Mismatch repair gene defects in sporadic colorectal cancer enhance immune surveillance

Oncotarget

Volumn 6, Issue 41, 2015, Pages 43472-43482

  Scarpa, Marco ^a   Ruffolo, Cesare ^b   Canal, Fabio ^b   Scarpa, Melania ^a   Basato, Silvia ^c   Erroi, Francesca ^c   Fiorot, Alain ^b   Dall'Agnese, Lucia ^c   Pozza, Anna ^c   Porzionato, Andrea ^c   Castagliuolo, Ignazio ^c   Dei Tos, Angelo P ^b   Bassi, Nicolò ^b   Castoro, Carlo ^a  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b 'Ca' Foncello' Hospital   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

CD80; Colorectal cancer; Immune surveillance; Mismatch repair

Indexed keywords

B7 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; MISMATCH REPAIR PROTEIN; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER STAGING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLORECTAL CANCER; COLORECTAL SURGERY; CONTROLLED STUDY; DNA MISMATCH REPAIR DEFICIENCY; FEMALE; FLOW CYTOMETRY; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC DISORDER; GENETIC TRANSFECTION; HT 29 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOSURVEILLANCE; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; MLH1 GENE; MSH2 GENE; MSH6 GENE; PSM2 GENE; RETROSPECTIVE STUDY; RNA INTERFERENCE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TISSUE MICROARRAY; TUMOR CELL; TUMOR IMMUNITY; TUMOR INFILTRATING MONONUCLEAR CELL; BIOSYNTHESIS; COLORECTAL TUMOR; GENETICS; HT-29 CELL LINE; IMMUNOLOGY; KAPLAN MEIER METHOD; MICROSATELLITE INSTABILITY; MIDDLE AGED; MISMATCH REPAIR; MORTALITY; POLYMERASE CHAIN REACTION; TUMOR ASSOCIATED LEUKOCYTE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANTIGENS, CD80; COLORECTAL NEOPLASMS; DNA MISMATCH REPAIR; FEMALE; FLOW CYTOMETRY; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDIES; TISSUE ARRAY ANALYSIS;

EID: 84952933302     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6179     Document Type: Article

References (44)

1. Jasperson KW, Tuohy TM, Neklason DW, Burt RW. Hereditary and familial colon cancer. Gastroenterology. 2010; 138:2044-58.
2. Thibodeau SN, Bren G, Schaid D. Microsatellite instability in cancer of the proximal colon. Science. 1993; 260:816-819.
3. Peltomäki P. Deficient DNA mismatch repair: a common etiologic factor for colon cancer. Hum Mol Genet. 2001;10:735-40.
4. Cunningham JM, Christensen ER, Tester DJ, Kim CY, Roche PC, Burgart LJ, Thibodeau SN. Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res. 1998;58:3455-3460.
5. Poynter JN, Siegmund KD, Weisenberger DJ, Long TI, Thibodeau SN, Lindor N, Young J, Jenkins MA, Hopper JL, Baron JA, Buchanan D, Casey G, Levine AJ et al. Molecular characterization of MSI-H colorectal cancer by MLHI promoter methylation, immunohistochemistry, and mismatch repair germline mutation screening. Cancer Epidemiol Biomarkers Prev. 2008;17:3208-3215.
6. Sinicrope F, Foster NR, Sargent DJ, Thibodeau SN, Smyrk TC, O'Connell MJ, the North Central Cancer Treatment Group. Model-based prediction of defective DNA Mismatch Repair using clinicopathological variables in sporadic colon cancer patients. Cancer. 2010; 116:1691-8.
7. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin. 2008; 58:71-96.
8. Sinicrope FA, Rego RL, Halling KC, Foster N, Sargent DJ, La Plant B, French AJ, Laurie JA, Goldberg RM, Thibodeau SN, Witzig TE. Prognostic impact of microsatellite instability and DNA ploidy in human colon carcinoma patients. Gastroenterology. 2006;131:729-737.
9. Gafà R, Maestri I, Matteuzzi M, Santini A, Ferretti S, Cavazzini L, Lanza G. Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer. 2000; 89:2025-2037.
10. Halling KC, French AJ, McDonnell SK, Burgart LJ, Schaid DJ, Peterson BJ, Moon-Tasson L, Mahoney MR, Sargent DJ, O'Connell MJ, Witzig TE, Farr GH Jr, Goldberg RM, et al. Microsatellite instability and 8p allelic imbalance in stage B2 and C colorectal cancers. J Natl Cancer Inst. 1999;91:1295-1303.
11. Lanza G, Gafa R, Santini A, Maestri I, Guerzoni L, Cavazzini L. Immunohistochemical test for MLH1 and MSH2 expression predicts clinical outcome in stage II and III colorectal cancer patients. J Clin Oncol. 2006; 24:2359-2367.
12. Samowitz WS, Curtin K, Ma KN, Schaffer D, Coleman LW, Leppert M, Slattery ML. Microsatellite instability in sporadic colon cancer is associated with an improved prognosis at the population level. Cancer Epidemiol Biomarkers Prev. 2001; 10:917-923.
13. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol. 2005; 23:609-618.
14. Malesci A, Laghi L, Bianchi P, Delconte G, Randolph A, Torri V, Carnaghi C, Doci R, Rosati R, Montorsi M, Roncalli M, Gennari L, Santoro A. Reduced likelihood of metastases in patients with microsatellite-unstable colorectal cancer. Clin Cancer Res. 2007;13:3831-9.
15. Dunn GP, Koebel CM, Schreiber, R.D. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006;6:836-848.
16. Dolcetti R, Viel A, Doglioni C, Russo A, Guidoboni M, Capozzi E, Vecchiato N, Macrì E, Fornasarig M, Boiocchi M. High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability. Am J Pathol. 1999;154:1805-1813.
17. Sinicrope FA, Rego RL, Garrity-Park MM, Foster NR, Sargent DJ, Goldberg RM, Wiesenfeld M, Witzig TE, Thibodeau SN, Burgart LJ. Alterations in cell proliferation and apoptosis in colon cancers with microsatellite instability. Int J Cancer. 2007; 120:1232-1238.
18. Koch M, Beckhove P, Op den Winkel J, Autenrieth D, Wagner P, Nummer D, Specht S, Antolovic D, Galindo L, Schmitz-Winnenthal FH, Schirrmacher V, Büchler MW, Weitz J. Tumor infiltrating T lymphocytes in colorectal cancer: Tumor-selective activation and cytotoxic activity in situ. Ann Surg. 2006;244:986-92.
19. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005; 353:2654-66.
20. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc PH, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006; 313:1960-4.
21. Chen L, Ashe S, Brady WA, Hellström I, Hellström KE, Ledbetter JA, McGowan P, Linsley PS. Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4. Cell. 1992;71:1093-102.
22. Janeway CA, Bottomly K. Signals and signs for lymphocyte responses. Cell 1994;76:275-285.
23. Schwartz RH. A cell culture model for T lymphocyte clonal anergy. Science 1990;248:1349-1356.
24. Antonia SJ, Muñoz-Antonia T, Soldevila G, Miller J, Flavell RA. B7-1 expression by a non-antigen presenting cell-derived tumor. Cancer Res. 1995;55:2253-6.
25. Scarpa M, Cardin R, Bortolami M, Kotsafti A, Scarpa MC, Pozza A, Maran G, Picciocchi M, Ruffolo C, D'Incà R, Sturniolo GC, Castagliuolo I, Castoro C et al. Mucosal immune environment in colonic carcinogenesis: CD80 expression is associated to oxidative DNA damage and TLR4-NFκB signalling. Eur J Cancer. 2013;49:254-63.
26. Scarpa M, Behboo R, Angriman I, Cecchetto A, D'Incà R, Termini B, Barollo M, Ruffolo C, Polese L, Sturniolo GC, D'Amico DF. Expression of costimulatory molecule CD80 in colonic dysplasia in ulcerative colitis: an immunosurveillance mechanism against colorectal cancer? Int J Colorectal Dis. 2006;21:776-83.
27. Scarpa M, Bortolami M, Cecchetto A, Faggian D, Kotsafti A, Ruffolo C, Navaglia F, Pozza A, D'Incà R, Plebani M, Sturniolo GC, Angriman I. Mucosal immune environment in colonic carcinogenesis: CD80 up-regulation in colonic dysplasia in ulcerative colitis. Eur J Cancer. 2011; 47:611-9.
28. Scarpa M, Brun P, Scarpa M, Morgan S, Porzionato A, Kotsafti A, Bortolami M, Buda A, D'Incà R, Macchi V, Sturniolo GC, Rugge M, Bardini R, et al. CD80-CD28 signaling controls the progression of inflammatory colorectal carcinogenesis. Oncotarget. 2015;6:20058-69.
29. Umar A, Boland CR, Terdiman JP, Syngal S, de la Chapelle A, Rüschoff J, Fishel R, Lindor NM, Burgart LJ, Hamelin R, Hamilton SR, Hiatt RA, Jass J, et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst. 2004; 96:261-268.
30. Schlemper RJ, Riddell RH, Kato Y, Borchard F, Cooper HS, Dawsey SM, Dixon MF, Fenoglio-Preiser CM, Fléjou JF, Geboes K, Hattori T, Hirota T, Itabashi M,et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut. 2000; 47:251-5.
31. Chang CL, Marra G, Chauhan DP, Ha HT, Chang DK, Ricciardiello L, Randolph A, Carethers JM, Boland CR. Oxidative stress inactivates the human DNA mismatch repair system. Am J Physiol Cell Physiol. 2002; 283:C148-54.
32. Abken H, Hombach A, Heuser C, Kronfeld K, Seliger B: Tuning tumor-specific T-cell activation: a matter of costimulation? Trends in Immunology 2002, 23:240-245.
33. Banerjea A, Ahmed S, Hands R, Huang F, Han X, Shaw P, Feakins R, Bustin S, Dorudi S. Colorectal cancers with microsatellite instability display mRNA expression signatures characteristic of increased immunogenicity. Molecular Cancer. 2004; 3:21.
34. Ahmed D, Eide PW, Eilertsen IA, Danielsen SA, Eknæs M, Hektoen M, Lind GE, Lothe RA. Epigenetic and genetic features of 24 colon cancer cell lines. Oncogenesis. 2013 Sep 16;2:e71. doi: 10.1038/oncsis.2013.35.
35. Du XH, Liu HL, Li L, Xia SY, Ning N, Zou ZY, Teng D, Xiao CH, Li R, Xu YX. Clinical significance of immunotherapy with combined three kinds of cells for operable colorectal cancer. Tumour Biol. 2015; DOI10.1007/s13277-015-3242-4.
36. Lindor NM, Rabe K, Petersen GM, Haile R, Casey G, Baron J, Gallinger S, Bapat B, Aronson M, Hopper J, Jass J, LeMarchand L, Grove J, et al. Lower cancer incidence in Amsterdam-I criteria families without mismatch repair deficiency: familial colorectal cancer type X. JAMA. 2005; 293:1979-85.
37. Valeri N, Gasparini P, Fabbri M, Braconi C, Veronese A, Lovat F, Adair B, Vannini I, Fanini F, Bottoni A, Costinean S, Sandhu SK, Nuovo GJ et al. Modulation of mismatch repair and genomic stability by miR-155. Proc. Natl. Acad. Sci. U.S.A. 2010; 107:6982-6987.
38. Luo X, Burwinkel B, Tao S, Brenner H. MicroRNA signatures: novel biomarker for colorectal cancer? Cancer Epidemiol. Biomarkers Prev. 2011; 20:1272-1286.
39. Valeri N, Gasparini P, Braconi C, Paone A, Lovat F, Fabbri M, Sumani KM, Alder H, Amadori D, Patel T, Nuovo GJ, Fishel R, Croce CM. MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc. Natl. Acad. Sci. U.S.A. 2010; 107, 21098-21103.
40. Naito Y, Saito K, Shiiba K, Ohuchi A, Saigenji K, Nagura H, Ohtani H. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 1998; 58:3491-3494.
41. Takemoto N, Konishi F, Yamashita K, Kojima M, Furukawa T, Miyakura Y, Shitoh K, Nagai H. The Correlation of Microsatellite Instability and Tumor-infiltrating Lymphocytes in Hereditary Non-polyposis Colorectal Cancer (HNPCC) and Sporadic Colorectal Cancers: the Significance of Different Types of Lymphocyte Infiltration. Jpn J Clin Oncol. 2004; 34:90-98.
42. Braig, M; Schmitt, CA. Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res. 2006; 66: 2881-2884.
43. Lynch, MD. "How does cellular senescence prevent cancer?". DNA Cell Biol. 2006; 25: 69-78.
44. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Rev Mol Cell Biol. 2007; 8: 729-40.