The effect of pH dependence of antibody-antigen interactions on subcellular trafficking dynamics

mAbs

Volumn 5, Issue 6, 2013, Pages 851-859

  Devanaboyina, Siva Charan ^a   Lynch, Sandra M ^a,e   Ober, Raimund J ^a,b   Ram, Sripad ^a,b   Kim, Dongyoung ^a,b   Puig Canto, Alberto ^a   Breen, Shannon ^c   Kasturirangan, Srinath ^d   Fowler, Susan ^d   Peng, Li ^d   Zhong, Haihong ^c   Jermutus, Lutz ^d   Wu, Herren ^d   Webster, Carl ^d   Ward, E Sally ^a   Gao, Changshou ^d  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b The University of Texas at Dallas   (United States)

^c MEDIMMUNE   (United States)

^d Department of Antibody Discovery and Protein Engineering Medimmune ^*  (United Kingdom)

^e ALBANY COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

Author keywords

Antigen buffering; Antigen antibody trafficking; PH dependent

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; ANTIGEN; MONOCLONAL ANTIBODY; PROTEIN BINDING;

ACUTE PHASE RESPONSE; ANTIBODY ENGINEERING; ANTIBODY RESPONSE; ANTIGEN ANTIBODY REACTION; ARTICLE; BINDING AFFINITY; CELL ASSAY; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; PH; SURFACE PLASMON RESONANCE; ANIMAL; CELL CULTURE; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; MOUSE; PROTEIN TRANSPORT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; HYDROGEN-ION CONCENTRATION; INTERLEUKIN-6; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84889828313     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.26389     Document Type: Article

References (57)

1. Chan AC, Carter PJ. Therapeutic antibodies for autoimmunity and inflammation. Nat Rev Immunol 2010; 10:301-16; PMID:20414204; http://dx.doi.org/10.1038/nri2761
2. Winter G, Griffiths AD, Hawkins RE, Hoogenboom HR. Making antibodies by phage display technology. Annu Rev Immunol 1994; 12:433-55; PMID:8011287; http://dx.doi.org/10.1146/annurev.iy.12.040194.002245
3. Gai SA, Wittrup KD. Yeast surface display for protein engineering and characterization. Curr Opin Struct Biol 2007; 17:467-73; PMID:17870469; http://dx.doi.org/10.1016/j.sbi.2007.08.012
4. Gao CS, Mao SL, Kaufmann G, Wirsching P, Lerner RA, Janda KD. A method for the generation of combinatorial antibody libraries using pIX phage display. Proc Natl Acad Sci U S A 2002; 99:12612-6; PMID:12239343; http://dx.doi.org/10. 1073/pnas.192467999
5. Desjarlais JR, Lazar GA, Zhukovsky EA, Chu SY. Optimizing engagement of the immune system by anti-tumor antibodies: an engineer's perspective. Drug Discov Today 2007; 12:898-910; PMID:17993407; http://dx.doi.org/10.1016/j. drudis.2007.08.009
6. Stavenhagen JB, Gorlatov S, Tuaillon N, Rankin CT, Li H, Burke S, Huang L, Johnson S, Koenig S, Bonvini E. Enhancing the potency of therapeutic monoclonal antibodies via Fc optimization. Adv Enzyme Regul 2008; 48:152-64; PMID:18177741; http://dx.doi.org/10.1016/j.advenzreg.2007.11.011
7. Ghetie V, Popov S, Borvak J, Radu C, Matesoi D, Medesan C, Ober RJ, Ward ES. Increasing the serum persistence of an IgG fragment by random mutagenesis. Nat Biotechnol 1997; 15:637-40; PMID:9219265; http://dx.doi.org/10.1038/nbt0797- 637
8. 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; 281:23514-24; PMID:16793771; http://dx.doi.org/10.1074/jbc.M604292200
9. 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; 176:346-56; PMID:16365427
10. Wu H, Pfarr DS, Losonsky GA, Kiener PA. Immunoprophylaxis of RSV infection: advancing from RSV-IGIV to palivizumab and motavizumab. Curr Top Microbiol Immunol 2008; 317:103-23; PMID:17990791; http://dx.doi.org/10.1007/ 978-3-540-72146-8-4
11. 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; 28:1203-7; PMID:20953198; http://dx.doi.org/10.1038/nbt. 1691
12. 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; 287:11090-7; PMID:22294692; http://dx.doi.org/10.1074/jbc.M111.319764
13. Junghans RP, Anderson CL. The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. Proc Natl Acad Sci U S A 1996; 93:5512-6; PMID:8643606; http://dx.doi.org/10.1073/ pnas.93.11.5512
14. O'Hear CE, Foote J. Antibody buffering of a ligand in vivo. Proc Natl Acad Sci U S A 2005; 102:40-4; PMID:15615858; http://dx.doi.org/10.1073/pnas. 0405797102
15. 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; 151:1235-44; PMID:8393043
16. Rehlaender BN, Cho MJ. Antibodies as carrier proteins. Pharm Res 1998; 15:1652-6; PMID:9833983; http://dx.doi.org/10.1023/A:1011936007457
17. Phelan JD, Orekov T, Finkelman FD. Cutting edge: mechanism of enhancement of in vivo cytokine effects by anti-cytokine monoclonal antibodies. J Immunol 2008; 180:44-8; PMID:18097002
18. Ober RJ, Martinez C, Vaccaro C, Zhou J, Ward ES. Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J Immunol 2004; 172:2021-9; PMID:14764666
19. Ward ES, Ober RJ. Chapter 4: Multitasking by exploitation of intracellular transport functions: the many faces of FcRn. Adv Immunol 2009; 103:77-115; PMID:19755184; http://dx.doi.org/10.1016/S0065-2776(09)03004-1
20. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 2007; 7:715-25; PMID:17703228; http://dx.doi.org/10.1038/nri2155
21. 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:e63236; PMID:23667591; http://dx.doi.org/10.1371/journal.pone.0063236
22. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev Immunol 2005; 23:1-21; PMID:15771564; http://dx.doi.org/10. 1146/annurev.immunol.23.021704.115806
23. Damas P, Ledoux D, Nys M, Vrindts Y, De Groote D, Franchimont P, Lamy M. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 1992; 215:356-62; PMID:1558416; http://dx.doi.org/10.1097/00000658- 199204000-00009
24. Lu ZY, Brailly H, Rossi JF, Wijdenes J, Bataille R, Klein B. Overall interleukin-6 production exceeds 7 mg/day in multiple myeloma complicated by sepsis. Cytokine 1993; 5:578-82; PMID:8186369; http://dx.doi.org/10.1016/S1043- 4666(05)80007-9
25. Tanaka T, Narazaki M, Kishimoto T. Therapeutic targeting of the interleukin-6 receptor. Annu Rev Pharmacol Toxicol 2012; 52:199-219; PMID:21910626; http://dx.doi.org/10.1146/annurev-pharmtox-010611-134715
26. Yamaguchi K, Itoh Y, Yokomizo C, Nishimura T, Niimi T, Umemura A, Fujii H, Okanoue T, Yoshikawa T. Blockade of IL-6 signaling exacerbates liver injury and suppresses antiapoptotic gene expression in methionine choline-deficient diet-fed db/db mice. Lab Invest 2011; 91:609-18; PMID:21321532; http://dx.doi.org/10.1038/labinvest.2011.2
27. van Rhee F, Fayad L, Voorhees P, Furman R, Lonial S, Borghaei H, Sokol L, Crawford J, Cornfeld M, Qi M, et al. Siltuximab, a novel anti-interleukin-6 monoclonal antibody, for Castleman's disease. J Clin Oncol 2010; 28:3701-8; PMID:20625121; http://dx.doi.org/10.1200/JCO.2009.27.2377
28. Xu ZH, Bouman-Thio E, Comisar C, Frederick B, Van Hartingsveldt B, Marini JC, Davis HM, Zhou H. Pharmacokinetics, pharmacodynamics and safety of a human anti-IL-6 monoclonal antibody (sirukumab) in healthy subjects in a first-in-human study. Br J Clin Pharmacol 2011; 72:270-81; PMID:21392075; http://dx.doi.org/10.1111/j.1365-2125.2011.03964.x
29. Heremans H, Dillen C, Put W, Van Damme J, Billiau A. Protective effect of anti-interleukin (IL)-6 antibody against endotoxin, associated with paradoxically increased IL-6 levels. Eur J Immunol 1992; 22:2395-401; PMID:1381315; http://dx.doi.org/10.1002/eji.1830220932
30. May LT, Neta R, Moldawer LL, Kenney JS, Patel K, Sehgal PB. Antibodies chaperone circulating IL-6. Paradoxical effects of anti-IL-6 "neutralizing" antibodies in vivo. J Immunol 1993; 151:3225-36; PMID:8376777
31. van Zaanen HC, Lokhorst HM, Aarden LA, Rensink HJ, Warnaar SO, van der Lelie J, van Oers MH. Chimaeric anti-interleukin 6 monoclonal antibodies in the treatment of advanced multiple myeloma: a phase I dose-escalating study. Br J Haematol 1998; 102:783-90; PMID:9722307; http://dx.doi.org/10.1046/j.1365-2141. 1998.00835.x
32. Martens E, Dillen C, Put W, Heremans H, van Damme J, Billiau A. Increased circulating interleukin-6 (IL-6) activity in endotoxin-challenged mice pretreated with anti-IL-6 antibody is due to IL-6 accumulated in antigen-antibody complexes. Eur J Immunol 1993; 23:2026-9; PMID:8344369; http://dx.doi.org/10.1002/eji.1830230846
33. May LT, Patel K, García D, Ndubuisi MI, Ferrone S, Mittelman A, Mackiewicz A, Sehgal PB. Sustained high levels of circulating chaperoned interleukin-6 after active specific cancer immunotherapy. Blood 1994; 84:1887-95; PMID:8080995
34. Frassanito MA, Cusmai A, Iodice G, Dammacco F. Autocrine interleukin-6 production and highly malignant multiple myeloma: relation with resistance to drug-induced apoptosis. Blood 2001; 97:483-9; PMID:11154226; http://dx.doi.org/10.1182/blood.V97.2.483
35. Sarkar CA, Lowenhaupt K, Horan T, Boone TC, Tidor B, Lauffenburger DA. Rational cytokine design for increased lifetime and enhanced potency using pH-activated "histidine switching". Nat Biotechnol 2002; 20:908-13; PMID:12161759; http://dx.doi.org/10.1038/nbt725
36. 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; 20:1619-31; PMID:21766385; http://dx.doi.org/10. 1002/pro.696
37. Zhou J, Mateos F, Ober RJ, Ward ES. Conferring the binding properties of the mouse MHC class I-related receptor, FcRn, onto the human ortholog by sequential rounds of site-directed mutagenesis. J Mol Biol 2005; 345:1071-81; PMID:15644205; http://dx.doi.org/10.1016/j.jmb.2004.11.014
38. Gan Z, Ram S, Vaccaro C, Ober RJ, Ward ES. Analyses of the recycling receptor, FcRn, in live cells reveal novel pathways for lysosomal delivery. Traffic 2009; 10:600-14; PMID:19192244; http://dx.doi.org/10.1111/j.1600-0854. 2009.00887.x
39. Zhou J, Johnson JE, Ghetie V, Ober RJ, Ward ES. Generation of mutated variants of the human form of the MHC class I-related receptor, FcRn, with increased affinity for mouse immunoglobulin G. J Mol Biol 2003; 332:901-13; PMID:12972260; http://dx.doi.org/10.1016/S0022-2836(03)00952-5
40. Goldenthal KL, Hedman K, Chen JW, August JT, Vihko P, Pastan I, Willingham MC. Pre-lysosomal divergence of alpha 2-macroglobulin and transferrin: a kinetic study using a monoclonal antibody against a lysosomal membrane glycoprotein (LAMP-1). J Histochem Cytochem 1988; 36:391-400; PMID:2450119; http://dx.doi.org/10.1177/36.4.2450119
41. Ober RJ, Martinez C, Lai X, Zhou J, Ward ES. Exocytosis of IgG as mediated by the receptor, FcRn: an analysis at the single-molecule level. Proc Natl Acad Sci U S A 2004; 101:11076-81; PMID:15258288; http://dx.doi.org/10. 1073/pnas.0402970101
42. Prabhat P, Gan Z, Chao J, Ram S, Vaccaro C, Gibbons S, Ober RJ, Ward ES. Elucidation of intracellular recycling pathways leading to exocytosis of the Fc receptor, FcRn, by using multifocal plane microscopy. Proc Natl Acad Sci U S A 2007; 104:5889-94; PMID:17384151; http://dx.doi.org/10.1073/pnas.0700337104
43. Ferris AL, Brown JC, Park RD, Storrie B. Chinese hamster ovary cell lysosomes rapidly exchange contents. J Cell Biol 1987; 105:2703-12; PMID:2447096; http://dx.doi.org/10.1083/jcb.105.6.2703
44. Pu Z, Lovitch SB, Bikoff EK, Unanue ER. T cells distinguish MHC-peptide complexes formed in separate vesicles and edited by H2-DM. Immunity 2004; 20:467-76.
45. Lovitch SB, Unanue ER. Conformational isomers of a peptide-class II major histocompatibility complex. Immunol Rev 2005; 207:293-313; PMID:16181344; http://dx.doi.org/10.1111/j.0105-2896.2005.00298.x
46. Huang JC, Han M, Minguela A, Pastor S, Qadri A, Ward ES. T cell recognition of distinct peptide:I-Au conformers in murine experimental autoimmune encephalomyelitis. J Immunol 2003; 171:2467-77; PMID:12928395
47. Sercarz EE, Maverakis E. Mhc-guided processing: binding of large antigen fragments. Nat Rev Immunol 2003; 3:621-9; PMID:12974477; http://dx.doi.org/10. 1038/nri1149
48. Simitsek PD, Campbell DG, Lanzavecchia A, Fairweather N, Watts C. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J Exp Med 1995; 181:1957-63; PMID:7539034; http://dx.doi.org/10. 1084/jem.181.6.1957
49. Watts C, Antoniou A, Manoury B, Hewitt EW, Mckay LM, Grayson L, Fairweather NF, Emsley P, Isaacs N, Simitsek PD. Modulation by epitope-specific antibodies of class II MHC-restricted presentation of the tetanus toxin antigen. Immunol Rev 1998; 164:11-6; PMID:9795759; http://dx.doi.org/10.1111/j.1600- 065X.1998.tb01203.x
50. Ozaki S, Berzofsky JA. Antibody conjugates mimic specific B cell presentation of antigen: relationship between T and B cell specificity. J Immunol 1987; 138:4133-42; PMID:2438335
51. Watts C, Lanzavecchia A. Suppressive effect of antibody on processing of T cell epitopes. J Exp Med 1993; 178:1459-63; PMID:7690836; http://dx.doi.org/ 10.1084/jem.178.4.1459
52. Mi WT, Wanjie S, Lo ST, Gan Z, Pickl-Herk B, Ober RJ, Ward ES. Targeting the neonatal Fc receptor for antigen delivery using engineered Fc fragments. J Immunol 2008; 181:7550-61; PMID:19017944
53. Manca F, Fenoglio D, Kunkl A, Cambiaggi C, Sasso M, Celada F. Differential activation of T cell clones stimulated by macrophages exposed to antigen complexed with monoclonal antibodies. A possible influence of paratope specificity on the mode of antigen processing. J Immunol 1988; 140:2893-8; PMID:3129502
54. Nimmerjahn F, Ravetch JV. Fc-receptors as regulators of immunity. Adv Immunol 2007; 96:179-204; PMID:17981207; http://dx.doi.org/10.1016/S0065- 2776(07)96005-8
55. Qiao SW, Kobayashi K, Johansen FE, Sollid LM, Andersen JT, Milford E, Roopenian DC, Lencer WI, Blumberg RS. Dependence of antibody-mediated presentation of antigen on FcRn. Proc Natl Acad Sci U S A 2008; 105:9337-42; PMID:18599440; http://dx.doi.org/10.1073/pnas.0801717105
56. Vaccaro C, Bawdon R, Wanjie S, Ober RJ, Ward ES. Divergent activities of an engineered antibody in murine and human systems have implications for therapeutic antibodies. Proc Natl Acad Sci U S A 2006; 103:18709-14; PMID:17116867; http://dx.doi.org/10.1073/pnas.0606304103
57. Ward ES, Martinez C, Vaccaro C, Zhou J, Tang Q, Ober RJ. From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol Biol Cell 2005; 16:2028-38; PMID:15689494; http://dx.doi.org/10.1091/mbc.E04-08-0735