Increased frequencies of CD8+ T lymphocytes recognizing wild-type p53-derived epitopes in peripheral blood correlate with presence of epitope loss tumor variants in patients with hepatocellular carcinoma

International Journal of Cancer

Volumn 119, Issue 12, 2006, Pages 2851-2860

  Cicinnati, Vito R ^a   Zhang, Xia ^a   Yu, Zhengya ^a   Ferencik, Stanislav ^a   Schmitz, Klaus J ^a   Dworacki, Grzegorz ^b   Kaczmarek, Elzbieta ^b   Oldhafer, Karl ^a   Frilling, Andrea ^a   Baba, Hideo A ^a   Schmid, Kurt W ^a   Grosse Wilde, Hans ^a   Broelsch, Christoph E ^a   DeLeo, Albert B ^c,d   Gerken, Guido ^a   Beckebaum, Susanne ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cytotoxic T lymphocyte; Hepatocellular carcinoma; Immunotherapy; p53; Tumor escape

Indexed keywords

CANCER VACCINE; EPITOPE; GAMMA INTERFERON; GRANZYME B; HLA A ANTIGEN; HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; PROTEIN P53; PROTEIN P53[149-157]; PROTEIN P53[264-272]; UNCLASSIFIED DRUG;

ADULT; AGED; ALLELE; ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNOLOGY; CANCER STAGING; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IMMUNOSURVEILLANCE; LIVER CELL CARCINOMA; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; WILD TYPE;

AGED; AGED, 80 AND OVER; ANTIBODIES; ANTIGENS, CD3; CARCINOMA, HEPATOCELLULAR; CD8-POSITIVE T-LYMPHOCYTES; DIMERIZATION; EPITOPES; FEMALE; FLOW CYTOMETRY; HLA-A2 ANTIGEN; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY; LIVER NEOPLASMS; MALE; MIDDLE AGED; PEPTIDE FRAGMENTS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33751571998     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22251     Document Type: Article

References (58)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
2. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 2004;127:S27-S34.
3. Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet 2003;362:1907-17.
4. Ercolani G, Grazi GL, Ravaioli M, Del GM, Gardini A, Cescon M, Varotti G, Cetta F, Cavallari A. Liver resection for hepatocellular carcinoma on cirrhosis: univariate and multivariate analysis of risk factors for intrahepatic recurrence. Ann Surg 2003;237:536-43.
5. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996;334:693-9.
6. Broelsch CE, Frilling A, Malago M. Hepatoma-resection or transplantation. Surg Clin North Am 2004;84:495-511, x.
7. Thomas MB, Zhu AX. Hepatocellular carcinoma: the need for progress. J Clin Oncol 2005;23:2892-9.
8. Takayama T, Sekine T, Makuuchi M, Yamasaki S, Kosuge T, Yamamoto J, Shimada K, Sakamoto M, Hirohashi S, Ohashi Y, Kakizoe T. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 2000;356:802-7.
9. DeLeo AB, Jay G, Appella E, Dubois GC, Law LW, Old LJ. Detection of a transformation-related antigen in chemically induced sarcomas and other transformed cells of the mouse. Proc Natl Acad Sci USA 1979;76:2420-4.
10. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991;253:49-53.
11. Staib F, Hussain SP, Hofseth LJ, Wang XW, Harris CC. TP53 and liver carcinogenesis. Hum Mutat 2003;21:201-16.
12. Wong N, Lai P, Pang E, Fung LF, Sheng Z, Wong V, Wang W, Hayashi Y, Perlman E, Yuna S, Lau JW, Johnson PJ. Genomic aberrations in human hepatocellular carcinomas of differing etiologies. Clin Cancer Res 2000;6:4000-9.
13. Lane DP, Hall PA. MDM2-arbiter of p53's destruction. Trends Biochem Sci 1997;22:372-4.
14. DeLeo AB. p53-based immunotherapy of cancer. Crit Rev Immunol 1998;18:29-35.
15. Cicinnati VR, Dworacki G, Albers A, Beckebaum S, Tuting T, Kaczmarek E, DeLeo AB. Impact of p53-based immunization on primary chemically-induced tumors. Int J Cancer 2005;113:961-70.
16. Beckebaum S, Zhang X, Chen X, Yu Z, Frilling A, Dworacki G, Grosse-Wilde H, Broelsch CE, Gerken G, Cicinnati VR. Increased levels of interleukin-10 in serum from patients with hepatocellular carcinoma correlate with profound numerical deficiencies and immature phenotype of circulating dendritic cell subsets. Clin Cancer Res 2004;10:7260-9.
17. Kotsch K, Wehling J, Kohler S, Blasczyk R. Sequencing of HLA class I genes based on the conserved diversity of the noncoding regions: sequencing-based typing of the HLA-A gene. Tissue Antigens 1997;50:178-91.
18. Theobald M, Biggs J, Dittmer D, Levine AJ, Sherman LA. Targeting p53 as a general tumor antigen. Proc Natl Acad Sci USA 1995;92:11993-7.
19. Houbiers JG, Nijman HW, van der Burg SH, Drijfhout JW, Kenemans P, van d V, Brand A, Momburg F, Kast WM, Melief CJ. In vitro induction of human cytotoxic T lymphocyte responses against peptides of mutant and wild-type p53. Eur J Immunol 1993;23:2072-7.
20. Zeh HJ, III, Leder GH, Lotze MT, Salter RD, Tector M, Stuber G, Modrow S, Storkus WJ. Flow-cytometric determination of peptide-class I complex formation. Identification of p53 peptides that bind to HLA-A2. Hum Immunol 1994;39:79-86.
21. Hoffmann TK, Nakano K, Elder EM, Dworacki G, Finkelstein SD, Appella E, Whiteside TL, DeLeo AB. Generation of T cells specific for the wild-type sequence p53(264-272) peptide in cancer patients: implications for immunoselection of epitope loss variants. J Immunol 2000;165:5938-44.
22. Hoffmann TK, Donnenberg AD, Finkelstein SD, Donnenberg VS, Friebe-Hoffmann U, Myers EN, Appella E, DeLeo AB, Whiteside TL. Frequencies of tetramer+ T cells specific for the wild-type sequence p53(264-272) peptide in the circulation of patients with head and neck cancer. Cancer Res 2002;62:3521-9.
23. Chikamatsu K, Nakano K, Storkus WJ, Appella E, Lotze MT, Whiteside TL, DeLeo AB. Generation of anti-p53 cytotoxic T lymphocytes from human peripheral blood using autologous dendritic cells. Clin Cancer Res 1999;5:1281-8.
24. Albers AE, Ferris RL, Kim GG, Chikamatsu K, DeLeo AB, Whiteside TL. Immune responses to p53 in patients with cancer: enrichment in tetramer+ p53 peptide-specific T cells and regulatory T cells at tumor sites. Cancer Immunol Immunother 2005;54:1072-81.
25. Hoffmann TK, Donnenberg VS, Friebe-Hoffmann U, Meyer EM, Rinaldo CR, DeLeo AB, Whiteside TL, Donnenberg AD. Competition of peptide-MHC class I tetrameric complexes with anti-CD3 provides evidence for specificity of peptide binding to the TCR complex. Cytometry 2000;41:321-8.
26. Kammula US, Marincola FM, Rosenberg SA. Real-time quantitative polymerase chain reaction assessment of immune reactivity in melanoma patients after tumor peptide vaccination. J Natl Cancer Inst 2000;92:1336-44.
27. Wei ML, Cresswell P. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature 1992;356:443-6.
28. Tsomides TJ, Walker BD, Eisen HN. An optimal viral peptide recognized by CD8+ T cells binds very tightly to the restricting class I major histocompatibility complex protein on intact cells but not to the purified class I protein. Proc Natl Acad Sci USA 1991;88:11276-80.
29. Simon T, Opelz G, Wiesel M, Ott RC, Susal C. Serial peripheral blood perform and granzyme B gene expression measurements for prediction of acute rejection in kidney graft recipients. Am J Transplant 2003;3:1121-7.
30. Diederichsen AC, Stenholm AC, Kronborg O, Fenger C, Jensenius JC, Zeuthen J, Christensen PB, Kristensen T. Flow cytometric investigation of immune-response-related surface molecules on human colorectal cancers. Int J Cancer 1998;79:283-7.
31. Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res 2001;61:4756-60.
32. Prince HE, York J, Jensen ER. Phenotypic comparison of the three populations of human lymphocytes defined by CD45RO and CD45RA expression. Cell Immunol 1992;145:254-62.
33. Butterfield LH Immunotherapeutic strategies for hepatocellular carcinoma. Gastroenterology 2004;127:S232-S241.
34. van der Burg SH, Menon AG, Redeker A, Bonnet MC, Drijfhout JW, Tollenaar RA, van d V, Moingeon P, Kuppen PJ, Offringa R, Melief CJ. Induction of p53-specific immune responses in colorectal cancer patients receiving a recombinant ALVAC-p53 candidate vaccine. Clin Cancer Res 2002;8:1019-27.
35. Lomas M, Liauw W, Packham D, Williams K, Kelleher A, Zaunders J, Ward R. Phase I clinical trial of a human idiotypic p53 vaccine in patients with advanced malignancy. Ann Oncol 2004;15:324-9.
36. Kuball J, Schuler M, Antunes FE, Herr W, Neumann M, Obenauer-Kutner L, Westreich L, Huber C, Wolfel T, Theobald M. Generating p53-specific cytotoxic T lymphocytes by recombinant adenoviral vector-based vaccination in mice, but not man. Gene Ther 2002;9:833-43.
37. Theobald M, Biggs J, Hernandez J, Lustgarten J, Labadie C, Sherman LA. Tolerance to p53 by A2.1-restricted cytotoxic T lymphocytes. J Exp Med 1997;185:833-41.
38. Ropke M, Hald J, Guldberg P, Zeuthen J, Norgaard L, Fugger L, Svejgaard A, Van der BS, Nijman HW, Melief CJ, Claesson MH. Spontaneous human squamous cell carcinomas are killed by a human cytotoxic T lymphocyte clone recognizing a wild-type p53-derived peptide. Proc Natl Acad Sci USA 1996;93:14704-7.
39. Gnjatic S, Cai Z, Viguier M, Chouaib S, Guillet JG, Choppin J. Accumulation of the p53 protein allows recognition by human CTL of a wild-type p53 epitope presented by breast carcinomas and melanomas. J Immunol 1998;160:328-33.
40. Hamann D, Baars PA, Rep MH, Hooibrink B, Kerkhof-Garde SR, Klein MR, van Lier RA. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med 1997;186:1407-18.
41. Altman JD, Moss PA, Goulder PJ, Barouch DH, Heyzer-Williams MG, Bell JI, McMichael AJ, Davis MM. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996;274:94-6.
42. Stuge TB, Holmes SP, Saharan S, Tuettenberg A, Roederer M, Weber JS, Lee PP Diversity and recognition efficiency of T cell responses to cancer. PLoS Med 2004;1:e28.
43. Malmberg KJ. Effective immunotherapy against cancer: a question of overcoming immune suppression and immune escape? Cancer Immunol Immunother 2004;53:879-92.
44. Whiteside TL. Immune suppression in cancer: effects on immune cells, mechanisms and future therapeutic intervention. Semin Cancer Biol 2005;16:3-15.
45. Laurent-Puig P, Flejou JF, Fabre M, Bedossa P, Belghiti J, Gayral F, Franco D. Overexpression of p53: a rare event in a large series of white patients with hepatocellular carcinoma. Hepatology 1992;16:1171-5.
46. Bourdon JC, D'Errico A, Paterlini P, Grigioni W, May E, Debuire B. p53 protein accumulation in European hepatocellular carcinoma is not always dependent on p53 gene mutation. Gastroenterology 1995;108:1176-82.
47. Marin MC, Jost CA, Brooks LA, Irwin MS, O'Nions J, Tidy JA, James N, McGregor JM, Harwood CA, Yulug IG, Vousden KH, Allday MJ et al. A common polymorphism acts as an intragenic modifier of mutant p53 behaviour. Nat Genet 2000;25:47-54.
48. Soussi T. p53 antibodies in the sera of patients with various types of cancer: a review. Cancer Res 2000;60:1777-88.
49. Vierboom MP, Nijman HW, Offringa R, van der Voort EI, van Hall T, van den Broek L, Fleuren GJ, Kenemans P, Kast WM, Melief CJ. Tumor eradication by wild-type p53-specific cytotoxic T lymphocytes. J Exp Med 1997;186:695-704.
50. Vierboom MP, Zwaveling S, Bos GMJ, Ooms M, Krietemeijer GM, Melief CJ, Offringa R. High steady-state levels of p53 are not a prerequisite for tumor eradication by wild-type p53-specific cytotoxic T lymphocytes. Cancer Res 2000;60:5508-13.
51. Sirianni N, Ha PK, Oelke M, Califano J, Gooding W, Westra W, Whiteside TL, Koch WM, Schneck JP, DeLeo A, Ferris RL. Effect of human papillomavirus-16 infection on CD8+ T-cell recognition of a wild-type sequence p53264-272 peptide in patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 2004;10:6929-37.
52. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993;75:495-505.
53. Jablkowski M, Bocian A, Bialkowska J, Bartkowiak J. A comparative study of P53/MDM2 genes alterations and P53/MDM2 proteins immunoreactivity in liver cirrhosis and hepatocellular carcinoma. J Exp Clin Cancer Res 2005;24:117-25.
54. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 2000;74:181-273.
55. Marincola FM, Wang E, Herlyn M, Seliger B, Ferrone S. Tumors as elusive targets of T-cell-based active immunotherapy. Trends Immunol 2003;24:335-42.
56. Ahmad M, Rees RC, Ali SA. Escape from immunotherapy: possible mechanisms that influence tumor regression/progression. Cancer Immunol Immunother 2004;53:844-54.
57. Le GS, Le DE, Labarriere N, Fonteneau JF, Viret C, Diez E, Jotereau F. LFA-3 co-stimulates cytokine secretion by cytotoxic T lymphocytes by providing a TCR-independent activation signal. Eur J Immunol 1998;28:1322-31.
58. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004;21:137-48.