FcγRIIIa-dependent IFN-γ release in whole blood assay is predictive of therapeutic IgG1 antibodies safety

References

• Lee DW, Gardner R, Porter DL, Louis CU, Ahmed N, Jensen M, Grupp SA, Mackall CL. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124(2):188–195. PubMed PMID: WOS:000342618600011. doi:10.1182/blood-2014-05-552729.
   PubMed Web of Science ®Google Scholar
• Finco D, Grimaldi C, Fort M, Walker M, Kiessling A, Wolf B, Salcedo T, Faggioni R, Schneider A, Ibraghimov A, et al. Cytokine release assays: current practices and future directions. Cytokine. 2014;66(2):143–155. PubMed PMID: WOS:000333729200008. doi:10.1016/j.cyto.2013.12.009.
   PubMed Web of Science ®Google Scholar
• Brady JL, Harrison LC, Goodman DJ, Cowan PJ, Hawthorne WJ, O'Connell PJ, Sutherland RM, Lew AM. Preclinical screening for acute toxicity of therapeutic monoclonal antibodies in a hu-SCID model. Clin Transl Immunol. 2014;3(12):e29. PubMed PMID: 25587392; PubMed Central PMCID: PMC4282178. doi:10.1038/cti.2014.28.
   PubMedGoogle Scholar
• Wing MG, Moreau T, Greenwood J, Smith RM, Hale G, Isaacs J, Waldmann H, Lachmann PJ, Compston A. Mechanism of first-dose cytokine-release syndrome by CAMPATH 1-H: involvement of CD16 (FcgammaRIII) and CD11a/CD18 (LFA-1) on NK cells. J Clin Invest. 1996;98(12):2819–2826. PubMed PMID: 8981930; PubMed Central PMCID: PMC507749. doi:10.1172/JCI119110.
   PubMed Web of Science ®Google Scholar
• Poirier N, Mary C, Dilek N, Hervouet J, Minault D, Blancho G, Vanhove B. Preclinical efficacy and immunological safety of FR104, an antagonist anti-CD28 monovalent Fab’ antibody. Am J Transplant. 2012;12(10):2630–2640. PubMed PMID: 22759318. doi:10.1111/j.1600-6143.2012.04164.x.
   PubMed Web of Science ®Google Scholar
• Brennan FR, Kiessling A. In vitro assays supporting the safety assessment of immunomodulatory monoclonal antibodies. Toxicol Vitro. 2017. PubMed PMID: 28263892. doi:10.1016/j.tiv.2017.02.025.
   Web of Science ®Google Scholar
• Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, Luo X, Cooley S, Verneris M, Walcheck B, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood. 2013;121(18):3599–3608. PubMed PMID: 23487023; PubMed Central PMCID: PMCPMC3643761. doi:10.1182/blood-2012-04-425397.
   PubMed Web of Science ®Google Scholar
• Almishri W, Santodomingo-Garzon T, Le T, Stack D, Mody CH, Swain MG. TNFalpha Augments Cytokine-Induced NK Cell IFNgamma Production through TNFR2. J Innate Immun. 2016;8(6):617–629. PubMed PMID: 27560480. doi:10.1159/000448077.
   PubMed Web of Science ®Google Scholar
• Anegon I, Cuturi MC, Trinchieri G, Perussia B. Interaction of Fc receptor (CD16) ligands induces transcription of interleukin 2 receptor (CD25) and lymphokine genes and expression of their products in human natural killer cells. J Exp Med. 1988;167(2):452–472. PubMed PMID: 2831292; PubMed Central PMCID: PMCPMC2188858.
   PubMed Web of Science ®Google Scholar
• Koene HR, Kleijer M, Algra J, Roos D, von dem Borne AE, de Haas M. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood. 1997;90(3):1109–1114. PubMed PMID: 9242542.
   PubMed Web of Science ®Google Scholar
• Holgate RG, Weldon R, Jones TD, Baker MP. Characterisation of a Novel Anti-CD52 Antibody with Improved Efficacy and Reduced Immunogenicity. Plos One. 2015;10(9):e0138123. PubMed PMID: 26372145; PubMed Central PMCID: PMCPMC4570798. doi:10.1371/journal.pone.0138123.
   PubMed Web of Science ®Google Scholar
• Vessillier S, Eastwood D, Fox B, Sathish J, Sethu S, Dougall T, Thorpe SJ, Thorpe R, Stebbings R. Cytokine release assays for the prediction of therapeutic mAb safety in first-in man trials - Whole blood cytokine release assays are poorly predictive for TGN1412 cytokine storm. J Immunol Methods. 2015. PubMed PMID: 25960173. doi:10.1016/j.jim.2015.04.020.
   PubMed Web of Science ®Google Scholar
• Hu Y, Turner MJ, Shields J, Gale MS, Hutto E, Roberts BL, Siders WM, Kaplan JM. Investigation of the mechanism of action of alemtuzumab in a human CD52 transgenic mouse model. Immunology. 2009;128(2):260–270. PubMed PMID: 19740383; PubMed Central PMCID: PMCPMC2767316. doi:10.1111/j.1365-2567.2009.03115.x.
   PubMed Web of Science ®Google Scholar
• Siders WM, Shields J, Garron C, Hu Y, Boutin P, Shankara S, Weber W, Roberts B, Kaplan JM. Involvement of neutrophils and natural killer cells in the anti-tumor activity of alemtuzumab in xenograft tumor models. Leuk Lymphoma. 2010;51(7):1293–1304. PubMed PMID: 20377308. doi:10.3109/10428191003777963.
   PubMed Web of Science ®Google Scholar
• Crowe JS, Hall VS, Smith MA, Cooper HJ, Tite JP. Humanized monoclonal antibody CAMPATH-1H: myeloma cell expression of genomic constructs, nucleotide sequence of cDNA constructs and comparison of effector mechanisms of myeloma and Chinese hamster ovary cell-derived material. Clin Exp Immunol. 1992;87(1):105–110. PubMed PMID: 1339322; PubMed Central PMCID: PMCPMC1554244.
   PubMed Web of Science ®Google Scholar
• Rowan W, Tite J, Topley P, Brett SJ. Cross-linking of the CAMPATH-1 antigen (CD52) mediates growth inhibition in human B- and T-lymphoma cell lines, and subsequent emergence of CD52-deficient cells. Immunology. 1998;95(3):427–436. PubMed PMID: 9824507; PubMed Central PMCID: PMCPMC1364410.
   PubMed Web of Science ®Google Scholar
• Lin TS, Flinn IW, Modali R, Lehman TA, Webb J, Waymer S, Moran ME, Lucas MS, Farag SS, Byrd JC. FCGR3A and FCGR2A polymorphisms may not correlate with response to alemtuzumab in chronic lymphocytic leukemia. Blood. 2005;105(1):289–291. PubMed PMID: 15217834. doi:10.1182/blood-2004-02-0651.
   PubMed Web of Science ®Google Scholar
• Herter S, Herting F, Muth G, van Puijenbroek E, Schlothauer T, Ferrara C, Brady K, Lang S, Bacac M, Mossner E, et al. GA101 P329GLALA, a variant of obinutuzumab with abolished ADCC, ADCP and CDC function but retained cell death induction, is as efficient as rituximab in B-cell depletion and antitumor activity. Haematologica. 2018;103(2):e78–e81. PubMed PMID: 29079598; PubMed Central PMCID: PMCPMC5792291. doi:10.3324/haematol.2017.178996.
   PubMed Web of Science ®Google Scholar
• Parihar R, Dierksheide J, Hu Y, Carson WE. IL-12 enhances the natural killer cell cytokine response to Ab-coated tumor cells. J Clin Invest. 2002;110(7):983–992. PubMed PMID: 12370276; PubMed Central PMCID: PMCPMC151155. doi:10.1172/JCI15950.
   PubMed Web of Science ®Google Scholar
• Bowles JA, Weiner GJ. CD16 polymorphisms and NK activation induced by monoclonal antibody-coated target cells. J Immunol Methods. 2005;304(1–2):88–99. PubMed PMID: 16109421. doi:10.1016/j.jim.2005.06.018.
   PubMed Web of Science ®Google Scholar
• Capuano C, Pighi C, Molfetta R, Paolini R, Battella S, Palmieri G, Giannini G, Belardinilli F, Santoni A, Galandrini R. Obinutuzumab-mediated high-affinity ligation of FcgammaRIIIA/CD16 primes NK cells for IFNgamma production. Oncoimmunology. 2017;6(3):e1290037. PubMed PMID: 28405525; PubMed Central PMCID: PMCPMC5384385. doi:10.1080/2162402X.2017.1290037.
   PubMed Web of Science ®Google Scholar
• Robinet E, Morel P, Assossou O, Revillard JP. TNF-alpha production as an in vitro assay predictive of cytokine-mediated toxic reactions induced by monoclonal antibodies. Toxicology. 1995;100(1–3):213–223. PubMed PMID: 7624879.
   PubMed Web of Science ®Google Scholar
• Bowles JA, Wang SY, Link BK, Allan B, Beuerlein G, Campbell MA, Marquis D, Ondek B, Wooldridge JE, Smith BJ, et al. Anti-CD20 monoclonal antibody with enhanced affinity for CD16 activates NK cells at lower concentrations and more effectively than rituximab. Blood. 2006;108(8):2648–2654. PubMed PMID: 16825493; PubMed Central PMCID: PMCPMC1895597. doi:10.1182/blood-2006-04-020057.
   PubMed Web of Science ®Google Scholar
• Veeramani S, Wang SY, Dahle C, Blackwell S, Jacobus L, Knutson T, Button A, Link BK, Weiner GJ. Rituximab infusion induces NK activation in lymphoma patients with the high-affinity CD16 polymorphism. Blood. 2011;118(12):3347–3349. PubMed PMID: 21768303; PubMed Central PMCID: PMCPMC3179401. doi:10.1182/blood-2011-05-351411.
   PubMed Web of Science ®Google Scholar
• Treon SP, Hansen M, Branagan AR, Verselis S, Emmanouilides C, Kimby E, Frankel SR, Touroutoglou N, Turnbull B, Anderson KC, et al. Polymorphisms in Fc gamma RIIIA (CD 16) receptor expression are associated with clinical response to rituximab in Waldenstrom’s macroglobulinemia. J Clin Oncol. 2005;23(3):474–481. PubMed PMID: WOS:000226591000012. doi:10.1200/jco.2005.06.059.
   PubMed Web of Science ®Google Scholar
• Bailey L, Moreno L, Manigold T, Krasniqi S, Kropshofer H, Hinton H, Singer T, Suter L, Hansel TT, Mitchell JA. A simple whole blood bioassay detects cytokine responses to anti-CD28SA and anti-CD52 antibodies. J Pharmacol Toxicol Methods. 2013;68(2):231–239. PubMed PMID: 23280407. doi:10.1016/j.vascn.2012.12.003.
   PubMed Web of Science ®Google Scholar
• Wolf B, Morgan H, Krieg J, Gani Z, Milicov A, Warncke M, Brennan F, Jones S, Sims J, Kiessling A. A whole blood in vitro cytokine release assay with aqueous monoclonal antibody presentation for the prediction of therapeutic protein induced cytokine release syndrome in humans. Cytokine. 2012;60(3):828–837. PubMed PMID: WOS:000311248000035. doi:10.1016/j.cyto.2012.08.018.
   PubMed Web of Science ®Google Scholar
• 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. 2013;6:10. PubMed PMID: WOS:000313957300001. doi:10.1186/1756-8722-6-1.
   PubMedGoogle Scholar