T cell responses against microsatellite instability-induced frameshift peptides and influence of regulatory T cells in colorectal cancer

Cancer Immunology, Immunotherapy

Volumn 62, Issue 1, 2013, Pages 27-37

  Bauer, Kathrin ^a,b   Nelius, Nina ^a,b   Reuschenbach, Miriam ^a,b   Koch, Moritz ^a   Weitz, Jürgen ^a   Steinert, Gunnar ^a   Kopitz, Jürgen ^a,b   Beckhove, Philipp ^b   Tariverdian, Mirjam ^a   Von Knebel Doeberitz, Magnus ^a,b   Kloor, Matthias ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Colorectal cancer; Frameshift peptides; High level microsatellite instability; Immune response; Regulatory T cells

Indexed keywords

FRAMESHIFT PEPTIDE; MUCIN 1; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIGEN DETECTION; ANTIGEN SPECIFICITY; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL SPECIFICITY; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; EFFECTOR CELL; ENZYME LINKED IMMUNOSPOT ASSAY; FRAMESHIFT MUTATION; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; MICROSATELLITE INSTABILITY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; TUMOR ASSOCIATED LEUKOCYTE;

ADULT; AGED; ANTIGENS, NEOPLASM; COLORECTAL NEOPLASMS; FEMALE; FLOW CYTOMETRY; FRAMESHIFT MUTATION; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY;

EID: 84872489426     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-012-1303-8     Document Type: Article

References (39)

1. Thibodeau SN, Bren G, Schaid D (1993) Microsatellite instability in cancer of the proximal colon. Science 260(5109):816-819
2. Lynch HT, de la Chapelle A (2003) Hereditary colorectal cancer. N Engl J Med 348(10):919-932
3. Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87(2):159-170
4. Saeterdal I, Bjorheim J, Lislerud K, Gjertsen MK, Bukholm IK, Olsen OC, Nesland JM, Eriksen JA, Moller M, Lindblom A, Gaudernack G (2001) Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer. Proc Natl Acad Sci USA 98(23):13255-13260
5. Smyrk TC, Watson P, Kaul K, Lynch HT (2001) Tumor-infiltrating lymphocytes are a marker for microsatellite instability in colorectal carcinoma. Cancer 91(12):2417-2422
6. Dolcetti R, Viel A, Doglioni C, Russo A, Guidoboni M, Capozzi E, Vecchiato N, Macri E, Fornasarig M, Boiocchi M (1999) High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability. Am J Pathol 154(6):1805-1813
7. Phillips SM, Banerjea A, Feakins R, Li SR, Bustin SA, Dorudi S (2004) Tumour-infiltrating lymphocytes in colorectal cancer with microsatellite instability are activated and cytotoxic. Br J Surg 91(4):469-475
8. Schwitalle Y, Kloor M, Eiermann S, Linnebacher M, Kienle P, Knaebel HP, Tariverdian M, Benner A, von Knebel Doeberitz M (2008) Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers. Gastroenterology 134(4):988-997
9. Reuschenbach M, Kloor M, Morak M, Wentzensen N, Germann A, Garbe Y, Tariverdian M, Findeisen P, Neumaier M, Holinski-Feder E, von Knebel Doeberitz M (2010) Serum antibodies against frameshift peptides in microsatellite unstable colorectal cancer patients with Lynch syndrome. Fam Cancer 9(2):173-179
10. Saeterdal I, Gjertsen MK, Straten P, Eriksen JA, Gaudernack G (2001) A TGF betaRII frameshift-mutation-derived CTL epitope recognised by HLA-A2-restricted CD8+ T cells. Cancer Immunol Immunother 50(9):469-476
11. Ishikawa T, Fujita T, Suzuki Y, Okabe S, Yuasa Y, Iwai T, Kawakami Y (2003) Tumor-specific immunological recognition of frameshift-mutated peptides in colon cancer with microsatellite instability. Cancer Res 63(17):5564-5572
12. Kloor M, Michel S, Buckowitz B, Ruschoff J, Buttner R, Holinski-Feder E, Dippold W, Wagner R, Tariverdian M, Benner A, Schwitalle Y, Kuchenbuch B, von Knebel Doeberitz M (2007) Beta2-microglobulin mutations in microsatellite unstable colorectal tumors. Int J Cancer 121(2):454-458
13. Michel S, Linnebacher M, Alcaniz J, Voss M, Wagner R, Dippold W, Becker C, von Knebel Doeberitz M, Ferrone S, Kloor M (2010) Lack of HLA class II antigen expression in microsatellite unstable colorectal carcinomas is caused by mutations in HLA class II regulatory genes. Int J Cancer 127(4):889-898
14. Kloor M, Becker C, Benner A, Woerner SM, Gebert J, Ferrone S, von Knebel Doeberitz M (2005) Immunoselective pressure and human leukocyte antigen class I antigen machinery defects in microsatellite unstable colorectal cancers. Cancer Res 65(14):6418-6424
15. Michel S, Benner A, Tariverdian M, Wentzensen N, Hoefler P, Pommerencke T, Grabe N, von Knebel Doeberitz M, Kloor M (2008) High density of FOXP3-positive T cells infiltrating colorectal cancers with microsatellite instability. Br J Cancer 99(11):1867-1873
16. Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, Harrop R, Torkington J, Rees BI, Williams GT, Gallimore AM, Godkin AJ (2006) CD4+ CD25+ FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 1:e129
17. Sakaguchi S (2004) Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562
18. Knutson KL, Disis ML, Salazar LG (2007) CD4 regulatory T cells in human cancer pathogenesis. Cancer Immunol Immunother 56(3):271-285
19. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 4(4):330-336
20. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299(5609):1057-1061
21. Bonertz A, Weitz J, Pietsch DH, Rahbari NN, Schlude C, Ge Y, Juenger S, Vlodavsky I, Khazaie K, Jaeger D, Reissfelder C, Antolovic D, Aigner M, Koch M, Beckhove P (2009) Antigen-specific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma. J Clin Invest 119(11):3311-3321
22. Lepisto AJ, Moser AJ, Zeh H, Lee K, Bartlett D, McKolanis JR, Geller BA, Schmotzer A, Potter DP, Whiteside T, Finn OJ, Ramanathan RK (2008) A phase I/II study of a MUC1 peptide pulsed autologous dendritic cell vaccine as adjuvant therapy in patients with resected pancreatic and biliary tumors. Cancer Ther 6(B):955-964
23. Zheng C, Feng J, Lu D, Wang P, Xing S, Coll JL, Yang D, Yan X (2011) A novel anti-CEACAM5 monoclonal antibody, CC4, suppresses colorectal tumor growth and enhances NK cells-mediated tumor immunity. PLoS One 6(6):e21146
24. Woerner SM, Benner A, Sutter C, Schiller M, Yuan YP, Keller G, Bork P, Doeberitz MK, Gebert JF (2003) Pathogenesis of DNA repair-deficient cancers: a statistical meta-analysis of putative real common target genes. Oncogene 22(15):2226-2235
25. Woerner SM, Kloor M, von Knebel Doeberitz M, Gebert JF (2006) Microsatellite instability in the development of DNA mismatch repair deficient tumors. Cancer Biomark 2(1-2):69-86
26. Linnebacher M, Gebert J, Rudy W, Woerner S, Yuan YP, Bork P, von Knebel Doeberitz M (2001) Frameshift peptide-derived T-cell epitopes: a source of novel tumor-specific antigens. Int J Cancer 93(1):6-11
27. Schwitalle Y, Linnebacher M, Ripberger E, Gebert J, von Knebel Doeberitz M (2004) Immunogenic peptides generated by frameshift mutations in DNA mismatch repair-deficient cancer cells. Cancer Immun 4:14
28. Ullenhag GJ, Frodin JE, Jeddi-Tehrani M, Strigard K, Eriksson E, Samanci A, Choudhury A, Nilsson B, Rossmann ED, Mosolits S, Mellstedt H (2004) Durable carcinoembryonic antigen (CEA)-specific humoral and cellular immune responses in colorectal carcinoma patients vaccinated with recombinant CEA and granulocyte/macrophage colony-stimulating factor. Clin Cancer Res 10(10):3273-3281
29. Lesterhuis WJ, De Vries IJ, Schreibelt G, Schuurhuis DH, Aarntzen EH, De Boer A, Scharenborg NM, Van de Rakt M, Hesselink EJ, Figdor CG, Adema GJ, Punt CJ (2010) Immunogenicity of dendritic cells pulsed with CEA peptide or transfected with CEA mRNA for vaccination of colorectal cancer patients. Anticancer Res 30(12):5091-5097
30. Findeisen P, Kloor M, Merx S, Sutter C, Woerner SM, Dostmann N, Benner A, Dondog B, Pawlita M, Dippold W, Wagner R, Gebert J, von Knebel Doeberitz M (2005) T25 repeat in the 3′ untranslated region of the CASP2 gene: a sensitive and specific marker for microsatellite instability in colorectal cancer. Cancer Res 65(18):8072-8078
31. Ryan SO, Vlad AM, Islam K, Gariepy J, Finn OL (2009) Tumor-associated MUC1 glycopeptide epitopes are not subject to self-tolerance and improve responses to MUC1 peptide epitopes in MUC1 transgenic mice. Biol Chem 390(7):611-618
32. Marshall J (2003) Carcinoembryonic antigen-based vaccines. Semin Oncol 30(3 Suppl 8):30-36
33. Hammarstrom S (1999) The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin Cancer Biol 9(2):67-81
34. Molling JW, de Gruijl TD, Glim J, Moreno M, Rozendaal L, Meijer CJ, van den Eertwegh AJ, Scheper RJ, von Blomberg ME, Bontkes HJ (2007) CD4 (+) CD25hi regulatory T-cell frequency correlates with persistence of human papillomavirus type 16 and T helper cell responses in patients with cervical intraepithelial neoplasia. Int J Cancer 121(8):1749-1755
35. Speetjens FM, Lauwen MM, Franken KL, van Janssen-Rhijn CM, van Duikeren S, Bres SA, van de Velde CJ, Melief CJ, Kuppen PJ, van der Burg SH, Morreau H, Offringa R (2008) Prediction of the immunogenic potential of frameshift-mutated antigens in microsatellite instable cancer. Int J Cancer 123(4):838-845
36. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S (1999) SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50(3-4):213-219
37. Barnetson R, Jass J, Tse R, Eckstein R, Robinson B, Schnitzler M (2000) Mutations associated with microsatellite unstable colorectal carcinomas exhibit widespread intratumoral heterogeneity. Genes Chromosomes Cancer 29(2):130-136
38. Urban JL, Kripke ML, Schreiber H (1986) Stepwise immunologic selection of antigenic variants during tumor growth. J Immunol 137(9):3036-3041
39. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3(11):991-998