Crystal structure of an HSA/FcRn complex reveals recycling by competitive mimicry of HSA ligands at a pH-dependent hydrophobic interface

Structure

Volumn 21, Issue 11, 2013, Pages 1966-1978

  Schmidt, Michael M ^a   Townson, Sharon A ^a,d   Andreucci, Amy J ^a   King, Bracken M ^a   Schirmer, Emily B ^a,e   Murillo, Alec J ^a,f   Dombrowski, Christian ^a   Tisdale, Alison W ^a   Lowden, Patricia A ^a   Masci, Allyson L ^a,g   Kovalchin, Joseph T ^a   Erbe, David V ^a,h   Wittrup, K Dane ^b,c   Furfine, Eric S ^a   Barnes, Thomas M ^a  

^a Eleven Biotherapeutics   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c KOCH INSTITUTE FOR INTEGRATIVE CANCER RESEARCH   (United States)

^d Epicenter ^*  (United States)

^e Epicenter   (United States)

^f EMD Serono Research Institute   (United States)

^g BIOGEN   (United States)

^h Pronutria   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; FC RECEPTOR; HISTIDINE; HUMAN SERUM ALBUMIN; TRYPTOPHAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANION EXCHANGE; ANTIBODY RESPONSE; AREA UNDER THE CURVE; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG HALF LIFE; ENDOSOME; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HYDROGEN BOND; HYDROPHOBICITY; LIGAND BINDING; MALE; MAXIMUM PLASMA CONCENTRATION; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; SECRETORY CELL; SEQUENCE ANALYSIS; SURFACE PLASMON RESONANCE; YEAST;

MAMMALIA; MUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BETA 2-MICROGLOBULIN; BINDING, COMPETITIVE; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; KINETICS; LIGANDS; MACACA FASCICULARIS; MALE; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RATS; RECEPTORS, FC; SEQUENCE HOMOLOGY; SERUM ALBUMIN;

EID: 84887332244     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.022     Document Type: Article

References (60)

1. E.J. Adams, and A.M. Luoma The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules Annu. Rev. Immunol. 31 2013 529 561
2. S. Akilesh, G.J. Christianson, D.C. Roopenian, and A.S. Shaw Neonatal FcR expression in bone marrow-derived cells functions to protect serum IgG from catabolism J. Immunol. 179 2007 4580 4588
3. J.T. Andersen, J. Dee Qian, and I. Sandlie The conserved histidine 166 residue of the human neonatal Fc receptor heavy chain is critical for the pH-dependent binding to albumin Eur. J. Immunol. 36 2006 3044 3051
4. J.T. Andersen, M.B. Daba, G. Berntzen, T.E. Michaelsen, and I. Sandlie Cross-species binding analyses of mouse and human neonatal Fc receptor show dramatic differences in immunoglobulin G and albumin binding J. Biol. Chem. 285 2010 4826 4836
5. J.T. Andersen, B. Dalhus, J. Cameron, M.B. Daba, A. Plumridge, L. Evans, S.O. Brennan, K.S. Gunnarsen, M. Bjørås, D. Sleep, and I. Sandlie Structure-based mutagenesis reveals the albumin-binding site of the neonatal Fc receptor Nat. Commun. 3 2012 610
6. J.T. Andersen, J. Cameron, A. Plumridge, L. Evans, D. Sleep, and I. Sandlie Single-chain variable fragment albumin fusions bind the neonatal Fc receptor (FcRn) in a species-dependent manner: Implications for in vivo half-life evaluation of albumin fusion therapeutics J. Biol. Chem. 288 2013 24277 24285
7. 131-albumin catabolism and distribution in normal young male adults J. Clin. Invest. 41 1962 1312 1333
8. 131-labeled albumins and nonradioactive human serum albumin in a case of analbuminemia J. Clin. Invest. 38 1959 863 872
9. A.A. Bhattacharya, S. Curry, and N.P. Franks Binding of the general anesthetics propofol and halothane to human serum albumin. High resolution crystal structures J. Biol. Chem. 275 2000 38731 38738
10. E.T. Boder, K.S. Midelfort, and K.D. Wittrup Directed evolution of antibody fragments with monovalent femtomolar antigen-binding affinity Proc. Natl. Acad. Sci. U. S. A. 97 2000 10701 10705
11. O.J. Bos, J.F. Labro, M.J. Fischer, J. Wilting, and L.H. Janssen The molecular mechanism of the neutral-to-base transition of human serum albumin. Acid/base titration and proton nuclear magnetic resonance studies on a large peptic and a large tryptic fragment of albumin J. Biol. Chem. 264 1989 953 959
12. R. Brodersen, S. Andersen, H. Vorum, S.U. Nielsen, and A.O. Pedersen Multiple fatty acid binding to albumin in human blood plasma Eur. J. Biochem. 189 1990 343 349
13. G. Chao, W.L. Lau, B.J. Hackel, S.L. Sazinsky, S.M. Lippow, and K.D. Wittrup Isolating and engineering human antibodies using yeast surface display Nat. Protoc. 1 2006 755 768
14. C. Chaudhury, S. Mehnaz, J.M. Robinson, W.L. Hayton, D.K. Pearl, D.C. Roopenian, and C.L. Anderson The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan J. Exp. Med. 197 2003 315 322
15. C. Chaudhury, C.L. Brooks, D.C. Carter, J.M. Robinson, and C.L. Anderson Albumin binding to FcRn: distinct from the FcRn-IgG interaction Biochemistry 45 2006 4983 4990
16. S. Curry Lessons from the crystallographic analysis of small molecule binding to human serum albumin Drug Metab. Pharmacokinet. 24 2009 342 357
17. S. Curry, H. Mandelkow, P. Brick, and N. Franks Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites Nat. Struct. Biol. 5 1998 827 835
18. W.F. Dall'Acqua, R.M. Woods, E.S. Ward, S.R. Palaszynski, N.K. Patel, Y.A. Brewah, H. Wu, P.A. Kiener, and S. Langermann Increasing the affinity of a human IgG1 for the neonatal Fc receptor: biological consequences J. Immunol. 169 2002 5171 5180
19. A. Datta-Mannan, D.R. Witcher, Y. Tang, J. Watkins, and V.J. Wroblewski Monoclonal antibody clearance. Impact of modulating the interaction of IgG with the neonatal Fc receptor J. Biol. Chem. 282 2007 1709 1717
20. A. Datta-Mannan, C.K. Chow, C. Dickinson, D. Driver, J. Lu, D.R. Witcher, and V.J. Wroblewski FcRn affinity-pharmacokinetic relationship of five human IgG4 antibodies engineered for improved in vitro FcRn binding properties in cynomolgus monkeys Drug Metab. Dispos. 40 2012 1545 1555
21. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
22. Y. Feng, R. Gong, and D.S. Dimitrov Design, expression and characterization of a soluble single-chain functional human neonatal Fc receptor Protein Expr. Purif. 79 2011 66 71
23. J. Gabrielsson, and D. Weiner Pharmacokinetic and Pharmacodynamic Data Analysis: Concepts and Applications Fourth Edition 2007 Swedish Pharmaceutical Press Stockholm
24. Gao, C., Chaudhury, C., and Yao, X. February 2013. HSA-related compositions and methods of use. U.S. patent 2013/0053322.
25. V. Ghetie, S. Popov, J. Borvak, C. Radu, D. Matesoi, C. Medesan, R.J. Ober, and E.S. Ward Increasing the serum persistence of an IgG fragment by random mutagenesis Nat. Biotechnol. 15 1997 637 640
26. J. Ghuman, P.A. Zunszain, I. Petitpas, A.A. Bhattacharya, M. Otagiri, and S. Curry Structural basis of the drug-binding specificity of human serum albumin J. Mol. Biol. 353 2005 38 52
27. B. Gurbaxani, L.L. Dela Cruz, K. Chintalacharuvu, and S.L. Morrison Analysis of a family of antibodies with different half-lives in mice fails to find a correlation between affinity for FcRn and serum half-life Mol. Immunol. 43 2006 1462 1473
28. B. Gurbaxani, M. Dostalek, and I. Gardner Are endosomal trafficking parameters better targets for improving mAb pharmacokinetics than FcRn binding affinity? Mol. Immunol. 56 2013 660 674
29. P.R. Hinton, M.G. Johlfs, J.M. Xiong, K. Hanestad, K.C. Ong, C. Bullock, S. Keller, M.T. Tang, J.Y. Tso, M. Vásquez, and N. Tsurushita Engineered human IgG antibodies with longer serum half-lives in primates J. Biol. Chem. 279 2004 6213 6216
30. P.R. Hinton, J.M. Xiong, M.G. Johlfs, M.T. Tang, S. Keller, and N. Tsurushita An engineered human IgG1 antibody with longer serum half-life J. Immunol. 176 2006 346 356
31. E.J. Israel, N. Simister, E. Freiberg, A. Caplan, and W.A. Walker Immunoglobulin G binding sites on the human foetal intestine: a possible mechanism for the passive transfer of immunity from mother to infant Immunology 79 1993 77 81
32. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
33. V.E. Kenanova, T. Olafsen, F.B. Salazar, L.E. Williams, S. Knowles, and A.M. Wu Tuning the serum persistence of human serum albumin domain III:diabody fusion proteins Protein Eng. Des. Sel. 23 2010 789 798
34. J. Kim, C.L. Bronson, W.L. Hayton, M.D. Radmacher, D.C. Roopenian, J.M. Robinson, and C.L. Anderson Albumin turnover: FcRn-mediated recycling saves as much albumin from degradation as the liver produces Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G352 G360
35. J. Kim, W.L. Hayton, J.M. Robinson, and C.L. Anderson Kinetics of FcRn-mediated recycling of IgG and albumin in human: pathophysiology and therapeutic implications using a simplified mechanism-based model Clin. Immunol. 122 2007 146 155
36. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
37. T.T. Kuo, and V.G. Aveson Neonatal Fc receptor and IgG-based therapeutics MAbs. 3 2011 422 430
38. J.F. Labro, and L.H. Janssen A proton nuclear magnetic resonance study of human serum albumin in the neutral pH region Biochim. Biophys. Acta 873 1986 267 278
39. R. Liu, J. Yang, C.E. Ha, N.V. Bhagavan, and R.G. Eckenhoff Truncated human serum albumin retains general anaesthetic binding activity Biochem. J. 388 2005 39 45
40. X. Liu, L. Lu, Z. Yang, S. Palaniyandi, R. Zeng, L.Y. Gao, D.M. Mosser, D.C. Roopenian, and X. Zhu The neonatal FcR-mediated presentation of immune-complexed antigen is associated with endosomal and phagosomal pH and antigen stability in macrophages and dendritic cells J. Immunol. 186 2011 4674 4686
41. W.L. Martin, A.P.J. West Jr., L. Gan, and P.J. Bjorkman Crystal structure at 2.8 A of an FcRn/heterodimeric Fc complex: mechanism of pH-dependent binding Mol. Cell 7 2001 867 877
42. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
43. A.R. Mezo, V. Sridhar, J. Badger, P. Sakorafas, and V. Nienaber X-ray crystal structures of monomeric and dimeric peptide inhibitors in complex with the human neonatal Fc receptor, FcRn J. Biol. Chem. 285 2010 27694 27701
44. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
45. H. Nielsen, U. Kragh-Hansen, L. Minchiotti, M. Galliano, S.O. Brennan, A.L. Tárnoky, M.H. Franco, F.M. Salzano, and O. Sugita Effect of genetic variation on the fatty acid-binding properties of human serum albumin and proalbumin Biochim. Biophys. Acta 1342 1997 191 204
46. R.J. Ober, C. Martinez, C. Vaccaro, J. Zhou, and E.S. Ward Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn J. Immunol. 172 2004 2021 2029
47. R.J. Peach, and S.O. Brennan Structural characterization of a glycoprotein variant of human serum albumin: albumin Casebrook (494 Asp - - Asn) Biochim. Biophys. Acta 1097 1991 49 54
48. I. Petitpas, C.E. Petersen, C.E. Ha, A.A. Bhattacharya, P.A. Zunszain, J. Ghuman, N.V. Bhagavan, and S. Curry Structural basis of albumin-thyroxine interactions and familial dysalbuminemic hyperthyroxinemia Proc. Natl. Acad. Sci. U. S. A. 100 2003 6440 6445
49. S.B. Petkova, S. Akilesh, T.J. Sproule, G.J. Christianson, H. Al Khabbaz, A.C. Brown, L.G. Presta, Y.G. Meng, and D.C. Roopenian Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: potential application in humorally mediated autoimmune disease Int. Immunol. 18 2006 1759 1769
50. Plumridge, A. Sleep, D., Cameron, J., Sandlie, I., Andersen, J.T., and Friis, E.P. August 2012. Albumin variants. U.S. patent 2012/0220530.
51. J.A. Rakestraw, A.R. Baskaran, and K.D. Wittrup A flow cytometric assay for screening improved heterologous protein secretion in yeast Biotechnol. Prog. 22 2006 1200 1208
52. J.A. Rakestraw, S.L. Sazinsky, A. Piatesi, E. Antipov, and K.D. Wittrup Directed evolution of a secretory leader for the improved expression of heterologous proteins and full-length antibodies in Saccharomyces cerevisiae Biotechnol. Bioeng. 103 2009 1192 1201
53. R. Rodewald, and J.P. Kraehenbuhl Receptor-mediated transport of IgG J. Cell Biol. 99 1984 159s 164s
54. J.R. Simard, P.A. Zunszain, C.-E. Ha, J.S. Yang, N.V. Bhagavan, I. Petitpas, S. Curry, and J.A. Hamilton Locating high-affinity fatty acid-binding sites on albumin by x-ray crystallography and NMR spectroscopy Proc. Natl. Acad. Sci. U. S. A. 102 2005 17958 17963
55. H.L. Spiegelberg, B.G. Fishkin, and H.M. Grey Catabolism of human gammaG-immunoglobulins of different heavy chain subclasses. I. Catabolism of gammaG-myeloma proteins in man J. Clin. Invest. 47 1968 2323 2330
56. N.M. Stapleton, J.T. Andersen, A.M. Stemerding, S.P. Bjarnarson, R.C. Verheul, J. Gerritsen, Y. Zhao, M. Kleijer, I. Sandlie, and M. de Haas Competition for FcRn-mediated transport gives rise to short half-life of human IgG3 and offers therapeutic potential Nat. Commun. 2 2011 599
57. S. Sugio, A. Kashima, S. Mochizuki, M. Noda, and K. Kobayashi Crystal structure of human serum albumin at 2.5 A resolution Protein Eng. 12 1999 439 446
58. W. Wang, P. Lu, Y. Fang, L. Hamuro, T. Pittman, B. Carr, J. Hochman, and T. Prueksaritanont Monoclonal antibodies with identical Fc sequences can bind to FcRn differentially with pharmacokinetic consequences Drug Metab. Dispos. 39 2011 1469 1477
59. A.P.J. West Jr., and P.J. Bjorkman Crystal structure and immunoglobulin G binding properties of the human major histocompatibility complex-related Fc receptor(,) Biochemistry 39 2000 9698 9708
60. Y.A. Yeung, M.K. Leabman, J.S. Marvin, J. Qiu, C.W. Adams, S. Lien, M.A. Starovasnik, and H.B. Lowman Engineering human IgG1 affinity to human neonatal Fc receptor: impact of affinity improvement on pharmacokinetics in primates J. Immunol. 182 2009 7663 7671