7,530
Views
82
CrossRef citations to date
0
Altmetric
Report

Selective targeting of the IL23 pathway: Generation and characterization of a novel high-affinity humanized anti-IL23A antibody

, , , , , , , , , , , , & show all
Pages 778-791 | Received 20 Jan 2015, Accepted 18 Mar 2015, Published online: 03 Jun 2015

References

  • Baeten DL, Kuchroo VK. How Cytokine networks fuel inflammation: interleukin-17 and a tale of two autoimmune diseases. Nat Med 2013; 19:824-5; PMID:23836225; http://dx.doi.org/10.1038/nm.3268
  • Gaffen SL, Jain R, Garg AV, Cua DJ. The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol 2014; 14:585-600; PMID:25145755; http://dx.doi.org/10.1038/nri3707
  • Toussirot E. The IL23/Th17 pathway as a therapeutic target in chronic inflammatory diseases. Inflamm Allergy Drug Targets 2012; 11:159-68; PMID:22280236; http://dx.doi.org/10.2174/187152812800392805
  • Elmaagacli AH, Koldehoff M, Landt O, Beelen DW. Relation of an interleukin-23 receptor gene polymorphism to graft-versus-host disease after hematopoietic-cell transplantation. Bone Marrow Transplant 2008; 41:821-6; PMID:18209723; http://dx.doi.org/10.1038/sj.bmt.1705980
  • Capon F, Di MP, Szaub J, Prescott NJ, Dunster C, Baumber L, Timms K, Gutin A, Abkevic V, Burden AD, et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum Genet 2007; 122:201-6; PMID:17587057; http://dx.doi.org/10.1007/s00439-007-0397-0
  • McGovern D, Powrie F. The IL23 axis plays a key role in the pathogenesis of IBD. Gut 2007; 56:1333-6; PMID:17872562; http://dx.doi.org/10.1136/gut.2006.115402
  • Tausend W, Downing C, Tyring S. Systematic review of interleukin-12, interleukin-17, and interleukin-23 pathway inhibitors for the treatment of moderate-to-severe chronic plaque psoriasis: ustekinumab, briakinumab, tildrakizumab, guselkumab, secukinumab, ixekizumab, and brodalumab. J Cutan Med Surg 2014; 18:156-69; PMID:24800703
  • McGeachy MJ, Chen Y, Tato CM, Laurence A, Joyce-Shaikh B, Blumenschein WM, McClanahan TK, O'Shea JJ, Cua DJ. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 2009; 10:314-24; PMID:19182808; http://dx.doi.org/10.1038/ni.1698
  • Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 1993; 260:547-9; PMID:8097338; http://dx.doi.org/10.1126/science.8097338
  • McGeachy MJ, Cua DJ. The link between IL-23 and Th17 cell-mediated immune pathologies. Semin Immunol 2007; 19:372-6; PMID:18319054; http://dx.doi.org/10.1016/j.smim.2007.10.012
  • Ghoreschi K, Laurence A, Yang XP, Tato CM, McGeachy MJ, Konkel JE, Ramos HL, Wei L, Davidson TS, Bouladoux N, et al. Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature 2010; 467:967-71; PMID:20962846; http://dx.doi.org/10.1038/nature09447
  • Teunissen MB, Munneke JM, Bernink JH, Spuls PI, Res PC, Te VA, Cheuk S, Brouwer MW, Menting SP, Eidsmo L, et al. Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR(+) ILC3 in lesional skin and blood of psoriasis patients. J Invest Dermatol 2014; 134:2351-60; PMID:24658504; http://dx.doi.org/10.1038/jid.2014.146
  • Villanova F, Flutter B, Tosi I, Grys K, Sreeneebus H, Perera GK, Chapman A, Smith CH, Di MP, Nestle FO. Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J Invest Dermatol 2014; 134:984-91; PMID:24352038; http://dx.doi.org/10.1038/jid.2013.477
  • Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-32; PMID:16200070; http://dx.doi.org/10.1038/ni1254
  • Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201:233-40; PMID:15657292; http://dx.doi.org/10.1084/jem.20041257
  • Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6:1133-41; PMID:16200068
  • Chung Y, Chang SH, Martinez GJ, Yang XO, Nurieva R, Kang HS, Ma L, Watowich SS, Jetten AM, Tian Q, et al. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009; 30:576-87; PMID:19362022
  • Abdi K, Singh NJ, Spooner E, Kessler BM, Radaev S, Lantz L, Xiao TS, Matzinger P, Sun PD, Ploegh HL. Free IL-12p40 monomer is a polyfunctional adaptor for generating novel IL-12-like heterodimers extracellularly. J Immunol 2014; 192:6028-36; PMID:24821971
  • Paunovic V, Carroll HP, Vandenbroeck K, Gadina M. Signalling, inflammation and arthritis: crossed signals: the role of interleukin (IL)-12, -17, -23 and -27 in autoimmunity. Rheumatology(Oxford) 2008; 47:771-6; PMID:18238793
  • Brand S. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009; 58:1152-67; PMID:19592695
  • Zhou L, Littman DR. Transcriptional regulatory networks in Th17 cell differentiation. Curr OpinImmunol 2009; 21:146-52
  • Yang XP, Ghoreschi K, Steward-Tharp SM, Rodriguez-Canales J, Zhu J, Grainger JR, Hirahara K, Sun HW, Wei L, Vahedi G, et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat Immunol 2011; 12:247-54; PMID:21278738
  • Krueger J, Ferris LK, Menter A, Wagner F, White A, Visvanatha S, Lalovic V, Aslanyan S, Hall D, Soinger A, et al. Anti-IL-23A monoclonal antibody BI 655066 for treatment of moderate-to-severe psoriasis: Safety, efficacy, pharmacokinetics and biomarker results of a single-rising-dose, randomised, double-blind, placebo-controlled trial. J All Clin Immunol 2014 ( in press)
  • Parham C, Chirica M, Timans J, Vaisberg E, Travis M, Cheung J, Pflanz S, Zhang R, Singh KP, Vega F, et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol 2002; 168:5699-708; PMID:12023369
  • Jones PT, Dear PH, Foote J, Neuberger MS, Winter G. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 1986; 321:522-5; PMID:3713831
  • Hale G, Dyer MJ, Clark MR, Phillips JM, Marcus R, Riechmann L, Winter G, Waldmann H. Remission induction in non-Hodgkin lymphoma with reshaped human monoclonal antibody CAMPATH-1H. Lancet 1988; 2:1394-9; PMID:2904526
  • Almagro JC, Fransson J. Humanization of antibodies. Front Biosci 2008; 13:1619-33; PMID:17981654
  • Xu D, Alegre ML, Varga SS, Rothermel AL, Collins AM, Pulito VL, Hanna LS, Dolan KP, Parren PW, Bluestone JA, et al. In vitro characterization of five humanized OKT3 effector function variant antibodies. Cell Immunol 2000; 200:16-26; PMID:10716879
  • Laue TM, Stafford WF, III. Modern applications of analytical ultracentrifugation. Annu Rev Biophys Biomol Struct 1999; 28:75-100; PMID:10410796
  • Torrens F. Valence topological charge-transfer indices for dipole moments. Mol Divers 2004; 8:365-70; PMID:15612640
  • Yadav S, Laue TM, Kalonia DS, Singh SN, Shire SJ. The influence of charge distribution on self-association and viscosity behavior of monoclonal antibody solutions. Mol Pharm 2012; 9:791-802; PMID:22352470; http://dx.doi.org/10.1021/mp200566k
  • Clementi N, Mancini N, Criscuolo E, Cappelletti F, Clementi M, Burioni R. Epitope mapping by epitope excision, hydrogen/deuterium exchange, and peptide-panning techniques combined with in silico analysis. Methods Mol Biol 2014; 1131:427-46; PMID:24515481; http://dx.doi.org/10.1007/978-1-62703-992-5_26
  • Ling J, Zhou H, Jiao Q, Davis HM. Interspecies scaling of therapeutic monoclonal antibodies: initial look. J Clin Pharmacol 2009; 49:1382-402; PMID:19837907; http://dx.doi.org/10.1177/0091270009337134
  • Griffiths CE, Strober BE, van de Kerkhof P, Ho V, Fidelus-Gort R, Yeilding N, Guzzo C, Xia Y, Zhou B, Li S, et al. Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med 2010; 362:118-28; PMID:20071701; http://dx.doi.org/10.1056/NEJMoa0810652
  • Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008; 28:454-67; PMID:18400188; http://dx.doi.org/10.1016/j.immuni.2008.03.004
  • Sherlock JP, Joyce-Shaikh B, Turner SP, Chao CC, Sathe M, Grein J, Gorman DM, Bowman EP, McClanahan TK, Yearley JH, et al. IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8- entheseal resident T cells. Nat Med 2012; 18:1069-76; PMID:22772566; http://dx.doi.org/10.1038/nm.2817
  • Witte E, Witte K, Warszawska K, Sabat R, Wolk K. Interleukin-22: a cytokine produced by T, NK and NKT cell subsets, with importance in the innate immune defense and tissue protection. Cytokine Growth Factor Rev 2010; 21:365-79; PMID:20870448; http://dx.doi.org/10.1016/j.cytogfr.2010.08.002
  • Paes AH, Bakker A, Soe-Agnie CJ. Impact of dosage frequency on patient compliance. Diabetes Care 1997; 20:1512-7; PMID:9314626; http://dx.doi.org/10.2337/diacare.20.10.1512
  • Lee EC, Liang Q, Ali H, Bayliss L, Beasley A, Bloomfield-Gerdes T, Bonoli L, Brown R, Campbell J, Carpenter A, et al. Complete humanization of the mouse immunoglobulin loci enables efficient therapeutic antibody discovery. Nat Biotechnol 2014; 32:356-63; PMID:24633243; http://dx.doi.org/10.1038/nbt.2825
  • Reichert JM. Antibodies to watch in 2014. MAbs 2014; 6:5-14; PMID:24284914; http://dx.doi.org/10.4161/mabs.27333
  • Rajewsky K. Clonal selection and learning in the antibody system. Nature 1996; 381:751-8; PMID:8657279; http://dx.doi.org/10.1038/381751a0
  • Takemori T, Kaji T, Takahashi Y, Shimoda M, Rajewsky K. Generation of memory B cells inside and outside germinal centers. Eur J Immunol 2014; 44:1258-64; PMID:24610726; http://dx.doi.org/10.1002/eji.201343716
  • De Groot AS, Moise L, McMurry JA, Wambre E, Van OL, Moingeon P, Scott DW, Martin W. Activation of natural regulatory T cells by IgG Fc-derived peptide “Tregitopes.“ Blood 2008; 112:3303-11; PMID:18660382; http://dx.doi.org/10.1182/blood-2008-02-138073
  • Rosok MJ, Yelton DE, Harris LJ, Bajorath J, Hellstrom KE, Hellstrom I, Cruz GA, Kristensson K, Lin H, Huse WD, et al. A combinatorial library strategy for the rapid humanization of anticarcinoma BR96 Fab. J Biol Chem 1996; 271:22611-8; PMID:8798431; http://dx.doi.org/10.1074/jbc.271.37.22611
  • Waldmann H. Human monoclonal antibodies: the residual challenge of antibody immunogenicity. Methods Mol Biol 2014; 1060:1-8; PMID:24037833; http://dx.doi.org/10.1007/978-1-62703-586-6_1
  • Ewert S, Huber T, Honegger A, Pluckthun A. Biophysical properties of human antibody variable domains. J Mol Biol 2003; 325:531-53; PMID:12498801; http://dx.doi.org/10.1016/S0022-2836(02)01237-8
  • Garber E, Demarest SJ. A broad range of Fab stabilities within a host of therapeutic IgGs. Biochem Biophys Res Commun 2007; 355:751-7; PMID:17321501; http://dx.doi.org/10.1016/j.bbrc.2007.02.042
  • Kuramochi T, Igawa T, Tsunoda H, Hattori K. Humanization and simultaneous optimization of monoclonal antibody. Methods Mol Biol 2014; 1060:123-37; PMID:24037839; http://dx.doi.org/10.1007/978-1-62703-586-6_7
  • Rosenberg AS. Effects of protein aggregates: an immunologic perspective. Amer Assoc Pharm Sci J 2006; 8:E501-E7
  • De Groot AS, Scott DW. Immunogenicity of protein therapeutics. Trends Immunol 2007; 28:482-90; PMID:17964218; http://dx.doi.org/10.1016/j.it.2007.07.011
  • Joshi V, Shivach T, Kumar V, Yadav N, Rathore A. Avoiding antibody aggregation during processing: Establishing hold times. Biotechnol J 2014; 9(9):1195-205; PMID:24753430
  • Manning MC, Chou DK, Murphy BM, Payne RW, Katayama DS. Stability of protein pharmaceuticals: an update. Pharm Res 2010; 27:544-75; PMID:20143256; http://dx.doi.org/10.1007/s11095-009-0045-6
  • He F, Woods CE, Trilisky E, Bower KM, Litowski JR, Kerwin BA, Becker GW, Narhi LO, Razinkov VI. Screening of monoclonal antibody formulations based on high-throughput thermostability and viscosity measurements: design of experiment and statistical analysis. J Pharm Sci 2011; 100:1330-40; PMID:24081468; http://dx.doi.org/10.1002/jps.22384
  • Lobo ED, Hansen RJ, Balthasar JP. Antibody pharmacokinetics and pharmacodynamics. J Pharm Sci 2004; 93:2645-68; PMID:15389672; http://dx.doi.org/10.1002/jps.20178
  • He R, Shepard LW, Chen J, Pan ZK, Ye RD. Serum amyloid A is an endogenous ligand that differentially induces IL-12 and IL-23. J Immunol 2006; 177:4072-9; PMID:16951371; http://dx.doi.org/10.4049/jimmunol.177.6.4072
  • Harlow E, Lane D. Using Antibodies: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory Press; 1999
  • Welschof M, Krauss J. Recombinant Antibodies for Cancer Therapy: Methods and Protocols. Totowa, NJ: Humana Press; 2003
  • Wu H, An LL. Tailoring kinetics of antibodies using focused combinatorial libraries. Methods Mol Biol 2003; 207:213-33; PMID:12412477
  • De Groot AS, Martin W. Reducing risk, improving outcomes: bioengineering less immunogenic protein therapeutics. Clin Immunol 2009; 131:189-201; PMID:19269256; http://dx.doi.org/10.1016/j.clim.2009.01.009
  • Schmidt M, Hafner M, Frech C. Modeling of salt and pH gradient elution in ion-exchange chromatography. J Sep Sci 2014; 37:5-13; PMID:24415551; http://dx.doi.org/10.1002/jssc.201301007
  • Sheeley DM, Merrill BM, Taylor LC. Characterization of monoclonal antibody glycosylation: comparison of expression systems and identification of terminal alpha-linked galactose. Anal Biochem 1997; 247:102-10; PMID:9126378; http://dx.doi.org/10.1006/abio.1997.2036
  • Brown NL, Bottomley SP, Gore MG. Affinity purification of human IgG using immobilised, mutated immunoglobulin-binding domains from protein A of Staphylococcus aureus. Biochem Soc Trans 1998; 26:S249; PMID:9765968
  • Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278:1910-4; PMID:12417590; http://dx.doi.org/10.1074/jbc.M207577200
  • Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 2000; 78:1606-19; PMID:10692345; http://dx.doi.org/10.1016/S0006-3495(00)76713-0
  • Chase S, Laue TM. The determination of protein valence by capillary electrophoresis. PACE Setter 2008; 12(1):1-5
  • Adamson NJ, Reynolds EC. Rules relating electrophoretic mobility, charge and molecular size of peptides and proteins. J Chromatogr B Biomed Sci Appl 1997; 699:133-47; PMID:9392373; http://dx.doi.org/10.1016/S0378-4347(97)00202-8
  • Brown PH, Schuck P. Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation. Biophys J 2006; 90:4651-61; PMID:16565040; http://dx.doi.org/10.1529/biophysj.106.081372