Antibody-dependent cellular cytotoxicity activity of a Novel Anti-PD-L1 antibody avelumab (MSB0010718C) on human tumor cells

Cancer Immunology Research

Volumn 3, Issue 10, 2015, Pages 1148-1157

  Boyerinas, Benjamin ^a   Jochems, Caroline ^a   Fantini, Massimo ^a   Heery, Christopher R ^a   Gulley, James L ^a   Tsang, Kwong Yok ^a   Schlom, Jeffrey ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVELUMAB; CD16 ANTIGEN; FC RECEPTOR IIIA; GAMMA INTERFERON; INTERLEUKIN 12; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; FC RECEPTOR; FCGR3A PROTEIN, HUMAN; MONOCLONAL ANTIBODY; PROGRAMMED DEATH 1 LIGAND 1; TUMOR MARKER;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIVITY; EFFECTOR CELL; GENOTYPE; HUMAN; HUMAN CELL; NATURAL KILLER CELL; NON SMALL CELL LUNG CANCER; PERIPHERAL BLOOD MONONUCLEAR CELL; TUMOR CELL; TUMOR CELL LINE; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; NEOPLASM;

ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL MEMBRANE; GENE EXPRESSION; GENOTYPE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; NEOPLASMS; RECEPTORS, IGG; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84951279998     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0059     Document Type: Article

References (54)

1. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
2. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med 2015;372:311-9.
3. Brahmer JR, Tykodi SS, Chow LQ, Hwu W-JJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. New Eng J Med 2012;366:2455-65.
4. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
5. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515:563-7.
6. Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, et al. Durable cancer regression off-Treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013;19:462-8.
7. Manusow JS, Khoja L, Pesin N, Joshua AM, Mandelcorn ED. Retinal vasculitis and ocular vitreous metastasis following complete response to PD-1 inhibition in a patient with metastatic cutaneous melanoma. J Immunother Cancer 2014;2:41.
8. Min L, Hodi FS. Anti-PD1 following ipilimumab for mucosal melanoma: durable tumor response associated with severe hypothyroidism and rhabdomyolysis. Cancer Immunol Res 2014;2:15-8.
9. Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeuticmodalities with durable clinical benefit in melanoma patients. Clin Cancer Res 2013;19:5300-9.
10. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, et al.MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014;515:558-62.
11. Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, et al. Antiprogrammed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: A randomised dose-comparison cohort of a phase 1 trial. Lancet 2014;384:1109-17.
12. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermottDF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. New Eng J Med 2012;366:2443-54.
13. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-Term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014;32:1020-30.
14. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advancedmelanoma.New Eng JMed 2013;369:122-33.
15. Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-Amplified breast cancer. Cancer Res 2010;70:4481-9.
16. Kohrt HE, Houot R, Weiskopf K, Goldstein MJ, Scheeren F, Czerwinski D, et al. Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J Clin Invest 2012;122:1066-75.
17. Kohrt HE, Thielens A, Marabelle A, Sagiv-Barfi I, Sola C, Chanuc F, et al. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood 2014;123:678-86.
18. Le Garff-Tavernier M, Decocq J, de Romeuf C, Parizot C, Dutertre CA, Chapiro E, et al. Analysis of CD16+CD56dim NK cells from CLL patients: evidence supporting a therapeutic strategy with optimized anti-CD20 monoclonal antibodies. Leukemia 2010;25:101-9.
19. Petricevic B, Laengle J, Singer J, Sachet M, Fazekas J, Steger G, et al. Trastuzumabmediates antibody-dependent cell-mediated cytotoxicity and phagocytosis to the same extent in both adjuvant andmetastatic HER2/neu breast cancer patients. J Transl Med 2012;11:307.
20. Shuptrine CW, Surana R, Weiner LM. Monoclonal antibodies for the treatment of cancer. Semin Cancer Biol 2012;22:3-13.
21. Srivastava RM, Lee SC, Andrade Filho PA, Lord CA, Jie HB, Davidson HC, et al. Cetuximab-Activated natural killer and dendritic cells collaborate to trigger tumor antigen-specific T-cell immunity in head and neck cancer patients. Clin Cancer Res 2013;19:1858-72.
22. Veeramani S, Wang S-YY, Dahle C, Blackwell S, Jacobus L, Knutson T, et al. Rituximab infusion induces NK activation in lymphoma patients with the high-Affinity CD16 polymorphism. Blood 2011;118:3347-9.
23. Vivier E, Ugolini S, Blaise D, Chabannon C. Targeting natural killer cells and natural killer T cells in cancer. Nature Rev Immunol 2012;12: 239-52.
24. Ward E, Mittereder N, Kuta E, Sims GP, Bowen MA, Dall'Acqua W, et al. A glycoengineered anti-CD19 antibody with potent antibody-dependent cellular cytotoxicity activity in vitro and lymphoma growth inhibition in vivo. Br J Haematol 2011;155:426-37.
25. Heery CR, O'Sullivan Coyne GH, Madan RA, SchlomJ, von Heydebreck A, Cuillerot J-M, et al. Phase I open-label, multiple ascending dose trial of MSB0010718C, an anti-PD-L1 monoclonal antibody, in advanced solid malignancies 2014 ASCO Annual Meeting, Chicago, IL J Clin Oncol 32:5s, 2014 (suppl; abstr 3064); 2014; 2014.
26. Madan RA, Tsang K-Y, Bilusic M, Vergati M, Poole DJ, Jochems C, et al. Effect of talactoferrin alfa on the immune system in adults with non-small cell lung cancer. Oncologist 2013;18:821-2.
27. Chan LY, Yam EKF, Choo ABH. Normalized median fluorescence: An alternative flow cytometry analysis method for tracking human embryonic stem cell states during differentiation. Tissue Eng Part C Methods 2013;19:156-65.
28. Qi CF, Nieroda C, De Filippi R, Greiner JW, Correale P, Schlom J, et al. Macrophage colony-stimulating factor enhancement of antibody-dependent cellular cytotoxicity against human colon carcinoma cells. Immunol Lett 1995;47:15-24.
29. Jochems C, Tucker JA, Vergati M, Boyerinas B, Gulley JL, Schlom J, et al. Identification and characterization of agonist epitopes of the MUC1-C oncoprotein. Cancer Immunol Immunother 2014;63:161-74.
30. Ravetch JV, Perussia B. Alternative membrane forms of Fc gamma RIII (CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions. J Exp Med 1989;170:481-97.
31. Schalper KA, Velcheti V, Carvajal D, Wimberly H, Brown J, Pusztai L, et al. In situ tumor PD-L1 mRNA expression is associated with increased TILs and better outcome in breast carcinomas. Clin Cancer Res 2014;20:2773-82.
32. Soliman H, Khalil F, Antonia S. PD-L1 expression is increased in a subset of basal type breast cancer cells. PLoS ONE 2013;9:e88557.
33. Devaiah BN, Singer DS.CIITA and Its dual roles inMHCgene transcription. Front Immunol 2012;4:476.
34. Roselli M, Fernando RI, Guadagni F, Spila A, Alessandroni J, Palmirotta R, et al. Brachyury, a driver of the epithelial-mesenchymal transition, is overexpressed in human lung tumors: An opportunity for novel interventions against lung cancer. Clin Cancer Res 2012;18:3868-79.
35. Hamilton DH, Huang B, Fernando RI, Tsang K-Y, Palena C. WEE1 inhibition alleviates resistance to immune attack of tumor cells undergoing epithelial-mesenchymal transition. Cancer Res 2014;74:2510-9.
36. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989;170:827-45.
37. Wolf SF, Sieburth D, Sypek J. Interleukin 12: A key modulator of immune function. Stem Cells 1994;12:154-68.
38. Fallon J, Tighe R, Kradjian G, GuzmanW, Bernhardt A, NeuteboomB, et al. The immunocytokine NHS-IL12 as a potential cancer therapeutic. Oncotarget 2014;5:1869-84.
39. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol 2008;26:1789-96.
40. Caligiuri MA. Human natural killer cells. Blood 2008;112:461-9.
41. Mellor JD, Brown MP, Irving HR, Zalcberg JR, Dobrovic A. A critical review of the role of Fc gamma receptor polymorphisms in the response to monoclonal antibodies in cancer. J Hematol Oncol 2012;6:1.
42. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cellmediated cytolysis. Annu Rev Immunol 2001;19:197-223.
43. Heeren AM, Koster BD, Samuels S, Ferns DM, Chondronasiou D, Kenter GG, et al. High and interrelated rates of PD-L1+CD14+antigen-presenting cells and regulatory T cells mark the microenvironment of metastatic lymph nodes from patients with cervical cancer. Cancer Immunol Res 2015;3:48-58.
44. Koehn TA, Trimble LL, Alderson KL, Erbe AK, McDowell KA, Grzywacz B, et al. Increasing the clinical efficacy of NK and antibody-mediated cancer immunotherapy: potential predictors of successful clinical outcome based on observations in high-risk neuroblastoma. Front Pharmacol 2012;3:91.
45. Watanabe M, Kono K, Kawaguchi Y, Mizukami Y, Mimura K, Maruyama T, et al. Interleukin-21 can efficiently restore impaired antibody-dependent cell-mediated cytotoxicity in patients with oesophageal squamous cell carcinoma. Br J Cancer 2010;102:520-9.
46. Conlon KC, Lugli E, Welles HC, Rosenberg SA, Fojo AT, Morris JC, et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol 2015;33:74-82.
47. Waldmann TA. Interleukin-15 in the treatment of cancer. Expert Rev Clin Immunol 2014;10:1689-701.
48. Waldmann TA. The shared and contrasting roles of IL2 and IL15 on the life and death of normal and neoplastic lymphocytes: implications for cancer therapy. Cancer Immunol Res 2015;3:219-27.
49. Ansell SM, Geyer SM, Maurer MJ, Kurtin PJ, Micallef INM, Stella P, et al. Randomized phase II study of interleukin-12 in combination with rituximab in previously treated non-Hodgkin's lymphoma patients. Clin Cancer Res 2006;12:6056-63.
50. Luedke E, Jaime-Ramirez AC, Bhave N, Roda J, Choudhary MM, Kumar B, et al. Cetuximab therapy in head and neck cancer: immune modulation with interleukin-12 and other natural killer cell-Activating cytokines. Surgery 2012;152:431-40.
51. Gibney GT, Kudchadkar RR, DeConti RC, Thebeau MS, Czupryn MP, Tetteh LF, et al. Safety, correlative markers and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma. Clin Cancer Res 2015;21:712-20.
52. Karyampudi L, Lamichhane P, Scheid AD, Kalli KR, Shreeder B, Krempski JW, et al. Accumulation of memory precursor CD8 T cells in regressing tumors following combination therapy with vaccine and anti-PD-1 antibody. Cancer Res 2014;74:2974-85.
53. Ferrone S, Whiteside TL. Tumor microenvironment and immune escape. Surg Oncol Clin N Am 2007;16:755-74, viii.
54. Mentlik James A, Cohen AD, Campbell KS. Combination immune therapies to enhance anti-Tumor responses by NK cells (Article 481). Front Immunol 2013;4:1-12.