Immunotherapy for metastatic colorectal cancer: Present status and new options

Scandinavian Journal of Gastroenterology

Volumn 47, Issue 3, 2012, Pages 315-324

  Ellebaek, Eva ^a   Andersen, Mads Hald ^a   Svane, Inge Marie ^a   Straten, Per Thor ^a  

^a GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

adoptive transfer; cancer vaccines; colorectal neoplasms; immunotherapy

Indexed keywords

13 CIS RETINOID ACID; CANCER VACCINE; DENDRITIC CELL VACCINE; DNA VACCINE; FLUOROURACIL; FOLINIC ACID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 2; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; OXALIPLATIN; RETINOIC ACID; TUMOR CELL VACCINE; UNCLASSIFIED DRUG;

ADOPTIVE CELL THERAPY; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER STAGING; CANCER THERAPY; COLORECTAL CANCER; HUMAN; IMMUNOGENICITY; PRIORITY JOURNAL; REVIEW;

ANTIGENS, NEOPLASM; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; COLORECTAL NEOPLASMS; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE;

EID: 84857161934     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.3109/00365521.2012.640831     Document Type: Review

References (60)

1. Higano CS, Small EJ, Schellhammer P, Yasothan U, Gubernick S, Kirkpatrick P, et al. Sipuleucel-T. Nat Rev Drug Discov 2010;9:513-14.
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl JMed 2010;363:711-23.
3. Robert C, Thomas L, Bondarenko I, O'Day S, Garbe C, Lebbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364: 2517-26.
4. Poschke I, Mougiakakos D, Kiessling R. Camouflage and sabotage: tumor escape from the immune system. Cancer Immunol Immunother 2011; [Epub ahead of print].
5. Ohtani H. Focus on TILs: prognostic significance of tumor infiltrating lymphocytes in human colorectal cancer. Cancer Immun 2007;7:4.
6. Di GA, Botti C, Tocchi A, Mingazzini P, Flammia M. The influence of tumor lymphocytic infiltration on long term survival of surgically treated colorectal cancer patients. Int Surg 1992;77:256-60.
7. Deschoolmeester V, Baay M, Van ME, Weyler J, Vermeulen P, Lardon F, et al. Tumor infiltrating lymphocytes: an intriguing player in the survival of colorectal cancer patients. BMC Immunol 2010;11:19.
8. Dutcher J. Current status of interleukin-2 therapy for metastatic renal cell carcinoma and metastatic melanoma. Oncology (Williston Park) 2002;16(11 Suppl 13):4-10.
9. Grande C, Firvida JL, Navas V, Casal J. Interleukin-2 for the treatment of solid tumors other than melanoma and renal cell carcinoma. Anticancer Drugs 2006;17:1-12.
10. Recchia F, Saggio G, Cesta A, Candeloro G, Di BA, Amiconi G, et al. Phase II study of interleukin-2 and 13- cis-retinoic acid as maintenance therapy in metastatic colorectal cancer. Cancer Immunol Immunother 2007;56: 699-708. (Pubitemid 46348737)
11. Gjertsen MK, Bakka A, Breivik J, Saeterdal I, Solheim BG, Soreide O, et al. Vaccination with mutant ras peptides and induction of T-cell responsiveness in pancreatic carcinoma patients carrying the corresponding RAS mutation. Lancet 1995;346:1399-400.
12. Tsang KY, Zaremba S, Nieroda CA, Zhu MZ, Hamilton JM, Schlom J. Generation of human cytotoxic T cells specific for human carcinoembryonic antigen epitopes from patients immunized with recombinant vaccinia- CEA vaccine. J Natl Cancer Inst 1995;87:982-90.
13. Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 2007;117: 1147-54.
14. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, Parmentier N, et al. Evidence for a tumoral immuneresistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 2003;9:1269-74. (Pubitemid 37279849)
15. Sorensen RB, Hadrup SR, Svane IM, Hjortso MC, Thor SP, Andersen MH. Indoleamine 2,3-dioxygenase specific, cytotoxic T cells as immune regulators. Blood 2011;117: 2200-10.
16. Sorensen RB, Berge-Hansen L, Junker N, Hansen CA, Hadrup SR, Schumacher TN, et al. The immune system strikes back: cellular immune responses against indoleamine 2,3-dioxygenase. PLoS ONE 2009;4:e6910.
17. Menon AG, Kuppen PJ, van der Burg SH, Offringa R, Bonnet MC, Harinck BI, et al. Safety of intravenous administration of a canarypox virus encoding the human wild-type p53 gene in colorectal cancer patients. Cancer Gene Ther 2003;10:509-17. (Pubitemid 36842008)
18. Saeterdal I, Bjorheim J, Lislerud K, Gjertsen MK, Bukholm IK, Olsen OC, et al. Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer. Proc Natl Acad Sci USA 2001;98: 13255-60. (Pubitemid 33051349)
19. Andersen MH, Fensterle J, Ugurel S, Reker S, Houben R, Guldberg P, et al. Immunogenicity of constitutively active V599EBRaf. Cancer Res 2004;64:5456-60.
20. Toubaji A, Achtar M, Provenzano M, Herrin VE, Behrens R, Hamilton M, et al. Pilot study of mutant ras peptide-based vaccine as an adjuvant treatment in pancreatic and colorectal cancers. Cancer Immunol Immunother 2008; 57:1413-20.
21. Moulton HM, Yoshihara PH, Mason DH, Iversen PL, Triozzi PL. Active specific immunotherapy with a betahuman chorionic gonadotropin peptide vaccine in patients with metastatic colorectal cancer: antibody response is associated with improved survival. Clin Cancer Res 2002;8: 2044-51. (Pubitemid 34753572)
22. Posner MC, Niedzwiecki D, Venook AP, Hollis DR, Kindler HL, Martin EW, et al. 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;15:158-64.
23. Conry RM, Curiel DT, Strong TV, Moore SE, Allen KO, Barlow DL, et al. Safety and immunogenicity of a DNA vaccine encoding carcinoembryonic antigen and hepatitis B surface antigen in colorectal carcinoma patients. Clin Cancer Res 2002;8:2782-7. (Pubitemid 35025720)
24. Hoover HC Jr, Brandhorst JS, Peters LC, Surdyke MG, Takeshita Y, Madariaga J, et al. Adjuvant active specific immunotherapy for human colorectal cancer: 6.5-year median follow-up of a phase III prospectively randomized trial. J Clin Oncol 1993;11:390-9. (Pubitemid 23071033)
25. Vermorken JB, Claessen AM, van TH, Gall HE, Ezinga R, Meijer S, et al. Active specific immunotherapy for stage II and stage III human colon cancer: a randomised trial. Lancet 1999;353:345-50. (Pubitemid 29088160)
26. Schlag P, Manasterski M, Gerneth T, Hohenberger P, Dueck M, Herfarth C, et al. Active specific immunotherapy with Newcastle-disease-virus-modified autologous tumor cells following resection of liver metastases in colorectal cancer. First evaluation of clinical response of a phase II-trial. Cancer Immunol Immunother 1992;35:325-30.
27. 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;58:61-9.
28. Hanna MG Jr, Hoover HC Jr, Vermorken JB, Harris JE, Pinedo HM. Adjuvant active specific immunotherapy of stage II and stage III colon cancer with an autologous tumor cell vaccine: first randomized phase III trials show promise. Vaccine 2001;19:2576-82. (Pubitemid 32234275)
29. Fong L, Engleman EG. Dendritic cells in cancer immunotherapy. Annu Rev Immunol 2000;18:245-73. (Pubitemid 30365381)
30. Fong L, Hou Y, Rivas A, Benike C, Yuen A, Fisher GA, et al. Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc Natl Acad Sci USA 2001;98:8809-14. (Pubitemid 32678109)
31. Kavanagh B, Ko A, Venook A, Margolin K, Zeh H, Lotze M, et al. Vaccination of metastatic colorectal cancer patients with matured dendritic cells loaded with multiple major histocompatibility complex class I peptides. J Immunother 2007;30:762-72. (Pubitemid 47480759)
32. Babatz J, Rollig C, Lobel B, Folprecht G, Haack M, Gunther H, et al. Induction of cellular immune responses against carcinoembryonic antigen in patients with metastatic tumors after vaccination with altered peptide ligand-loaded dendritic cells. Cancer Immunol Immunother 2006;55: 268-76. (Pubitemid 41682575)
33. Morse MA, Nair SK, Mosca PJ, Hobeika AC, Clay TM, Deng Y, et al. Immunotherapy with autologous, human dendritic cells transfected with carcinoembryonic antigen mRNA. Cancer Invest 2003;21:341-9. (Pubitemid 37055665)
34. Liu KJ, Wang CC, Chen LT, Cheng AL, Lin DT, Wu YC, et al. Generation of carcinoembryonic antigen (CEA)-specific T-cell responses in HLA-A. *0201 and HLA-A. *2402 late-stage colorectal cancer patients after vaccination with dendritic cells loaded with CEA peptides. Clin Cancer Res 2004;10:2645-51.
35. Matsuda K, Tsunoda T, Tanaka H, Umano Y, Tanimura H, Nukaya I, et al. Enhancement of cytotoxic T-lymphocyte responses in patients with gastrointestinal malignancies following vaccination with CEA peptide-pulsed dendritic cells. Cancer Immunol Immunother 2004;53:609-16. (Pubitemid 38858334)
36. Emens LA. Chemoimmunotherapy. Cancer J 2010;16: 295-303.
37. Lesterhuis WJ, de VI, Aarntzen EA, de BA, Scharenborg NM, van de RM, et al. A pilot study on the immunogenicity of dendritic cell vaccination during adjuvant oxaliplatin/capecitabine chemotherapy in colon cancer patients. Br J Cancer 2010;103:1415-21.
38. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotheray for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-57. (Pubitemid 46218728)
39. Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, et al. 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;56:641-8. (Pubitemid 46348738)
40. Locher C, Conforti R, Aymeric L, Ma Y, Yamazaki T, Rusakiewicz S, et al. Desirable cell death during anticancer chemotherapy. Ann NY Acad Sci 2010;1209:99-108.
41. Apetoh L, Vegran F, Ladoire S, Ghiringhelli F. Restoration of antitumor immunity through selective inhibition of myeloid derived suppressor cells by anticancer therapies. Curr Mol Med 2011;5:365-72.
42. Backus HH, Dukers DF, van Groeningen CJ, Vos W, Bloemena E, Wouters D, et al. 5-Fluorouracil induced Fas upregulation associated with apoptosis in liver metastases of colorectal cancer patients. Ann Oncol 2001;12:209-16. (Pubitemid 32223870)
43. Harrop R, Connolly N, Redchenko I, Valle J, Saunders M, Ryan MG, et al. Vaccination of colorectal cancer patients with modified vaccinia Ankara delivering the tumor antigen 5T4 (TroVax) induces immune responses which correlate with disease control: a phase I/II trial. Clin Cancer Res 2006; 12(11 Pt 1):3416-24.
44. Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW, et al. Vaccination of colorectal cancer patients with modified vaccinia ankara encoding the tumor antigen 5T4 (TroVax) given alongside chemotherapy induces potent immune responses. Clin Cancer Res 2007; 13(15 Pt 1):4487-94. (Pubitemid 47219718)
45. Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW, et al. Vaccination of colorectal cancer patients with TroVax given alongside chemotherapy (5-fluorouracil, leukovorin and irinotecan) is safe and induces potent immune responses. Cancer Immunol Immunother 2008;57:977-86.
46. Correale P, Cusi MG, Tsang KY, Del Vecchio MT, Marsili S, Placa ML, et al. 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 2005;23:8950-8. (Pubitemid 46211480)
47. Correale P, Tagliaferri P, Fioravanti A, Del Vecchio MT, Remondo C, Montagnani F, et al. Immunity feedback and clinical outcome in colon cancer patients undergoing chemoimmunotherapy with gemcitabine + FOLFOX followed by subcutaneous granulocyte macrophage colonystimulating factor and aldesleukin (GOLFIG-1 Trial). Clin Cancer Res 2008;14:4192-9.
48. Correale P, Rotundo MS, Del Vecchio MT, Remondo C, Migali C, Ginanneschi C, et al. Regulatory (FoxP3+) T-cell tumor infiltration is a favourable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy. J Immunother 2010;33:435-41.
49. Gardini A, Ercolani G, Riccobon A, Ravaioli M, Ridolfi L, Flamini E, et al. Adjuvant, adoptive immunotherapy with tumor infiltrating lymphocytes plus interleukin-2 after radical hepatic resection for colorectal liver metastases: 5-year analysis. J Surg Oncol 2004;87:46-52. (Pubitemid 38880279)
50. Marits P, Karlsson M, Dahl K, Larsson P, Wanders A, Thorn M, et al. Sentinel node lymphocytes: tumour reactive lymphocytes identified intraoperatively for the use inimmunotherapy of colon cancer. Br J Cancer 2006;94: 1478-84. (Pubitemid 43772284)
51. Karlsson M, Marits P, Dahl K, Dagoo T, Enerback S, Thorn M, et al. Pilot study of sentinel-node-based adoptive immunotherapy in advanced colorectal cancer. Ann Surg Oncol 2010;17:1747-57.
52. Rapoport AP, Aqui NA, Stadtmauer EA, Vogl DT, Fang HB, Cai L, et al. Combination immunotherapy using adoptive T-cell transfer and tumor antigen vaccination on the basis of hTERT and survivin after ASCT for myeloma. Blood 2011;117:788-97.
53. Hombach A, Schlimper C, Sievers E, Frank S, Schild HH, Sauerbruch T, et al. A recombinant anti-carcinoembryonic antigen immunoreceptor with combined CD3zeta- CD28 signalling targets T cells from colorectal cancer patients against their tumour cells. Gut 2006;55:1156-64. (Pubitemid 44085685)
54. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011;19:620-6.
55. Heslop HE. Safer CARS. Mol Ther 2010;18:661-2.
56. Kojima R, Kami M, Hori A, Murashige N, Ohnishi M, Kim SW, et al. Reduced-intensity allogeneic hematopoietic stem-cell transplantation as an immunotherapy for metastatic colorectal cancer. Transplantation 2004;78:1740-6. (Pubitemid 40041640)
57. Hentschke P, Barkholt L, Uzunel M, Mattsson J, Wersall P, Pisa P, et al. Low-intensity conditioning and hematopoietic stem cell transplantation in patients with renal and colon carcinoma. Bone Marrow Transplant 2003;31:253-61. (Pubitemid 36336227)
58. Aglietta M, Barkholt L, Schianca FC, Caravelli D, Omazic B, Minotto C, et al. Reduced-intensity allogeneic hematopoietic stem cell transplantation in metastatic colorectal cancer as a novel adoptive cell therapy approach. The European group for blood and marrow transplantation experience. Biol Blood Marrow Transplant 2009;15:326-35.
59. Carnevale-Schianca F, Cignetti A, Capaldi A, Vitaggio K, Vallario A, Ricchiardi A, et al. Allogeneic nonmyeloablative hematopoietic cell transplantation in metastatic colon cancer: tumor-specific T cells directed to a tumor-associated antigen are generated in vivo during GVHD. Blood 2006;107:3795-803.
60. Hoos A, Eggermont AM, Janetzki S, Hodi FS, Ibrahim R, Anderson A, et al. Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst 2010;102:1388-97.