NY-ESO-1 cancer testis antigen demonstrates high immunogenicity in triple negative breast cancer

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Ademuyiwa, Foluso O ^a   Bshara, Wiam ^a   Attwood, Kristopher ^a   Morrison, Carl ^a   Edge, Stephen B ^a   Ambrosone, Christine B ^a   O'Connor, Tracey L ^a   Levine, Ellis G ^a   Miliotto, Anthony ^a   Ritter, Erika ^b   Ritter, Gerd ^b   Gnjatic, Sacha ^b   Odunsi, Kunle ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; NY ESO 1 ANTIGEN;

ADULT; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; BREAST CANCER; CANCER IMMUNOTHERAPY; CANCER INFILTRATION; CANCER TISSUE; CD8+ T LYMPHOCYTE; COHORT ANALYSIS; CONTROLLED STUDY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; TRIPLE NEGATIVE BREAST CANCER;

ANTIBODIES, NEOPLASM; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; CD8-POSITIVE T-LYMPHOCYTES; DNA METHYLATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PROGNOSIS; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SURVIVAL RATE;

EID: 84863008358     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038783     Document Type: Article

References (48)

1. (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365: 1687-1717.
2. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, et al. (2007) Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13: 4429-4434.
3. Almeida LG, Sakabe NJ, deOliveira AR, Silva MC, Mundstein AS, et al. (2009) CTdatabase: a knowledge-base of high-throughput and curated data on cancer-testis antigens. Nucleic Acids Res 37: D816-819.
4. Hofmann O, Caballero OL, Stevenson BJ, Chen YT, Cohen T, et al. (2008) Genome-wide analysis of cancer/testis gene expression. Proc Natl Acad Sci U S A 105: 20422-20427.
5. Chen YT, Ross DS, Chiu R, Zhou XK, Chen YY, et al. (2011) Multiple cancer/testis antigens are preferentially expressed in hormone-receptor negative and high-grade breast cancers. PLoS One 6: e17876.
6. Grigoriadis A, Caballero OL, Hoek KS, da Silva L, Chen YT, et al. (2009) CT-X antigen expression in human breast cancer. Proc Natl Acad Sci U S A 106: 13493-13498.
7. Hamai A, Duperrier-Amouriaux K, Pignon P, Raimbaud I, Memeo L, et al. (2011) Antibody responses to NY-ESO-1 in primary breast cancer identify a subtype target for immunotherapy. PLoS One 6: e21129.
8. Mischo A, Kubuschok B, Ertan K, Preuss KD, Romeike B, et al. (2006) Prospective study on the expression of cancer testis genes and antibody responses in 100 consecutive patients with primary breast cancer. Int J Cancer 118: 696-703.
9. Theurillat JP, Ingold F, Frei C, Zippelius A, Varga Z, et al. (2007) NY-ESO-1 protein expression in primary breast carcinoma and metastases: correlation with CD8+ T-cell and CD79a+ plasmacytic/B-cell infiltration. Int J Cancer 120: 2411-2417.
10. Jager E, Chen YT, Drijfhout JW, Karbach J, Ringhoffer M, et al. (1998) Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187: 265-270.
11. Valmori D, Dutoit V, Lienard D, Rimoldi D, Pittet MJ, et al. (2000) Naturally occurring human lymphocyte antigen-A2 restricted CD8+ T-cell response to the cancer testis antigen NY-ESO-1 in melanoma patients. Cancer Res 60: 4499-4506.
12. Nicholaou T, Chen W, Davis ID, Jackson HM, Dimopoulos N, et al. (2011) Immunoediting and persistence of antigen-specific immunity in patients who have previously been vaccinated with NY-ESO-1 protein formulated in ISCOMATRIX. Cancer Immunol Immunother.
13. Kakimi K, Isobe M, Uenaka A, Wada H, Sato E, et al. (2011) A phase I study of vaccination with NY-ESO-1f peptide mixed with Picibanil OK-432 and Montanide ISA-51 in patients with cancers expressing the NY-ESO-1 antigen. Int J Cancer.
14. Gnjatic S, Altorki NK, Tang DN, Tu SM, Kundra V, et al. (2009) NY-ESO-1 DNA vaccine induces T-cell responses that are suppressed by regulatory T cells. Clin Cancer Res 15: 2130-2139.
15. Odunsi K, Qian F, Matsuzaki J, Mhawech-Fauceglia P, Andrews C, et al. (2007) Vaccination with an NY-ESO-1 peptide of HLA class I/II specificities induces integrated humoral and T cell responses in ovarian cancer. Proc Natl Acad Sci U S A 104: 12837-12842.
16. Bender A, Karbach J, Neumann A, Jager D, Al-Batran SE, et al. (2007) LUD 00-009: phase 1 study of intensive course immunization with NY-ESO-1 peptides in HLA-A2 positive patients with NY-ESO-1-expressing cancer. Cancer Immun 7: 16.
17. Jager E, Nagata Y, Gnjatic S, Wada H, Stockert E, et al. (2000) Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral and cellular immune responses. Proc Natl Acad Sci U S A 97: 4760-4765.
18. Ambrosone CB, Nesline MK, Davis W, (2006) Establishing a cancer center data bank and biorepository for multidisciplinary research. Cancer Epidemiol Biomarkers Prev 15: 1575-1577.
19. Odunsi K, Jungbluth AA, Stockert E, Qian F, Gnjatic S, et al. (2003) NY-ESO-1 and LAGE-1 cancer-testis antigens are potential targets for immunotherapy in epithelial ovarian cancer. Cancer Res 63: 6076-6083.
20. Jungbluth AA, Chen YT, Stockert E, Busam KJ, Kolb D, et al. (2001) Immunohistochemical analysis of NY-ESO-1 antigen expression in normal and malignant human tissues. Int J Cancer 92: 856-860.
21. Gnjatic S, Ritter E, Buchler MW, Giese NA, Brors B, et al. (2010) Seromic profiling of ovarian and pancreatic cancer. Proc Natl Acad Sci U S A 107: 5088-5093.
22. Woloszynska-Read A, Mhawech-Fauceglia P, Yu J, Odunsi K, Karpf AR, (2008) Intertumor and intratumor NY-ESO-1 expression heterogeneity is associated with promoter-specific and global DNA methylation status in ovarian cancer. Clin Cancer Res 14: 3283-3290.
23. Lethe B, Lucas S, Michaux L, De Smet C, Godelaine D, et al. (1998) LAGE-1, a new gene with tumor specificity. Int J Cancer 76: 903-908.
24. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, et al. (1996) The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc Natl Acad Sci U S A 93: 7149-7153.
25. Urban JL, Schreiber H, (1992) Tumor antigens. Annu Rev Immunol 10: 617-644.
26. Houghton AN, (1994) Cancer antigens: immune recognition of self and altered self. J Exp Med 180: 1-4.
27. Sugita Y, Wada H, Fujita S, Nakata T, Sato S, et al. (2004) NY-ESO-1 expression and immunogenicity in malignant and benign breast tumors. Cancer Res 64: 2199-2204.
28. Mashino K, Sadanaga N, Tanaka F, Yamaguchi H, Nagashima H, et al. (2001) Expression of multiple cancer-testis antigen genes in gastrointestinal and breast carcinomas. Br J Cancer 85: 713-720.
29. Sahin U, Tureci O, Chen YT, Seitz G, Villena-Heinsen C, et al. (1998) Expression of multiple cancer/testis (CT) antigens in breast cancer and melanoma: basis for polyvalent CT vaccine strategies. Int J Cancer 78: 387-389.
30. Curigliano G, Viale G, Ghioni M, Jungbluth AA, Bagnardi V, et al. (2011) Cancer-testis antigen expression in triple-negative breast cancer. Ann Oncol 22: 98-103.
31. Tanja BC, Giulio S, Antonio J, Jasminka JR, Paula P, et al. (2011) High expression of MAGE-A10 cancer-testis antigen in triple-negative breast cancer. Med Oncol.
32. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, et al. (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348: 203-213.
33. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, et al. (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 102: 18538-18543.
34. Nosho K, Baba Y, Tanaka N, Shima K, Hayashi M, et al. (2010) Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol 222: 350-366.
35. Horne ZD, Jack R, Gray ZT, Siegfried JM, Wilson DO, et al. (2011) Increased levels of tumor-infiltrating lymphocytes are associated with improved recurrence-free survival in stage 1A non-small-cell lung cancer. J Surg Res 171: 1-5.
36. Taylor RC, Patel A, Panageas KS, Busam KJ, Brady MS, (2007) Tumor-infiltrating lymphocytes predict sentinel lymph node positivity in patients with cutaneous melanoma. J Clin Oncol 25: 869-875.
37. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, et al. (2011) Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 29: 1949-1955.
38. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, et al. (2011) Tumor infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 13: R126.
39. Fang F, Balch C, Schilder J, Breen T, Zhang S, et al. (2010) A phase 1 and pharmacodynamic study of decitabine in combination with carboplatin in patients with recurrent, platinum-resistant, epithelial ovarian cancer. Cancer 116: 4043-4053.
40. Stockert E, Jager E, Chen YT, Scanlan MJ, Gout I, et al. (1998) A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J Exp Med 187: 1349-1354.
41. Gnjatic S, Atanackovic D, Jager E, Matsuo M, Selvakumar A, et al. (2003) Survey of naturally occurring CD4+ T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses. Proc Natl Acad Sci U S A 100: 8862-8867.
42. Nakayama E, Uenaka A, (1985) Effect of in vivo administration of Lyt antibodies. Lyt phenotype of T cells in lymphoid tissues and blocking of tumor rejection. J Exp Med 161: 345-355.
43. Greenwald RJ, Freeman GJ, Sharpe AH, (2005) The B7 family revisited. Annu Rev Immunol 23: 515-548.
44. del Rio ML, Penuelas-Rivas G, Dominguez-Perles R, Ramirez P, Parrilla P, et al. (2005) Antibody-mediated signaling through PD-1 costimulates T cells and enhances CD28-dependent proliferation. Eur J Immunol 35: 3545-3560.
45. Shin T, Yoshimura K, Crafton EB, Tsuchiya H, Housseau F, et al. (2005) In vivo costimulatory role of B7-DC in tuning T helper cell 1 and cytotoxic T lymphocyte responses. J Exp Med 201: 1531-1541.
46. Ghebeh H, Mohammed S, Al-Omair A, Qattan A, Lehe C, et al. (2006) The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors. Neoplasia 8: 190-198.
47. Grosso JF, Kelleher CC, Harris TJ, Maris CH, Hipkiss EL, et al. (2007) LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems. J Clin Invest 117: 3383-3392.
48. Yuan J, Adamow M, Ginsberg BA, Rasalan TS, Ritter E, et al. (2011) Integrated NY-ESO-1 antibody and CD8+ T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci U S A 108: 16723-16728.