Serology in the 21st century: The molecular-level analysis of the serum antibody repertoire

Current Opinion in Immunology

Volumn 35, Issue , 2015, Pages 89-97

  Wine, Yariv ^a   Horton, Andrew P ^b,c   Ippolito, Gregory C ^c   Georgiou, George ^b,c  

^a TEL AVIV UNIVERSITY   (Israel)

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

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; IMMUNOGLOBULIN; VACCINE; ANTIGEN;

ANTIBODY BLOOD LEVEL; ANTIBODY TITER; ANTIGEN DETECTION; B LYMPHOCYTE; BODILY SECRETIONS; HIGH THROUGHPUT SEQUENCING; HISTORY OF MEDICINE; HUMAN; HUMORAL IMMUNITY; IMMUNOCHEMISTRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROORGANISM; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN CONFORMATION; PROTEIN PROCESSING; REVIEW; SEROLOGY; ANIMAL; ANTIBODY SPECIFICITY; BLOOD; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR PATHOLOGY; PROCEDURES; PROTEOMICS;

ANIMALS; ANTIBODIES; ANTIBODY DIVERSITY; ANTIGENS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNITY, HUMORAL; PATHOLOGY, MOLECULAR; PROTEOMICS; SEROLOGY;

EID: 84936880720     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2015.06.009     Document Type: Review

References (74)

1. Landsteiner K., van der Scheer J. On cross reactions of egg albumin sera. J Exp Med 1940, 71:445-454.
2. Cooper M.D. The early history of B cells. Nat Rev Immunol 2015, 15:191-197.
3. Yoshida T., Mei H.E., Dörner T., Hiepe F., Radbruch A., Fillatreau S., Hoyer B.F. Memory B and memory plasma cells. Immunol Rev 2010, 237:117-139.
4. Kometani K., Kurosaki T. Differentiation and maintenance of long-lived plasma cells. Curr Opin Immunol 2015, 33c:64-69.
5. Mei H.E., Wirries I., Frolich D., Brisslert M., Giesecke C., Grun J.R., Alexander T., Schmidt S., Luda K., Kuhl A.A., et al. A unique population of IgG-expressing plasma cells lacking CD19 is enriched in human bone marrow. Blood 2015, 125:1739-1748.
6. Panda S., Ding J.L. Natural antibodies bridge innate and adaptive immunity. J Immunol 2015, 194:13-20.
7. Galili U. Anti-Gal: an abundant human natural antibody of multiple pathogeneses and clinical benefits. Immunology 2013, 140:1-11.
8. Amanna I.J., Carlson N.E., Slifka M.K. Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med 2007, 357:1903-1915.
9. Radbruch A., Muehlinghaus G., Luger E.O., Inamine A., Smith K.G., Dorner T., Hiepe F. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 2006, 6:741-750.
10. Plotkin S.A. Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis 2008, 47:401-409.
11. Plotkin S.A. Correlates of protection induced by vaccination. Clin Vaccine Immunol 2010, 1055-1065.
12. Rappuoli R. Bridging the knowledge gaps in vaccine design. Nat Biotechnol 2007, 25:1361-1366.
13. Talmage D.W. Immunological specificity: unique combinations of selected natural globulins provide an alternative to the classical concept. Science 1959, 129:1643-1648.
14. Fonville J.M., Wilks S.H., James S.L., Fox A., Ventresca M., Aban M., Xue L., Jones T.C., Le N.M., Pham Q.T., et al. Antibody landscapes after influenza virus infection or vaccination. Science 2014, 346:996-1000.
15. Corti D., Lanzavecchia A. Broadly neutralizing antiviral antibodies. Annu Rev Immunol 2013, 31:705-742.
16. 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., et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 2013, 496:469-476.
17. Doria-Rose N.A., Schramm C.A., Gorman J., Moore P.L., Bhiman J.N., DeKosky B.J., Ernandes M.J., Georgiev I.S., Kim H.J., Pancera M., et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 2014, 509:55-62.
18. DiLillo D.J., Tan G.S., Palese P., Ravetch J.V. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med 2014, 20:143-151.
19. Mascola J.R., Haynes B.F. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol Rev 2013, 254:225-244.
20. Georgiev I.S., Doria-Rose N.A., Zhou T., Kwon Y.D., Staupe R.P., Moquin S., Chuang G.Y., Louder M.K., Schmidt S.D., Altae-Tran H.R., et al. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 2013, 340:751-756.
21. Burnet: F.M. The Clonal Selection Theory of Acquired Immunity 1959, 95. Vanderbilt University Press.
22. Lavinder J.J., Wine Y., Giesecke C., Ippolito G.C., Horton A.P., Lungu O.I., Hoi K.H., DeKosky B.J., Murrin E.M., Wirth M.M., et al. Identification and characterization of the constituent human serum antibodies elicited by vaccination. Proc Natl Acad Sci USA 2014, 111:2259-2264.
23. Lavinder J.J., Horton A.P., Georgiou G., Ippolito G.C. Next-generation sequencing and protein mass spectrometry for the comprehensive analysis of human cellular and serum antibody repertoires. Curr Opin Chem Biol 2015, 24c:112-120.
24. Dimitrov J.D., Planchais C., Roumenina L.T., Vassilev T.L., Kaveri S.V., Lacroix-Desmazes S. Antibody polyreactivity in health and disease: statu variabilis. J Immunol 2013, 191:993-999.
25. Zhou Z.H., Zhang Y., Hu Y.F., Wahl L.M., Cisar J.O., Notkins A.L. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe 2007, 1:51-61.
26. Tiller T., Tsuiji M., Yurasov S., Velinzon K., Nussenzweig M.C., Wardemann H. Autoreactivity in human IgG+ memory B cells. Immunity 2007, 26:205-213.
27. Liu M., Yang G., Wiehe K., Nicely N.I., Vandergrift N.A., Rountree W., Bonsignori M., Alam S.M., Gao J., Haynes B.F., Kelsoe G. Polyreactivity and autoreactivity among HIV-1 antibodies. J Virol 2015, 89:784-798.
28. Mouquet H., Nussenzweig M.C. Polyreactive antibodies in adaptive immune responses to viruses. Cell Mol Life Sci 2012, 69:1435-1445.
29. Kodadek T. Chemical tools to monitor and manipulate the adaptive immune system. Chem Biol 2014, 21:1066-1074.
30. Weiss-Ottolenghi Y., Gershoni J.M. Profiling the IgOme: meeting the challenge. FEBS Lett 2014, 588:318-325.
31. Sokolove J., Lindstrom T.M., Robinson W.H. Development and deployment of antigen arrays for investigation of B-cell fine specificity in autoimmune disease. Front Biosci (Elite Ed) 2012, 4:320-330.
32. Kügler J., Zantow J., Meyer T., Hust M. Oligopeptide M13 phage display in pathogen research. Viruses 2013, 5:2531-2545.
33. Daugherty P.S., Chen G., Olsen M.J., Iverson B.L., Georgiou G. Antibody affinity maturation using bacterial surface display. Protein Eng 1998, 11:825-832.
34. Ballew J.T., Murray J.A., Collin P., Mäki M., Kagnoff M.F., Kaukinen K., Daugherty P.S. Antibody biomarker discovery through in vitro directed evolution of consensus recognition epitopes. Proc Natl Acad Sci USA 2013, 110:19330-19335.
35. Elliott S.E., Parchim N.F., Liu C., Xia Y., Kellems R.E., Soffici A.R., Daugherty P.S. Characterization of antibody specificities associated with preeclampsia. Hypertension 2014, 63:1086-1093.
36. Larman H.B., Zhao Z., Laserson U., Li M.Z., Ciccia A., Gakidis M.A.M., Church G.M., Kesari S., Leproust E.M., Solimini N.L., Elledge S.J. Autoantigen discovery with a synthetic human peptidome. Nat Biotechnol 2011, 29:535-541.
37. Stafford P., Cichacz Z., Woodbury N.W., Johnston S.A. Immunosignature system for diagnosis of cancer. Proc Natl Acad Sci USA 2014, 111:3072-3080.
38. Navalkar K.A., Johnston S.A., Stafford P. Peptide based diagnostics: are random-sequence peptides more useful than tiling proteome sequences?. J Immunol Methods 2015, 417:10-21.
39. Doran T.M., Simanski S., Kodadek T. Discovery of native autoantigens via antigen surrogate technology: application to type 1 diabetes. ACS Chem Biol 2015, 10:401-412.
40. Yeste A., Quintana F.J. Antigen microarrays for the study of autoimmune diseases. Clin Chem 2013, 59:1036-1044.
41. Kloppot P., Selle M., Kohler C., Stentzel S., Fuchs S., Liebscher V., Muller E., Kale D., Ohlsen K., Broker B.M., et al. Microarray based identification of human antibodies against Staphylococcus aureus antigens. Proteomics Clin Appl 2015, [Epub ahead of print]. 10.1002/prca.201400123.
42. Miersch S., Bian X., Wallstrom G., Sibani S., Logvinenko T., Wasserfall C.H., Schatz D., Atkinson M., Qiu J., LaBaer J. Serological autoantibody profiling of type 1 diabetes by protein arrays. J Proteomics 2013, 94:486-496.
43. Ayoglu B., Haggmark A., Khademi M., Olsson T., Uhlen M., Schwenk J.M., Nilsson P. Autoantibody profiling in multiple sclerosis using arrays of human protein fragments. Mol Cell Proteomics 2013, 12:2657-2672.
44. Price J.V., Haddon D.J., Kemmer D., Delepine G., Mandelbaum G., Jarrell J.A., Gupta R., Balboni I., Chakravarty E.F., Sokolove J., et al. Protein microarray analysis reveals BAFF-binding autoantibodies in systemic lupus erythematosus. J Clin Invest 2013, 123:5135-5145.
45. Shum A.K., Alimohammadi M., Tan C.L., Cheng M.H., Metzger T.C., Law C.S., Lwin W., Perheentupa J., Bour-Jordan H., Carel J.C., et al. BPIFB1 is a lung-specific autoantigen associated with interstitial lung disease. Sci Transl Med 2013, 5:206ra139.
46. Joseph C.G., Darrah E., Shah A.A., Skora A.D., Casciola-Rosen L.A., Wigley F.M., Boin F., Fava A., Thoburn C., Kinde I., et al. Association of the autoimmune disease scleroderma with an immunologic response to cancer. Science 2014, 343:152-157.
47. Ustinova J., Zusinaite E., Utt M., Metskula K., Reimand K., Huchaiah V., Merits A., Uibo R. Development of a luciferase-based system for the detection of ZnT8 autoantibodies. J Immunol Methods 2014, 405:67-73.
48. Ching K.H., Burbelo P.D., Tipton C., Wei C., Petri M., Sanz I., Iadarola M.J. Two major autoantibody clusters in systemic lupus erythematosus. PLoS ONE 2012, 7:e32001.
49. Obermeier B., Mentele R., Malotka J., Kellermann J., Kumpfel T., Wekerle H., Lottspeich F., Hohlfeld R., Dornmair K. Matching of oligoclonal immunoglobulin transcriptomes and proteomes of cerebrospinal fluid in multiple sclerosis. Nat Med 2008, 14:688-693.
50. VanDuijn M.M., Dekker L.J., Zeneyedpour L., Smitt P.A., Luider T.M. Immune responses are characterized by specific shared immunoglobulin peptides that can be detected by proteomic techniques. J Biol Chem 2010, 285:29247-29253.
51. Cheung W.C., Beausoleil S.A., Zhang X., Sato S., Schieferl S.M., Wieler J.S., Beaudet J.G., Ramenani R.K., Popova L., Comb M.J., Rush J., Polakiewicz R.D. A proteomics approach for the identification and cloning of monoclonal antibodies from serum. Nat Biotechnol 2012, 30:447-452.
52. Sato S., Beausoleil S.A., Popova L., Beaudet J.G., Ramenani R.K., Zhang X., Wieler J.S., Schieferl S.M., Cheung W.C., Polakiewicz R.D. Proteomics-directed cloning of circulating antiviral human monoclonal antibodies. Nat Biotechnol 2012, 30:1039-1043.
53. Reddy S., Ge X., Lavinder J., Boutz D., Ellington A.D., Marcotte E.M., Georgiou G. Rapid Isolation of Monoclonal Antibodies from Animals 2011, US Patent.
54. Wine Y., Lavinder J.J., Boutz D.R., Miklos A.E., Hughes R.A., Hoi K.H., Jung S.T., Horton A.P., Murrin E.M., Ellington A.D., Marcotte E.M., Georgiou G. Molecular deconvolution of the monoclonal antibodies that comprise the polyclonal serum response. Proc Natl Acad Sci USA 2013, 110:2993-2998.
55. Boutz D.R., Horton A.P., Wine Y., Lavinder J.J., Georgiou G., Marcotte E.M. Proteomic identification of monoclonal antibodies from serum. Anal Chem 2014, 86:4758-4766.
56. DeKosky B.J., Ippolito G.C., Deschner R.P., Lavinder J.J., Wine Y., Rawlings B.M., Varadarajan N., Giesecke C., Dörner T., Andrews S.F., et al. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat Biotechnol 2013, 31:166-169.
57. DeKosky B.J., Kojima T., Rodin A., Charab W., Ippolito G.C., Ellington A.D., Georgiou G. In-depth determination and analysis of the human paired heavy- and light-chain antibody repertoire. Nat Med 2015, 21:86-91.
58. Foote J., Eisen H.N. Breaking the affinity ceiling for antibodies and T cell receptors. Proc Natl Acad Sci USA 2000, 97:10679-10681.
59. Swaney D.L., Wenger C.D., Coon J.J. Value of using multiple proteases for large-scale mass spectrometry-based proteomics. J Proteome Res 2010, 9:1323-1329.
60. Sigurdardottir E., Turesson I., Lund S., et al. THe role of diagnosis and clinical follow-up of monoclonal gammopathy of undetermined significance on survival in multiple myeloma. JAMA Oncol 2015, 1:168-174.
61. Rowley M., Buchanan H., Mackay I. Reciprocal change with age in antibody to extrinsic and intrinsic antigens. The Lancet 1968, 292:24-26.
62. Murphy K., Travers P., Walport M., Janeway C. Janeway's Immunobiology 2012, Garland Science.
63. Kurosaki T., Kometani K., Ise W. Memory B cells. Nat Rev Immunol 2015, 15:149-159.
64. Briney B.S., Willis J.R., Finn J.A., McKinney B.A., Crowe J.E. Tissue-specific expressed antibody variable gene repertoires. PLoS One 2014, 9:e100839.
65. Georgiou G., Ippolito G.C., Beausang J., Busse C.E., Wardemann H., Quake S.R. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat Biotech 2014, 32:158-168.
66. Hmiel L.K., Brorson K.A., Boyne M.T. Post-translational structural modifications of immunoglobulin G and their effect on biological activity. Anal Bioanal Chem 2015, 407:79-94.
67. Pincetic A., Bournazos S., DiLillo D.J., Maamary J., Wang T.T., Dahan R., Fiebiger B.M., Ravetch J.V. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 2014, 15:707-716.
68. Pucic M., Knezevic A., Vidic J., Adamczyk B., Novokmet M., Polasek O., Gornik O., Supraha-Goreta S., Wormald M.R., Redzic I., et al. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics 2011, 10. M111.010090.
69. Thaysen-Andersen M., Packer N.H. Advances in LC-MS/MS-based glycoproteomics: getting closer to system-wide site-specific mapping of the N- and O-glycoproteome. Biochim Biophys Acta 2014, 1844:1437-1452.
70. Klein F., Mouquet H., Dosenovic P., Scheid J.F., Scharf L., Nussenzweig M.C. Antibodies in HIV-1 vaccine development and therapy. Science 2013, 341:1199-1204.
71. Xu Y., Roach W., Sun T., Jain T., Prinz B., Yu T.-Y., Torrey J., Thomas J., Bobrowicz P., Vásquez M., Wittrup K.D., Krauland E. Addressing polyspecificity of antibodies selected from an in vitro yeast presentation system: a FACS-based, high-throughput selection and analytical tool. Protein Eng Des Sel 2013, 26:663-670.
72. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
73. Chen Z.J., Wheeler C.J., Shi W., Wu A.J., Yarboro C.H., Gallagher M., Notkins A.L. Polyreactive antigen-binding B cells are the predominant cell type in the newborn B cell repertoire. Eur J Immunol 1998, 28:989-994.
74. Scheid J.F., Mouquet H., Kofer J., Yurasov S., Nussenzweig M.C., Wardemann H. Differential regulation of self-reactivity discriminates between IgG+ human circulating memory B cells and bone marrow plasma cells. Proc Natl Acad Sci USA 2011, 108:18044-18048.