Cancer testis antigen vaccination affords long-term protection in a murine model of ovarian cancer

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Chiriva Internati, Maurizio ^a   Yu, Yuefei ^a   Mirandola, Leonardo ^a   Jenkins, Marjorie R ^a,b   Chapman, Caroline ^c   Cannon, Martin ^d   Cobos, Everardo ^a   Kast Martin, W ^e,f  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^f UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER TESTIS ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; SPERM PROTEIN 17 VACCINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CANCER VACCINE; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CANCER CELL CULTURE; CANCER CONTROL; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DRUG EFFICACY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CANCER; PROTECTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL; WESTERN BLOTTING; ANIMAL; BLOOD; C57BL MOUSE; CELL LINE; DISEASE MODEL; HELPER CELL; HUMAN; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; MAJOR HISTOCOMPATIBILITY COMPLEX; OVARY TUMOR; PATHOLOGY; SURVIVAL; TIME; VACCINATION;

MURINAE; MUS;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INJECTIONS, INTRAPERITONEAL; INTERFERON-GAMMA; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED C57BL; OVARIAN NEOPLASMS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; VACCINATION;

EID: 77956276231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010471     Document Type: Article

References (59)

1. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, et al. (2005) Cancer statistics, 2005. CA Cancer J Clin 55: 10-30.
2. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74-108.
3. Cheng W, Liu J, Yoshida H, Rosen D, Naora H (2005) Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract. Nat Med 11: 531-537.
4. Feeley KM, Wells M (2001) Precursor lesions of ovarian epithelial malignancy. Histopathology 38: 87-95.
5. Russo A, Calo V, Bruno L, Rizzo S, Bazan V, et al. (2009) Hereditary ovarian cancer. Crit Rev Oncol Hematol 69: 28-44.
6. Coukos G, Rubin SC (2002) Prophylactic oophorectomy. Best Pract Res Clin Obstet Gynaecol 16: 597-609.
7. Narod SA, Dube MP, Klijn J, Lubinski J, Lynch HT, et al. (2002) Oral contraceptives and the risk of breast cancer in BRCA1 and BRCA2 mutation carriers. J Natl Cancer Inst 94: 1773-1779.
8. Hwu P, Freedman RS (2002) The immunotherapy of patients with ovarian cancer. J Immunother 25: 189-201.
9. Chiriva-Internati M, Grizzi F, Weidanz JA, Ferrari R, Yuefei Y, et al. (2007) A NOD/SCID tumor model for human ovarian cancer that allows tracking of tumor progression through the biomarker Sp17. J Immunol Methods 321: 86-93.
10. Grizzi F, Gaetani P, Franceschini B, Di Ieva A, Colombo P, et al. (2006) Sperm protein 17 is expressed in human nervous system tumours. BMC Cancer 6: 23.
11. Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen YT (2002) Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol Rev 188: 22-32.
12. Scanlan MJ, Simpson AJ, Old LJ (2004) The cancer/testis genes: review, standardization, and commentary. Cancer Immun 4: 1.
13. Chiriva-Internati M, Wang Z, Salati E, Bumm K, Barlogie B, et al. (2002) Sperm protein 17 (Sp17) is a suitable target for immunotherapy of multiple myeloma. Blood 100: 961-965.
14. Chiriva-Internati M, Weidanz JA, Yu Y, Frezza EE, Jenkins MR, et al. (2008) Sperm protein 17 is a suitable target for adoptive T-cell-based immunotherapy in human ovarian cancer. J Immunother 31: 693-703.
15. Dadabayev AR, Wang Z, Zhang Y, Zhang J, Robinson WR, et al. (2005) Cancer immunotherapy targeting Sp17: when should the laboratory findings be translated to the clinics? Am J Hematol 80: 6-11.
16. Grizzi F, Chiriva-Internati M, Franceschini B, Bumm K, Colombo P, et al. (2004) Sperm protein 17 is expressed in human somatic ciliated epithelia. J Histochem Cytochem 52: 549-554.
17. Boon T, Coulie PG, Van den Eynde BJ, van der Bruggen P (2006) Human T cell responses against melanoma. Annu Rev Immunol 24: 175-208.
18. Gattinoni L, Powell DJ, Jr., Rosenberg SA, Restifo NP (2006) Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 6: 383-393.
19. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129.
20. O'Rand MG, Widgren EE, Fisher SJ (1988) Characterization of the rabbit sperm membrane autoantigen, RSA, as a lectin-like zona binding protein. Dev Biol 129: 231-240.
21. Chiriva-Internati M, Wang Z, Salati E, Timmins P, Lim SH (2002) Tumor vaccine for ovarian carcinoma targeting sperm protein 17. Cancer 94: 2447-2453.
22. Chiriva-Internati M, Wang Z, Xue Y, Bumm K, Hahn AB, et al. (2001) Sperm protein 17 (Sp17) in multiple myeloma: opportunity for myeloma-specific donor T cell infusion to enhance graft-versus-myeloma effect without increasing graftversus- host disease risk. Eur J Immunol 31: 2277-2283.
23. Jin B, Wang RY, Qiu Q, Sugauchi F, Grandinetti T, et al. (2007) Induction of potent cellular immune response in mice by hepatitis C virus NS3 protein with double-stranded RNA. Immunology 122: 15-27.
24. Straughn JM, Jr., Shaw DR, Guerrero A, Bhoola SM, Racelis A, et al. (2004) Expression of sperm protein 17 (Sp17) in ovarian cancer. Int J Cancer 108: 805-811.
25. Wen Y, Richardson RT, Widgren EE, O'Rand MG (2001) Characterization of Sp17: a ubiquitous three domain protein that binds heparin. Biochem J 357: 25-31.
26. Overwijk WW, Lee DS, Surman DR, Irvine KR, Touloukian CE, et al. (1999) Vaccination with a recombinant vaccinia virus encoding a "self" antigen induces autoimmune vitiligo and tumor cell destruction in mice: requirement for CD4(+) T lymphocytes. Proc Natl Acad Sci U S A 96: 2982-2987.
27. Valmori D, Souleimanian NE, Tosello V, Bhardwaj N, Adams S, et al. (2007) Vaccination with NY-ESO-1 protein and CpG in Montanide induces integrated antibody/Th1 responses and CD8 T cells through cross-priming. Proc Natl Acad Sci U S A 104: 8947-8952.
28. Van Der Bruggen P, Zhang Y, Chaux P, Stroobant V, Panichelli C, et al. (2002) Tumor-specific shared antigenic peptides recognized by human T cells. Immunol Rev 188: 51-64.
29. Verthelyi D, Zeuner RA (2003) Differential signaling by CpG DNA in DCs and B cells: not just TLR9. Trends Immunol 24: 519-522.
30. Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, et al. (2009) IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 183: 2475-2483.
31. Mendez S, Tabbara K, Belkaid Y, Bertholet S, Verthelyi D, et al. (2003) Coinjection with CpG-containing immunostimulatory oligodeoxynucleotides reduces the pathogenicity of a live vaccine against cutaneous Leishmaniasis but maintains its potency and durability. Infect Immun 71: 5121-5129.
32. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, et al. (1993) Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041-1048.
33. Markiewicz MA, Kast WM (2004) Progress in the development of immunotherapy of cancer using ex vivo-generated dendritic cells expressing multiple tumor antigen epitopes. Cancer Invest 22: 417-434.
34. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, et al. (2000) Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21: 585-591.
35. Cannon MJ, O'Brien TJ (2009) Cellular immunotherapy for ovarian cancer. Expert Opin Biol Ther 9: 677-688.
36. Holtz DO, Krafty RT, Mohamed-Hadley A, Zhang L, Alagkiozidis I, et al. (2008) Should tumor VEGF expression influence decisions on combining lowdose chemotherapy with antiangiogenic therapy? Preclinical modeling in ovarian cancer. J Transl Med 6: 2.
37. Benencia F, Courreges MC, Coukos G (2008) Whole tumor antigen vaccination using dendritic cells: comparison of RNA electroporation and pulsing with UVirradiated tumor cells. J Transl Med 6: 21.
38. Foster T, Brown TM, Chang J, Menssen HD, Blieden MB, et al. (2009) A review of the current evidence for maintenance therapy in ovarian cancer. Gynecol Oncol 115: 290-301.
39. Wagner H (2009) The immunogenicity of CpG-antigen conjugates. Adv Drug Deliv Rev 61: 243-247.
40. Chiriva-Internati M, Liu Y, Weidanz JA, Grizzi F, You H, et al. (2003) Testing recombinant adeno-associated virus-gene loading of dendritic cells for generating potent cytotoxic T lymphocytes against a prototype self-antigen, multiple myeloma HM1.24. Blood 102: 3100-3107.
41. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
42. Zhou H, Luo Y, Mizutani M, Mizutani N, Reisfeld RA, et al. (2005) T cellmediated suppression of angiogenesis results in tumor protective immunity. Blood 106: 2026-2032.
43. Sprent J, Zhang X, Sun S, Tough D (2000) T-cell proliferation in vivo and the role of cytokines. Philos Trans R Soc Lond B Biol Sci 355: 317-322.
44. Sun S, Zhang X, Tough D, Sprent J (2000) Multiple effects of immunostimulatory DNA on T cells and the role of type I interferons. Springer Semin Immunopathol 22: 77-84.
45. Leveque L, Deknuydt F, Bioley G, Old LJ, Matsuzaki J, et al. (2009) Interleukin 2-mediated conversion of ovarian cancer-associated CD4+ regulatory T cells into proinflammatory interleukin 17-producing helper T cells. J Immunother 32: 101-108.
46. Chen W, Jin W, Hardegen N, Lei KJ, Li L, et al. (2003) Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875-1886.
47. Milner JD, Brenchley JM, Laurence A, Freeman AF, Hill BJ, et al. (2008) Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper- IgE syndrome. Nature 452: 773-776.
48. Noben-Trauth N, Hu-Li J, Paul WE (2002) IL-4 secreted from individual naive CD4+ T cells acts in an autocrine manner to induce Th2 differentiation. Eur J Immunol 32: 1428-1433.
49. Zhu J, Yamane H, Paul WE (2010) Differentiation of effector CD4 T cell populations. Annu Rev Immunol 28: 445-489.
50. Charles KA, Kulbe H, Soper R, Escorcio-Correia M, Lawrence T, et al. (2009) The tumor-promoting actions of TNF-alpha involve TNFR1 and IL-17 in ovarian cancer in mice and humans. J Clin Invest 119: 3011-3023.
51. Miyahara Y, Odunsi K, Chen W, Peng G, Matsuzaki J, et al. (2008) Generation and regulation of human CD4+ IL-17-producing T cells in ovarian cancer. Proc Natl Acad Sci U S A 105: 15505-15510.
52. Benatar T, Cao MY, Lee Y, Li H, Feng N, et al. (2008) Virulizin induces production of IL-17E to enhance antitumor activity by recruitment of eosinophils into tumors. Cancer Immunol Immunother 57: 1757-1769.
53. Giuntoli RL, 2nd, Webb TJ, Zoso A, Rogers O, Diaz-Montes TP, et al. (2009) Ovarian cancer-associated ascites demonstrates altered immune environment: implications for antitumor immunity. Anticancer Res 29: 2875-2884.
54. Kryczek I, Banerjee M, Cheng P, Vatan L, Szeliga W, et al. (2009) Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 114: 1141-1149.
55. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, et al. (2008) Tumorspecific Th17-polarized cells eradicate large established melanoma. Blood 112: 362-373.
56. Munn DH (2009) Th17 cells in ovarian cancer. Blood 114: 1134-1135.
57. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, et al. (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10: 942-949.
58. Radhakrishnan S, Cabrera R, Schenk EL, Nava-Parada P, Bell MP, et al. (2008) Reprogrammed FoxP3+ T regulatory cells become IL-17+ antigen-specific autoimmune effectors in vitro and in vivo. J Immunol 181: 3137-3147.
59. Oumouna M, Mapletoft JW, Karvonen BC, Babiuk LA, van Drunen Littel-van den Hurk S (2005) Formulation with CpG oligodeoxynucleotides prevents induction of pulmonary immunopathology following priming with formalininactivated or commercial killed bovine respiratory syncytial virus vaccine. J Virol 79: 2024-2032.