Peptide epitopes from the Wilms' tumor 1 oncoprotein stimulate CD4 + and CD8+ T cells that recognize and kill human malignant mesothelioma tumor cells

Clinical Cancer Research

Volumn 13, Issue 15, 2007, Pages 4547-4555

  May, Rena J ^a   Dao, Tao ^a   Pinilla Ibarz, Javier ^a,b   Korontsvit, Tatyana ^a   Zakhaleva, Victoriya ^a   Zhang, Rong H ^a   Maslak, Peter ^a   Scheinberg, David A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA ANTIGEN CLASS 2; HLA DR ANTIGEN; MUTANT PROTEIN; WT1 PROTEIN;

ALGORITHM; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIGEN PRESENTING CELL; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN; HUMAN CELL; IMMUNOPHARMACOLOGY; MALIGNANT MESOTHELIOMA; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHROMIUM; DENDRITIC CELLS; EPITOPES; HLA-DR ANTIGENS; HUMANS; IMMUNIZATION; INTERFERON TYPE II; LEUKEMIA; MESOTHELIOMA; PEPTIDE FRAGMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR CELLS, CULTURED; WT1 PROTEINS;

EID: 34547660192     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-0708     Document Type: Article

References (49)

1. Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 1993;119:1329-41.
2. Inoue K, Ogawa H, Sonoda Y, et al. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia. Blood 1997;89:1405-12.
3. Brieger J, Weidmann E, Maurer U, Hoelzer D, Mitrou PS, Bergmann L. The Wilms' tumor gene is frequently expressed in acute myeloblastic leukemias and may provide a marker for residual blast cells detectable by PCR. Ann Oncol 1995;6:811-6.
4. Oji Y, Ogawa H, Tamaki H, et al. Expression of the Wilms' tumor gene WT1 in solid tumors and its involvement in tumor cell growth. Jpn J Cancer Res 1999;90:194-204.
5. Selikoff IJ, Hammond EC, Seidman H. Latency of asbestos disease among in sulation workers in the United States and Canada. Cancer 1980;46:2736-40.
6. van Ruth S, Baas P, Zoetmulder FA. Surgical treatment of malignant pleural mesothelioma: a review. Chest 2003;123:551-61.
7. Leigh RA, Webster I. Lymphocytic infiltration of pleural mesothelioma and its significance for survival. S Afr Med J 1982;61:1007-9.
8. Robinson BW, Robinson C, Lake RA. Localised spontaneous regression in mesothelioma - possible immunological mechanism. Lung Cancer 2001;32:197-201.
9. Hegmans JP, Hemmes A, Aerts JG, Hoogsteden HC, Lambrecht BN. Immunotherapy of murine malignant mesothelioma using tumor lysate-pulsed dendritic cells. Am J Respir Crit Care Med 2005;171:1168-77.
10. Odaka M, Sterman DH, Wiewrodt R, et al. Eradication of intraperitoneal and distant tumor by adenovirus-mediated interferon-β gene therapy is attributable to induction of systemic immunity. Cancer Res 2001;61:6201-12.
11. Amin KM, Litzky LA, Smythe WR, et al. Wilms' tumor 1 susceptibility (WT1) gene products are selectively expressed in malignant mesothelioma. Am J Pathol 1995;146:344-56.
12. Foster MR, Johnson JE, Olson SJ, Allred DC. Immunohistochemical analysis of nuclear versus cytoplasmic staining of WT1 in malignant mesotheliomas and primary pulmonary adenocarcinomas. Arch Pathol Lab Med 2001;125:1316-20.
13. Oka Y, Elisseeva OA, Tsuboi A, et al. Human cytotoxic T-lymphocyte responses specific for peptides of the wild-type Wilms' tumor gene (WT1) product. Immunogenetics 2000;51:99-107.
14. Gao L, Bellantuono I, Elsasser A, et al. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood 2000;95:2198-203.
15. Ohminami H, Yasukawa M, Fujita S. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood 2000;95:286-93.
16. Azuma T, Makita M, Ninomiya K, Fujita S, Harada M, Yasukawa M. Identification of a novel WT1-derived peptide which induces human leukocyte antigen-A24-restricted anti-leukemia cytotoxic T lymphocytes. Br J Haematol 2002;116:601-3.
17. Bellantuono I, Gao L, Parry S, et al. Two distinct HLA-A0201-presented epitopes of the Wilms tumor antigen 1can function as targets for leukemia-reactive CTL. Blood 2002;100:3835-7.
18. Doubrovina ES, Doubrovin MM, Lee S, et al. In vitro stimulation with WT1 peptide-loaded Epstein-Barr virus-positive B cells elicits high frequencies of WT1 peptide-specific T cells with in vitro and in vivo tumoricidal activity. Clin Cancer Res 2004;10:7207-19.
19. Pinilla-Ibarz J, May RJ, Korontsvit T, et al. Improved human T cell responses against synthetic HLA 0201 analogp eptides derived from the WT1 oncoprotein. Leukemia 2006;11:2025-33.
20. + T cells generated depends on the nature of the initial nonspecific stimulation. Eur J Immunol 2002;32:1541-9.
21. Mintern JD, Davey GM, Belz GT, Carbone FR, Heath WR. Cuttinge dge: precursor frequency affects the helper dependence of cytotoxic T cells. J Immunol 2002;168:977-80.
22. Wu F, Oka Y, Tsuboi A, et al. Th1-biased humoral immune responses against Wilms tumor gene WT1 product in the patients with hematopoietic malignancies. Leukemia 2005;19:268-74.
23. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999;50:213-9.
24. Khokhar NZ, Lam AF, Rusch VW, Sirotnak FM. Despite some expression of folate receptor a in human mesothelioma cells, internalization of methotrexate is predominantly carrier mediated. J Thorac Cardiovasc Surg 2002;123:862-8.
25. Adusumilli PS, Chan MK, Chun YS, et al. Cisplatin-induced GADD34 upregulation potentiates oncolytic viral therapy in the treatment of malignant pleural mesothelioma. Cancer Biol Ther 2006;5:48-53.
26. Ebstein F, Sapede C, Royer PJ, et al. Cytotoxic T cell responses against mesothelioma by apoptotic cell-pulsed dendritic cells. Am J Respir Crit Care Med 2004;169:1322-30.
27. Pinilla-Ibarz J, Korontsvit T, Zakhaleva V, Roberts W, Scheinberg DA. Synthetic peptide analogs derived from bcr/abl fusion proteins and the induction of heteroclitic human T-cell responses. Haematologica 2005;90:1324-32.
28. Cilloni D, Gottardi E, DeMicheli D, et al. Quantitative assessment of WT1 expression by real time quantitative PCR may be a useful tool for monitoring minimal residual disease in acute leukemia patients. Leukemia 2002;16:2115-21.
29. Muller L, Knights A, Pawelec G. Synthetic peptides derived from Wilms' tumor 1 protein sensitize human T lymphocytes to recognize chronicmyelogenous leukemia cells. Hematol J 2003;4:57-66.
30. + T lymphocytes in an HLA class II-restricted manner. Blood 2005;106:1415-8.
31. Kobayashi H, Nagato T, Aoki N, et al. Defining MHC class II T helper epitopes for WT1 tumor antigen. Cancer Immunol Immunother 2005;55:850-60.
32. Gillmore R, Xue SA, Holler A, et al. J. Detection of Wilms' tumor antigen-specific CTL in tumor-draining lymph nodes of patients with early breast cancer. Clin Cancer Res 2006;12:34-42.
33. Tsuboi A, Oka Y, Osaki T, et al. WT1 peptide-based immunotherapy for patients with lung cancer: report of two cases. Microbiol Immunol 2004;48:175-84.
34. Mutti L, Valle MT, Balbi B, et al. Primary human mesothelioma cells express class II MHC, ICAM-1 and B7-2 and can present recall antigens to autologous blood lymphocytes. Int J Cancer 1998;78:740-9.
35. Bae J, Martinson JA, Klingemann HG. Heteroclitic CD33 peptide with enhanced anti-acute myeloid leukemic immunogenicity. Clin Cancer Res 2004;10:7043-52.
36. + T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J Immunol 2000;165:6047-55.
37. Hung K , Hayashi R, Lafond-Walker A, Lowenstein C, Pardoll D, Levitsky H. The central role of CD4(+) T cells in the antitumor immune response. J Exp Med 1998;188:2357-68.
38. Elsawa SF, Rodeberg DA, Celis E. T-cell epitope peptide vaccines. Expert Rev Vaccines 2004;3:563-75.
39. Pawelec G, Heinzel S, Kiessling R, Muller L, Ouyang Q , Zeuthen J. Escape mechanisms in tumor immunity: a year 2000 update. Crit Rev Oncog 2000;11:97-133.
40. Scheibenbogen C, Schadendorf D, Bechrakis NE, et al. Effects of granulocyte-macrophage colony-stimulating factor and foreign helper protein as immunologic adjuvants on the T-cell response to vaccination with tyrosinase peptides. Int J Cancer 2003;104:188-94.
41. Panina-Bordignon P, Tan A, Termijtelen A, Demotz S, Corradin G, Lanzavecchia A. Universally immunogenic T cell epitopes: promiscuous binding to human MHC class II and promiscuous recognition by T cells. Eur J Immunol 1989;19:2237-42.
42. Eisenlohr LC, Yewdell JW, Bennink JR. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J Exp Med 1992;175:481-7.
43. Rezvani K, Mielke S, Kilical Y, et al. Identification of novel MHC class I and class II epitopes of WT1 using a peptide library screen. Atlanta (GA): American Society of Hematology; 2005.
44. Zwaveling S, Ferreira Mota SC, Nouta J, et al. Established human papillomavirus type 16-expressing tumors are effectively eradicated following vaccination with long peptides. J Immunol 2002;169:350-8.
45. Ahlers JD, Takeshita T, Pendleton CD, Berzofsky JA. Enhanced immunogenicity of HIV-1 vaccine construct by modification of the native peptide sequence. Proc Natl Acad Sci USA 1997;94:10856-61.
46. + class II-restricted cytotoxic T lymphocytes are contained within an influenza nucleoprotein peptide. J Immunol 1992;148:894-9.
47. Ayyoub M, Merlo A, Hesdorffer CS, et al. Distinct but overlapping T helper epitopes in the 37-58 region of SSX-2. Clin Immunol 2005;114:70-8.
48. Knutson KL, Schiffman K, Disis ML. Immunization with a HER-2/neu helper peptide vaccine generates HER-2/neu CD8 T-cell immunity in cancer patients. J Clin Invest 2001;107:477-84.
49. Southwood S, Sidney J, Kondo A, et al. Several common HLA-DR types share largely overlapping peptide bindingr epertoires. J Immunol 1998;160:3363-73.