Prevalence and gene characteristics of antibodies with cofactor-induced HIV-1 specificity

Journal of Biological Chemistry

Volumn 290, Issue 8, 2015, Pages 5203-5213

  Lecerf, Maxime ^a,b   Scheel, Tobias ^c   Pashov, Anastas D ^d   Jarossay, Annaelle ^a,b   Ohayon, Delphine ^a,b   Planchais, Cyril ^a,b   Mesnage, Stephane ^e   Berek, Claudia ^c   Kaveri, Srinivas V ^a,b   Lacroix Desmazes, Sébastien ^a,b   Dimitrov, Jordan D ^a,b  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^d INSTITUTE OF MICROBIOLOGY   (Bulgaria)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; PORPHYRINS;

COFACTOR BINDING; COFACTORS; HIGH FREQUENCY HF; MOLECULAR FEATURE; VARIABLE REGIONS;

ANTIBODIES;

ANTIBODY; GLYCOPROTEIN GP 120; HEME; IMMUNOGLOBULIN G; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN VARIABLE REGION;

ADAPTIVE IMMUNITY; ANTIBODY COMBINING SITE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE SUBPOPULATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; SOMATIC MUTATION; VIRUS STRAIN; B LYMPHOCYTE; GENETICS; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTIVE IMMUNITY; B-LYMPHOCYTES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNOGLOBULIN VARIABLE REGION;

EID: 84925415904     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.618124     Document Type: Article

References (72)

1. Baker, H., Frank, O., Feingold, S., and Leevy, C. M. (1967) Vitamin distribution in human plasma proteins. Nature 215, 84-85
2. Watson, C. D., and Ford, H. C. (1988) High-affinity binding of riboflavin and FAD by immunoglobulins from normal human serum. Biochem. Int. 16, 1067-1074
3. Rajagopalan, K., Pavlinkova, G., Levy, S., Pokkuluri, P. R., Schiffer, M., Haley, B. E., and Kohler, H. (1996) Novel unconventional binding site in the variable region of immunoglobulins. Proc. Natl. Acad. Sci. U.S.A. 93, 6019-6024
4. Brancaleon, L., and Moseley, H. (2002) Effects of photoproducts on the binding properties of protoporphyrin IX to proteins. Biophys. Chem. 96, 77-87
5. Zhou, T., Hamer, D. H., Hendrickson, W. A., Sattentau, Q. J., and Kwong, P. D. (2005) Interfacial metal and antibody recognition. Proc. Natl. Acad. Sci. U.S.A. 102, 14575-14580
6. Zhu, X., Wentworth, P., Jr., Kyle, R. A., Lerner, R. A., and Wilson, I. A. (2006) Cofactor-containing antibodies: crystal structure of the original yellow antibody. Proc. Natl. Acad. Sci. U.S.A. 103, 3581-3585
7. Dimitrov, J. D., Roumenina, L. T., Doltchinkova, V. R., Mihaylova, N. M., Lacroix-Desmazes, S., Kaveri, S. V., and Vassilev, T. L. (2007) Antibodies use heme as a cofactor to extend their pathogen elimination activity and to acquire new effector functions. J. Biol. Chem. 282, 26696-26706
8. Karjalainen, K., and Mäkelä, O. (1976) Concentrations of three haptenbinding immunoglobulins in pooled normal human serum. Eur. J. Immunol. 6, 88-93
9. Farah, F. S. (1973) Natural antibodies specific to the 2,4-dinitrophenyl group. Immunology 25, 217-226
10. Ternynck, T., and Avrameas, S. (1986) Murine natural monoclonal autoantibodies: a study of their polyspecificities and their affinities. Immunol. Rev. 94, 99-112
11. Stopa, B., Konieczny, L., Piekarska, B., Roterman, I., Rybarska, J., and Skowronek, M. (1997) Effect of self association of bis-ANS and bis-azo dyes on protein binding. Biochimie 79, 23-26
12. Krol, M., Roterman, I., Drozd, A., Konieczny, L., Piekarska, B., Rybarska, J., Spolnik, P., and Stopa, B. (2006) The increased flexibility of CDR loops generated in antibodies by Congo red complexation favors antigen binding. J. Biomol. Struct. Dyn. 23, 407-416
13. Xu, Y., Hixon, M. S., Yamamoto, N., McAllister, L. A., Wentworth, A. D., Wentworth, P., Jr., and Janda, K. D. (2007) Antibody-catalyzed anaerobic destruction of methamphetamine. Proc. Natl. Acad. Sci. U.S.A. 104, 3681-3686
14. Murelli, R. P., Zhang, A. X., Michel, J., Jorgensen, W. L., and Spiegel, D. A. (2009) Chemical control over immune recognition: a class of antibodyrecruiting small molecules that target prostate cancer. J. Am. Chem. Soc. 131, 17090-17092
15. Parker, C. G., Domaoal, R. A., Anderson, K. S., and Spiegel, D. A. (2009) An antibody-recruiting small molecule that targets HIV gp120. J. Am. Chem. Soc. 131, 16392-16394
16. Zhang, A. X., Murelli, R. P., Barinka, C., Michel, J., Cocleaza, A., Jorgensen, W. L., Lubkowski, J., and Spiegel, D. A. (2010)Aremote arene-binding site on prostate specific membrane antigen revealed by antibody-recruiting small molecules. J. Am. Chem. Soc. 132, 12711-12716
17. McEnaney, P. J., Parker, C. G., Zhang, A. X., and Spiegel, D. A. (2012) Antibody-recruiting molecules: an emerging paradigm for engaging immune function in treating human disease. ACS Chem. Biol. 7, 1139-1151
18. McIntyre, J. A. (2004) The appearance and disappearance of antiphospholipid autoantibodies subsequent to oxidation-reduction reactions. Thromb. Res. 114, 579-587
19. McIntyre, J. A., Wagenknecht, D. R., and Faulk, W. P. (2005) Autoantibodies unmasked by redox reactions. J. Autoimmun. 24, 311-317
20. Dimitrov, J. D., Ivanovska, N. D., Lacroix-Desmazes, S., Doltchinkova, V. R., Kaveri, S. V., and Vassilev, T. L. (2006) Ferrous ions and reactive oxygen species increase antigen-binding and anti-inflammatory activities of immunoglobulin G. J. Biol. Chem. 281, 439-446
21. Dimitrov, J. D., and Vassilev, T. L. (2009) Cofactor-mediated protein promiscuity. Nat. Biotechnol. 27, 892
22. McIntyre, J. A., and Faulk, W. P. (2009) Redox-reactive autoantibodies: biochemistry, characterization, and specificities. Clin. Rev. Allergy Immunol. 37, 49-54
23. McIntyre, J. A., and Faulk, W. P. (2010) Autoantibody potential of cancer therapeutic monoclonal antibodies. Int. J. Cancer 127, 491-496
24. Pavlovic, S., Zdravkovic, N., Dimitrov, J. D., Djukic, A., Arsenijevic, N., Vassilev, T. L., and Lukic, M. L. (2011) Intravenous immunoglobulins exposed to heme (heme IVIG) are more efficient than IVIG in attenuating autoimmune diabetes. Clin. Immunol. 138, 162-171
25. Wagener, F. A., Volk, H. D., Willis, D., Abraham, N. G., Soares, M. P., Adema, G. J., and Figdor, C. G. (2003) Different faces of the heme-heme oxygenase system in inflammation. Pharmacol. Rev. 55, 551-571
26. Kumar, S., and Bandyopadhyay, U. (2005) Free heme toxicity and its detoxification systems in human. Toxicol. Lett. 157, 175-188
27. Gladwin, M. T., Kanias, T., and Kim-Shapiro, D. B. (2012) Hemolysis and cell-free hemoglobin drive an intrinsic mechanism for human disease. J. Clin. Invest. 122, 1205-1208
28. Scheel, T. (2009) [The B-cell response in the synovial tissue of patients with rheumatoid arthritis.] Ph.D. thesis, Humboldt-Universität zu Berlin
29. Scheel, T., Gursche, A., Zacher, J., Häupl, T., and Berek, C. (2011) V-region gene analysis of locally defined synovial B and plasma cells reveals selected B cell expansion and accumulation of plasma cell clones in rheumatoid arthritis. Arthritis Rheum. 63, 63-72
30. Padlan, E. A. (1994) Anatomy of the antibody molecule. Mol. Immunol. 31, 169-217
31. Dimitrov, J. D., Planchais, C., Scheel, T., Ohayon, D., Mesnage, S., Berek, C., Kaveri, S. V., and Lacroix-Desmazes, S. (2014) A cryptic polyreactive antibody recognizes distinct clades of HIV-1 gp120 by an identical binding mechanism. J. Biol. Chem. 289, 17767-17779
32. Munro, A. W., Girvan, H. M., McLean, K., Cheesman, M. R., and Leys, D. (2009) Heme and hemeproteins, in Tetrapyrroles Birth, Life and Death (Warren, M. J., and Smith, A. G., eds), pp. 160-207, Springer Science, New York
33. Smith, A. (2009) Novel heme-protein interactions: some more radical than others, in Tetrapyrroles Birth, Life and Death (Warren, M. J., and Smith, A. G., eds), pp. 184-207, Springer Science, New York
34. Wedemayer, G. J., Patten, P. A., Wang, L. H., Schultz, P. G., and Stevens, R. C. (1997) Structural insights into the evolution of an antibody combining site. Science 276, 1665-1669
35. Manivel, V., Sahoo, N. C., Salunke, D. M., and Rao, K. V. (2000) Maturation of an antibody response is governed by modulations in flexibility of the antigen-combining site. Immunity 13, 611-620
36. James, L. C., Roversi, P., and Tawfik, D. S. (2003) Antibody multispecificity mediated by conformational diversity. Science 299, 1362-1367
37. Nguyen, H. P., Seto, N. O., MacKenzie, C. R., Brade, L., Kosma, P., Brade, H., and Evans, S. V. (2003) Germline antibody recognition of distinct carbohydrate epitopes. Nat. Struct. Biol. 10, 1019-1025
38. Jimenez, R., Salazar, G., Yin, J., Joo, T., and Romesberg, F. E. (2004) Protein dynamics and the immunological evolution of molecular recognition. Proc. Natl. Acad. Sci. U.S.A. 101, 3803-3808
39. Wang, F., Sen, S., Zhang, Y., Ahmad, I., Zhu, X., Wilson, I. A., Smider, V. V., Magliery, T. J., and Schultz, P. G. (2013) Somatic hypermutation maintains antibody thermodynamic stability during affinity maturation. Proc. Natl. Acad. Sci. U.S.A. 110, 4261-4266
40. Sun, S. B., Sen, S., Kim, N. J., Magliery, T. J., Schultz, P. G., and Wang, F. (2013) Mutational analysis of 48G7 reveals that somatic hypermutation affects both antibody stability and binding affinity. J. Am. Chem. Soc. 135, 9980-9983
41. Dimitrov, J. D., Kaveri, S. V., and Lacroix-Desmazes, S. (2014) Thermodynamic stability contributes to immunoglobulin specificity. Trends Biochem. Sci. 39, 221-226
42. Yin, J., Beuscher, A. E., 4th, Andryski, S. E., Stevens, R. C., and Schultz, P. G. (2003) Structural plasticity and the evolution of antibody affinity and specificity. J. Mol. Biol. 330, 651-656
43. James, L. C., and Tawfik, D. S. (2005) Structure and kinetics of a transient antibody binding intermediate reveal a kinetic discrimination mechanism in antigen recognition. Proc. Natl. Acad. Sci. U.S.A. 102, 12730-12735
44. Smith, L. J., Kahraman, A., and Thornton, J. M. (2010) Heme proteins-diversity in structural characteristics, function, and folding. Proteins 78, 2349-2368
45. Kühl, T., Sahoo, N., Nikolajski, M., Schlott, B., Heinemann, S. H., and Imhof, D. (2011) Determination of hemin-binding characteristics of proteins by a combinatorial peptide library approach. Chembiochem. 12, 2846-2855
46. Debnath, A. K., Jiang, S., Strick, N., Lin, K., Haberfield, P., and Neurath, A. R. (1994) Three-dimensional structure-activity analysis of a series of porphyrin derivatives with anti-HIV-1 activity targeted to the V3 loop of the gp120 envelope glycoprotein of the human immunodeficiency virus type 37. J. Med. Chem. 37, 1099-1108
47. Neurath, A. R., Strick, N., and Debnath, A. K. (1995) Structural requirements for and consequences of an antiviral porphyrin binding to the V3 loop of the human immunodeficiency virus (HIV-1) envelope glycoprotein gp120. J. Mol. Recognit. 8, 345-357
48. Vzorov, A. N., Dixon, D. W., Trommel, J. S., Marzilli, L. G., and Compans, R. W. (2002) Inactivation of human immunodeficiency virus type 1 by porphyrins. Antimicrob. Agents Chemother. 46, 3917-3925
49. Dairou, J., Vever-Bizet, C., and Brault, D. (2004) Interaction of sulfonated anionic porphyrins with HIV glycoprotein gp120: photodamages revealed by inhibition of antibody binding to V3 and C5 domains. Antiviral Res. 61, 37-47
50. Lathrop, J. T., and Timko, M. P. (1993) Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259, 522-525
51. Zhang, L., and Guarente, L. (1995) Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J. 14, 313-320
52. Tang, X. D., Xu, R., Reynolds, M. F., Garcia, M. L., Heinemann, S. H., and Hoshi, T. (2003) Haem can bind to and inhibit mammalian calcium-dependent Slo1 BK channels. Nature 425, 531-535
53. Kaasik, K., and Lee, C. C. (2004) Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430, 467-471
54. Raghuram, S., Stayrook, K. R., Huang, P., Rogers, P. M., Nosie, A. K., McClure, D. B., Burris, L. L., Khorasanizadeh, S., Burris, T. P., and Rastinejad, F. (2007) Identification of heme as the ligand for the orphan nuclear receptors REV-ERBα and REV-ERBβ. Nat. Struct. Mol. Biol. 14, 1207-1213
55. Roumenina, L. T., Radanova, M., Atanasov, B. P., Popov, K. T., Kaveri, S. V., Lacroix-Desmazes, S., Frémeaux-Bacchi, V., and Dimitrov, J. D. (2011) Heme interacts with C1q and inhibits the classical complement pathway. J. Biol. Chem. 286, 16459-16469
56. Sahoo, N., Goradia, N., Ohlenschläger, O., Schönherr, R., Friedrich, M., Plass, W., Kappl, R., Hoshi, T., and Heinemann, S. H. (2013) Heme impairs the ball-and-chain inactivation of potassium channels. Proc. Natl. Acad. Sci. U.S.A. 110, E4036-E4044
57. Frimat, M., Tabarin, F., Dimitrov, J. D., Poitou, C., Halbwachs-Mecarelli, L., Fremeaux-Bacchi, V., and Roumenina, L. T. (2013) Complement activation by heme as a secondary hit for atypical hemolytic uremic syndrome. Blood 122, 282-292
58. Belcher, J. D., Chen, C., Nguyen, J., Milbauer, L., Abdulla, F., Alayash, A. I., Smith, A., Nath, K. A., Hebbel, R. P., and Vercellotti, G. M. (2014) Heme triggers TLR4 signaling leading to endothelial cell activation and vasoocclusion in murine sickle cell disease. Blood 123, 377-390
59. Kühl, T., and Imhof, D. (2014) Regulatory Fe(II/III) heme: the reconstruction of a molecule's biography. Chembiochem. 15, 2024-2035
60. Planchais, C., Gupta, N., Kaveri, S. V., Lacroix-Desmazes, S., and Dimitrov, J. D. (2013) [Post-translational diversification of immunoglobulins specificity]. Med. Sci. (Paris) 29, 937-940
61. Larsen, R., Gozzelino, R., Jeney, V., Tokaji, L., Bozza, F. A., Japiassú, A. M., Bonaparte, D., Cavalcante, M. M., Chora, A., Ferreira, A., Marguti, I., Cardoso, S., Sepúlveda, N., Smith, A., and Soares, M. P. (2010) A central role for free heme in the pathogenesis of severe sepsis. Sci. Transl. Med. 2, 51ra71
62. Devadas, K., and Dhawan, S. (2006) Hemin activation ameliorates HIV-1 infection via heme oxygenase-1 induction. J. Immunol. 176, 4252-4257
63. Levere, R. D., Gong, Y. F., Kappas, A., Bucher, D. J., Wormser, G. P., and Abraham, N. G. (1991) Heme inhibits human immunodeficiency virus 1 replication in cell cultures and enhances the antiviral effect of zidovudine. Proc. Natl. Acad. Sci. U.S.A. 88, 1756-1759
64. Staudinger, R., Abraham, N. G., Levere, R. D., and Kappas, A. (1996) Inhibition of human immunodeficiency virus-1 reverse transcriptase by heme and synthetic heme analogs. Proc. Assoc. Am. Physicians 108, 47-54
65. Argyris, E. G., Vanderkooi, J. M., Venkateswaran, P. S., Kay, B. K., and Paterson, Y. (1999) The connection domain is implicated in metalloporphyrin binding and inhibition of HIV reverse transcriptase. J. Biol. Chem. 274, 1549-1556
66. Nouraie, M., Nekhai, S., and Gordeuk, V. R. (2012) Sickle cell disease is associated with decreased HIV but higherHBVandHCVcomorbidities in U.S. hospital discharge records: a cross-sectional study. Sex Transm. Infect. 88, 528-533
67. Ditzel, H. J., Itoh, K., and Burton, D. R. (1996) Determinants of polyreactivity in a large panel of recombinant human antibodies from HIV-1 infection. J. Immunol. 157, 739-749
68. Haynes, B. F., Fleming, J., St Clair, E. W., Katinger, H., Stiegler, G., Kunert, R., Robinson, J., Scearce, R. M., Plonk, K., Staats, H. F., Ortel, T. L., Liao, H. X., and Alam, S. M. (2005) Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308, 1906-1908
69. Mouquet, H., Scheid, J. F., Zoller, M. J., Krogsgaard, M., Ott, R. G., Shukair, S., Artyomov, M. N., Pietzsch, J., Connors, M., Pereyra, F., Walker, B. D., Ho, D. D., Wilson, P. C., Seaman, M. S., Eisen, H. N., Chakraborty, A. K., Hope, T. J., Ravetch, J. V., Wardemann, H., and Nussenzweig, M. C. (2010) Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467, 591-595
70. Mouquet, H., Klein, F., Scheid, J. F., Warncke, M., Pietzsch, J., Oliveira, T. Y., Velinzon, K., Seaman, M. S., and Nussenzweig, M. C. (2011) Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses. PLoS One 6, e24078
71. Zhu, Z., Qin, H. R., Chen, W., Zhao, Q., Shen, X., Schutte, R., Wang, Y., Ofek, G., Streaker, E., Prabakaran, P., Fouda, G. G., Liao, H. X., Owens, J., Louder, M., Yang, Y., Klaric, K. A., Moody, M. A., Mascola, J. R., Scott, J. K., Kwong, P. D., Montefiori, D., Haynes, B. F., Tomaras, G. D., and Dimitrov, D. S. (2011) Cross-reactive HIV-1-neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J. Virol. 85, 11401-11408
72. Liao, H. X., Lynch, R., Zhou, T., Gao, F., Alam, S. M., Boyd, S. D., Fire, A. Z., Roskin, K. M., Schramm, C. A., Zhang, Z., Zhu, J., Shapiro, L., NISC Comparative Sequencing Program, Mullikin, J. C., Gnanakaran, S., Hraber, P., Wiehe, K., Kelsoe, G., Yang, G., Xia, S. M., Montefiori, D. C., Parks, R., Lloyd, K. E., Scearce, R. M., Soderberg, K. A., Cohen, M., Kamanga, G., Louder, M. K., Tran, L. M., Chen, Y., Cai, F., Chen, S., Moquin, S., Du, X., Joyce, M. G., Srivatsan, S., Zhang, B., Zheng, A., Shaw, G. M., Hahn, B. H., Kepler, T. B., Korber, B. T., Kwong, P. D., Mascola, J. R., and Haynes, B. F. (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496, 469-476