Immunotherapy and immunoescape in colorectal cancer

World Journal of Gastroenterology

Volumn 13, Issue 44, 2007, Pages 5822-5831

  Mazzolini, Guillermo ^a   Murillo, Oihana ^b   Atorrasagasti, Catalina ^a   Dubrot, Juan ^b   Tirapu, Iñigo ^b   Rizzo, Miguel ^a   Arina, Ainhoa ^b   Alfaro, Carlos ^b   Azpilicueta, Arantza ^b   Berasain, Carmen ^b   Perez Gracia, José L ^b   Gonzalez, Alvaro ^b   Melero, Ignacio ^b  

^a UNIVERSIDAD AUSTRAL   (Argentina)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

CD137; Colorectal carcinoma; Dendritic cells; Gene therapy; Immunotherapy; Indoleamine 2, 3 dioxygenase; Interleukin 12

Indexed keywords

ADENOVIRUS VECTOR; ALLOVECTIN 7; BCG VACCINE; BETA 2 MICROGLOBULIN; CAPECITABINE; CD137 ANTIGEN; CD137 LIGAND; CD40 LIGAND; CYCLOPHOSPHAMIDE; DENDRITIC CELL VACCINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEAT SHOCK PROTEIN; HLA B27 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 7; IRINOTECAN; MACROPHAGE INFLAMMATORY PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD137; MONOCLONAL ANTIBODY CTLA4; OXALIPLATIN; PROTEIN E7; RECOMBINANT INTERLEUKIN 12; RETROVIRUS VECTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; TNFERADE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADJUVANT THERAPY; ADOPTIVE IMMUNOTHERAPY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CLINICAL TRIAL; COLON CANCER; COLORECTAL CANCER; COLORECTAL CARCINOMA; CYTOKINE PRODUCTION; DENDRITIC CELL; DIGESTIVE SYSTEM CANCER; DRUG EFFICACY; EPIGENETICS; GENE TRANSFER; HUMAN; IMMUNOREGULATION; KIDNEY CARCINOMA; LIVER METASTASIS; LIVER TUMOR; MELANOMA; NONHUMAN; RECTUM CANCER; REGULATORY T LYMPHOCYTE; SOLID TUMOR; T LYMPHOCYTE ACTIVATION; TH1 CELL; TUMOR IMMUNITY; UNSPECIFIED SIDE EFFECT; VIRAL GENE THERAPY;

EID: 36348954489     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v13.i44.5822     Document Type: Article

References (83)

1. Prieto J, Qian C, Sangro B, Melero I, Mazzolini G. Biologic therapy of liver tumors. Surg Clin North Am 2004; 84: 673-696
2. Tabernero J, Salazar R, Casado E, Martinelli E, Gomez P, Baselga J. Targeted therapy in advanced colon cancer: the role of new therapies. Ann Oncol 2004; 15 Suppl 4: iv55-iv62
3. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74-108
4. Lorenz M, Staib-Sebler E, Hochmuth K, Heinrich S, Gog C, Vetter G, Encke A, Muller HH. Surgical resection of liver metastases of colorectal carcinoma: short and long-term results. Semin Oncol 2000; 27: 112-119
5. Yee C, Riddell SR, Greenberg PD. Prospects for adoptive T cell therapy. Curr Opin Immunol 1997; 9: 702-708
6. Pardoll D. Does the immune system see tumors as foreign or self? Annu Rev Immunol 2003; 21: 807-839
7. Garcia-Lora A, Algarra I, Garrido F. MHC class I antigens, immune surveillance, and tumor immune escape. J Cell Physiol 2003; 195: 346-355
8. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006; 90: 51-81
9. Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 2007; 7: 41-51
10. Mazzolini G, Narvaiza I, Bustos M, Duarte M, Tirapu I, Bilbao R, Qian C, Prieto J, Melero I. Alpha(v)beta(3) integrin-mediated adenoviral transfer of interleukin-12 at the periphery of hepatic colon cancer metastases induces VCAM-1 expression and T-cell recruitment. Mol Ther 2001; 3: 665-672
11. Munn DH. Indoleamine 2,3-dioxygenase, tumor-induced tolerance and counter-regulation. Curr Opin Immunol 2006; 18: 220-225
12. Munn DH, Sharma MD, Hou D, Baban B, Lee JR, Antonia SJ, Messina JL, Chandler P, Koni PA, Mellor AL. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest 2004; 114: 280-290
13. Fallarino F, Grohmann U, Vacca C, Orabona C, Spreca A, Fioretti MC, Puccetti P. T cell apoptosis by kynurenines. Adv Exp Med Biol 2003; 527: 183-190
14. Brandacher G, Perathoner A, Ladurner R, Schneeberger S, Obrist P, Winkler C, Werner ER, Werner-Felmayer G, Weiss HG, Gobel G, Margreiter R, Konigsrainer A, Fuchs D, Amberger A. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin Cancer Res 2006; 12: 1144-1151
15. Janeway CA Jr, Bottomly K. Signals and signs for lymphocyte responses. Cell 1994; 76: 275-285
16. Wang S, Chen L. T lymphocyte co-signaling pathways of the B7-CD28 family. Cell Mol Immunol 2004; 1: 37-42
17. Flies DB, Chen L. The new B7s: playing a pivotal role in tumor immunity. J Immunother (1997) 2007; 30: 251-260
18. Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, Lackner A, Alvarez X, Ochoa A, Chen L, Zou W. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 2006; 203: 871-881
19. Gallina G, Dolcetti L, Serafini P, De Santo C, Marigo I, Colombo MP, Basso G, Brombacher F, Borrello I, Zanovello P, Bicciato S, Bronte V. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 2006; 116: 2777-2790
20. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006; 6: 295-307
21. Valzasina B, Guiducci C, Dislich H, Killeen N, Weinberg AD, Colombo MP. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood 2005; 105: 2845-2851
22. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10: 942-949
23. Muranski P, Boni A, Wrzesinski C, Citrin DE, Rosenberg SA, Childs R, Restifo NP. Increased intensity lymphodepletion and adoptive immunotherapy--how far can we go? Nat Clin Pract Oncol 2006; 3: 668-681
24. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, Hwang LN, Yu Z, Wrzesinski C, Heimann DM, Surh CD, Rosenberg SA, Restifo NP. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005; 202: 907-912
25. Chen L. Immunological ignorance of silent antigens as an explanation of tumor evasion. Immunol Today 1998; 19: 27-30
26. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001; 19: 47-64
27. Ohashi PS, Oehen S, Buerki K, Pircher H, Ohashi CT, Odermatt B, Malissen B, Zinkernagel RM, Hengartner H. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991; 65: 305-317
28. Ochsenbein AF, Klenerman P, Karrer U, Ludewig B, Pericin M, Hengartner H, Zinkernagel RM. Immune surveillance against a solid tumor fails because of immunological ignorance. Proc Natl Acad Sci USA 1999; 96: 2233-2238
29. Melero I, Singhal MC, McGowan P, Haugen HS, Blake J, Hellstrom KE, Yang G, Clegg CH, Chen L. Immunological ignorance of an E7-encoded cytolytic T-lymphocyte epitope in transgenic mice expressing the E7 and E6 oncogenes of human papillomavirus type 16. J Virol 1997; 71: 3998-4004
30. Sogn JA: Tumor immunology: the glass is half full. Immunity 1998; 9: 757-763
31. Folkman J. Angiogenesis. Annu Rev Med 2006; 57: 1-18
32. Li H, Fan X, Houghton J. Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem 2007; 101: 805-815
33. Pardoll DM. Cancer vaccines. Nat Med 1998; 4: 525-531
34. Figdor CG, de Vries IJ, Lesterhuis WJ, Melief CJ. Dendritic cell immunotherapy: mapping the way. Nat Med 2004; 10: 475-480
35. Gattinoni L, Powell DJ Jr, Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 2006; 6: 383-393
36. Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 2007; 7: 95-106
37. Goodwin RG, Din WS, Davis-Smith T, Anderson DM, Gimpel SD, Sato TA, Maliszewski CR, Brannan CI, Copeland NG, Jenkins NA. Molecular cloning of a ligand for the inducible T cell gene 4-1BB: a member of an emerging family of cytokines with homology to tumor necrosis factor. Eur J Immunol 1993; 23: 2631-2641
38. Sica G, Chen L. Modulation of the immune response through 4-1BB. Adv Exp Med Biol 2000; 465: 355-362
39. Teft WA, Kirchhof MG, Madrenas J. A molecular perspective of CTLA-4 function. Annu Rev Immunol 2006; 24: 65-97
40. Kocak E, Lute K, Chang X, May KF Jr, Exten KR, Zhang H, Abdessalam SF, Lehman AM, Jarjoura D, Zheng P, Liu Y. Combination the rapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res 2006; 66: 7276-7284
41. Martinet O, Ermekova V, Qiao JQ Sauter B, Mandeli J, Chen L, Chen SH. Immunomodulatory gene therapy with interleukin 12 and 4-1BB ligand: long- term remission of liver metastases in a mouse model. J Natl Cancer Inst 2000; 92: 931-936
42. Martinet O, Divino CM, Zang Y, Gan Y, Mandeli J, Thung S, Pan PY, Chen SH. T cell activation with systemic agonistic antibody versus local 4-1BB ligand gene delivery combined with interleukin-12 eradicate liver metastases of breast cancer. Gene Ther 2002; 9: 786-792
43. Wilcox RA, Flies DB, Zhu G, Johnson AJ, Tamada K, Chapoval AI, Strome SE, Pease LR, Chen L. Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly inummogenic tumors. J Clin Invest 2002; 109: 651-659
44. Allison JP, Krummel MF. The Yin and Yang of T cell costimulation. Science 1995; 270: 932-933
45. Tirapu I, Arina A, Mazzolini G, Duarte M, Alfaro C, Feijoo E, Qian C, Chen L, Prieto J, Melero I. Improving efficacy of interleukin-12-transfected dendritic cells injected into murine colon cancer with anti-CD137 monoclonal antibodies and alloantigens. Int J Cancer 2004; 110: 51-60
46. Mazzolini G, Alfaro C, Sangro B, Feijoo E, Ruiz J, Benito A, Tirapu I, Arina A, Sola J, Herraiz M, Lucena F, Olague C, Subtil J, Quiroga J, Herrero I, Sadaba B, Bendandi M, Qian C, Prieto J, Melero I. Intratumoral injection of dendritic cells engineered to secrete interleukin-12 by recombinant adenovirus in patients with metastatic gastrointestinal carcinomas. J Clin Oncol 2005; 23: 999-1010
47. Podhajcer OL, Lopez MV, Mazzolini G. Cytokine gene transfer for cancer therapy. Cytokine Growth Factor Rev 2007; 18:183-194
48. Prieto J, Qian C, Hernandez-Alcoceba R, Gonzalez-Aseguinolaza G, Mazzolini G, Sangro B, Kramer MG. Gene therapy of liver diseases. Expert Opin Biol Ther 2004; 4: 1073-1091
49. Trinchieri G. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv Immunol 1998; 70: 83-243
50. Mazzolini G, Prieto J, Melero I. Gene therapy of cancer with interleukin-12. Curr Pharm Des 2003; 9: 1981-1991
51. Narvaiza I, Mazzolini G, Barajas M, Duarte M, Zaratiegui M, Qian C, Melero I, Prieto J. Intratumoral coinjection of two adenoviruses, one encoding the chemokine IFN-gamma-inducible protein-10 and another encoding IL-12, results in marked antitumoral synergy. J Immunol 2000; 164: 3112-3122
52. Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, Kleinman HK, Reaman GH, Tosato G. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J Exp Med 1995; 182: 155-162
53. Mazzolini G, Narvaiza I, Perez-Diez A, Rodriguez-Calvillo M, Qian C, Sangro B, Ruiz J, Prieto J, Melero I. Genetic heterogeneity in the toxicity to systemic adenoviral gene transfer of interleukin-12. Gene Ther 2001; 8: 259-267
54. Adris S, Klein S, Jasnis M, Chuluyan E, Ledda M, Bravo A, Carbone C, Chernajovsky Y, Podhajcer O. IL-10 expression by CT26 colon carcinoma cells inhibits their malignant phenotype and induces a T cell-mediated tumor rejection in the context of a systemic Th2 response. Gene Ther 1999; 6: 1705-1712
55. Lopez MV, Adris SK, Bravo AI, Chernajovsky Y, Podhajcer OL. IL-12 and IL-10 expression synergize to induce the immune-mediated eradication of established colon and mammary tumors and lung metastasis. J Immunol 2005; 175: 5885-5894
56. Chu NR, Wu HB, Wu T, Boux LJ, Siegel MI, Mizzen LA. Immunotherapy of a human papillomavirus (HPV) type 16 E7-expressing tumour by administration of fusion protein comprising Mycobacterium bovis bacille Calmette-Guerin (BCG) hsp65 and HPV16 E7. Clin Exp Immunol 2000; 121: 216-225
57. Wu Y, Wan T, Zhou X, Wang B, Yang F, Li N, Chen G, Dai S, Liu S, Zhang M, Cao X. Hsp70-like protein 1 fusion protein enhances induction of carcinoembryonic antigen-specific CD8+ CTL response by dendritic cell vaccine. Cancer Res 2005; 65: 4947-4954
58. Rosenberg SA, Lotze MT, Yang JC, Aebersold PM, Linehan WM, Seipp CA, White DE. Experience with the use of high-dose interleukin-2 in the treatment of 652 cancer patients. Ann Surg 1989; 210: 474-484; discussion 484-485
59. Chen SH, Chen XH, Wang Y, Kosai K, Finegold MJ, Rich SS, Woo SL. Combination gene therapy for liver metastasis of colon carcinoma in vivo. Proc Natl Acad Sci USA 1995; 92: 2577-2581
60. Mazzolini G, Narvaiza I, Martinez-Cruz LA, Arina A, Barajas M, Galofre JC, Qian C, Mato JM, Prieto J, Melero I. Pancreatic cancer escape variants that evade immunogene therapy through loss of sensitivity to IFNgamma-induced apoptosis. Gene Ther 2003; 10: 1067-1078
61. Hisada M, Yoshimoto T, Kamiya S, Magami Y, Miyaji H, Yoneto T, Tamada K, Aoki T, Koyanagi Y, Mizuguchi J. Synergistic antitumor effect by coexpression of chemokine CCL21/SLC and costimulatory molecule LIGHT. Cancer Gene Ther 2004; 11: 280-288
62. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252
63. Reis e Sousa C. Dendritic cells in a mature age. Nat Rev Immunol 2006; 6:476-483
64. Melero I, Duarte M, Ruiz J, Sangro B, Galofre J, Mazzolini G, Bustos M, Qian C, Prieto J. Intratumoral injection of bone-marrow derived dendritic cells engineered to produce interleukin-12 induces complete regression of established murine transplantable colon adenocarcinomas. Gene Ther 1999; 6: 1779-1784
65. Miller PW, Sharma S, Stolina M, Butterfield LH, Luo J, Lin Y, Dohadwala M, Batra RK, Wu L, Economou JS, Dubinett SM. Intratumoral administration of adenoviral interleukin 7 gene-modified dendritic cells augments specific antitumor immunity and achieves tumor eradication. Hum Gene Ther 2000; 11: 53-65
66. Vera M, Razquin N, Prieto J, Melero I, Fortes P, Gonzalez-Aseguinolaza G. Intratumoral injection of dendritic cells transduced by an SV40-based vector expressing interleukin-15 induces curative immunity mediated by CD8+ T lymphocytes and NK cells. Mol Ther 2005; 12: 950-959
67. Chu XY, Chen LB, Zang J, Wang JH, Zhang Q, Geng HC. Effect of bone marrow-derived monocytes transfected with RNA of mouse colon carcinoma on specific antitumor immunity. World J Gastroenterol 2005; 11: 760-763
68. Saha A, Chatterjee SK, Foon KA, Primus FJ, Sreedharan S, Mohanty K, Bhattacharya-Chatterjee M. Dendritic cells pulsed with an anti-idiotype antibody mimicking carcinoembryonic antigen (CEA) can reverse immunological tolerance to CEA and induce antitumor immunity in CEA transgenic mice. Cancer Res 2004; 64: 4995-5003
69. Furumoto K, Soares L, Engleman EG, Merad M. Induction of potent antitumor immunity by in situ targeting of intratumoral DCs. J Clin Invest 2004; 113: 774-783
70. Kikuchi T, Miyazawa N, Moore MA, Crystal RG. Tumor regression induced by intratumor administration of adenovirus vector expressing CD40 ligand and naive dendritic cells. Cancer Res 2000; 60: 6391-6395
71. Kikuchi T, Moore MA, Crystal RG. Dendritic cells modified to express CD40 ligand elicit therapeutic immunity against preexisting murine tumors. Blood 2000; 96: 91-99
72. Morse MA, Deng Y, Coleman D, Hull S, Kitrell-Fisher E, Nair S, Schlom J, Ryback ME, Lyerly HK. A Phase I study of active immunotherapy with carcinoembryonic antigen peptide (CAP-1)-pulsed, autologous human cultured dendritic cells in patients with metastatic malignancies expressing carcinoembryonic antigen. Clin Cancer Res 1999; 5: 1331-1338
73. Fong L, Hou Y, Rivas A, Benike C, Yuen A, Fisher GA, Davis MM, Engleman EG. Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc Natl Acad Sci USA 2001; 98: 8809-8814
74. Feijoo E, Alfaro C, Mazzolini G, Serra P, Penuelas I, Arina A, Huarte E, Tirapu I, Palencia B, Murillo O, Ruiz J, Sangro B, Richter JA, Prieto J, Melero I. Dendritic cells delivered inside human carcinomas are sequestered by interleukin-8. Int J Cancer 2005; 116: 275-281
75. Senzer N, Mani S, Rosemurgy A, Nemunaitis J, Cunningham C, Guha C, Bayol N, Gillen M, Chu K, Rasmussen C, Rasmussen H, Kufe D, Weichselbaum R, Hanna N. TNFerade biologic, an adenovector with a radiation-inducible promoter, carrying the human tumor necrosis factor alpha gene: a phase I study in patients with solid tumors. J Clin Oncol 2004; 22: 592-601
76. Rubin J, Galanis E, Pitot HC, Richardson RL, Burch PA, Charboneau JW, Reading CC, Lewis BD, Stahl S, Akporiaye ET, Harris DT. Phase I study of immunotherapy of hepatic metastases of colorectal carcinoma by direct gene transfer of an allogeneic histocompatibility antigen, HLA-B7. Gene Ther 1997; 4: 419-425
77. Vanhoefer U. Molecular mechanisms and targeting of colorectal cancer. Semin Oncol 2005; 32: 7-10
78. 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
79. 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
80. 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. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-1964
81. Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, Solary E, Le Cesne A, Zitvogel L, Chauffert B. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007; 56: 641-648
82. Pardoll D, Allison J. Cancer immunotherapy: breaking the barriers to harvest the crop. Nat Med 2004; 10: 887-892
83. Takikawa O, Kuroiwa T, Yamazaki F, Kido R. Mechanism of interferon-gamma action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J Biol Chem 1988; 263: 2041-2048