Survivin as a cancer vaccine target

Journal of Vaccines and Vaccination

Volumn 5, Issue 3, 2014, Pages

  Ciesielski, Michael J ^a   Qiu, Jingxin ^a   Fenstermaker, Robert A ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Apoptosis; Immunotherapy; Peptide; Survivin; Vaccine

Indexed keywords

EID: 84902590628     PISSN: None     EISSN: 21577560     Source Type: Journal    
DOI: 10.4172/2157-7560.1000230     Document Type: Review

References (100)

1. Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3: 917-921.
2. Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, et al. (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396: 580-584.
3. Tamm I, Wang Y, Sausville E, Scudiero DA, Vigna N, et al. (1998) IAPfamily protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 58: 5315-5320.
4. Zhao J, Tenev T, Martins LM, Downward J, Lemoine NR (2000) The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J Cell Sci 113 Pt 23: 4363-4371.
5. Fortugno P, Wall NR, Giodini A, O'Connor DS, Plescia J, et al. (2002) Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function. J Cell Sci 115: 575-585.
6. Carrasco RA, Stamm NB, Marcusson E, Sandusky G, Iversen P, et al. (2011) Antisense inhibition of survivin expression as a cancer therapeutic. Mol Cancer Ther 10: 221-232.
7. Conway EM, Pollefeyt S, Cornelissen J, DeBaere I, Steiner-Mosonyi M, et al. (2000) Three differentially expressed survivin cDNA variants encode proteins with distinct antiapoptotic functions. Blood 95: 1435-1442.
8. Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, et al. (2001) An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 40: 1117-1123.
9. Kajiwara Y, Yamasaki F, Hama S, Yahara K, Yoshioka H, et al. (2003) Expression of survivin in astrocytic tumors: correlation with malignant grade and prognosis. Cancer 97: 1077-1083.
10. Islam A, Kageyama H, Takada N, Kawamoto T, Takayasu H, et al. (2000) High expression of Survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 19: 617-623.
11. Altieri DC (2013) Targeting survivin in cancer. Cancer Lett 332: 225-228.
12. Altieri DC (2010) Survivin and IAP proteins in cell-death mechanisms. Biochem J 430: 199-205.
13. Li F, Brattain MG (2006) Role of the Survivin gene in pathophysiology. Am J Pathol 169: 1-11.
14. Mahotka C, Liebmann J, Wenzel M, Suschek CV, Schmitt M, et al. (2002) Differential subcellular localization of functionally divergent survivin splice variants. Cell Death Differ 9: 1334-1342.
15. Dohi T, Beltrami E, Wall NR, Plescia J, Altieri DC (2004) Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 114: 1117-1127.
16. Khan S, Jutzy JM, Valenzuela MM, Turay D, Aspe JR, et al. (2012) Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PLoS One 7: e46737.
17. Khan S, Jutzy JM, Aspe JR, McGregor DW, Neidigh JW, et al. (2011) Survivin is released from cancer cells via exosomes. Apoptosis 16: 1-12.
18. Hoffmann AC, Warnecke-Eberz U, Luebke T, Prenzel K, Metzger R, et al. (2007) Survivin mRNA in peripheral blood is frequently detected and significantly decreased following resection of gastrointestinal cancers. J Surg Oncol 95: 51-54.
19. Hoffmann AC, Vallböhmer D, Grimminger P, Metzger R, Prenzel KL, et al. (2010) Preoperative survivin mRNA detection in peripheral blood is an independent predictor of outcome in esophageal carcinoma. Pharmacogenomics 11: 341-347.
20. Adida C, Crotty PL, McGrath J, Berrebi D, Diebold J, et al. (1998) Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am J Pathol 152: 43-49.
21. Ciesielski MJ, Apfel L, Barone TA, Castro CA, Weiss TC, et al. (2006) Antitumor effects of a xenogeneic survivin bone marrow derived dendritic cell vaccine against murine GL261 gliomas. Cancer Immunol Immunother 55: 1491-1503.
22. Satoh K, Kaneko K, Hirota M, Masamune A, Satoh A, et al. (2001) Expression of survivin is correlated with cancer cell apoptosis and is involved in the development of human pancreatic duct cell tumors. Cancer 92: 271-278.
23. Altieri DC (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3: 46-54.
24. Andersen MH, thor SP (2002) Survivin--a universal tumor antigen. Histol Histopathol 17: 669-675.
25. Ciesielski MJ, Ahluwalia MS, Munich SA, Orton M, Barone T, et al. (2010) Antitumor cytotoxic T-cell response induced by a survivin peptide mimic. Cancer Immunol Immunother 59: 1211-1221.
26. Ciesielski MJ, Kozbor D, Castanaro CA, Barone TA, Fenstermaker RA (2008) Therapeutic effect of a T helper cell supported CTL response induced by a survivin peptide vaccine against murine cerebral glioma. Cancer Immunol Immunother 57: 1827-1835.
27. Mahalingam D, Medina EC, Esquivel JA, Espitia CM, Smith S, et al. (2010) Vorinostat enhances the activity of temsirolimus in renal cell carcinoma through suppression of survivin levels. Clin Cancer Res 16: 141-153.
28. Zhang W, Chen X, Qiu F (2003) An antisense plasmid targeting survivin expression induces apoptosis and sensitizes hepatocarcinoma cells to chemotherapy. J Huazhong Univ Sci Technolog Med Sci 23: 387-391.
29. Li HL, Ma AN (2010) Induction of apoptosis of non-small cell lung cancer by a methylated oligonucleotide targeting survivin gene. Cancer Gene Ther 17: 441-446.
30. Wesierska-Gadek J, Schmid G (2007) Transcriptional repression of antiapoptotic proteins mediated by the tumor suppressor protein p53. Cancer Ther 5: 203-212.
31. UniProt Consortium (2014) Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 42: D191-198.
32. Zheng W, Ma X, Wei D, Wang T, Ma Y, et al. (2005) Molecular cloning and bioinformatics analysis of a novel spliced variant of survivin from human breast cancer cells. DNA Seq 16: 321-328.
33. Krieg A, Mahotka C, Krieg T, Grabsch H, Müller W, et al. (2002) Expression of different survivin variants in gastric carcinomas: first clues to a role of survivin-2B in tumour progression. Br J Cancer 86: 737-743.
34. Takashima H, Nakajima T, Moriguchi M, Sekoguchi S, Nishikawa T, et al. (2005) In vivo expression patterns of survivin and its splicing variants in chronic liver disease and hepatocellular carcinoma. Liver Int 25: 77-84.
35. Wagner, Schmelz K, Wuchter C, Ludwig WD, Dörken B, et al. (2006) In vivo expression of survivin and its splice variant survivin-2B: impact on clinical outcome in acute myeloid leukemia. Int J Cancer 119: 1291-1297.
36. Caldas H, Jiang Y, Holloway MP, Fangusaro J, Mahotka C, et al. (2005) Survivin splice variants regulate the balance between proliferation and cell death. Oncogene 24: 1994-2007.
37. Vivas-Mejia PE, Rodriguez-Aguayo C, Han HD, Shahzad MM, Valiyeva F, et al. (2011) Silencing survivin splice variant 2B leads to antitumor activity in taxane--resistant ovarian cancer. Clin Cancer Res 17: 3716-3726.
38. Ling X, Cheng Q, Black JD, 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.
39. Atlasi Y, Mowla SJ, Ziaee SA (2009) Differential expression of survivin and its splice variants, survivin-DeltaEx3 and survivin-2B, in bladder cancer. Cancer Detect Prev 32: 308-313.
40. Cheng Z, Hu L, Fu W, Zhang Q, Liao X (2007) Expression of survivin and its splice variants in gastric cancer. J Huazhong Univ Sci Technolog Med Sci 27: 393-398.
41. Mahotka C, Wenzel M, Springer E, Gabbert HE, Gerharz CD (1999) Survivin-deltaEx3 and survivin-2B: two novel splice variants of the apoptosis inhibitor survivin with different antiapoptotic properties. Cancer Res 59: 6097-6102.
42. Li F (2005) Role of survivin and its splice variants in tumorigenesis. Br J Cancer 92: 212-216.
43. Moore AS, Alonzo TA, Gerbing RB, Lange BJ, Heerema NA, et al. (2014) BIRC5 (survivin) splice variant expression correlates with refractory disease and poor outcome in pediatric acute myeloid leukemia: A report from the Children's Oncology Group. Pediatr Blood Cancer 61: 647-652.
44. Cho GS, Ahn TS, Jeong D, Kim JJ, Kim CJ, et al. (2011) Expression of the survivin-2B splice variant related to the progression of colorectal carcinoma. J Korean Surg Soc 80: 404-411.
45. Mahotka C, Krieg T, Krieg A, Wenzel M, Suschek CV, et al. (2002) Distinct in vivo expression patterns of survivin splice variants in renal cell carcinomas. Int J Cancer 100: 30-36.
46. Mull AN, Klar A, Navara CS (2014) Differential localization and high expression of SURVIVIN splice variants in human embryonic stem cells but not in differentiated cells implicate a role for SURVIVIN in pluripotency. Stem Cell Res 12: 539-549.
47. Marioni G, Agostini M, Bedin C, Blandamura S, Stellini E, et al. (2012) Survivin and laryngeal carcinoma prognosis: nuclear localization and expression of splice variants. Histopathology 61: 247-256.
48. Caldas H, Honsey LE, Altura RA (2005) Survivin 2alpha: a novel Survivin splice variant expressed in human malignancies. Mol Cancer 4: 11.
49. Badran A, Yoshida A, Ishikawa K, Goi T, Yamaguchi A, et al. (2004) Identification of a novel splice variant of the human anti-apoptopsis gene survivin. Biochem Biophys Res Commun 314: 902-907.
50. Jacob NK, Cooley JV, Shirai K, Chakravarti A (2012) Survivin splice variants are not essential for mitotic progression or inhibition of apoptosis induced by doxorubicin and radiation. Onco Targets Ther 5: 7-20.
51. Small TW, Pickering JG (2009) Nuclear degradation of Wilms tumor 1- associating protein and survivin splice variant switching underlie IGF-1- mediated survival. J Biol Chem 284: 24684-24695.
52. Luwor RB, Johns TG, Murone C, Huang HJ, Cavenee WK, et al. (2001) Monoclonal antibody 806 inhibits the growth of tumor xenografts expressing either the de2-7 or amplified epidermal growth factor receptor (EGFR) but not wild-type EGFR. Cancer Res 61: 5355-5361.
53. Wikstrand CJ, Hale LP, Batra SK, Hill ML, Humphrey PA, et al. (1995) Monoclonal antibodies against EGFRvIII are tumor specific and react with breast and lung carcinomas and malignant gliomas. Cancer Res 55: 3140-3148.
54. Dela Cruz CS, Chamberlain JW, MacDonald KS, Barber BH (1999) Xenogeneic and allogeneic anti-MHC immune responses induced by plasmid DNA immunization. Vaccine 17: 2479-2492.
55. Ciesielski MJ, Kazim AL, Barth RF, Fenstermaker RA (2005) Cellular antitumor immune response to a branched lysine multiple antigenic peptide containing epitopes of a common tumor-specific antigen in a rat glioma model. Cancer Immunol Immunother 54: 107-119.
56. Yang W, Barth RF, Wu G, Ciesielski MJ, Fenstermaker RA, et al. (2005) Development of a syngeneic rat brain tumor model expressing EGFRvIII and its use for molecular targeting studies with monoclonal antibody L8A4. Clin Cancer Res 11: 341-350.
57. Fenstermaker RA, Ciesielski MJ (2014) Challenges in the development of a survivin vaccine (SurVaxM) for malignant glioma. Expert Rev Vaccines 13: 377-385.
58. Godet Y, Bonnin A, Guilloux Y, Vignard V, Schadendorf D, et al. (2009) A new tyrosinase epitope recognized in the HLA-B*4002 context by CTL from melanoma patients. Cancer Immunol Immunother 58: 271-280.
59. Andersen MH, Pedersen LO, Capeller B, Bröcker EB, Becker JC, et al. (2001) Spontaneous cytotoxic T-cell responses against survivin-derived MHC class I-restricted T-cell epitopes in situ as well as ex vivo in cancer patients. Cancer Res 61: 5964-5968.
60. Coulie PG, Brichard V, Van Pel A, Wölfel T, Schneider J, et al. (1994) A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med 180: 35-42.
61. Cox AL, Skipper J, Chen Y, Henderson RA, Darrow TL, et al. (1994) Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines. Science 264: 716-719.
62. Rohayem J, Diestelkoetter P, Weigle B, Oehmichen A, Schmitz M, et al. (2000) Antibody response to the tumor-associated inhibitor of apoptosis protein survivin in cancer patients. Cancer Res 60: 1815-1817.
63. Hadrup SR, Gehl J, Sørensen RB, Geertsen PF, Straten PT, et al. (2006) Persistence of survivin specific T cells for seven years in a melanoma patient during complete remission. Cancer Biol Ther 5: 480-482.
64. Yagihashi A, Asanuma K, Nakamura M, Araya J, Mano Y, et al. (2001) Detection of anti-survivin antibody in gastrointestinal cancer patients. Clin Chem 47: 1729-1731.
65. Karanikas V, Khalil S, Kerenidi T, Gourgoulianis KI, Germenis AE (2009) Anti-survivin antibody responses in lung cancer. Cancer Lett 282: 159-166.
66. Reker S, Meier A, Holten-Andersen L, Svane IM, Becker JC, et al. (2004) Identification of novel survivin-derived CTL epitopes. Cancer Biol Ther 3: 173-179.
67. Hirschowitz EA, Foody T, Hidalgo GE, Yannelli JR (2007) Immunization of NSCLC patients with antigen-pulsed immature autologous dendritic cells. Lung Cancer 57: 365-372.
68. Berntsen A, Trepiakas R, Wenandy L, Geertsen PF, thor Straten P, et al. (2008) Therapeutic dendritic cell vaccination of patients with metastatic renal cell carcinoma: a clinical phase 1/2 trial. J Immunother 31: 771-780.
69. Soleimani A, Berntsen A, Svane IM, Pedersen AE (2009) Immune responses in patients with metastatic renal cell carcinoma treated with dendritic cells pulsed with tumor lysate. Scand J Immunol 70: 481-489.
70. Hobo W, Strobbe L, Maas F, Fredrix H, Greupink-Draaisma A, et al. (2013) Immunogenicity of dendritic cells pulsed with MAGE3, Survivin and B-cell maturation antigen mRNA for vaccination of multiple myeloma patients. Cancer Immunol Immunother 62: 1381-1392.
71. Wobser M, Keikavoussi P, Kunzmann V, Weininger M, Andersen MH, et al. (2006) Complete remission of liver metastasis of pancreatic cancer under vaccination with a HLA-A2 restricted peptide derived from the universal tumor antigen survivin. Cancer Immunol Immunother 55: 1294-1298.
72. Tsuruma T, Hata F, Torigoe T, Furuhata T, Idenoue S, et al. (2004) Phase I clinical study of anti-apoptosis protein, survivin-derived peptide vaccine therapy for patients with advanced or recurrent colorectal cancer. J Transl Med 2: 19.
73. Tsuruma T, Iwayama Y, Ohmura T, Katsuramaki T, Hata F, et al. (2008) Clinical and immunological evaluation of anti-apoptosis protein, survivin-derived peptide vaccine in phase I clinical study for patients with advanced or recurrent breast cancer. J Transl Med 6: 24.
74. Honma I, Kitamura H, Torigoe T, Takahashi A, Tanaka T, et al. (2009) Phase I clinical study of anti-apoptosis protein survivin-derived peptide vaccination for patients with advanced or recurrent urothelial cancer. Cancer Immunol Immunother 58: 1801-1807.
75. Miyazaki A, Kobayashi J, Torigoe T, Hirohashi Y, Yamamoto T, et al. (2011) Phase I clinical trial of survivin-derived peptide vaccine therapy for patients with advanced or recurrent oral cancer. Cancer Sci 102: 324-329.
76. Tanaka M, Butler MO, Ansén S, Imataki O, Berezovskaya A, et al. (2011) Induction of HLA-DP4-restricted anti-survivin Th1 and Th2 responses using an artificial antigen-presenting cell. Clin Cancer Res 17: 5392-5401.
77. Tanaka T, Kitamura H, Inoue R, Nishida S, Takahashi-Takaya A, et al. (2013) Potential survival benefit of anti-apoptosis protein: survivinderived peptide vaccine with and without interferon alpha therapy for patients with advanced or recurrent urothelial cancer--results from phase I clinical trials. Clin Dev Immunol 2013: 262967.
78. Becker JC, Andersen MH, Hofmeister-Muller V, Wobser M, Frey L, et al. (2012) Survivin-specific T-cell reactivity correlates with tumor response and patient survival: a phase-II peptide vaccination trial in metastatic melanoma. Cancer Immunol Immunother 61: 2091-2103.
79. Lennerz V, Gross S, Gallerani E, Sessa C, Mach N, et al. (2014) Immunologic response to the survivin-derived multi-epitope vaccine EMD640744 in patients with advanced solid tumors. Cancer Immunol Immunother 63: 381-394.
80. Riedmann EM (2012) Ovarian cancer vaccine candidate DPX-Survivac: positive interim results from phase 1. Hum Vaccin Immunother 8: 1743.
81. Widenmeyer M, Griesemann H, Stevanovi S, Feyerabend S, Klein R, et al. (2012) Promiscuous survivin peptide induces robust CD4+ T-cell responses in the majority of vaccinated cancer patients. Int J Cancer 131: 140-149.
82. Kim EK, Cho HI, Yoon SH, Park MJ, Sohn HJ, et al. (2008) Efficient generation of survivin-specific cytotoxic T lymphocytes from healthy persons in vitro: quantitative and qualitative effects of CD4+ T cells. Vaccine 26: 3987-3997.
83. Moeller M, Kershaw MH, Cameron R, Westwood JA, Trapani JA, et al. (2007) Sustained antigen-specific antitumor recall response mediated by gene-modified CD4+ T helper-1 and CD8+ T cells. Cancer Res 67: 11428-11437.
84. Yu J, Ren X, Cao S, Zhang W, Hao X (2006) Th1 polarization and apoptosis-inducing activity of CD4+ T -cells in cytokine-induced killers might favor the antitumor cytotoxicity of cytokine-induced killers in vivo. Cancer Biother Radiopharm 21: 276-284.
85. Pardoll DM (1999) Inducing autoimmune disease to treat cancer. Proc Natl Acad Sci U S A 96: 5340-5342.
86. Hung K, Hayashi R, Lafond-Walker A, Lowenstein C, Pardoll D, et al. (1998) The central role of CD4(+) T cells in the antitumor immune response. J Exp Med 188: 2357-2368.
87. Piesche M, Hildebrandt Y, Zettl F, Chapuy B, Schmitz M, et al. (2007) Identification of a promiscuous HLA DR-restricted T-cell epitope derived from the inhibitor of apoptosis protein survivin. Hum Immunol 68: 572-576.
88. Wang XF, Kerzerho J, Adotevi O, Nuyttens H, Badoual C, et al. (2008) Comprehensive analysis of HLA-DR- and HLA-DP4-restricted CD4+ T cell response specific for the tumor-shared antigen survivin in healthy donors and cancer patients. J Immunol 181: 431-439.
89. Overwijk WW, Restifo NP (2000) Autoimmunity and the immunotherapy of cancer: targeting the self to destroy the other. Crit Rev Immunol 20: 433-450.
90. Lohr J, Knoechel B, Nagabhushanam V, Abbas AK (2005) T-cell tolerance and autoimmunity to systemic and tissue-restricted selfantigens. Immunol Rev 204: 116-127.
91. Fikes JD, Sette A (2003) Design of multi-epitope, analogue-based cancer vaccines. Expert Opin Biol Ther 3: 985-993.
92. Guevara-Patiño JA, Turk MJ, Wolchok JD, Houghton AN (2003) Immunity to cancer through immune recognition of altered self: studies with melanoma. Adv Cancer Res 90: 157-177.
93. Parkhurst MR, Salgaller ML, Southwood S, Robbins PF, Sette A, et al. (1996) Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J Immunol 157: 2539-2548.
94. Valmori D, Fonteneau JF, Lizana CM, Gervois N, Liénard D, et al. (1998) Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J Immunol 160: 1750-1758.
95. Trojan A, Witzens M, Schultze JL, Vonderheide RH, Harig S, et al. (2001) Generation of cytotoxic T lymphocytes against native and altered peptides of human leukocyte antigen-A*0201 restricted epitopes from the human epithelial cell adhesion molecule. Cancer Res 61: 4761-4765.
96. Keogh E, Fikes J, Southwood S, Celis E, Chesnut R, et al. (2001) Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-A*0201-binding affinity. J Immunol 167: 787-796.
97. Evavold BD, Sloan-Lancaster J, Allen PM (1993) Tickling the TCR: selective T-cell functions stimulated by altered peptide ligands. Immunol Today 14: 602-609.
98. Loftus DJ, Squarcina P, Nielsen MB, Geisler C, Castelli C, et al. (1998) Peptides derived from self-proteins as partial agonists and antagonists of human CD8+ T-cell clones reactive to melanoma/melanocyte epitope MART1(27-35). Cancer Res 58: 2433-2439.
99. Rudolph MG, Stanfield RL, Wilson IA (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 24: 419-466.
100. Shen L, Ciesielski M, Ramakrishnan S, Miles KM, Ellis L, et al. (2012) Class I histone deacetylase inhibitor entinostat suppresses regulatory T cells and enhances immunotherapies in renal and prostate cancer models. PLoS One 7: e30815.