Elimination of plasma soluble antigen in cynomolgus monkeys by combining pH-dependent antigen binding and novel Fc engineering

References

• Martin PL, Cornacoff J, Prabhakar U, Lohr T, Treacy G, Sutherland JE, Hersey S, Martin E. Reviews preclinical safety and immune-modulating effects of therapeutic monoclonal antibodies to interleukin-6 and tumor necrosis factor-alpha in cynomolgus macaques. J Immunotoxicol. 2005 Jul 1;1(3):131–11. doi:10.1080/15476910490894904.
   PubMedGoogle Scholar
• Jayson GC, Mulatero C, Ranson M, Zweit J, Jackson A, Broughton L, Wagstaff J, Hakansson L, Groenewegen G, Lawrance J, et al. Phase I investigation of recombinant anti-human vascular endothelial growth factor antibody in patients with advanced cancer. Eur J Cancer. 2005 Mar;41(4):555–63. doi:10.1016/j.ejca.2004.11.021.
   PubMed Web of Science ®Google Scholar
• Haringman JJ, Gerlag DM, Smeets TJ, Baeten D, van den Bosch F, Bresnihan B, Breedveld FC, Dinant HJ, Legay F, Gram H, et al. A randomized controlled trial with an anti-CCL2 (anti-monocyte chemotactic protein 1) monoclonal antibody in patients with rheumatoid arthritis. Arthritis Rheum. 2006 Aug;54(8):2387–92. doi:10.1002/art.21975.
   PubMed Web of Science ®Google Scholar
• Byrd JC, O’Brien S, Flinn IW, Kipps TJ, Weiss M, Rai K, Lin TS, Woodworth J, Wynne D, Reid J, et al. Phase 1 study of lumiliximab with detailed pharmacokinetic and pharmacodynamic measurements in patients with relapsed or refractory chronic lymphocytic leukemia. Clin Cancer Res. 2007 Aug 1;13(15 Pt 1):4448–55. doi:10.1158/1078-0432.CCR-06-1463.
   PubMed Web of Science ®Google Scholar
• Xiao JJ, Krzyzanski W, Wang YM, Li H, Rose MJ, Ma M, Wu Y, Hinkle B, Perez-Ruixo JJ. Pharmacokinetics of anti-hepcidin monoclonal antibody Ab 12B9m and hepcidin in cynomolgus monkeys. Aaps j. 2010 Dec;12(4):646–57. doi:10.1208/s12248-010-9222-0.
   PubMed Web of Science ®Google Scholar
• Finkelman FD, Madden KB, Morris SC, Holmes JM, Boiani N, Katona IM, Maliszewski CR. Anti-cytokine antibodies as carrier proteins. Prolongation of in vivo effects of exogenous cytokines by injection of cytokine-anti-cytokine antibody complexes. J Immunol. 1993 Aug 1;151(3):1235–44.
   PubMed Web of Science ®Google Scholar
• Devanaboyina SC, Lynch SM, Ober RJ, Ram S, Kim D, Puig-Canto A, Breen S, Kasturirangan S, Fowler S, Peng L, et al. The effect of pH dependence of antibody-antigen interactions on subcellular trafficking dynamics. MAbs. 2013 Nov-Dec;5(6):851–59. doi:10.4161/mabs.26389.
   PubMed Web of Science ®Google Scholar
• Igawa T, Mimoto F, Hattori K. pH-dependent antigen-binding antibodies as a novel therapeutic modality. Biochim Biophys Acta. 2014 Nov;1844(11):1943–50. doi:10.1016/j.bbapap.2014.08.003.
   PubMed Web of Science ®Google Scholar
• Murtaugh ML, Fanning SW, Sharma TM, Terry AM, Horn JR. A combinatorial histidine scanning library approach to engineer highly pH-dependent protein switches. Protein Sci. 2011 Sep;20(9):1619–31. doi:10.1002/pro.696.
   PubMed Web of Science ®Google Scholar
• Chaparro-Riggers J, Liang H, DeVay RM, Bai L, Sutton JE, Chen W, Geng T, Lindquist K, Casas MG, Boustany LM, et al. Increasing serum half-life and extending cholesterol lowering in vivo by engineering antibody with pH-sensitive binding to PCSK9. J Biol Chem. 2012 Mar 30;287(14):11090–97. doi:10.1074/jbc.M111.319764.
   PubMed Web of Science ®Google Scholar
• Henne KR, Ason B, Howard M, Wang W, Sun J, Higbee J, Tang J, Matsuda KC, Xu R, Zhou L, et al. Anti-PCSK9 antibody pharmacokinetics and low-density lipoprotein-cholesterol pharmacodynamics in nonhuman primates are antigen affinity-dependent and exhibit limited sensitivity to neonatal Fc receptor-binding enhancement. J Pharmacol Exp Ther. 2015 Apr;353(1):119–31. doi:10.1124/jpet.114.221242.
   PubMed Web of Science ®Google Scholar
• Sampei Z, Haraya K, Tachibana T, Fukuzawa T, Shida-Kawazoe M, Gan SW, Shimizu Y, Ruike Y, Feng S, Kuramochi T, et al. Antibody engineering to generate SKY59, a long-acting anti-C5 recycling antibody. Plos One. 2018;13(12):e0209509. doi:10.1371/journal.pone.0209509.
   PubMed Web of Science ®Google Scholar
• Igawa T, Ishii S, Tachibana T, Maeda A, Higuchi Y, Shimaoka S, Moriyama C, Watanabe T, Takubo R, Doi Y, et al. Antibody recycling by engineered pH-dependent antigen binding improves the duration of antigen neutralization. Nat Biotechnol. 2010 Nov;28(11):1203–07. doi:10.1038/nbt.1691.
   PubMed Web of Science ®Google Scholar
• Fukuzawa T, Sampei Z, Haraya K, Ruike Y, Shida-Kawazoe M, Shimizu Y, Gan SW, Irie M, Tsuboi Y, Tai H, et al. Long lasting neutralization of C5 by SKY59, a novel recycling antibody, is a potential therapy for complement-mediated diseases. Sci Rep. 2017 Apr 24;7(1):1080. doi:10.1038/s41598-017-01087-7.
   PubMed Web of Science ®Google Scholar
• Bonvin P, Venet S, Fontaine G, Ravn U, Gueneau F, Kosco-Vilbois M, Proudfoot AE, Fischer N. De novo isolation of antibodies with pH-dependent binding properties. MAbs. 2015;7(2):294–302. doi:10.1080/19420862.2015.1006993.
   PubMed Web of Science ®Google Scholar
• Schröter C, Günther R, Rhiel L, Becker S, Toleikis L, Doerner A, Becker J, Schönemann A, Nasu D, Neuteboom B, et al. A generic approach to engineer antibody pH-switches using combinatorial histidine scanning libraries and yeast display. MAbs. 2015;7(1):138–51. doi:10.4161/19420862.2014.985993.
   PubMed Web of Science ®Google Scholar
• Iwayanagi Y, Igawa T, Maeda A, Haraya K, Wada NA, Shibahara N, Ohmine K, Nambu T, Nakamura G, Mimoto F, et al. Inhibitory FcγRIIb-mediated soluble antigen clearance from plasma by a pH-dependent antigen-binding antibody and its enhancement by Fc engineering. J Immunol. 2015 Oct 1;195(7):3198–205. doi:10.4049/jimmunol.1401470.
   PubMed Web of Science ®Google Scholar
• Igawa T, Maeda A, Haraya K, Tachibana T, Iwayanagi Y, Mimoto F, Higuchi Y, Ishii S, Tamba S, Hironiwa N, et al. Engineered monoclonal antibody with novel antigen-sweeping activity in vivo. PLoS One. 2013;8(5):e63236. doi:10.1371/journal.pone.0063236.
   PubMed Web of Science ®Google Scholar
• Igawa T, Haraya K, Hattori K. Sweeping antibody as a novel therapeutic antibody modality capable of eliminating soluble antigens from circulation. Immunol Rev. 2016 Mar;270(1):132–51. doi:10.1111/imr.12392.
   PubMed Web of Science ®Google Scholar
• Li B, Tesar D, Boswell CA, Cahaya HS, Wong A, Zhang J, Meng YG, Eigenbrot C, Pantua H, Diao J, et al. Framework selection can influence pharmacokinetics of a humanized therapeutic antibody through differences in molecule charge. MAbs. 2014;6(5):1255–64. doi:10.4161/mabs.29809.
   PubMed Web of Science ®Google Scholar
• Igawa T, Tsunoda H, Tachibana T, Maeda A, Mimoto F, Moriyama C, Nanami M, Sekimori Y, Nabuchi Y, Aso Y, et al. Reduced elimination of IgG antibodies by engineering the variable region. Protein Eng Des Sel. 2010 May;23(5):385–92. doi:10.1093/protein/gzq009.
   PubMed Web of Science ®Google Scholar
• Datta-Mannan A, Thangaraju A, Leung D, Tang Y, Witcher DR, Lu J, Wroblewski VJ. Balancing charge in the complementarity-determining regions of humanized mAbs without affecting pI reduces non-specific binding and improves the pharmacokinetics. MAbs. 2015;7(3):483–93. doi:10.1080/19420862.2015.1016696.
   PubMed Web of Science ®Google Scholar
• Sampei Z, Igawa T, Soeda T, Okuyama-Nishida Y, Moriyama C, Wakabayashi T, Tanaka E, Muto A, Kojima T, Kitazawa T, et al. Identification and multidimensional optimization of an asymmetric bispecific IgG antibody mimicking the function of factor VIII cofactor activity. Plos One. 2013;8(2):e57479. doi:10.1371/journal.pone.0057479.
   PubMed Web of Science ®Google Scholar
• Rujas E, Leaman DP, Insausti S, Ortigosa-Pascual L, Zhang L, Zwick MB, Nieva JL. Functional optimization of broadly neutralizing HIV-1 antibody 10E8 by promotion of membrane interactions. J Virol. 2018 Apr 15;92(8). doi:10.1128/JVI.02249-17.
   PubMed Web of Science ®Google Scholar
• Mimoto F, Katada H, Kadono S, Igawa T, Kuramochi T, Muraoka M, Wada Y, Haraya K, Miyazaki T, Hattori K. Engineered antibody Fc variant with selectively enhanced FcγRIIb binding over both FcγRIIa(R131) and FcγRIIa(H131). Protein Eng Des Sel. 2013 Oct;26(10):589–98. doi:10.1093/protein/gzt022.
   PubMed Web of Science ®Google Scholar
• Chu SY, Vostiar I, Karki S, Moore GL, Lazar GA, Pong E, Joyce PF, Szymkowski DE, Desjarlais JR. Inhibition of B cell receptor-mediated activation of primary human B cells by coengagement of CD19 and FcgammaRIIb with Fc-engineered antibodies. Mol Immunol. 2008 Sep;45(15):3926–33.
   PubMed Web of Science ®Google Scholar
• Smith P, DiLillo DJ, Bournazos S, Li F, Ravetch JV. Mouse model recapitulating human Fcγ receptor structural and functional diversity. Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6181–86. doi:10.1073/pnas.1203954109.
   PubMed Web of Science ®Google Scholar
• Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, Jung N, Petkova S, Avanessian L, Choi EY, Shaffer DJ, et al. The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J Immunol. 2003 Apr 1;170(7):3528–33. doi:10.4049/jimmunol.170.7.3528.
   PubMed Web of Science ®Google Scholar
• Muramatsu H, Kuramochi T, Katada H, Ueyama A, Ruike Y, Ohmine K, Shida-Kawazoe M, Miyano-Nishizawa R, Shimizu Y, Okuda M, et al. Novel myostatin-specific antibody enhances muscle strength in muscle disease models. Sci Rep. 2021 Jan 25;11(1):2160. doi:10.1038/s41598-021-81669-8.
   PubMed Web of Science ®Google Scholar
• Lee SJ. Targeting the myostatin signaling pathway to treat muscle loss and metabolic dysfunction. J Clin Invest. 2021 May 3;131(9). doi:10.1172/JCI148372.
   Web of Science ®Google Scholar
• Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, et al. Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15842–46. doi:10.1073/pnas.2534946100.
   PubMed Web of Science ®Google Scholar
• Hinton PR, Xiong JM, Johlfs MG, Tang MT, Keller S, Tsurushita N. An engineered human IgG1 antibody with longer serum half-life. J Immunol. 2006 Jan 1;176(1):346–56. doi:10.4049/jimmunol.176.1.346.
   PubMed Web of Science ®Google Scholar
• Dall’Acqua WF, Kiener PA, Wu H. Properties of human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J Biol Chem. 2006 Aug 18;281(33):23514–24. doi:10.1074/jbc.M604292200.
   PubMed Web of Science ®Google Scholar
• Zalevsky J, Chamberlain AK, Horton HM, Karki S, Leung IW, Sproule TJ, Lazar GA, Roopenian DC, Desjarlais JR. Enhanced antibody half-life improves in vivo activity. Nat Biotechnol. 2010 Feb;28(2):157–59. doi:10.1038/nbt.1601.
   PubMed Web of Science ®Google Scholar
• Maeda A, Iwayanagi Y, Haraya K, Tachibana T, Nakamura G, Nambu T, Esaki K, Hattori K, Igawa T. Identification of human IgG1 variant with enhanced FcRn binding and without increased binding to rheumatoid factor autoantibody. MAbs. 2017 Jul;9(5):844–53. doi:10.1080/19420862.2017.1314873.
   PubMed Web of Science ®Google Scholar
• Petkova SB, Akilesh S, Sproule TJ, Christianson GJ, Al Khabbaz H, Brown AC, Presta LG, Meng YG, Roopenian DC. Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease. Int Immunol. 2006 Dec;18(12):1759–69. doi:10.1093/intimm/dxl110.
   PubMed Web of Science ®Google Scholar
• Deng R, Loyet KM, Lien S, Iyer S, DeForge LE, Theil FP, Lowman HB, Fielder PJ, Prabhu S. Pharmacokinetics of humanized monoclonal anti-tumor necrosis factor-{alpha} antibody and its neonatal Fc receptor variants in mice and cynomolgus monkeys. Drug Metab Dispos. 2010 Apr;38(4):600–05. doi:10.1124/dmd.109.031310.
   PubMed Web of Science ®Google Scholar
• Johansson AG, Løvdal T, Magnusson KE, Berg T, Skogh T. Liver cell uptake and degradation of soluble immunoglobulin G immune complexes in vivo and in vitro in rats. Hepatology. 1996 Jul;24(1):169–75. doi:10.1002/hep.510240128.
   PubMed Web of Science ®Google Scholar
• Ganesan LP, Kim J, Wu Y, Mohanty S, Phillips GS, Birmingham DJ, Robinson JM, Anderson CL. FcγRIIb on liver sinusoidal endothelium clears small immune complexes. J Immunol. 2012 Nov 15;189(10):4981–88. doi:10.4049/jimmunol.1202017.
   PubMed Web of Science ®Google Scholar
• Veri MC, Gorlatov S, Li H, Burke S, Johnson S, Stavenhagen J, Stein KE, Bonvini E, Koenig S. Monoclonal antibodies capable of discriminating the human inhibitory Fcγ-receptor IIB (CD32B) from the activating Fcγ-receptor IIA (CD32A): biochemical, biological and functional characterization. Immunology. 2007 Jul;121(3):392–404. doi:10.1111/j.1365-2567.2007.02588.x.
   PubMed Web of Science ®Google Scholar
• Kang C, Xia L, Chen Y, Zhang T, Wang Y, Zhou B, You M, Yuan Q, Tzeng CM, An Z, et al. A novel therapeutic anti-HBV antibody with increased binding to human FcRn improves in vivo PK in mice and monkeys. Protein Cell. 2018 Jan;9(1):130–34. doi:10.1007/s13238-017-0438-y.
   PubMed Web of Science ®Google Scholar
• Haj AK, Arbanas JM, Yamniuk AP, Karl JA, Bussan HE, Drinkwater KY, Graham ME, Ericsen AJ, Prall TM, Moore K, et al. Characterization of Mauritian cynomolgus macaque FcγR alleles using long-read sequencing. J Immunol. 2019 Jan 1;202(1):151–59. doi:10.4049/jimmunol.1800843.
   PubMed Web of Science ®Google Scholar
• Warncke M, Calzascia T, Coulot M, Balke N, Touil R, Kolbinger F, Heusser C. Different adaptations of IgG effector function in human and nonhuman primates and implications for therapeutic antibody treatment. J Immunol. 2012 May 1;188(9):4405–11. doi:10.4049/jimmunol.1200090.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Quintela A, Alende R, Gude F, Campos J, Rey J, Meijide LM, Fernandez-Merino C, Vidal C. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin Exp Immunol. 2008 Jan;151(1):42–50. doi:10.1111/j.1365-2249.2007.03545.x.
   PubMed Web of Science ®Google Scholar
• Cole MF, Bowen WH. Immunoglobulins A, G, and M in serum and in some secretions of monkeys (Macaca fascicularis syn. irus). Infect Immun. 1976 May;13(5):1354–59. doi:10.1128/iai.13.5.1354-1359.1976.
   PubMed Web of Science ®Google Scholar
• Tam SH, McCarthy SG, Brosnan K, Goldberg KM, Scallon BJ. Correlations between pharmacokinetics of IgG antibodies in primates vs. FcRn-transgenic mice reveal a rodent model with predictive capabilities. MAbs. 2013 May-Jun;5(3):397–405. doi:10.4161/mabs.23836.
   PubMed Web of Science ®Google Scholar