Immune checkpoints and immunotherapy for colorectal cancer

Gastroenterology Report

Volumn 3, Issue 4, 2015, Pages 289-297

  Singh, Preet Paul ^a   Sharma, Piyush K ^a   Krishnan, Gayathri ^a   Lockhart, A Craig ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Checkpoint inhibition blockade; Colorectal cancer; Cytotoxic Tlymphocyte associated antigen 4 (CTLA 4); Immunotherapy; Pembrolizumab; Programmed death 1 (PD 1); Vaccine

Indexed keywords

EID: 85045371624     PISSN: None     EISSN: 20520034     Source Type: Journal    
DOI: 10.1093/gastro/gov053     Document Type: Review

References (77)

1. Torre LA, Bray F, Siegel RL et al. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87-108.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
3. Kerr D. Clinical development of gene therapy for colorectal cancer. Nat Rev Cancer 2003;3:615-22.
4. Cunningham D, Atkin W, Lenz HJ et al. Colorectal cancer. Lancet 2010;375:1030-47.
5. Oberg A, Samii S, Stenling R et al. Different occurrence of CD8+, CD45R0+, and CD68+ immune cells in regional lymph node metastases from colorectal cancer as potential prognostic predictors. Int J Colorectal Dis 2002;17:25-9.
6. Galon J, Costes A, Sanchez-Cabo F et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
7. Pages F, Kirilovsky A, Mlecnik B et al. In situ cytotoxic and memory T-cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009;27:5944-51.
8. Hodi FS, O'Day SJ, McDermott DF et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
9. Ribats A, Puzanov I, Dummer R et al. Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): A randomised, controlled, phase 2 trial. Lancet Oncol 2015;16:908-18.
10. Brahmer J, Reckamp KL, Baas P et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N Engl J Med 2015;373:123-35.
11. Greenwald RJ, Boussiotis VA, Lorsbach RB et al. CTLA-4 regulates induction of anergy in vivo. Immunity 2001;14:145-55.
12. Waterhouse P, Penninger JM, Timms E et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995;270:985-8.
13. Takahashi T, Tagami T, Yamazaki S et al. Immunologic selftolerance maintained by CD25(+)CD4(+) regulatory T-cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000;192:303-10.
14. Read S, Greenwald R, Izcue A et al. Blockade of CTLA-4 on CD4+CD25+regulatory T-cells abrogates their function in vivo. J Immunol 2006;177:4376-83.
15. Leach DR, Krummel MF, Allison JP. Enhancement of anti-tumor immunity by CTLA-4 blockade. Science 1996;271:1734-6.
16. Jure-Kunkel M, Masters G, Girit E et al. Synergy between chemotherapeutic agents and CTLA-4 blockade in preclinical tumor models. Cancer Immunol Immunother 2013;62: 1533-45.
17. Dewan MZ, Galloway AE, Kawashima n et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 2009;15:5379-88.
18. Kocak E, Lute K, Chang X et al. Combination therapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res 2006;66:7276-84.
19. Dong H, Strome SE, Salomao DR et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 2002;8:793-800.
20. Yamazaki T, Akiba H, Iwai H et al. Expression of programmed death 1 ligands by murine T-cells and APC. J Immunol 2002;169:5538-45.
21. Eppihimer MJ, Gunn J, Freeman GJ et al. Expression and regulation of the PD-L1 immunoinhibitory molecule on microvascular endothelial cells. Microcirculation 2002;9:133-45.
22. Nishimura H, Nose M, Hiai H et al. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999;11:141-51.
23. Kim K, Skora AD, Li Z et al. Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc Natl Acad Sci USA 2014;111:11774-9.
24. Iwai Y, Terawaki S, Honjo T. PD-1 blockade inhibits hematogenous spread of poorly immunogenic tumor cells by enhanced recruitment of effector T-cells. Int Immunol 2005;17:133-44.
25. Yu P, Steel JC, Zhang M et al. Simultaneous blockade of multiple immune system inhibitory checkpoints enhances anti-tumor activity mediated by interleukin-15 in a murine metastatic colon carcinoma model. Clin Cancer Res 2010;16:6019-28.
26. Deng L, Liang H, Burnette B et al. Irradiation and anti-PD-L1 treatment synergistically promote anti-tumor immunity in mice. J Clin Invest 2014;124:687-95.
27. Duraiswamy J, Kaluza KM, Freeman GJ et al. Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors. Cancer Res 2013;73:3591-603.
28. Huard B, Tournier M, Hercend T et al. Lymphocyte-activation gene 3/major histocompatibility complex class II interaction modulates the antigenic response of CD4+ T lymphocytes. Eur J Immunol 1994;24:3216-21.
29. Huang CT, Workman CJ, Flies D et al. Role of LAG-3 in regulatory T-cells. Immunity 2004;21:503-13.
30. Workman CJ, Cauley LS, Kim IJ et al. Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T-cell population following antigen activation in vivo. J Immunol 2004;172:5450-5.
31. Workman CJ and Vignali DA. The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T-cells. Eur J Immunol 2003;33:970-9.
32. Grosso JF, Kelleher CC, Harris TJ et al. LAG-3 regulates CD8+ T-cell accumulation and effector function in murine self- and tumor-tolerance systems. J Clin Invest 2007;117:3383-92.
33. Blackburn SD, Shin H, HainingWN et al. Coregulation of CD8+ T-cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009;10:29-37.
34. Tesniere A, Schlemmer F, Boige V et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010;29:482-91.
35. Correale P, Tagliaferri P, Fioravanti A 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.
36. Correale P, Botta C, Rotundo MS et al. Gemcitabine, oxaliplatin, levofolinate, 5-fluorouracil, granulocyte-macrophage colony-stimulating factor, and interleukin-2 (GOLFIG) versus FOLFOX chemotherapy in metastatic colorectal cancer patients: The GOLFIG-2 multicentric open-label randomized phase II I trial. J Immunother 2014;37:26-35.
37. Topalian SL, Hodi FS, Brahmer JR et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
38. Topalian SL, Sznol M, McDermott DF et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014;32:1020-30.
39. Ansell SM, Lesokhin AM, Borrello I et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med 2015;372:311-19.
40. Herbst RS, Soria JC, Kowanetz M et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515:563-7.
41. Taube JM, Klein A, Brahmer JR et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014;20:5064-74.
42. Lipson EJ, Sharfman WH, Drake CG et al. Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013;19:462-8.
43. Le, DT Uram, JN Wang, H et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. N Engl J Med 2015;372:2509-20.
44. Brahmer JR, Tykodi SS, Chow LQ et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
45. Herbst RS, Gordon MS, Fine GD et al. A study of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic tumors. In ASCO Annual Meeting Proceedings. 2013;3000.
46. Bendell JC, Powderly JD, Lieu CH et al. Safety and efficacy of MPDL3280A (anti-PDL1) in combination with bevacizumab (bev) and/or FOLFOX in patients (pts) with metastatic colorectal cancer (mCRC). In ASCO Annual Meeting Proceedings. 2015;704.
47. Goldstein J, Tran B, Ensor J et al. Multicenter retrospective analysis of metastatic colorectal cancer (CRC) with high-level microsatellite instability (MSI-H). Ann Oncol 2014;25:1032-8.
48. Koopman M, Kortman GA, Mekenkamp L et al. Deficient mismatch repair system in patients with sporadic advanced colorectal cancer. Br J Cancer 2009;100:266-73.
49. Segal NH, Parsons DW, Peggs KS et al. Epitope landscape in breast and colorectal cancer. Cancer Res 2008;68:889-92.
50. Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487:330-7.
51. Timmermann B, Kerick M, Roehr C et al. Somatic mutation profiles of MSI and MSS colorectal cancer identified by whole exome next generation sequencing and bioinformatics analysis. PLoS One 2010;5:e15661.
52. Dolcetti R, Viel A, Doglioni C et al. High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability. Am J Pathol 1999;154:1805-13.
53. Smyrk TC, Watson P, Kaul K et al. Tumor-infiltrating lymphocytes are a marker for microsatellite instability in colorectal carcinoma. Cancer 2001;91:2417-22.
54. Zoran G, Snyder C, Yeatts K et al. Programmed death 1 (PD-1) lymphocytes and ligand (PD-L1) in colorectal cancer and their relationship to microsatellite instability status. J Clin Oncol 2014;32:5s.
55. Chung KY, Gore I, Fong L et al. Phase II study of the anticytotoxic T-lymphocyte-associated antigen 4monoclonal antibody, tremelimumab, in patients with refractory metastatic colorectal cancer. J Clin Oncol 2010;28:3485-90.
56. Llosa NJ, Cruise M, Tam A et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov 2015;5:43-51.
57. Harris JE, Ryan L, Hoover HC, Jr.et al. 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;18:148-57.
58. Vermorken JB, Claessen AM, van Tinteren H et al. Active specific immunotherapy for stage II and stage III human colon cancer: A randomised trial. Lancet 1999;353:345-50.
59. Hanna MG, Jr., Hoover HC, Jr., Vermorken JB et al. Adjuvant active specific immunotherapy of stage II and stage III colon cancer with an autologous tumor cell vaccine: First randomized phase II I trials show promise. Vaccine 2001;19:2576-82.
60. Lokhov PG and Balashova EE. Cellular cancer vaccines: An update on the development of vaccines generated from cell surface antigens. J Cancer 2010;1:230-41.
61. Schlag P, Manasterski M, Gerneth T 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.
62. Schulze T, Kemmner W, Weitz J et al. 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.
63. Nemunaitis J. Vaccines in cancer: GVAX, a GM-CSF gene vaccine. Expert Rev Vaccines 2005;4:259-74.
64. Staff C, Mozaffari F, Haller BK et al. A Phase I safety study of plasmid DNA immunization targeting carcinoembryonic antigen in colorectal cancer patients. Vaccine 2011;29:6817-22.
65. Tsuruma T, Hata F, Torigoe T et al. Phase I clinical study of anti-apoptosis protein, survivin-derived peptide vaccine therapy for patients with advanced or recurrent colorectal cancer. J Transl Med 2004;2:19.
66. Okuno K, Sugiura F, Hida JI et al. Phase I clinical trial of a novel peptide vaccine in combination with UFT/LV for metastatic colorectal cancer. Exp Ther Med 2011;2:73-9.
67. Moulton HM, Yoshihara PH, Mason DH et al. 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;8:2044-51.
68. Kaufman HL, Lenz HJ, Marshall J et al. Combination chemotherapy and ALVAC-CEA/B7.1 vaccine in patients with metastatic colorectal cancer. Clin Cancer Res 2008;14: 4843-9.
69. Celluzzi CM, Mayordomo JI, Storkus WJ et al. Peptide-pulsed dendritic cells induce antigen-specific CTL-mediated protective tumor immunity. J Exp Med 1996;183:283-7.
70. Koido S, Kashiwaba M, Chen D et al. Induction of anti-tumor immunity by vaccination of dendritic cells transfected with MUC1 RNA. J Immunol 2000;165:5713-19.
71. Nestle FO, Alijagic S, Gilliet M et al. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 1998;4:328-32.
72. Morse MA, Deng Y, Coleman D et al. 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;5:1331-8.
73. Fong L, Hou Y, Rivas A et al. Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc Natl Acad Sci U S A 2001;98:8809-14.
74. Soda H, Koda K, Yasutomi J et al. Adoptive immunotherapy for advanced cancer patients using in vitro activated cytotoxic T lymphocytes. J Surg Oncol 1999;72:211-17.
75. Parkhurst MR, Yang JC, Langan RC 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.
76. Morgan RA, Yang JC, Kitano M et al. Case report of a serious adverse event following the administration of T-cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010;18:843-51.
77. Hoos A, Eggermont AM, Janetzki S et al. Improved Endpoints for Cancer Immunotherapy Trials. J Nat Cancer Inst 2010;102:1388-97.