Ipilimumab augments antitumor activity of bispecific antibody-armed T cells

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Yano, Hiroshi ^a   Thakur, Archana ^a   Tomaszewski, Elyse N ^a   Choi, Minsig ^a   Deol, Abhinav ^a   Lum, Lawrence G ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Activated T cells; Bispecific antibody; Burkitt's lymphoma; Colorectal cancer; Cytotoxic T lymphocyte antigen 4 (CTLA 4); Immunotherapy; Ipilimumab; Pancreatic cancer

Indexed keywords

BISPECIFIC ANTIBODY; CD3 ANTIGEN; CXCL9 CHEMOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 2 RECEPTOR; IPILIMUMAB; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; OKT 3; RANTES; RITUXIMAB; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MONOCLONAL ANTIBODY;

ACTIVATED T LYMPHOCYTE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BURKITT LYMPHOMA CELL LINE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG POTENTIATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MOLECULAR DYNAMICS; NATURAL KILLER T CELL; PANCREATIC CANCER CELL LINE; PERIPHERAL BLOOD MONONUCLEAR CELL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT; IMMUNOLOGY; TUMOR CELL LINE;

ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; CELL LINE, TUMOR; CTLA-4 ANTIGEN; HUMANS; T-LYMPHOCYTES;

EID: 84903870609     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-12-191     Document Type: Article

References (41)

1. Kalathil S, Lugade AA, Miller A, Iyer R, Thanavala Y. Higher frequencies of GARP(+)CTLA-4(+)Foxp3(+) T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T-cell functionality. Cancer Res 2013, 73:2435-2444.
2. Suarez N, Alfaro C, Dubrot J, Palazon A, Bolanos E, Erro L, Hervas-Stubbs S, Martinez-Forero I, Morales-Kastresana A, Martin-Algarra S, Sangro B, Lecanda F, Perez-Gracia JL, Gonzalez A, Melero I. Synergistic effects of CTLA-4 blockade with tremelimumab and elimination of regulatory T lymphocytes in vitro and in vivo. International Journal of Cancer 2011, 129:374-386.
3. Maszyna F, Hoff H, Kunkel D, Radbruch A, Brunner-Weinzierl MC. Diversity of clonal T cell proliferation is mediated by differential expression of CD152 (CTLA-4) on the cell surface of activated individual T lymphocytes. J Immunol 2003, 171:3459-3466.
4. Jago CB, Yates J, Camara NO, Lechler RI, Lombardi G. Differential expression of CTLA-4 among T cell subsets. Clin Exp Immunol 2004, 136:463-471.
5. Linsley PS, Nadler SG, Bajorath J, Peach R, Leung HT, Rogers J, Bradshaw J, Stebbins M, Leytze G, Brady W, Malacko AR, Marquardt H, Shaw SY. Binding stoichiometry of the cytotoxic T lymphocyte-associated molecule-4 (CTLA-4). A disulfide-linked homodimer binds two CD86 molecules. The Journal of Biological Chemistry 1995, 270:15417-15424.
6. van der Merwe PA, Bodian DL, Daenke S, Linsley PS, Davis SJ. CD80 (B7-1) Binds Both CD28 and CTLA-4 with a Low Affinity and Very Fast Kinetics. J Exp Med 1997, 185:393-404.
7. Peggs KS, Quezada SA, Korman AJ, Allison JP. Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr Opin Immunol 2006, 18:206-213.
8. Walunas TL, Lenschow DJ, Bakker CY, Linsley PS, Freeman GJ, Green JM, Thompson CB, Bluestone JA. Pillars article: CTLA-4 Can function as a negative regulator of T cell activation. Immunity. 1994. 1: 405-413. J Immunol 2011, 187:3466-3474.
9. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995, 182:459-465.
10. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996, 271:1734-1736.
11. Fecci PE, Ochiai H, Mitchell DA, Grossi PM, Sweeney AE, Archer GE, Cummings T, Allison JP, Bigner DD, Sampson JH. Systemic CTLA-4 blockade ameliorates glioma-induced changes to the CD4+ T cell compartment without affecting regulatory T-cell function. Clin Cancer Res 2007, 13:2158-2167.
12. Sorensen MR, Holst PJ, Steffensen MA, Christensen JP, Thomsen AR. Adenoviral vaccination combined with CD40 stimulation and CTLA-4 blockage can lead to complete tumor regression in a murine melanoma model. Vaccine 2010, 28:6757-6764.
13. Sutmuller RP, van Duivenvoorde LM, van Elsas A, Schumacher TN, Wildenberg ME, Allison JP, Toes RE, Offringa R, Melief CJ. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001, 194:823-832.
14. 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, Lebbe 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. The New England Journal of Medicine 2010, 363:711-723.
15. Gall JM, Davol PA, Grabert RC, Deaver M, Lum LG. T cells armed with anti-CD3 × anti-CD20 bispecific antibody enhance killing of CD20+ malignant B cells and bypass complement-mediated rituximab resistance in vitro. Exp Hematol 2005, 33:452-459.
16. Reusch U, Sundaram M, Davol PA, Olson SD, Davis JB, Demel K, Nissim J, Rathore R, Liu PY, Lum LG. Anti-CD3 × anti-epidermal growth factor receptor (EGFR) bispecific antibody redirects T-cell cytolytic activity to EGFR-positive cancers In vitro and in an animal model. Clin Cancer Res 2006, 12:183-190.
17. Sen M, Wankowski DM, Garlie NK, Siebenlist RE, Van Epps D, LeFever AV, Lum LG. Use of anti-CD3 x anti-HER2/neu bispecific antibody for redirecting cytotoxicity of activated T cells toward HER2/neu + tumors. J Hematother Stem Cell Res 2001, 10:247-260.
18. Thakur A, Norkina O, Lum LG. In vitro synthesis of primary specific anti-breast cancer antibodies by normal human peripheral blood mononuclear cells. Cancer Immunol Immunother 2011, 60:1707-1720.
19. Thakur A, Schalk D, Tomaszewski E, Kondadasula SV, Yano H, Sarkar FH, Lum LG. Microenvironment generated during EGFR targeted killing of pancreatic tumor cells by ATC inhibits myeloid-derived suppressor cells through COX2 and PGE2 dependent pathway. J Transl Med 2013, 11:35.
20. Zitron IM, Thakur A, Norkina O, Barger GR, Lum LG, Mittal S. Targeting and killing of glioblastoma with activated T cells armed with bispecific antibodies. BMC Cancer 2013, 13:83.
21. Fryar CD, Gu Q, Ogden CL. Anthropometric reference data for children and adults: United States, 2007-2010. Vital Health Stat 2012, 11:1-48.
22. Pistoia V, Morandi F, Bianchi G, Pezzolo A, Prigione I, Raffaghello L. Immunosuppressive microenvironment in neuroblastoma. Front Oncol 2013, 3:167.
23. 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. The Journal of Clinical Investigation 2006, 116:2777-2790.
24. Jackson C, Ruzevick J, Phallen J, Belcaid Z, Lim M. Challenges in immunotherapy presented by the glioblastoma multiforme microenvironment. Clin Dev Immunol 2011, 2011:20.
25. Evans C, Dalgleish AG, Kumar D. Review article: immune suppression and colorectal cancer. Aliment Pharmacol Ther 2006, 24:1163-1177.
26. Pancione M, Giordano G, Remo A, Febbraro A, Sabatino L, Manfrin E, Ceccarelli M, Colantuoni V. Immune escape mechanisms in colorectal cancer pathogenesis and liver metastasis. J Immunol Res 2014, 2014:11.
27. Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, Vonderheide RH. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell 2012, 21:822-835.
28. Weber JS, Hamid O, Chasalow SD, Wu DY, Parker SM, Galbraith S, Gnjatic S, Berman D. Ipilimumab increases activated T cells and enhances humoral immunity in patients with advanced melanoma. J Immunother 2012, 35:89-97.
29. Kavanagh B, O'Brien S, Lee D, Hou Y, Weinberg V, Rini B, Allison JP, Small EJ, Fong L. CTLA4 blockade expands FoxP3+ regulatory and activated effector CD4+ T cells in a dose-dependent fashion. Blood 2008, 112:1175-1183.
30. Lum LG, Thakur A, Pray C, Kouttab N, Abedi M, Deol A, Colaiace WM, Rathore R. Multiple infusions of CD20-targeted T cells and low-dose IL-2 after SCT for high-risk non-Hodgkin's lymphoma: a pilot study. Bone Marrow Transplant 2014, 49:73-79.
31. Lum LG, Thakur A, Liu Q, Deol A, Al-Kadhimi Z, Ayash L, Abidi MH, Pray C, Tomaszewski EN, Steele PA, Schalk DL, Yano H, Mitchell A, Dufresne M, Uberti JP, Ratanatharathorn V. CD20-targeted T cells after stem cell transplantation for high risk and refractory non-Hodgkin's lymphoma. Biol Blood Marrow Transplant 2013, 19:925-933.
32. Grabert RC, Cousens LP, Smith JA, Olson S, Gall J, Young WB, Davol PA, Lum LG. Human T cells armed with Her2/neu bispecific antibodies divide, Are cytotoxic, and secrete cytokines with repeated stimulation. Clin Cancer Res 2006, 12:569-576.
33. Yankelevich M, Kondadasula SV, Thakur A, Buck S, Cheung NK, Lum LG. Anti-CD3 × anti-GD2 bispecific antibody redirects T-cell cytolytic activity to neuroblastoma targets. Pediatr Blood Cancer 2012, 59:1198-1205.
34. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 2013, 31:227-258.
35. Boyman O, Krieg C, Homann D, Sprent J. Homeostatic maintenance of T cells and natural killer cells. Cell Mol Life Sci 2012, 69:1597-1608.
36. Lindqvist CA, Christiansson LH, Simonsson B, Enblad G, Olsson-Stromberg U, Loskog AS. T regulatory cells control T-cell proliferation partly by the release of soluble CD25 in patients with B-cell malignancies. Immunology 2010, 131:371-376.
37. Boyman O, Sprent J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat Rev Immunol 2012, 12:180-190.
38. Yang ZZ, Grote DM, Ziesmer SC, Manske MK, Witzig TE, Novak AJ, Ansell SM. Soluble IL-2Ralpha facilitates IL-2-mediated immune responses and predicts reduced survival in follicular B-cell non-Hodgkin lymphoma. Blood 2011, 118:2809-2820.
39. Kim R, Emi M, Tanabe K, Arihiro K. Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 2006, 66:5527-5536.
40. Brooks DG, Walsh KB, Elsaesser H, Oldstone MB. IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc Natl Acad Sci U S A 2010, 107:3018-3023.
41. Beckebaum S, Zhang X, Chen X, Yu Z, Frilling A, Dworacki G, Grosse-Wilde H, Broelsch CE, Gerken G, Cicinnati VR. Increased levels of interleukin-10 in serum from patients with hepatocellular carcinoma correlate with profound numerical deficiencies and immature phenotype of circulating dendritic cell subsets. Clin Cancer Res 2004, 10:7260-7269.