Modulation of immune system inhibitory checkpoints in colorectal cancer

Current Colorectal Cancer Reports

Volumn 9, Issue 4, 2013, Pages 391-397

  Patel, Sandip P ^a   Osada, Takuya ^a   Osada, Koya ^a   Hurwitz, Herbert ^a   Lyerly, H Kim ^a   Morse, Michael A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Colon cancer; Colorectal cancer; CTLA 4; Immune checkpoint; Immunomodulation; Ipilimumab; Lambrolizumab; MCRC; Nivolumab; PD 1; PD L1; Tremelimumab; Vaccine

Indexed keywords

BEVACIZUMAB; BMS 936559; BMS 93658; CARBOPLATIN; CD137 LIGAND; CETUXIMAB; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 12; IPILIMUMAB; LAMBROLIZUMAB; MASITINIB; MEDI 4736; MK 3475; MPDL 3280A; NIVOLUMAB; OX40 LIGAND; OXALIPLATIN; PACLITAXEL; PIDILIZUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; SUNITINIB; TICILIMUMAB; UNCLASSIFIED DRUG;

ADVANCED CANCER; ARTICLE; AUTOIMMUNITY; CANCER CONTROL; CANCER PROGNOSIS; CANCER REGRESSION; CANCER SURVIVAL; COLORECTAL CANCER; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSTIMULATION; IMMUNOSURVEILLANCE; KIDNEY CARCINOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; LYMPHOCYTIC INFILTRATION; LYMPHOMA; MACROPHAGE; MELANOMA; METASTATIC COLORECTAL CANCER; METASTATIC MELANOMA; MYELOMA; NONHUMAN; OUTCOME ASSESSMENT; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; PROTEIN EXPRESSION; SOLID TUMOR; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 84892439961     PISSN: 15563790     EISSN: 15563804     Source Type: Journal    
DOI: 10.1007/s11888-013-0184-3     Document Type: Article

References (65)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin. 2011;61:69-90.
2. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350:2335-42.
3. Sandler A, Gray R, Ph D, et al.. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. 2006; 2542-2550
4. Chu E. An update on the current and emerging targeted agents in metastatic colorectal cancer. Clin Colorectal Cancer. 2012;11:1-13.
5. Pagès F, Galon J, Dieu-Nosjean M-C, et al. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene. 2010;29:1093-102.
6. Osada T, Hsu D, Hammond S, et al. Metastatic colorectal cancer cells from patients previously treated with chemotherapy are sensitive to T cell killing mediated by CEA/CD3-bispecific T cell-engaging BiTE antibody. Br J Cancer. 2009;102:124-33.
7. Ferrone C, Dranoff G. Dual roles for immunity in gastrointestinal cancers. J Clin Oncol. 2010;28:4045-51.
8. Ellebaek E, Andersen MH, Svane IM, et al. Immunotherapy for metastatic colorectal cancer: Present status and new options. Scand j gastroenterol. 2012;47:315-24.
9. Boghossian S, Robinson S, Von Delwig A, et al. Immunotherapy for treating metastatic colorectal cancer. Surg Oncol. 2012;21:67-77.
10. 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.
11. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (Anti-PD-1) in Melanoma. N Engl J Med 0:null
12. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 0:null
13. 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. Large phase 1 trial assessing anti-PD-1 and establishment of PD-L1 on tumor as putative predictive biomarker for response.
14. Brahmer JR, Tykodi SS, Chow LQM, et al. Safety and Activity of Anti-PD-L1 Antibody in Patients with Advanced Cancer. N Engl J Med. 2012;366:2455-65. Large phase 1 trial assessing anti-PD-L1 therapy.
15. Prieto PA, Yang JC, Sherry RM, et al. CTLA-4 Blockade with Ipilimumab: Long-term Follow-up of 177 Patients with Metastatic Melanoma. Clin Cancer Res. 2012;18:2039-47.
16. Bretscher PA. A two-step, two-signal model for the primary activation of precursor helper Tcells. Proc Natl Acad Sci. 1999;96:185-90.
17. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252-64. Excellent review of basic biology of immune checkpoints and translational development of immune checkpoint inhibitors.
18. Peggs KS, Quezada SA, Chambers CA, et al. Blockade of CTLA-4 on both effector and regulatory Tcell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J exp med. 2009;206:1717-25.
19. Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270:985-8.
20. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271:1734-6.
21. Keir ME, Liang SC, Guleria I, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J exp med. 2006;203:883-95.
22. Francisco LM, Salinas VH, Brown KE, et al.: PD-L1 regulates the development , maintenance , and function of induced regulatory T cells. 206:3015-3029, 2009
23. Curran MA, Montalvo W, Yagita H, et al. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci. 2010;107:4275-80.
24. Sharpe AH, Wherry EJ, Ahmed R, et al. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol. 2007;8:239-45.
25. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. nature. 2005;439:682-7.
26. Zou W, Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol. 2008;8:467-77.
27. Blank C, Gajewski T, Mackensen A. Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy. Cancer Immunol Immunother. 2005;54:307-14.
28. Blank C, Mackensen A. Contribution of the PD-L1/PD-1 pathway to T cell exhaustion: an update on implications for chronic infections and tumor evasion. Cancer Immunol Immunother. 2007;56:739-45.
29. Iwai Y, Ishida M, Tanaka Y, et al. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci. 2002;99:12293-7.
30. Hamanishi J, Mandai M, Iwasaki M, et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci. 2007;104:3360-5.
31. Hino R, Kabashima K, Kato Y, et al. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor formalignant melanoma. Cancer. 2010;116:1757-66.
32. Mu C-Y, Huang J-A, Chen Y, et al. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol. 2011;28:682-8.
33. Thompson RH, Kuntz SM, Leibovich BC, et al. Tumor B7-H1 Is Associated with Poor Prognosis in Renal Cell Carcinoma Patients with Long-term Follow-up. Cancer Res. 2006;66:3381-5.
34. 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.
35. Ogino S, Nosho K, Irahara N, et al. Lymphocytic Reaction to Colorectal Cancer Is Associated with Longer Survival, Independent of Lymph Node Count, Microsatellite Instability, and CpG IslandMethylator Phenotype. Clin Cancer Res. 2009;15:6412-20.
36. Pagès F, Berger A, Camus M, et al. Effector Memory T Cells, Early Metastasis, and Survival in Colorectal Cancer. N Engl J Med. 2005;353:2654-66.
37. Pagès 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. Development of prognostic immunoscore assessing effector and memory T cells within colorectal tumor specimens which are associated with improved prognosis.
38. Naito Y, Saito K, Shiiba K, et al. CD8+ T Cells Infiltrated within Cancer Cell Nests as a Prognostic Factor in Human Colorectal Cancer. Cancer Res. 1998;58:3491-4.
39. Salama P, Phillips M, Grieu F, et al. Tumor-Infiltrating FOXP3+ T Regulatory Cells Show Strong Prognostic Significance in Colorectal Cancer. J Clin Oncol. 2009;27:186-92.
40. 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.
41. 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.
42. Hirano F, Kaneko K, Tamura H, et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer res. 2005;65:1089-96.
43. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes Tcell apoptosis: a potentialmechanism of immune evasion. Nat med. 2002;8:793-800.
44. M. Grimm MG, M. Koenigshausen, C. Stein, J. Lutz, S. Krol, A. Thiede, U. Heemann and A. Waaga-Gasser: Abstract: Clinical significance and therapeutic potential of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human colorectal cancer. J Clin Oncol 26;: suppl 15005 (ASCO Meeting Abstracts), 2008
45. Terme M, Ullrich E, Aymeric L, et al. IL-18 Induces PD-1-Dependent Immunosuppression in Cancer. Cancer Res. 2011;71:5393-9.
46. 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.
47. Yu P, Steel JC, Zhang M, et al. Simultaneous Blockade of Multiple Immune System Inhibitory Checkpoints Enhances Antitumor Activity Mediated by Interleukin-15 in a Murine Metastatic Colon Carcinoma Model. Clin Cancer Res. 2010;16:6019-28.
48. Ngiow SF, von Scheidt B, Akiba H, et al. Anti-TIM3 Antibody Promotes T Cell IFN-γ-Mediated Antitumor Immunity and Suppresses Established Tumors. Cancer res. 2011;71:3540-51.
49. Sakuishi K, Apetoh L, Sullivan JM, et al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med. 2010;207:2187-94.
50. Tel J, Hato SV, Torensma R, et al. The chemotherapeutic drug oxaliplatin differentially affects blood DC function dependent on environmental cues. Cancer Immunol Immunother. 2012;61:1101-11.
51. Lesterhuis WJ, Punt CJ, Hato SV, et al. Platinum-based drugs disrupt STAT6-mediated suppression of immune responses against cancer in humans and mice. J clin investig. 2011;121:3100.
52. Pander J, Heusinkveld M, van der Straaten T, et al. Activation of Tumor-Promoting Type 2 Macrophages by EGFR-Targeting Antibody Cetuximab. Clin Cancer Res. 2011;17:5668-73.
53. Pander J, Gelderblom H, Antonini NF, et al. Correlation of FCGR3A and EGFR germline polymorphisms with the efficacy of cetuximab in KRAS wild-type metastatic colorectal cancer. Eur j cancer (Oxford, England : 1990). 2010;46:1829-34.
54. Simon Pernot MT, Marcheteau E, Voron T, Colussi O, Tartour E, Taïeb J. Impact of antiangiogenic treatments on exhausted PD-1+ T lymphocytes in colorectal cancer. J Clin Oncol, 2013
55. Petty JK, He K, Corless CL, et al. Survival in human colorectal cancer correlates with expression of the Tcell costimulatorymolecule OX-40 (CD134). Am J Surg. 2002;183:512-8.
56. Pan PY, Zang Y, Weber K, et al. OX40 ligation enhances primary and memory cytotoxic T lymphocyte responses in an immunotherapy for hepatic colon metastases. Mol Ther. 2002;6:528-36.
57. Martinet O, Ermekova V, Qiao JQ, et al. Immunomodulatory Gene TherapyWith Interleukin 12 and 4-1BB Ligand: Long-Term Remission of Liver Metastases in a Mouse Model. J Natl Cancer Inst. 2000;92:931-6.
58. Yang JC, Hughes M, Kammula U, et al. Ipilimumab (Anti-CTLA4 Antibody) Causes Regression of Metastatic Renal Cell Cancer Associated With Enteritis and Hypophysitis. J Immunother. 2007;30:825-30. doi:10.1097/CJI.0b013e318156e47e.
59. Lynch T, Bondarenko I, Luft A, et al. Phase II trial of ipilimumab (IPI) and paclitaxel/carboplatin (P/C) in first-line stage IIIb/IV nonsmall cell lung cancer (NSCLC). J Clin Oncol. 2010;28:7531.
60. NCT01769222: Ipilimumab and Local Radiation Therapy in Treating Patients With Recurrent Melanoma, Non-Hodgkin Lymphoma, Colon, or Rectal Cancer (Phase 1/2).
61. Chung KY, Gore I, Fong L, et al. Phase II Study of theAnti-Cytotoxic T-Lymphocyte-Associated Antigen 4 Monoclonal Antibody, Tremelimumab, in Patients With Refractory Metastatic Colorectal Cancer. J Clin Oncol. 2010;28:3485-90.
62. Wolchok JD, Hoos A, O'Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412-20. Excellent overview of the novel immune response criteria and definitions of progression related to all immunotherapeutics.
63. Hoos A, Eggermont AMM, Janetzki S, et al. Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst. 2010;102:1388-97. Comprehensive overview of the pitfalls of classical clinial trial design and statistical criteria in evaluating immunotherapy.
64. Ribas A, Kefford R, Marshall MA, et al. Phase III Randomized Clinical Trial Comparing Tremelimumab With Standard-of-Care Chemotherapy in Patients With Advanced Melanoma. J Clin Oncol. 2013;31:616-22.
65. Brahmer JR, Drake CG, Wollner I, et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol. 2010;28:3167-75.