes. Apoptosis, 2010, 16(1),1-12
29. Bokarewa, M.; Lindblad, S.; Bokarew, D.; Tarkowski, A. Balance between survivin, a key member of the apoptosis inhibitor family, and its specific antibodies determines erosivity in rheumatoid arthritis. Arthritis Res. Ther., 2005, 7, R349-358.
30. Mera, S.; Magnusson, M.; Tarkowski, A.; Bokarewa, M. Extracellular survivin up-regulates adhesion molecules on the surface of leukocytes changing their reactivity pattern. J. Leukoc. Biol., 2008, 83, 149-55.
31. 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.; Yang, A. G. Survivin stable knockdown by siRNA inhibits tumor cell growth and angiogenesis in breast and cervical cancers. Cancer Biol. Ther., 2006, 5, 860-866.
32. Caldas, H.; Jiang, Y.; Holloway, M. P.; Fangusaro, J.; Mahotka, C.; Conway, E. M.; Altura, R. A. Survivin Splice Variants Regulate the Balance Between Proliferation and Cell Death. Oncogene, 2005, 24, 1994-2007.
33. Caldas, H.; Honsey, L. E.; Altura, R. A. Survivin 2alpha: a novel survivin splice variant expressed in human malignancies. Mol. Cancer, 2005, 4, 11.
34. Pennati, M.; Folini, M.; Zaffaroni, N. Targeting survivin in cancer therapy. Expert Opin. Ther. Targets, 2008, 12, 463-76.
35. Adida, C.; Crotty, P. L.; McGrath, J.; Berrei, D.; Diebold, J.; Altieri, D. C. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am. J. Pathol., 1998, 152, 43-49.
36. Fukuda, S.; Pelus, L. M. Survivin, a cancer target with an emerging role in normal adult tissues. Mol. Cancer Ther., 2006, 5, 1087-1098.
37. Duffy, M. J.; O'Donovan, N.; Brennan, D. J.; Gallagher, W. M.; Ryan, B. M. Survivin: a promising tumor biomarker. Cancer Lett., 2007, 249, 49-60.
38. Giodini, A.; Kallio, M. J.; Wall, N. R.; Gorbsky, G. J.; Tognin, S.; Marchisio, P. C.; Altieri, D. C. Regulation of microtubule stability and mitotic progression by survivin. Cancer Res., 2002, 62, 2462-2467.
39. Zaffaroni, N.; Pennati, M.; Colella, G.; Perego, P.; Supino, R.; Gatti, L.; Pilotti, S.; Zunino, F.; Daidone, M. G. Expression of the anti-apoptotic gene survivin correlates with taxol resistance in human ovarian cancer. Cell. Mol. Life Sci., 2002, 59, 1406-1412.
40. Zhang, M.; Mukherjee, N.; Bermudez, R. S.; Latham, D. E.; Delaney, M. A.; Zietman, A. L.; Shipley, W. U.; Chakravarti, A. Adenovirus-mediated inhibition of survivin expression sensitizes human prostate cancer cells to paclitaxel in Vitro and in Vivo. Prostate, 2005a, 64, 293-302.
41. Nomura, T.; Yamasaki, M.; Nomura, Y.; Mimata, H. Expression of the inhibitors of apoptosis proteins in cisplatin-resistant prostate cancer cells. Oncol. Rep., 2005, 14, 993-997.
42. Tirro, E.; Consoli, M. L.; Massimino, M.; Manzella, L.; Frasca, F.; Sciacca, L.; Vicari, L.; Stassi, G.; Messina, L.; Messina, A.; Vigneri, P. Altered expression of c-IAP1, survivin, and smac contributes to chemotherapy resistance in thyroid cancer cells. Cancer Res., 2006, 66, 4263-4272.
43. Van Geelen, C. M.; De Vries, E. G.; De Jong, S. Lessons from TRAIL-resistance mechanisms in colorectal cancer cells: paving the road to patient-tailored therapy. Drug Resist. Updat, 2004, 7, 345-358.
44. Asanuma, K.; Moriai, R.; Yajima, T. Survivin as a radio-resistance factor in pancreatic cancer. Jap. J. Cancer Res., 2000, 91, 1204-1209.
45. Pennati, M.; Binda, M.; Colella, G.; Folini, M.; Citti, L.; Villa, R.; Daidone, M. G.; Zaffaroni, N. Radiosensitization of human melanoma cells by ribozyme-mediated inhibition of survivin expression. J. Invest. Dermatol., 2003, 120, 648-654.
46. Rodel, C.; Haas, J.; Groth, A.; Grabenbauer, G. G.; Sauer, R.; Rodel, F. Spontaneous and radiation-induced apoptosis in colorectal carcinoma cells with different intrinsic radiosensitivities: survivin as a radioresistance factor. Int. J. Radiat. Oncol. Biol. Phys., 2003, 55, 1341-1347.
47. Zhang, M.; Latham, D. E.; Delaney, M. A.; Chakravarti, A. Survivin mediates resistance to antiandrogen therapy in prostate cancer. Oncogene, 2005, 24, 2474-2482.
48. Paik, S.; Shak, S.; Tang, G.; Baker, J.; Cronin, M.; Baehner, F. L.; Walker, M. G.; Watson, D.; Park, T.; Hiller, W.; Fisher, E. R.; Wickerham, D. L., Bryant, J.; Wolmark, N. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med., 2004, 351, 2817-2826.
49. Folini, M.; Pennati, M.; Zaffaroni, N. RNA interference-mediated validation of genes involved in telomere maintenance and evasion of apoptosis as cancer therapeutic targets. Methods Mol. Biol., 2009, 487, 303-330.
50. Elbashir, S. M.; Harborth, J.; Weber, K.; Tuschl, T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 2002, 26, 199-213.
51. Dykxhoorn, D. M.; Novina, C. D.; Sharp, P. A. Killing the messenger: short RNAs that silence gene expression. Nat. Rev. Mol. Cell. Biol., 2003, 4, 457-467.
52. Izquierdo M. Short interfering RNAs as a tool for cancer gene therapy. Cancer Gene Ther., 2005, 12, 217-227.
53. Martinez, A.; Bellosillo, B.; Bosch, F.; Ferrer, A.; Marce, S.; Villamor, N.; Ott, G.; Montserrat, E.; Campo, E.; Colomer, D. Nuclear survivin expression in mantle cell lymphoma is associated with cell proliferation and survival. Am. J. Pathol., 2004, 164, 501-510.
54. Carvalho, A.; Carmena, M.; Sambade, C.; Earnshaw, W. C.; Wheatley, S. P. Survivin is required for stable checkpoint activation in taxol-treated hela cells. J. Cell. Sci., 2003, 116, 2987-2998.
55. Tsuji, N.; Asanuma, K.; Kobayashi, D.; Yagihashi, A.; Watanabe, N. Introduction of a survivin gene-specific small inhibitory RNA inhibits growth of pancreatic cancer cells. Anticancer Res., 2005, 25, 3967-3972.
56. Ai, Z.; Yin, L.; Zhou, X.; Zhu, Y.; Zhu, D.; Yu, Y.; Feng, Y. Inhibition of survivin reduces cell proliferation and induces apoptosis in human endometrial cancer. Cancer, 2006, 107, 746-756.
57. Congmin, G.; Mu, Z.; Yihui, M.; Hanliang, L. Survivin--an attractive target for RNAi in non-hodgkin's lymphoma, daudi cell line as a model. Leuk. Lymphoma, 2006, 47, 1941-1948.
58. Jiang, G.; Li, J.; Zeng, Z.; Xian, L. Lentivirus-mediated gene therapy by suppressing survivin in BALB/c nude mice bearing oral squamous cell carcinoma. Cancer Biol. Ther., 2006, 5, 435-440.
59. Sarthy, A. V.; Morgan-Lappe, S. E.; Zakula, D.; Vernetti, L.; Schurdak, M.; Packer, J. C.; Anderson, M. G.; Shirasawa, S.; Sasazuki, T.; Fesik, S. W. Survivin depletion preferentially reduces the survival of activated K-ras-Transformed Cells. Mol. Cancer Ther. 2007, 6, 269-276.
60. Yang, H.; Fu, J. H.; Hu, Y.; Huang, W. Z.; Zheng, B.; Wang, G.; Zhang, X.; Wen, J. Influence of siRNA targeting survivin on chemosensitivity of H460/CDDP Lung Cancer Cells. J. Int. Med. Res., 2008, 36, 734-747.
61. Yonesaka, K.; Tamura, K.; Kurata, T.; Satoh, T.; Ikeda, M.; Fukuoka, M.; Nakagawa, K. Small interfering RNA targeting survivin sensitizes lung cancer cell with mutant p53 to adriamycin. Int. J. Cancer, 2006, 118, 812-820.
62. Paduano, F.; Villa, R.; Pennati, M.; Folini, M.; Binda, M.; Daidone, M. G.; Zaffaroni, N. Silencing of survivin gene by small interfering RNAs produces supra-additive growth suppression in combination with 17-allylamino-17-demethoxygeldanamycin in human rostate cancer cells. Mol. Cancer Ther., 2006, 5, 179-186.
63. Moriai, R.; Tsuji, N.; Moriai, M.; Kobayashi, D.; Watanabe, N. Survivin plays as a resistant factor against tamoxifen-induced apoptosis in human breast cancer cells. Breast Cancer Res. Treat., 2009, 117, 261-271.
64. Liu, W. S.; Yan, H. J.; Qin, R. Y.; Tian, R.; Wang, M.; Jiang, J. X.; Shen, M.; Shi, C. J. siRNA directed against survivin enhances pancreatic cancer cell gemcitabine chemosensitivity. Dig. Dis. Sci., 2009, 54, 89-96.
65. Yuan-Jing, F.; Nan-Shan, H.; Lian, X. Genistein synergizes with RNA interference inhibiting survivin for inducing DU-145 of prostate cancer cells to apoptosis. Cancer Lett., 2009, 284, 189-197.
66. Nakano, K.; Hamasaki, K.; Ichikawa, T.; Arima, K.; Eguchi, K.; Ishii, N. Survivin downregulation by siRNA sensitizes human hepatoma cells to TRAIL-induced apoptosis. Oncol. Rep., 2006, 16, 389-392.
67. Lin, Y.; Liu, X.; Yue, P.; Benbrook, D. M.; Berlin, K. D.; Khuri, F. R.; Sun, S. Y. involvement of c-FLIP and survivin down-regulation in flexible heteroarotinoid-induced apoptosis and enhancement of TRAIL-initiated apoptosis in lung cancer cells. Mol. Cancer Ther., 2008, 7, 3556-3565.
68. Kappler, M.; Taubert, H.; Bartel, F.; Blumke, K.; Panian, M.; Schmidt, H.; Dunst, J.; Bache, M. Radiosensitization, after a combined treatment of survivin siRNA and irradiation, is correlated with the activation of caspases 3 and 7 in a wtp53 sarcoma cell line, but not in a mt-p53 sarcoma cell line. Oncol. Rep., 2005, 13, 167-172.
69. Yang, C. T.; Li, J. M.; Wenig, H. H.; Li, Y. C.; Chen, H. C.; Chen, M. F. Adenovirus-mediated transfer of siRNA against survivin enhances the radiosensitivity of human non-small cell lung cancer cells. Cancer Gene Ther., 2009, 17(2),120-130
70. Zhang, R.; Ma, L.; Zheng, M.; Ren, J.; Wang, T.; Meng, Y.; Zhao, J.; Jia, L.; Yao, L.; Han, H.; Li, K.; Yang, A. Survivin knockdown by short hairpin RNA abrogates the growth of human hepatocellular carcinoma xenografts in nude mice. Cancer Gene, Ther., 2009, 17(4), 275-288.
71. Coma, S.; Noe, V.; Lavarino, C.; Adán, J.; Rivas, M.; López-Matas, M.; Pagan, R.; Mitjans, F.; Vilaró, S.; Piulats, J.; Ciudad, C. J. Use of siRNAs and antisense oligonucleotides against survivin RNA to inhibit steps leading to tumor angiogenesis. Oligonucleotides, 2004, 14, 100-103.
72. Coumoul, X.; Li, W.; Wang, R. H.; Deng, C. Inducible suppression of Fgfr2 and survivin in ES cells using a combination of the RNA interference (RNAi) and the cre-LoxP system. Nucleic Acids Res., 2004, 32, e85.
73. 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.; Wirth, M. P. Are overexpressed alternative survivin transcripts in human bladder cancer suitable targets for siRNA-mediated in Vitro inhibition? Int. J. Oncol., 2007, 30, 1317-1324.
74. Kappler, M.; Rot, S.; Taubert, H.; Greither, T.; Bartel, F.; Dellas, K.; Hänsgen, G.; Trott, K. R.; Bache, M. 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., 2007, 14, 994-1001.
75. Nielsen, P. E. Peptide nucleic acids and the origin of life. Chem. Biodiv., 2007, 4, 1996-2002.
76. Richard, J. P.; Melikov, K.; Vives, E.; Ramos, C.; Verbeure, B.; Gait, M. J.; Chernomordik, L. V.; Lebleu, B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem., 2003, 278, 585-590.
77. Berg, K.; Folini, M.; Prasmickaite, L.; Selbo, P. K., Bonsted, A.; Engesaeter, B. Ø.; Zaffaroni, N.; Weyergang, A.; Dietze, A.; Maelandsmo, G. M.; Wagner, E.; Norum, O. J.; Høgset, A. Photochemical internalization: a new tool for drug delivery. Curr. Pharm. Biotechnol., 2007, 8, 362-372.
78. Hauser, H. P.; Bardroff, M.; Pyrowolakis, G.; Jentsch, S. A giant ubiquitin-conjugating enzyme related to IAP apoptosis inhibitors. J. Cell. Biol., 1998, 141, 1415-1414.
79. Bartke, T.; Pohl, C.; Pyrowolakis, G.; Jentsch, S. Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol. Cell 2004, 14, 801-811.
80. Qiu, X. B.; Goldberg, A. L. The membrane-associated inhibitor of apoptosis protein, BRUCE/apollon, antagonizes both the precursor and mature forms of smac and caspase-9. J. Biol. Chem., 2005, 280, 174-182.
81. Hao, Y.; Sekine, S.; Kawabata, A.; Nakamura, H.; Ishioka, T.; Ohata, H.; Katayama, R.; Hashimoto, C.; Zhang, X.; Noda, T.; Tsuruo, T.; Naito, M. Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function. Nat. Cell. Biol., 2004, 6, 849-860.
82. Qiu, X. B.; Markant, S. L.; Yuan, J.; Goldberg, A. L. Nrdp1-mediated degradation of the gigantic IAP, BRUCE, is a novel pathway for triggering apoptosis. EMBO J., 2004, 23, 800-810.
83. Ren, J.; Shi, M.; Liu, R.; Yang, Q. H.; Johnson, T.; Skarnes, W. C.; Du, C. The birc6 (Bruce) gene regulates p53 and the mitochondrial pathway of apoptosis and is essential for mouse embryonic development. Proc. Natl. Acad. Sci. USA, 2005, 102, 565-570.
84. Lopergolo, A.; Pennati, M.; Gandellini, P.; Orlotti, N. I.; Poma, P.; Daidone, M. G.; Folini, M.; Zaffaroni, N. Apollon gene silencing induces apoptosis in breast cancer cells through p53 stabilisation and caspase-3 activation. Br. J. Cancer, 2009, 100, 739-746.
85. Chen, Z.; Naito, M.; Hori, S.; Mashima, T.; Yamori, T.; Tsuruo, T. A human IAP-family gene, apollon, expressed in human brain cancer cells. Biochem. Biophys. Res. Commun., 1999, 264, 847-854.
86. Sung, K. W.; Choi, J.; Hwang, Y. K.; Lee, S. J.; Kim, H. J.; Lee, S. H.; Yoo, K. H.; Jung, H. L.; Koo, H. H. Overexpression of apollon, an antiapoptotic protein, is associated with poor prognosis in childhood de novo acute myeloid leukemia. Clin. Cancer Res., 2007, 13, 5109-5114.
87. Chu, L.; Gu, J.; Sun, L.; Qian, Q.; Qian, C.; Liu, X. Oncolytic adenovirus-mediated shRNA against apollon inhibits tumor cell growth and enhances antitumor effect of 5-fluorouracil. Gene Ther., 2008, 15, 484-494.
88. 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. Phase I and pharmacokinetic study of YM155, a small-molecule inhibitor of survivin. J. Clin. Oncol., 2008, 26, 5198-5203.