Leukocyte infiltrate in gastrointestinal adenocarcinomas is strongly associated with tumor microsatellite instability but not with tumor immunogenicity

Cancer Immunology, Immunotherapy

Volumn 60, Issue 6, 2011, Pages 869-882

  Bernal, Mónica ^a   Concha, Angel ^a   Sáenz López, Pablo ^a   Rodríguez, Ana Isabel ^a   Cabrera, Teresa ^a,b   Garrido, Federico ^a,b   Ruiz Cabello, Francisco ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Gastrointestinal adenocarcinomas (GIACs); HLA class I; Microsatellite instability (MSI); Tumor leukocyte infiltrate

Indexed keywords

BETA 2 MICROGLOBULIN; CD8 ANTIGEN; GALECTIN 3; HLA ANTIGEN CLASS 1; PROGRAMMED DEATH 1 LIGAND 1;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER STAGING; CD8+ T LYMPHOCYTE; CELL COMPOSITION; CELL DENSITY; CELL INFILTRATION; CELL SURFACE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; COLORECTAL CARCINOMA; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; GASTROINTESTINAL CARCINOMA; GENE SEQUENCE; HUMAN; HUMAN TISSUE; IMMUNOGENICITY; LEUKOCYTE; MACROPHAGE; MALE; MICROSATELLITE INSTABILITY; MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SMALL INTESTINE CARCINOMA; TUMOR LOCALIZATION; UPREGULATION;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; BETA 2-MICROGLOBULIN; DOWN-REGULATION; FEMALE; GALECTIN 3; GASTROINTESTINAL NEOPLASMS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; NEOPLASM STAGING; TREATMENT OUTCOME;

EID: 79959763400     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-0999-1     Document Type: Article

References (57)

1. GP Dunn LJ Old RD Schreiber 2004 The immunobiology of cancer immunosurveillance and immunoediting Immunity 21 137 148 (Pubitemid 39094044)
2. MJ Smyth GP Dunn RD Schreiber 2006 Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity Adv Immunol 90 1 50 (Pubitemid 43765795)
3. JD Bui RD Schreiber 2007 Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr Opin Immunol 19 203 208 (Pubitemid 46356963)
4. PF Robbins Y Kawakami 1996 Human tumor antigens recognized by T cells Curr Opin Immunol 8 628 636 (Pubitemid 26385390)
5. T Boon PG Coulie BJ Van den Eynde P Van der Bruggen 2006 Human T cell responses against melanoma Annu Rev Immunol 24 175 208
6. M Philip DA Rowley H Schreiber 2004 Inflammation as a tumor promoter in cancer induction Semin Cancer Biol 14 433 439 (Pubitemid 39360991)
7. KE de Visser A Eichten LM Coussens 2006 Paradoxical roles of the immune system during cancer development Nat Rev Cancer 6 24 37 (Pubitemid 43053650)
8. C Lengauer KW Kinzler B Vogelstein 1998 Genetic instabilities in human cancers Nature 396 643 649 (Pubitemid 29003936)
9. M Perucho 2003 Tumors with microsatellite instability: many mutations, targets and paradoxes Oncogene 22 2223 2225 (Pubitemid 36566778)
10. R Dolcetti A Viel C Doglioni A Russo M Guidoboni E Capozzi N Vecchiato E Macrì M Fornasarig M Boiocchi 1999 High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability Am J Pathol 154 1805 1813 (Pubitemid 29262862)
11. TC Smyrk P Watson K Kaul HT Lynch 2001 Tumor-infiltrating lymphocytes are a marker for microsatellite instability in colorectal carcinoma Cancer 91 2417 2422 (Pubitemid 32552830)
12. M Linnebacher J Gebert W Rudy S Woerner YP Yuan P Bork M von Knebel Doeberitz 2001 Frameshift peptide-derived T-cell epitopes: a source of novel tumor-specific antigens Int J Cancer 93 6 11 (Pubitemid 32539494)
13. I Saeterdal J Bjørheim K Lislerud MK Gjertsen IK Bukholm OC Olsen JM Nesland JA Eriksen M Møller A Lindblom G Gaudernack 2001 Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer Proc Natl Acad Sci USA 98 13255 13260 (Pubitemid 33051349)
14. B Seliger T Cabrera F Garrido S Ferrone 2002 HLA class I antigen abnormalities and immune escape by malignant cells Semin Cancer Biol 12 3 13 (Pubitemid 34087893)
15. W Peng HY Wang Y Miyahara G Peng RF Wan 2008 Tumor-Associated Galectin-3 modulates the function of tumor-reactive T cells Cancer Res 68 7228 7236
16. GJ Freeman AJ Long Y Iwai K Bourque T Chernova H Nishimura LJ Fitz N Malenkovich T Okazaki MC Byrne HF Horton L Fouser, et al. 2000 Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation J Exp Med 192 1027 1034
17. W Zou 2005 Immunosuppressive networks in the tumour environment and their therapeutic relevance Nat Rev Cancer 5 263 274 (Pubitemid 40488632)
18. A Sica P Allavena A Mantovani 2008 Cancer related inflammation: the macrophage connection Cancer Lett 267 204 215
19. F Pagès A Berger M Camus F Sanchez-Cabo A Costes R Molidor B Mlecnik A Kirilovsky M Nilsson D Damotte T Meatchi P Bruneval PH Cugnenc Z Trajanoski WH Fridman J Galon 2005 Effector memory T cells, early metastasis, and survival in colorectal cancer N Engl J Med 353 2654 2666 (Pubitemid 41817714)
20. J Galon A Costes F Sanchez-Cabo A Kirilovsky B Mlecnik C Lagorce-Pagès M Tosolini M Camus A Berger P Wind F Zinzindohoué P Bruneval PH Cugnenc Z Trajanoski WH Fridman F Pagès 2006 Type, density, and location of immune cells within human colorectal tumors predict clinical outcome Science 313 1960 1964 (Pubitemid 44498003)
21. P Allavena A Sica C Garlanda A Mantovani 2008 The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance Immunol Rev 222 155 161 (Pubitemid 351430369)
22. Sobin L, Gospodarowiaz M, Wittekind CH (2009) TNM classification of malignant tumours UICC, 7th edn. Wiley, Blackwell
23. MA López Nevot T Cabrera B de la Higuera F Ruiz-Cabello F Ga-rrido 1986 Obtención y caracterización de anticuerpos monoclonales frente a leucemias humanas Inmunología 5 51 59
24. NJ Stam H Spits HL Ploegh 1986 Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products J Immunol 137 2299 2306 (Pubitemid 16020728)
25. C Huelin M Gonzalez S Pedrinaci B de la Higuera MA Piris J San Miguel F Ruiz-Cabello F Garrido 1988 Distribution of the CD45R antigen in the maturation of lymphoid and myeloid seri-es.- The CD45R negative phenotype is a constant finding in T CD4 positive lympho-proliferative disor-ders British J Haematol 69 173 179
26. CR Boland SN Thibodeau SR Hamilton D Sidransky JR Eshleman RW Burt SJ Meltzer MA Rodriguez-Bigas R Fodde GN Ranzani, et al. 1998 A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer Cancer Res 58 5248 5257 (Pubitemid 28521189)
27. M Kloor C Becker A Benner SM Woerner J Gebert S Ferrone M von Knebel Doeberitz 2005 Immunoselective pressure and human leukocyte antigen class I antigen machinery defects in microsatellite unstable colorectal cancers Cancer Res 65 6418 6424 (Pubitemid 40994430)
28. I Maleno CM Cabrera T Cabrera L Paco MA López-Nevot A Collado A Ferrón F Garrido 2004 Distribution of HLA class I altered phenotypes in colorectal carcinomas: high frequency of HLA haplotype loss associated with loss of heterozygosity in chromosome region 6p21 Immunogenetics 56 244 253 (Pubitemid 39119279)
29. CM Cabrera P Jiménez T Cabrera C Esparza F Ruiz-Cabello F Garrido 2003 Total loss of MHC class I in colorectal tumors can be explained by two molecular pathways: beta2-microglobulin inactivation in MSI-positive tumors and LMP7/TAP2 downregulation in MSI-negative tumors Tissue Antigens 61 211 219 (Pubitemid 36605543)
30. JW Dierssen NF de Miranda S Ferrone M van Puijenbroek CJ Cornelisse GJ Fleuren T van Wezel H Morreau 2007 HNPCC versus sporadic microsatellite-unstable colon cancers follow different routes toward loss of HLA class I expression BMC Cancer 7 33
31. F Garrido F Ruiz-Cabello T Cabrera, et al. 1997 Implications for immunosurveillance of altered HLA class I phenotypes in human tumours Immunol Today 18 89 95 (Pubitemid 27107103)
32. FM Marincola E Jaffee D Hicklin, et al. 2000 Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance Adv Immunol 74 181 273
33. CG Drake E Jaffee DM Pardoll 2006 Mechanisms of immune evasion by tumors Adv Immunol 90 51 81 (Pubitemid 43765799)
34. CM D'Urso ZG Wang Y Cao R Tatake RA Zeff S Ferrone 1991 Lack of HLA class I antigen expression by cultured melanoma cells FO-1 due to a defect in B2m gene expression J Clin Invest 87 284 292
35. NP Restifo FM Marincola Y Kawakami J Taubenberger JR Yannelli SA Rosenberg 1996 Loss of functional beta 2-microglobulin in metastatic melanomas from five patients receiving immunotherapy J Natl Cancer Inst 88 100 108
36. R Benitez D Godelaine MA Lopez-Nevot F Brasseur P Jiménez M Marchand MR Oliva N van Baren T Cabrera G Andry C Landry F Ruiz-Cabello, et al. 1998 Mutations of the beta2-microglobulin gene result in a lack of HLA class I molecules on melanoma cells of two patients immunized with MAGE peptides Tissue Antigens 52 520 529 (Pubitemid 29002755)
37. A Paschen RM Méndez P Jiménez A Sucker F Ruiz-Cabello F Garrido D Schadendorf 2003 Complete loss of HLA class I antigen expression on melanoma cells: a result of successive mutational events Int J Cancer 103 759 767 (Pubitemid 36110232)
38. B Seliger A Hohne A Knuth H Bernhard B Ehring R Tampe C Huber 1996 Reduced membrane major histocompatibility complex class I density and stability in a subset of human renal cell carcinomas with low TAP and LMP expression Clin Cancer Res 2 1427 1433 (Pubitemid 26299444)
39. Q Ye Y Shen X Wang J Yang F Miao C Shen J Zhang 2010 Hypermethylation of HLA class I gene is associated with HLA class I down-regulation in human gastric cancer Tissue Antigens 75 30 39
40. M Kloor S Michel B Buckowitz J Rüschoff R Büttner E Holinski-Feder W Dippold R Wagner M Tariverdian A Benner Y Schwitalle B Kuchenbuch, et al. 2007 Beta2-microglobulin mutations in microsatellite unstable colorectal tumors Int J Cancer 121 454 458 (Pubitemid 46917717)
41. Y Schwitalle M Linnebacher E Ripberger J Gebert M von Knebel Doeberitz 2004 Immunogenic peptides generated by frameshift mutations in DNA mismatch repair-deficient cancer cells Cancer Immun 4 14
42. M Kloor S Michel M von Knebel Doeberitz 2010 Immune evasion of microsatellite unstable colorectal cancers Int J Cancer 127 1001 1010
43. M Guidoboni R Gafà A Viel C Doglioni A Russo A Santini L Del Tin E Macrí G Lanza M Boiocchi R Dolcetti 2001 Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favourable prognosis Am J Pathol 159 297 304 (Pubitemid 33704214)
44. SM Phillips A Banerjea R Feakins SR Li SA Bustin S Dorudi 2004 Tumour-infiltrating lymphocytes in colorectal cancer with microsatellite instability are activated and cytotoxic Br J Surg 91 469 475 (Pubitemid 38491119)
45. A Banerjea S Ahmed RE Hands F Huang X Han PM Shaw R Feakins SA Bustin S Dorudi 2004 Colorectal cancers with microsatellite instability display mRNA expression signatures characteristic of increased immunogenicity Mol Cancer 3 21
46. MH Sandel FM Speetjens AG Menon PA Albertsson PH Basse M Hokland JF Nagelkerke RA Tollenaar CJ van de Velde PJ Kuppen 2005 Natural killer cells infiltrating colorectal cancer and MHC class I expression Mol Immunol 42 541 546 (Pubitemid 39655966)
47. JM Cozar J Canton M Tallada A Concha T Cabrera F Garrido F Ruiz-Cabello Osuna 2005 Analysis of NK cells and chemokine receptors in tumor infiltrating CD4 T lymphocytes in human renal carcinomas Cancer Immunol Immunother 54 858 866 (Pubitemid 40991328)
48. J Forssell A Oberg ML Henriksson R Stenling A Jung R Palmqvist 2007 High macrophage infiltration along the tumor front correlates with improved survival in colon cancer Clin Cancer Res 13 1472 1479 (Pubitemid 46450437)
49. C Murdoch M Muthana SB Coffelt CE Lewis 2008 The role of myeloid cells in the promotion of tumor angiogenesis Nat Rev Cancer 8 618 631
50. BZ Qian JW Pollard 2010 Macrophage diversity enhances tumor progression and metastasis Cell 141 39 51
51. P Nangia-Makker V Balan A Raz 2008 Regulation of tumor progression by extracellular galectin-3 Cancer Microenviron 1 43 51
52. H Lahm S Andre A Hoeflich, et al. 2001 Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures J Cancer Res Clin Oncol 127 375 386 (Pubitemid 32453680)
53. R Lotan Y Matsushita D Ohannesian, et al. 1991 Lactose binding lectin expression in human colorectal carcinomas. Relation to tumor progression Carbohydr Res 213 47 57
54. J Miyazaki R Hokari S Kato, et al. 2002 Increased expression of galectin-3 in primary gastric cancer and the metastatic lymph nodes Oncol Rep 9 1307 1312
55. H Dong SE Strome DR Salomao H Tamura F Hirano DB Flies PC Roche J Lu G Zhu K Tamada VA Lennon E Celis, et al. 2002 Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion Nat Med 8 793 800
56. Shi F, Shi M, Zeng Z, Qi RZ, Liu ZW, Zhang JY, Yang YP, Tien P, Wang FS (2010) PD-1 and PDL-1 upregulation promotes CD8(+) T-cell apoptosis and postoperative recurrence in hepatocellular carcinoma patients. Int J Cancer. [Epub ahead of print] PubMed PMID: 20473887
57. M Muhlbauer M Fleck C Schutz T Weiss M Froh C Blank J Scholmerich C Hellerbrand 2006 PDL-1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis J Hepatol 45 520 528 (Pubitemid 44307379)