Major histocompatibility complex class i expression impacts on patient survival and type and density of immune cells in biliary tract cancer

British Journal of Cancer

Volumn 113, Issue 9, 2015, Pages 1343-1349

  Goeppert, Benjamin ^a   Frauenschuh, Lena ^a   Zucknick, Manuela ^b   Roessler, Stephanie ^a   Mehrabi, Arianeb ^a   Hafezi, Mohammadreza ^a   Stenzinger, Albrecht ^a   Warth, Arne ^a   Pathil, Anita ^a   Renner, Marcus ^a   Schirmacher, Peter ^a   Weichert, Wilko ^a,b,c,d  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c National Center for Tumours   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; HLA ANTIGEN CLASS 1;

ADULT; AGED; ARTICLE; BILE DUCT CARCINOMA; CANCER GRADING; CANCER INFILTRATION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLS BY BODY ANATOMY; FEMALE; GALLBLADDER CARCINOMA; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; INFLAMMATORY INFILTRATE; MACROPHAGE; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROBABILITY; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; T LYMPHOCYTE; TUMOR INVASION; VERY ELDERLY; ADENOCARCINOMA; GALLBLADDER TUMOR; HEPATOBILIARY SYSTEM; IMMUNOLOGY; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; TUMOR ASSOCIATED LEUKOCYTE;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; BILIARY TRACT; FEMALE; GALLBLADDER NEOPLASMS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; PROGNOSIS;

EID: 84946497307     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.337     Document Type: Article

References (49)

1. Boon T, Cerottini JC, Van den Eynde B, van der Bruggen P, Van Pel A (1994) Tumour antigens recognized by T lymphocytes. Annu Rev Immunol 12: 337-365.
2. Bosman FT, Carneiro F, Hruban RH, Theise ND (2010) WHO Classification of Tumours of the Digestive System. 4th edn (International Agency for Research on Cancer (IARC).
3. Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, Waterhouse D, Ready N, Gainor J, Aren Frontera O, Havel L, Steins M, Garassino MC, Aerts JG, Domine M, Paz-Ares L, Reck M, Baudelet C, Harbison CT, Lestini B, Spigel DR (2015) Nivolumab versus Docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373(2): 123-135.
4. Cabrera T, Lopez-Nevot MA, Gaforio JJ, Ruiz-Cabello F, Garrido F (2003) Analysis of HLA expression in human tumour tissues. Cancer Immunol Immunother 52(1): 1-9.
5. Campoli M, Ferrone S (2008) HLA antigen changes in malignant cells: epigenetic mechanisms and biologic significance. Oncogene 27(45): 5869-5885.
6. Du C, Wang Y (2011) The immunoregulatory mechanisms of carcinoma for its survival and development. J Exp Clin Cancer Res 30: 12.
7. Dunn GP, Old LJ, Schreiber RD (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22: 329-360.
8. Errico A (2015) Melanoma: CheckMate 067-frontline nivolumab improves PFS alone or in combination with ipilimumab. Nat Rev Clin Oncol 12(8): 435.
9. Facoetti A, Nano R, Zelini P, Morbini P, Benericetti E, Ceroni M, Campoli M, Ferrone S (2005) Human leukocyte antigen and antigen processing machinery component defects in astrocytic tumours. Clin Cancer Res 11(23): 8304-8311.
10. Fukunaga A, Miyamoto M, Cho Y, Murakami S, Kawarada Y, Oshikiri T, Kato K, Kurokawa T, Suzuoki M, Nakakubo Y, Hiraoka K, Itoh T, Morikawa T, Okushiba S, Kondo S, Katoh H (2004) CD8+ tumourinfiltrating lymphocytes together with CD4+ tumour-infiltrating lymphocytes and dendritic cells improve the prognosis of patients with pancreatic adenocarcinoma. Pancreas 28(1): e26-e31.
11. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pages F (2006) Type, density, and location of immune cells within human colorectal tumours predict clinical outcome. Science 313(5795): 1960-1964.
12. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, Carcereny E, Ahn MJ, Felip E, Lee JS, Hellmann MD, Hamid O, Goldman JW, Soria JC, Dolled-Filhart M, Rutledge RZ, Zhang J, Lunceford JK, Rangwala R, Lubiniecki GM, Roach C, Emancipator K, Gandhi L. Investigators K-(2015) Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl JMed 372(21): 2018-2028.
13. Garrido F, Cabrera T, Aptsiauri N (2010) 'Hard' and 'soft' lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer 127(2): 249-256.
14. Garrido F, Ruiz-Cabello F, Cabrera T, Perez-Villar JJ, Lopez-Botet M, Duggan-Keen M, Stern PL (1997) Implications for immuno surveillance of altered HLA class I phenotypes in human tumours. Immunol Today 18(2): 89-95.
15. Goeppert B, Frauenschuh L, Zucknick M, Stenzinger A, Andrulis M, Klauschen F, Joehrens K, Warth A, Renner M, Mehrabi A, Hafezi M, Thelen A, Schirmacher P, Weichert W (2013) Prognostic impact of tumour-infiltrating immune cells on biliary tract cancer. Br J Cancer 109(10): 2665-2674.
16. Goeppert B, Konermann C, Schmidt CR, Bogatyrova O, Geiselhart L, Ernst C, Gu L, Becker N, Zucknick M, Mehrabi A, Hafezi M, Klauschen F, Stenzinger A, Warth A, Breuhahn K, Renner M,WeichertW, Schirmacher P, Plass C, Weichenhan D (2014) Global alterations of DNA methylation in cholangiocarcinoma target the Wnt signaling pathway. Hepatology 59(2): 544-554.
17. Goeppert B, Schmezer P, Dutruel C, Oakes C, Renner M, Breinig M, Warth A, Vogel MN, Mittelbronn M, Mehrabi A, Gdynia G, Penzel R, Longerich T, Breuhahn K, Popanda O, Plass C, Schirmacher P, Kern MA (2010) Downregulation of tumour suppressor A kinase anchor protein 12 in human hepatocarcinogenesis by epigenetic mechanisms. Hepatology 52(6): 2023-2033.
18. Grandis JR, Falkner DM, Melhem MF, Gooding WE, Drenning SD, Morel PA (2000) Human leukocyte antigen class I allelic and haplotype loss in squamous cell carcinoma of the head and neck: clinical and immunogenetic consequences. Clin Cancer Res 6(7): 2794-2802.
19. Han LY, Fletcher MS, Urbauer DL, Mueller P, Landen CN, Kamat AA, Lin YG, Merritt WM, Spannuth WA, Deavers MT, De Geest K, Gershenson DM, Lutgendorf SK, Ferrone S, Sood AK (2008) HLA class I antigen processing machinery component expression and intratumoural T-Cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res 14(11): 3372-3379.
20. Hezel AF, Deshpande V, Zhu AX (2010) Genetics of biliary tract cancers and emerging targeted therapies. J Clin Oncol 28(21): 3531-3540.
21. Humphreys EH, Williams KT, Adams DH, Afford SC (2010) Primary and malignant cholangiocytes undergo CD40 mediated Fas dependent apoptosis, but are insensitive to direct activation with exogenous Fas ligand. PLoS One 5(11): e14037.
22. Kaklamanis L, Gatter KC, Hill AB, Mortensen N, Harris AL, Krausa P, McMichael A, Bodmer JG, Bodmer WF (1992) Loss of HLA class-I alleles, heavy chains and beta 2-microglobulin in colorectal cancer. Int J Cancer 51(3): 379-385.
23. Kasajima A, Sers C, Sasano H, Johrens K, Stenzinger A, Noske A, Buckendahl AC, Darb-Esfahani S, Muller BM, Budczies J, Lehman A, Dietel M, Denkert C, Weichert W (2010) Down-regulation of the antigen processing machinery is linked to a loss of inflammatory response in colorectal cancer. Hum Pathol 41(12): 1758-1769.
24. Kawai O, Ishii G, Kubota K, Murata Y, Naito Y, Mizuno T, Aokage K, Saijo N, Nishiwaki Y, Gemma A, Kudoh S, Ochiai A (2008) Predominant infiltration of macrophages and CD8(+) T Cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer 113(6): 1387-1395.
25. Kirkwood JM, Butterfield LH, Tarhini AA, Zarour H, Kalinski P, Ferrone S (2012) Immunotherapy of cancer in 2012. CA Cancer J Clin 62(5): 309-335.
26. Koopman LA, Corver WE, van der Slik AR, Giphart MJ, Fleuren GJ (2000) Multiple genetic alterations cause frequent and heterogeneous human histocompatibility leukocyte antigen class I loss in cervical cancer. J Exp Med 191(6): 961-976.
27. Larkin J, Lao CD, Urba WJ, McDermott DF, Horak C, Jiang J, Wolchok JD (2015) Efficacy and safety of nivolumab in patients with BRAF V600 mutant and BRAF wild-type advanced melanoma: A pooled analysis of 4 clinical trials. JAMA Oncol 1(4): 433-440.
28. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, Ellis IO, Green AR (2011) Tumour-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 29(15): 1949-1955.
29. Meissner M, Reichert TE, Kunkel M, Gooding W, Whiteside TL, Ferrone S, Seliger B (2005) Defects in the human leukocyte antigen class I antigen processing machinery in head and neck squamous cell carcinoma: association with clinical outcome. Clin Cancer Res 11(7): 2552-2560.
30. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, Bruneval P, Trajanoski Z, Fridman WH, Pages F, Galon J (2011) Histopathologicbased prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 29(6): 610-618.
31. Natali PG, Nicotra MR, Bigotti A, Venturo I, Marcenaro L, Giacomini P, Russo C (1989) Selective changes in expression of HLA class I polymorphic determinants in human solid tumours. Proc Natl Acad Sci USA 86(17): 6719-6723.
32. Nie Y, Yang G, Song Y, Zhao X, So C, Liao J, Wang LD, Yang CS (2001) DNA hypermethylation is a mechanism for loss of expression of the HLA class I genes in human esophageal squamous cell carcinomas. Carcinogenesis 22(10): 1615-1623.
33. Norris S, Doherty DG, Curry M, McEntee G, Traynor O, Hegarty JE, O'Farrelly C (2003) Selective reduction of natural killer cells and T cells expressing inhibitory receptors for MHC class I in the livers of patients with hepatic malignancy. Cancer Immunol Immunother 52(1): 53-58.
34. Ogino T, Shigyo H, Ishii H, Katayama A, Miyokawa N, Harabuchi Y, Ferrone S (2006) HLA class I antigen down-regulation in primary laryngeal squamous cell carcinoma lesions as a poor prognostic marker. Cancer Res 66(18): 9281-9289.
35. Patel T (2011) Cholangiocarcinoma-controversies and challenges. Nat Rev Gastroenterol Hepatol 8(4): 189-200.
36. Que FG, Phan VA, Phan VH, Celli A, Batts K, LaRusso NF, Gores GJ (1999) Cholangiocarcinomas express Fas ligand and disable the Fas receptor. Hepatology 30(6): 1398-1404.
37. Rabinovich GA, Gabrilovich D, Sotomayor EM (2007) Immunosuppressive strategies that are mediated by tumour cells. Annu Rev Immunol 25: 267-296.
38. Rodriguez T, Aptsiauri N, Mendez R, Jimenez P, Ruiz-Cabello F, Garrido F (2007) Different mechanisms can lead to the same altered HLA class I phenotype in tumours. Tissue Antigens 69(Suppl 1): 259-263.
39. Ryschich E, Notzel T, Hinz U, Autschbach F, Ferguson J, Simon I, Weitz J, Frohlich B, Klar E, Buchler MW, Schmidt J (2005) Control of T-cellmediated immune response by HLA class I in human pancreatic carcinoma. Clin Cancer Res 11(2 Pt 1): 498-504.
40. Scott AM, Wolchok JD, Old LJ (2012) Antibody therapy of cancer. Nat Rev Cancer 12(4): 278-287.
41. Seliger B (2008) Molecular mechanisms of MHC class I abnormalities and APM components in human tumours. Cancer Immunol Immunother 57(11): 1719-1726.
42. Seliger B (2012) Novel insights into the molecular mechanisms of HLA class I abnormalities. Cancer Immunol Immunother 61(2): 249-254.
43. Shimonishi T, Isse K, Shibata F, Aburatani I, Tsuneyama K, Sabit H, Harada K, Miyazaki K, Nakanuma Y (2000) Up-regulation of fas ligand at early stages and down-regulation of Fas at progressed stages of intrahepatic cholangiocarcinoma reflect evasion from immune surveillance. Hepatology 32(4 Pt 1): 761-769.
44. Shimura S, Yang G, Ebara S, Wheeler TM, Frolov A, Thompson TC (2000) Reduced infiltration of tumour-associated macrophages in human prostate cancer: association with cancer progression. Cancer Res 60(20): 5857-5861.
45. Smyth MJ, Dunn GP, Schreiber RD (2006) Cancer immunosurveillance and immunoediting: The roles of immunity in suppressing tumour development and shaping tumour immunogenicity. Adv Immunol 90: 1-50.
46. Tsioulias G, Godwin TA, Goldstein MF, McDougall CJ, Ngoi SS, DeCosse JJ, Rigas B (1992) Loss of colonic HLA antigens in familial adenomatous polyposis. Cancer Res 52(12): 3449-3452.
47. Tsioulias GJ, Triadafilopoulos G, Goldin E, Papavassiliou ED, Rizos S, Bassioukas P, Rigas B (1993) Expression of HLA class I antigens in sporadic adenomas and histologically normal mucosa of the colon. Cancer Res 53(10 Suppl): 2374-2378.
48. Weber JS, O'Day S, Urba W, Powderly J, Nichol G, Yellin M, Snively J, Hersh E (2008) Phase I/II study of ipilimumab for patients with metastatic melanoma. J Clin Oncol 26(36): 5950-5956.
49. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, Rubin SC, Coukos G (2003) Intratumoural T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348(3): 203-213.