Colorectal cancer and immunity: What we know and perspectives

World Journal of Gastroenterology

Volumn 20, Issue 14, 2014, Pages 3738-3750

  Pernot, Simon ^a   Terme, Magali ^b   Voron, Thibault ^b   Colussi, Orianne ^a   Marcheteau, Elie ^b   Tartour, Eric ^a,b   Taieb, Julien ^a,b  

^a HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

Colorectal cancer; Immunity; Immunoregulation; Immunotherapy; Vaccination

Indexed keywords

BEVACIZUMAB; CARCINOEMBRYONIC ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; CETUXIMAB; DENDRITIC CELL VACCINE; HLA ANTIGEN; INTERLEUKIN 17; MASITINIB; OXALIPLATIN; SUNITINIB; TRANSCRIPTION FACTOR FOXP3; TUMOR CELL VACCINE; ANTINEOPLASTIC AGENT; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MICROSATELLITE DNA; PDCD1 PROTEIN, HUMAN; PROGRAMMED DEATH 1 RECEPTOR;

ADAPTIVE IMMUNITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL DEATH; COLORECTAL CANCER; GENE MUTATION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOSURVEILLANCE; LYMPHOCYTE CULTURE; MACROPHAGE; MICROSATELLITE INSTABILITY; NATURAL KILLER CELL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); RECEPTOR DOWN REGULATION; SINGLE NUCLEOTIDE POLYMORPHISM; CD8+ T LYMPHOCYTE; COLORECTAL TUMOR; CYTOLOGY; IMMUNOLOGY; IMMUNOTHERAPY; INNATE IMMUNITY; LYMPHOCYTE; METABOLISM; PROCEDURES; PROGNOSIS; VACCINATION;

ANTIGENS, CD45; ANTINEOPLASTIC AGENTS; CD8-POSITIVE T-LYMPHOCYTES; COLORECTAL NEOPLASMS; CTLA-4 ANTIGEN; HLA ANTIGENS; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LYMPHOCYTES; MACROPHAGES; MICROSATELLITE REPEATS; PROGNOSIS; PROGRAMMED CELL DEATH 1 RECEPTOR; VACCINATION;

EID: 84898471811     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i14.3738     Document Type: Article

References (92)

1. Pham SM, Kormos RL, Landreneau RJ, Kawai A, Gonzalez-Cancel I, Hardesty RL, Hattler BG, Griffith BP. Solid tumors after heart transplantation: lethality of lung cancer. Ann Thorac Surg 1995; 60: 1623-1626[PMID: 8787454 DOI: 10.1016/00 03-4975(95)00120-4]
2. Frisch M, Biggar RJ, Engels EA, Goedert JJ. Association of cancer with AIDS-related immunosuppression in adults. JAMA 2001; 285: 1736-1745[PMID: 11277828]
3. Engels EA, Pfeiffer RM, Fraumeni JF, Kasiske BL, Israni AK, Snyder JJ, Wolfe RA, Goodrich NP, Bayakly AR, Clarke CA, Copeland G, Finch JL, Fleissner ML, Goodman MT, Kahn A, Koch L, Lynch CF, Madeleine MM, Pawlish K, Rao C, Williams MA, Castenson D, Curry M, Parsons R, Fant G, Lin M. Spectrum of cancer risk among US solid organ transplant recipients. JAMA 2011; 306: 1891-1901[PMID: 22045767 DOI: 10.1001/jama.2011.1592]
4. Collett D, Mumford L, Banner NR, Neuberger J, Watson C. Comparison of the incidence of malignancy in recipients of different types of organ: a UK Registry audit. Am J Transplant 2010; 10: 1889-1896[PMID: 20659094 DOI: 10.1111/ j.1600-6143.2010.03181.x]
5. Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 2007; 370: 59-67[PMID: 17617273 DOI: 10.1016/ S0140-6736(07)61050-2]
6. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001; 410: 1107-1111[PMID: 11323675 DOI: 10.1038/35074122]
7. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002; 3: 991-998[PMID: 12407406 DOI: 10.1038/ ni1102-991]
8. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci USA 2000; 97: 2731-2736[PMID: 10694580 DOI: 10.1073/pnas.050588297]
9. Smyth MJ, Hayakawa Y, Takeda K, Yagita H. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2002; 2: 850-861[PMID: 12415255 DOI: 10.1038/ nrc928]
10. Malmberg KJ, Bryceson YT, Carlsten M, Andersson S, Björklund A, Björkström NK, Baumann BC, Fauriat C, Alici E, Dilber MS, Ljunggren HG. NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol Immunother 2008; 57: 1541-1552[PMID: 18317755 DOI: 10.1007/s00262-008-0492-7]
11. Carbone E, Neri P, Mesuraca M, Fulciniti MT, Otsuki T, Pende D, Groh V, Spies T, Pollio G, Cosman D, Catalano L, Tassone P, Rotoli B, Venuta S. HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 2005; 105: 251-258[PMID: 15328155 DOI: 10.1182/blood-2004-04-1422]
12. Terme M, Fridman WH, Tartour E. NK cells from pleural effusions are potent antitumor effector cells. Eur J Immunol 2013; 43: 331-334[PMID: 23322344 DOI: 10.1002/eji.201243264]
13. Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C, Martos JA, Moreno M. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 1997; 79: 2320-2328[PMID: 9191519]
14. Sandel MH, Speetjens FM, Menon AG, Albertsson PA, Basse PH, Hokland M, Nagelkerke JF, Tollenaar RA, van de Velde CJ, Kuppen PJ. Natural killer cells infiltrating colorectal cancer and MHC class I expression. Mol Immunol 2005; 42: 541-546[PMID: 15607811 DOI: 10.1016/j.molimm.2004.07.039]
15. Tallerico R, Todaro M, Di Franco S, Maccalli C, Garofalo C, Sottile R, Palmieri C, Tirinato L, Pangigadde PN, La Rocca R, Mandelboim O, Stassi G, Di Fabrizio E, Parmiani G, Moretta A, Dieli F, Kärre K, Carbone E. Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J Immunol 2013; 190: 2381-2390[PMID: 23345327 DOI: 10.4049/jimmunol. 1201542]
16. Tachibana T, Onodera H, Tsuruyama T, Mori A, Nagayama S, Hiai H, Imamura M. Increased intratumor Valpha24- positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin Cancer Res 2005; 11: 7322-7327[PMID: 16243803 DOI: 10.1158/1078-0432.CCR-05-0877]
17. Corvaisier M, Moreau-Aubry A, Diez E, Bennouna J, Mosnier JF, Scotet E, Bonneville M, Jotereau F. V gamma 9V delta 2 T cell response to colon carcinoma cells. J Immunol 2005; 175: 5481-5488[PMID: 16210656]
18. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 2010; 11: 889-896[PMID: 20856220 DOI: 10.1038/ ni.1937]
19. Edin S, Wikberg ML, Rutegård J, Oldenborg PA, Palmqvist R. Phenotypic skewing of macrophages in vitro by secreted factors from colorectal cancer cells. PLoS One 2013; 8: e74982[PMID: 24058644 DOI: 10.1371/journal.pone.0074982]
20. Hammarström S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin Cancer Biol 1999; 9: 67-81[PMID: 10202129 DOI: 10.1006/scbi.1998.0119]
21. Keogh E, Fikes J, Southwood S, Celis E, Chesnut R, Sette A. Identification of new epitopes from four different tumorassociated antigens: recognition of naturally processed epitopes correlates with HLA-A*0201-binding affinity. J Immunol 2001; 167: 787-796[PMID: 11441084]
22. Fauquembergue E, Toutirais O, Tougeron D, Drouet A, Le Gallo M, Desille M, Cabillic F, de La Pintière CT, Iero M, Rivoltini L, Baert-Desurmont S, Leprince J, Vaudry H, Sesboué R, Frébourg T, Latouche JB, Catros V. HLA-A*0201-restricted CEA-derived peptide CAP1 is not a suitable target for T-cellbased immunotherapy. J Immunother 2010; 33: 402-413[PMID: 20386466 DOI: 10.1097/CJI.0b013e3181d366da]
23. Nagorsen D, Keilholz U, Rivoltini L, Schmittel A, Letsch A, Asemissen AM, Berger G, Buhr HJ, Thiel E, Scheibenbogen C. Natural T-cell response against MHC class I epitopes of epithelial cell adhesion molecule, her-2/neu, and carcinoembryonic antigen in patients with colorectal cancer. Cancer Res 2000; 60: 4850-4854[PMID: 10987297]
24. Smyrk TC, Watson P, Kaul K, Lynch HT. Tumor-infiltrating lymphocytes are a marker for microsatellite instability in colorectal carcinoma. Cancer 2001; 91: 2417-2422[PMID: 11413533]
25. Michael-Robinson JM, Biemer-Hüttmann A, Purdie DM, Walsh MD, Simms LA, Biden KG, Young JP, Leggett BA, Jass JR, Radford-Smith GL. Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status. Gut 2001; 48: 360-366[PMID: 11171826]
26. Benatti P, Gafà R, Barana D, Marino M, Scarselli A, Pedroni M, Maestri I, Guerzoni L, Roncucci L, Menigatti M, Roncari B, Maffei S, Rossi G, Ponti G, Santini A, Losi L, Di Gregorio C, Oliani C, Ponz de Leon M, Lanza G. Microsatellite instability and colorectal cancer prognosis. Clin Cancer Res 2005; 11: 8332-8340[PMID: 16322293 DOI: 10.1158/1078-0432. CCR-05-1030]
27. Saeterdal I, Gjertsen MK, Straten P, Eriksen JA, Gaudernack G. A TGF betaRII frameshift-mutation-derived CTL epitope recognised by HLA-A2-restricted CD8+ T cells. Cancer Immunol Immunother 2001; 50: 469-476[PMID: 11761441]
28. Ripberger E, Linnebacher M, Schwitalle Y, Gebert J, von Knebel Doeberitz M. Identification of an HLA-A0201- restricted CTL epitope generated by a tumor-specific frameshift mutation in a coding microsatellite of the OGT gene. J Clin Immunol 2003; 23: 415-423[PMID: 14601650]
29. Garbe Y, Maletzki C, Linnebacher M. An MSI tumor specific frameshift mutation in a coding microsatellite of MSH3 encodes for HLA-A0201-restricted CD8+ cytotoxic T cell epitopes. PLoS One 2011; 6: e26517[PMID: 22110587 DOI: 10.1371/journal.pone.0026517]
30. Tougeron D, Fauquembergue E, Rouquette A, Le Pessot F, Sesboüé R, Laurent M, Berthet P, Mauillon J, Di Fiore F, Sabourin JC, Michel P, Tosi M, Frébourg T, Latouche JB. Tumorinfiltrating lymphocytes in colorectal cancers with microsatellite instability are correlated with the number and spectrum of frameshift mutations. Mod Pathol 2009; 22: 1186-1195[PMID: 19503063 DOI: 10.1038/modpathol.2009.80]
31. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR, Sargent DJ. Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 2009; 137: 1270-1279[PMID: 19577568 DOI: 10.1053/j.gastro.2009.06.053]
32. Bernal M, Ruiz-Cabello F, Concha A, Paschen A, Garrido F. Implication of the β2-microglobulin gene in the generation of tumor escape phenotypes. Cancer Immunol Immunother 2012; 61: 1359-1371[PMID: 22833104 DOI: 10.1007/ s00262-012-1321-6]
33. Cabrera CM, Jiménez P, Cabrera T, Esparza C, Ruiz-Cabello F, Garrido F. 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 2003; 61: 211-219[PMID: 12694570]
34. 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, Trajanoski Z, Fridman WH, Galon J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005; 353: 2654-2666[PMID: 16371631 DOI: 10.1056/NEJMoa051424]
35. 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, Trajanoski Z, Fridman WH, Pagès F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-1964[PMID: 17008531 DOI: 10.1126/science.1129139]
36. Pagès F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, Lagorce C, Wind P, Marliot F, Bruneval P, Zatloukal K, Trajanoski Z, Berger A, Fridman WH, Galon J. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009; 27: 5944-5951[PMID: 19858404 DOI: 10.1200/JCO.2008.19.6147]
37. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, Bruneval P, Trajanoski Z, Fridman WH, Pagès F, Galon J. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 2011; 29: 610-618[PMID: 21245428 DOI: 10.1200/JCO.2010.30.5425]
38. Allard MA, Bachet JB, Beauchet A, Julie C, Malafosse R, Penna C, Nordlinger B, Emile JF. Linear quantification of lymphoid infiltration of the tumor margin: a reproducible method, developed with colorectal cancer tissues, for assessing a highly variable prognostic factor. Diagn Pathol 2012; 7: 156[PMID: 23148481 DOI: 10.1186/1746-1596-7-156]
39. Menon AG, Morreau H, Tollenaar RA, Alphenaar E, Van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ. Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest 2002; 82: 1725-1733[PMID: 12480922]
40. Watson NF, Ramage JM, Madjd Z, Spendlove I, Ellis IO, Scholefield JH, Durrant LG. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int J Cancer 2006; 118: 6-10[PMID: 16003753 DOI: 10.1002/ ijc.21303]
41. Pere H, Tanchot C, Bayry J, Terme M, Taieb J, Badoual C, Adotevi O, Merillon N, Marcheteau E, Quillien VR, Banissi C, Carpentier A, Sandoval F, Nizard M, Quintin-Colonna F, Kroemer G, Fridman WH, Zitvogel L, Oudard SP, Tartour E. Comprehensive analysis of current approaches to inhibit regulatory T cells in cancer. Oncoimmunology 2012; 1: 326-333[PMID: 22737608 DOI: 10.4161/onci.18852]
42. Sellitto A, Galizia G, De Fanis U, Lieto E, Zamboli A, Orditura M, De Vita F, Giunta R, Lucivero G, Romano C. Behavior of circulating CD4+CD25+Foxp3+ regulatory T cells in colon cancer patients undergoing surgery. J Clin Immunol 2011; 31: 1095-1104[PMID: 21915633 DOI: 10.1007/s10875-011-9585-8]
43. Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B. Tumor-infiltrating FOXP3 T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009; 27: 186-192[PMID: 19064967 DOI: 10.1200/JCO.2008.18.7229]
44. Chaput N, Louafi S, Bardier A, Charlotte F, Vaillant JC, Ménégaux F, Rosenzwajg M, Lemoine F, Klatzmann D, Taieb J. Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue. Gut 2009; 58: 520-529[PMID: 19022917 DOI: 10.1136/gut.2008.158824]
45. Casares N, Arribillaga L, Sarobe P, Dotor J, Lopez-Diaz de Cerio A, Melero I, Prieto J, Borrás-Cuesta F, Lasarte JJ. CD4+/CD25+ regulatory cells inhibit activation of tumorprimed CD4+ T cells with IFN-gamma-dependent antiangiogenic activity, as well as long-lasting tumor immunity elicited by peptide vaccination. J Immunol 2003; 171: 5931-5939[PMID: 14634104]
46. Taieb J, Chaput N, Schartz N, Roux S, Novault S, Ménard C, Ghiringhelli F, Terme M, Carpentier AF, Darrasse-Jèze G, Lemonnier F, Zitvogel L. Chemoimmunotherapy of tumors: cyclophosphamide synergizes with exosome based vaccines. J Immunol 2006; 176: 2722-2729[PMID: 16493027]
47. 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. Antigenspecific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma. J Clin Invest 2009; 119: 3311-3321[PMID: 19809157 DOI: 10.1172/JCI39608]
48. Yaqub S, Henjum K, Mahic M, Jahnsen FL, Aandahl EM, Bjørnbeth BA, Taskén K. Regulatory T cells in colorectal cancer patients suppress anti-tumor immune activity in a COX-2 dependent manner. Cancer Immunol Immunother 2008; 57: 813-821[PMID: 17962941 DOI: 10.1007/s00262-007-0417-x]
49. Tanchot C, Terme M, Pere H, Tran T, Benhamouda N, Strioga M, Banissi C, Galluzzi L, Kroemer G, Tartour E. Tumorinfiltrating regulatory T cells: phenotype, role, mechanism of expansion in situ and clinical significance. Cancer Microenviron 2013; 6: 147-157[PMID: 23104434 DOI: 10.1007/s12307- 012-0122-y]
50. Pere H, Montier Y, Bayry J, Quintin-Colonna F, Merillon N, Dransart E, Badoual C, Gey A, Ravel P, Marcheteau E, Batteux F, Sandoval F, Adotevi O, Chiu C, Garcia S, Tanchot C, Lone YC, Ferreira LC, Nelson BH, Hanahan D, Fridman WH, Johannes L, Tartour E. A CCR4 antagonist combined with vaccines induces antigen-specific CD8+ T cells and tumor immunity against self antigens. Blood 2011; 118: 4853-4862[PMID: 21908423 DOI: 10.1182/blood-2011-01-329656]
51. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP, Gimotty PA, Gilks CB, Lal P, Zhang L, Coukos G. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 2011; 475: 226-230[PMID: 21753853 DOI: 10.1038/nature10169]
52. Belkaid Y, Oldenhove G. Tuning microenvironments: induction of regulatory T cells by dendritic cells. Immunity 2008; 29: 362-371[PMID: 18799144 DOI: 10.1016/j.immuni.2008.08.005]
53. Ghiringhelli F, Puig PE, Roux S, Parcellier A, Schmitt E, Solary E, Kroemer G, Martin F, Chauffert B, Zitvogel L. Tumor cells convert immature myeloid dendritic cells into TGFbeta- secreting cells inducing CD4+CD25+ regulatory T cell proliferation. J Exp Med 2005; 202: 919-929[PMID: 16186184 DOI: 10.1084/jem.20050463]
54. Terme M, Pernot S, Marcheteau E, Sandoval F, Benhamouda N, Colussi O, Dubreuil O, Carpentier AF, Tartour E, Taieb J. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res 2013; 73: 539-549[PMID: 23108136 DOI: 10.1158/0008-5472. CAN-12-2325]
55. Suzuki H, Onishi H, Morisaki T, Tanaka M, Katano M. Intratumoral FOXP3+VEGFR2+ regulatory T cells are predictive markers for recurrence and survival in patients with colorectal cancer. Clin Immunol 2013; 146: 26-33[PMID: 23202541 DOI: 10.1016/j.clim.2012.10.007]
56. Hua D, Sun J, Mao Y, Chen LJ, Wu YY, Zhang XG. B7-H1 expression is associated with expansion of regulatory T cells in colorectal carcinoma. World J Gastroenterol 2012; 18: 971-978[PMID: 22408358 DOI: 10.3748/wjg.v18.i9.971]
57. Shi SJ, Wang LJ, Wang GD, Guo ZY, Wei M, Meng YL, Yang AG, Wen WH. B7-H1 expression is associated with poor prognosis in colorectal carcinoma and regulates the proliferation and invasion of HCT116 colorectal cancer cells. PLoS One 2013; 8: e76012[PMID: 24124529 DOI: 10.1371/journal. pone.0076012]
58. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbé C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-723[PMID: 20525992 DOI: 10.1056/ NEJMoa1003466]
59. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, Burke MM, Caldwell A, Kronenberg SA, Agunwamba BU, Zhang X, Lowy I, Inzunza HD, Feely W, Horak CE, Hong Q, Korman AJ, Wigginton JM, Gupta A, Sznol M. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369: 122-133[PMID: 23724867 DOI: 10.1056/NEJMoa1302369]
60. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, Dronca R, Gangadhar TC, Patnaik A, Zarour H, Joshua AM, Gergich K, Elassaiss-Schaap J, Algazi A, Mateus C, Boasberg P, Tumeh PC, Chmielowski B, Ebbinghaus SW, Li XN, Kang SP, Ribas A. Safety and tumor responses with lambrolizumab (anti- PD-1) in melanoma. N Engl J Med 2013; 369: 134-144[PMID: 23724846 DOI: 10.1056/NEJMoa1305133]
61. Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, Martin F, Apetoh L, Rébé C, Ghiringhelli F. 5-Fluorouracil selectively kills tumor-associated myeloidderived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010; 70: 3052-3061[PMID: 20388795 DOI: 10.1158/0008-5472.CAN-09-3690]
62. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, Métivier D, Larochette N, van Endert P, Ciccosanti F, Piacentini M, Zitvogel L, Kroemer G. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61[PMID: 17187072 DOI: 10.1038/nm1523]
63. Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F, Aymeric L, Michaud M, Apetoh L, Barault L, Mendiboure J, Pignon JP, Jooste V, van Endert P, Ducreux M, Zitvogel L, Piard F, Kroemer G. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010; 29: 482-491[PMID: 19881547 DOI: 10.1038/onc.2009.356]
64. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011; 8: 151-160[PMID: 21364688 DOI: 10.1038/nrclinonc. 2010.223]
65. Ozao-Choy J, Ma G, Kao J, Wang GX, Meseck M, Sung M, Schwartz M, Divino CM, Pan PY, Chen SH. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune- based cancer therapies. Cancer Res 2009; 69: 2514-2522[PMID: 19276342 DOI: 10.1158/0008-5472.CAN-08-4709]
66. Adotevi O, Pere H, Ravel P, Haicheur N, Badoual C, Merillon N, Medioni J, Peyrard S, Roncelin S, Verkarre V, Mejean A, Fridman WH, Oudard S, Tartour E. A decrease of regulatory T cells correlates with overall survival after sunitinibbased antiangiogenic therapy in metastatic renal cancer patients. J Immunother 2010; 33: 991-998[PMID: 20948437 DOI: 10.1097/CJI.0b013e3181f4c208]
67. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004; 350: 2335-2342[PMID: 15175435 DOI: 10.1056/NEJMoa032691]
68. Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, Golshayan A, Rayman PA, Wood L, Garcia J, Dreicer R, Bukowski R, Finke JH. Sunitinib mediates reversal of myeloidderived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 2009; 15: 2148-2157[PMID: 19276286 DOI: 10.1158/1078-0432.CCR-08-1332]
69. Yang X, Zhang X, Mortenson ED, Radkevich-Brown O, Wang Y, Fu YX. Cetuximab-mediated tumor regression depends on innate and adaptive immune responses. Mol Ther 2013; 21: 91-100[PMID: 22990672 DOI: 10.1038/mt.2012.184]
70. Mellor JD, Brown MP, Irving HR, Zalcberg JR, Dobrovic A. A critical review of the role of Fc gamma receptor polymorphisms in the response to monoclonal antibodies in cancer. J Hematol Oncol 2013; 6: 1[PMID: 23286345 DOI: 10.1186/1756-8722-6-1]
71. Correale P, Cusi MG, Tsang KY, Del Vecchio MT, Marsili S, Placa ML, Intrivici C, Aquino A, Micheli L, Nencini C, Ferrari F, Giorgi G, Bonmassar E, Francini G. Chemo-immunotherapy of metastatic colorectal carcinoma with gemcitabine plus FOLFOX 4 followed by subcutaneous granulocyte macrophage colony-stimulating factor and interleukin-2 induces strong immunologic and antitumor activity in metastatic colon cancer patients. J Clin Oncol Off J Am Soc Clin Oncol 2005; 23: 8950-8958
72. Correale P, Tagliaferri P, Fioravanti A, Del Vecchio MT, Remondo C, Montagnani F, Rotundo MS, Ginanneschi C, Martellucci I, Francini E, Cusi MG, Tassone P, Francini G. Immunity feedback and clinical outcome in colon cancer patients undergoing chemoimmunotherapy with gemcitabine + FOLFOX followed by subcutaneous granulocyte macrophage colony-stimulating factor and aldesleukin (GOLFIG-1 Trial). Clin Cancer Res 2008; 14: 4192-4199[PMID: 18593999 DOI: 10.1158/1078-0432.CCR-07-5278]
73. Correale P, Rotundo MS, Botta C, Apollinari S, Remondo C, Tsang KY, Ciliberto D, Tassone P, Ridolfi R, Tagliaferri P. Chemo-immunotherapy with gemcitabine FOLFOX followed by granulocyte-macrophage colony stimulating factor and low dose aldesleukine (GOLFIG regimen) is a highly active frontline treatment for advanced colorectal carcinoma: Results from the GOLFIG/2 phase III trial. Proc 102nd Annual Meeting of the American Association for Cancer Research; 2011, Apr 2-6. Orlando Florida. Philadelphia: AACR, 2011. Abstract nr 5511. Available from: URL: http://www.abstractsonline.com/Plan/ViewAbstract.aspx?sKey=0752a705-7e85-4337-a2c7-02b492ae7ecc&cKey=c71f5dc7-32f2-47e8-abcc-47692b7524eb&mKey={507D311A-B6EC-436A-BD67- 6D14ED39622C}
74. Moulton HM, Yoshihara PH, Mason DH, Iversen PL, Triozzi PL. Active specific immunotherapy with a beta-human chorionic gonadotropin peptide vaccine in patients with metastatic colorectal cancer: antibody response is associated with improved survival. Clin Cancer Res 2002; 8: 2044-2051[PMID: 12114402]
75. Posner MC, Niedzwiecki D, Venook AP, Hollis DR, Kindler HL, Martin EW, Schilsky RL, Goldberg RM, Mayer RJ. A phase II prospective multi-institutional trial of adjuvant active specific immunotherapy following curative resection of colorectal cancer hepatic metastases: cancer and leukemia group B study 89903. Ann Surg Oncol 2008; 15: 158-164[PMID: 18008108 DOI: 10.1245/s10434-007-9654-7]
76. Toubaji A, Achtar M, Provenzano M, Herrin VE, Behrens R, Hamilton M, Bernstein S, Venzon D, Gause B, Marincola F, Khleif SN. Pilot study of mutant ras peptide-based vaccine as an adjuvant treatment in pancreatic and colorectal cancers. Cancer Immunol Immunother 2008; 57: 1413-1420[PMID: 18297281 DOI: 10.1007/s00262-008-0477-6]
77. Schulze T, Kemmner W, Weitz J, Wernecke KD, Schirrmacher V, Schlag PM. Efficiency of adjuvant active specific immunization with Newcastle disease virus modified tumor cells in colorectal cancer patients following resection of liver metastases: results of a prospective randomized trial. Cancer Immunol Immunother 2009; 58: 61-69[PMID: 18488223 DOI: 10.1007/s00262-008-0526-1]
78. Vermorken JB, Claessen AM, van Tinteren H, Gall HE, Ezinga R, Meijer S, Scheper RJ, Meijer CJ, Bloemena E, Ransom JH, Hanna MG, Pinedo HM. Active specific immunotherapy for stage II and stage III human colon cancer: a randomised trial. Lancet 1999; 353: 345-350[PMID: 9950438 DOI: 10.1016/ S0140-6736(98)07186-4]
79. Harris JE, Ryan L, Hoover HC, Stuart RK, Oken MM, Benson AB, Mansour E, Haller DG, Manola J, Hanna MG. Adjuvant active specific immunotherapy for stage II and III colon cancer with an autologous tumor cell vaccine: Eastern Cooperative Oncology Group Study E5283. J Clin Oncol 2000; 18: 148-157[PMID: 10623705]
80. Uyl-Degroot CA, Vermorken JB, Hanna MG, Verboom P, Groot MT, Bonsel GJ, Meijer CJ, Pinedo HM. Immunotherapy with autologous tumor cell-BCG vaccine in patients with colon cancer: a prospective study of medical and economic benefits. Vaccine 2005; 23: 2379-2387[PMID: 15755632 DOI: 10.1016/j.vaccine.2005.01.015]
81. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012; 12: 265-277[PMID: 22437871 DOI: 10.1038/nrc3258]
82. Morse MA, Nair SK, Mosca PJ, Hobeika AC, Clay TM, Deng Y, Boczkowski D, Proia A, Neidzwiecki D, Clavien PA, Hurwitz HI, Schlom J, Gilboa E, Lyerly HK. Immunotherapy with autologous, human dendritic cells transfected with carcinoembryonic antigen mRNA. Cancer Invest 2003; 21: 341-349[PMID: 12901279]
83. Liu Y, Zhang W, Zhang B, Yin X, Pang Y. DC vaccine therapy combined concurrently with oral capecitabine in metastatic colorectal cancer patients. Hepatogastroenterology 2013; 60: 23-27[PMID: 22945335 DOI: 10.5754/hge12522]
84. Lesterhuis WJ, de Vries IJ, Aarntzen EA, de Boer A, Scharenborg NM, van de Rakt M, van Spronsen DJ, Preijers FW, Figdor CG, Adema GJ, Punt CJ. A pilot study on the immunogenicity of dendritic cell vaccination during adjuvant oxaliplatin/capecitabine chemotherapy in colon cancer patients. Br J Cancer 2010; 103: 1415-1421[PMID: 20924373 DOI: 10.1038/sj.bjc.6605935]
85. Morse MA, Niedzwiecki D, Marshall JL, Garrett C, Chang DZ, Aklilu M, Crocenzi TS, Cole DJ, Dessureault S, Hobeika AC, Osada T, Onaitis M, Clary BM, Hsu D, Devi GR, Bulusu A, Annechiarico RP, Chadaram V, Clay TM, Lyerly HK. A randomized phase II study of immunization with dendritic cells modified with poxvectors encoding CEA and MUC1 compared with the same poxvectors plus GM-CSF for resected metastatic colorectal cancer. Ann Surg 2013; 258: 879-886[PMID: 23657083 DOI: 10.1097/SLA.0b013e318292919e]
86. Kavanagh B, Ko A, Venook A, Margolin K, Zeh H, Lotze M, Schillinger B, Liu W, Lu Y, Mitsky P, Schilling M, Bercovici N, Loudovaris M, Guillermo R, Lee SM, Bender J, Mills B, Fong L. Vaccination of metastatic colorectal cancer patients with matured dendritic cells loaded with multiple major histocompatibility complex class I peptides. J Immunother 2007; 30: 762-772[PMID: 17893568 DOI: 10.1097/ CJI.0b013e318133451c]
87. Barth RJ, Fisher DA, Wallace PK, Channon JY, Noelle RJ, Gui J, Ernstoff MS. A randomized trial of ex vivo CD40L activation of a dendritic cell vaccine in colorectal cancer patients: tumor-specific immune responses are associated with improved survival. Clin Cancer Res 2010; 16: 5548-5556[PMID: 20884622 DOI: 10.1158/1078-0432.CCR-10-2138]
88. Burgdorf SK, Fischer A, Myschetzky PS, Munksgaard SB, Zocca MB, Claesson MH, Rosenberg J. Clinical responses in patients with advanced colorectal cancer to a dendritic cell based vaccine. Oncol Rep 2008; 20: 1305-1311[PMID: 19020707]
89. Tartour E, Benchetrit F, Haicheur N, Adotevi O, Fridman WH. Synthetic and natural non-live vectors: rationale for their clinical development in cancer vaccine protocols. Vaccine 2002; 20 Suppl 4: A32-A39[PMID: 12477426]
90. Karlsson M, Marits P, Dahl K, Dagöö T, Enerbäck S, Thörn M, Winqvist O. Pilot study of sentinel-node-based adoptive immunotherapy in advanced colorectal cancer. Ann Surg Oncol 2010; 17: 1747-1757[PMID: 20119674 DOI: 10.1245/ s10434-010-0920-8]
91. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, Davis JL, Morgan RA, Merino MJ, Sherry RM, Hughes MS, Kammula US, Phan GQ, Lim RM, Wank SA, Restifo NP, Robbins PF, Laurencot CM, Rosenberg SA. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011; 19: 620-626[PMID: 21157437 DOI: 10.1038/mt.2010.272]
92. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010; 18: 843-851[PMID: 20179677 DOI: 10.1038/mt.2010.24]