Accurate and predictive antibody repertoire profiling by molecular amplification fingerprinting

Science Advances

Volumn 2, Issue 3, 2016, Pages

  Khan, Tarik A ^a   Friedensohn, Simon ^a   De Vries, Arthur R Gorter ^a   Straszewski, Jakub ^a   Ruscheweyh, Hans Joachim ^a,b   Reddy, Sai T ^a  

^a ETH ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CLONING; ERROR CORRECTION; ERRORS; POLYMERASE CHAIN REACTION; REGRESSION ANALYSIS;

ANTIBODY DIVERSITY; CLONAL EXPANSION; LOGISTIC REGRESSION MODELING; MOLECULAR AMPLIFICATION; MOLECULAR INFORMATION; QUANTITATIVE METRIC; SEQUENCING ERRORS; SOMATIC HYPERMUTATION;

ANTIBODIES;

ANTIBODY;

ANIMAL; CHEMISTRY; HIGH THROUGHPUT SCREENING; IMMUNOLOGY; MOUSE; MULTIPLEX POLYMERASE CHAIN REACTION; PROCEDURES; VALIDATION STUDY;

ANIMALS; ANTIBODIES; HIGH-THROUGHPUT SCREENING ASSAYS; MICE; MULTIPLEX POLYMERASE CHAIN REACTION;

EID: 84978131547     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1501371     Document Type: Article

References (54)

1. G. Georgiou, G. C. Ippolito, J. Beausang, C. E. Busse, H. Wardemann, S. R. Quake, The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat. Biotech. 32, 158-168 (2014).
2. J. D. Galson, A. J. Pollard, J. Trück, D. F. Kelly, Studying the antibody repertoire after vaccination: Practical applications. Trends Immunol. 35, 319-331 (2014).
3. J. J. A. Calis, B. R. Rosenberg, Characterizing immune repertoires by high throughput sequencing: Strategies and applications. Trends Immunol. 35, 581-590 (2014).
4. V. Greiff, E. Miho, U. Menzel, S. T. Reddy, Bioinformatic and Statistical Analysis of Adaptive Immune Repertoires. Trends Immunol 36, 738-749 (2015).
5. J. Kaplinsky, A. Li, A. Sun, M. Coffre, S. B. Koralov, R. Arnaout, Antibody repertoire deep sequencing reveals antigen-independent selection in maturing B cells. Proc. Natl. Acad. Sci. U.S.A. 111, E2622-E2629 (2014).
6. M. Uduman, M. J. Shlomchik, F. Vigneault, G. M. Church, S. H. Kleinstein, Integrating B cell lineage information into statistical tests for detecting selection in Ig sequences. J. Immunol. 192, 867-874 (2014).
7. N. Jiang, J. A. Weinstein, L. Penland, R. A. White III, D. S. Fisher, S. R. Quake, Determinism and stochasticity during maturation of the zebrafish antibody repertoire. Proc. Natl. Acad. Sci. U.S.A. 108, 5348-5353 (2011).
8. J. A. Weinstein, N. Jiang, R. A. White III, D. S. Fisher, S. R. Quake, High-throughput sequencing of the zebrafish antibody repertoire. Science 324, 807-810 (2009).
9. D. Sok, U. Laserson, J. Laserson, Y. Liu, F. Vigneault, J.-P. Julien, B. Briney, A. Ramos, K. F. Saye, K. Le, A. Mahan, S. Wang, M. Kardar, G. Yaari, L. M. Walker, B. B. Simen, E. P. St John, P.-Y. Chan-Hui, K. Swiderek, S. H. Kleinstein, G. Alter, M. S. Seaman, A. K. Chakraborty, D. Koller, I. A. Wilson, G. M. Church, D. R. Burton, P. Poignard, A. Trkola, The effects of somatic hypermutation on neutralization and binding in the PGT121 family of broadly neutralizing HIV antibodies. PLOS Pathog 9, e1003754 (2013).
10. K. J. L. Jackson, Y. Liu, K. M. Roskin, J. Glanville, R. A. Hoh, K. Seo, E. L. Marshall, T. C. Gurley, M. A. Moody, B. F. Haynes, E. B. Walter, H.-X. Liao, R. A. Albrecht, A. García-Sastre, J. ChaparroRiggers, A. Rajpal, J. Pons, B. B. Simen, B. Hanczaruk, C. L. Dekker, J. Laserson, D. Koller, M. M. Davis, A. Z. Fire, S. D. Boyd, Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16, 105-114 (2014).
11. N. Jiang, J. He, J. A. Weinstein, L. Penland, S. Sasaki, X.-S. He, C. L. Dekker, N.-Y. Zheng, M. Huang, M. Sullivan, P. C. Wilson, H. B. Greenberg, M. M. Davis, D. S. Fisher, S. R. Quake, Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med. 5, 171ra19 (2013).
12. J. J. Lavinder, Y. Wine, C. Giesecke, G. C. Ippolito, A. P. Horton, O. I. Lungu, K. H. Hoi, B. J. DeKosky, E. M. Murrin, M. M. Wirth, A. D. Ellington, T. Dörner, E. M. Marcotte, D. R. Boutz, G. Georgiou, Identification and characterization of the constituent human serum antibodies elicited by vaccination. Proc. Natl. Acad. Sci. U.S.A. 111, 2259-2264 (2014).
13. U. Laserson, F. Vigneault, D. Gadala-Maria, G. Yaari, M. Uduman, J. A. Vander Heiden, W. Kelton, S. Taek Jung, Y. Liu, J. Laserson, R. Chari, J.-H. Lee, I. Bachelet, B. Hickey, E. Lieberman-Aiden, B. Hanczaruk, B. B. Simen, M. Egholm, D. Koller, G. Georgiou, S. H. Kleinstein, G. M. Church, High-resolution antibody dynamics of vaccine-induced immune responses. Proc. Natl. Acad. Sci. U.S.A. 111, 4928-4933 (2014).
14. P. Parameswaran, Y. Liu, K. M. Roskin, K. K. L. Jackson, V. P. Dixit, J.-Y. Lee, K. L. Artiles, S. Zompi, M. J. Vargas, B. B. Simen, B. Hanczaruk, K. R. McGowan, M. A. Tariq, N. Pourmand, D. Koller, A. Balmaseda, S. D. Boyd, E. Harris, A. Z. Fire, Convergent antibody signatures in human dengue. Cell Host Microbe 13, 691-700 (2013).
15. S. D. Boyd, E. L. Marshall, J. D. Merker, J. M. Maniar, L. N. Zhang, B. Sahaf, C. D. Jones, B. B. Simen, B. Hanczaruk, K. D. Nguyen, K. C. Nadeau, M. Egholm, D. B. Miklos, J. L. Zehnder, A. Z. Fire, Measurement and clinical monitoring of human lymphocyte clonality by massively parallel V-D-J pyrosequencing. Sci. Transl. Med. 1, 12ra23 (2009).
16. V. Greiff, P. Bhat, S. C. Cook, U. Menzel, W. Kang, S. T. Reddy, A bioinformatic framework for immune repertoire diversity profiling enables detection of immunological status. Genome Med. 7, 49 (2015).
17. S. T. Reddy, X. Ge, A. E. Miklos, R. A. Hughes, S. H. Kang, K. H. Hoi, C. Chrysostomou, S. P. Hunicke-Smith, B. L. Iverson, P. W. Tucker, A. D. Ellington, G. Georgiou, Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells. Nat. Biotech. 28, 965-969 (2010).
18. B. J. DeKosky, G. C. Ippolito, R. P. Deschner, J. J. Lavinder, Y. Wine, B. M. Rawlings, N. Varadarajan, C. Giesecke, T. Dörner, S. F. Andrews, P. C. Wilson, S. P. Hunicke-Smith, C. G. Willson, A. D. Ellington, G. Georgiou, High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat. Biotech. 31, 166-169 (2013).
19. W. C. Cheung, S. A. Beausoleil, X. Zhang, S. Sato, S. M. Schieferl, J. S. Wieler, J. G. Beaudet, R. K. Ramenani, L. Popova, M. J. Comb, J. Rush, R. D. Polakiewicz, A proteomics approach for the identification and cloning of monoclonal antibodies from serum. Nat. Biotech. 30, 447-452 (2012).
20. J. Glanville, W. Zhai, J. Berka, D. Telman, G. Huerta, G. R. Mehta, I. Ni, L. Mei, P. D. Sundar, G. M. R. Day, D. Cox, A. Rajpal, J. Pons, Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. Proc. Natl. Acad. Sci. U.S.A. 106, 20216-20221 (2009).
21. J. Zhu, X. Wu, B. Zhang, K. McKee, S. O'Dell, C. Soto, T. Zhou, J. P. Casazza; NISC Comparative Sequencing Program, J. C. Mullikin, P. D. Kwong, J. R. Mascola, L. Shapiro, De novo identification of VRC01 class HIV-1-neutralizing antibodies by next-generation sequencing of B-cell transcripts. Proc. Natl. Acad. Sci. U.S.A. 110, E4088-E4097 (2013).
22. P. C. Fridy, Y. Li, S. Keegan, M. K. Thompson, I. Nudelman, J. F. Scheid, M. Oeffinger, M. C. Nussenzweig, D. Fenyö, B. T. Chait, M. P. Rout, A robust pipeline for rapid production of versatile nanobody repertoires. Nat. Methods 11, 1253-1260 (2014).
23. J. Glanville, S. D'Angelo, T. A. Khan, S. T. Reddy, L. Naranjo, F. Ferrara, A. R. M. Bradbury, Deep sequencing in library selection projects: What insight does it bring? Curr. Opin. Struct. Biol. 33, 146-160 (2015).
24. P. D. Baum, V. Venturi, D. A. Price, Wrestling with the repertoire: The promise and perils of next generation sequencing for antigen receptors. Eur. J. Immunol. 42, 2834-2839 (2012).
25. M. Shugay, O. V. Britanova, E. M. Merzlyak, M. A. Turchaninova, I. Z. Mamedov, T. R. Tuganbaev, D. A. Bolotin, D. B. Staroverov, E. V. Putintseva, K. Plevova, C. Linnemann, D. Shagin, S. Pospisilova, S. Lukyanov, T. N. Schumacher, D. M. Chudakov, Towards error-free profiling of immune repertoires. Nat. Methods 11, 653-655 (2014).
26. B. J. DeKosky, T. Kojima, A. Rodin, W. Charab, G. C. Ippolito, A. D. Ellington, G. Georgiou, Indepth determination and analysis of the human paired heavy- and light-chain antibody repertoire. Nat. Med. 21, 86-91 (2015).
27. C. Vollmers, R. V. Sit, J. A. Weinstein, C. L. Dekker, S. R. Quake, Genetic measurement of memory B-cell recall using antibody repertoire sequencing. Proc. Natl. Acad. Sci. U.S.A. 110, 13463-13468 (2013).
28. J. Lu, T. Panavas, K. Thys, J. Aerssens, M. Naso, J. Fisher, M. Rycyzyn, R. W. Sweet, IgG variable region and VH CDR3 diversity in unimmunized mice analyzed by massively parallel sequencing. Mol. Immunol. 57, 274-283 (2014).
29. L. He, D. Sok, P. Azadnia, J. Hsueh, E. Landais, M. Simek, W. C. Koff, P. Poignard, D. R. Burton, J. Zhu, Toward a more accurate view of human B-cell repertoire by next-generation sequencing, unbiased repertoire capture and single-molecule barcoding. Sci. Rep. 4, 6778 (2014).
30. C. S. Carlson, R. O. Emerson, A. M. Sherwood, C. Desmarais, M.-W. Chung, J. M. Parsons, M. S. Steen, M. A. LaMadrid-Herrmannsfeldt, D. W. Williamson, R. J. Livingston, D. Wu, B. L. Wood, M. J. Rieder, H. Robins, Using synthetic templates to design an unbiased multiplex PCR assay. Nat. Commun. 4, 2680 (2013).
31. J. R. Francica, Z. Sheng, Z. Zhang, Y. Nishimura, M. Shingai, A. Ramesh, B. F. Keele, S. D. Schmidt, B. J. Flynn, S. Darko, R. M. Lynch, T. Yamamoto, R. Matus-Nicodemos, D. Wolinsky; NISC Comparative Sequencing Program, M. Nason, N. M. Valiante, P. Malyala, E. De Gregorio, S. W. Barnett, M. Singh, D. T. O'Hagan, R. A. Koup, J. R. Mascola, M. A. Martin, T. B. Kepler, D. C. Douek, L. Shapiro, R. A. Seder, Analysis of immunoglobulin transcripts and hypermutation following SHIVAD8 infection and proteinplus- adjuvant immunization. Nat. Commun. 6, 6565 (2015).
32. D. T. P. Tang, C. Plessy, M. Salimullah, A. M. Suzuki, R. Calligaris, S. Gustincich, P. Carninci, Suppression of artifacts and barcode bias in high-throughput transcriptome analyses utilizing template switching. Nucleic Acids Res. 41, e44 (2013).
33. G. K. Fu, J. Wilhelmy, D. Stern, H. C. Fan, S. P. A. Fodor, Digital encoding of cellular mRNAs enabling precise and absolute gene expression measurement by single-molecule counting. Anal. Chem. 86, 2867-2870 (2014).
34. J. Cocquet, A. Chong, G. Zhang, R. A. Veitia, Reverse transcriptase template switching and false alternative transcripts. Genomics 88, 127-131 (2006).
35. K. Best, T. Oakes, J. M. Heather, J. Shawe-Taylor, B. Chain, Computational analysis of stochastic heterogeneity in PCR amplification efficiency revealed by single molecule barcoding. Sci. Rep. 5, 14629 (2015).
36. L. Jiang, F. Schlesinger, C. A. Davis, Y. Zhang, R. Li, M. Salit, T. R. Gingeras, B. Oliver, Synthetic spike-in standards for RNA-seq experiments. Genome Res. 21, 1543-1551 (2011).
37. A. Krebber, S. Bornhauser, J. Burmester, A. Honegger, J. Willuda, H. R. Bosshard, A. Plückthun, Reliable cloning of functional antibody variable domains from hybridomas and spleen cell repertoires employing a reengineered phage display system. J. Immunol. Methods 201, 35-55 (1997).
38. K. Shiroguchi, T. Z. Jia, P. A. Sims, X. S. Xie, Digital RNA sequencing minimizes sequencedependent bias and amplification noise with optimized single-molecule barcodes. Proc. Natl. Acad. Sci. U.S.A. 109, 1347-1352 (2012).
39. I. Kinde, J. Wu, N. Papadopoulos, K. W. Kinzler, B. Vogelstein, Detection and quantification of rare mutations with massively parallel sequencing. Proc. Natl. Acad. Sci. U.S.A. 108, 9530-9535 (2011).
40. C. T. Deakin, J. J. Deakin, S. L. Ginn, P. Young, D. Humphreys, C. M. Suter, I. E. Alexander, C. V. Hallwirth, Impact of next-generation sequencing error on analysis of barcoded plasmid libraries of known complexity and sequence. Nucleic Acids Res. 42, e129 (2014).
41. J. Brodin, C. Hedskog, A. Heddini, E. Benard, R. A. Neher, M. Mild, J. Albert, Challenges with using primer IDs to improve accuracy of next generation sequencing. PLOS One 10, e0119123 (2015).
42. E. S. Egorov, E. M. Merzlyak, A. A. Shelenkov, O. V. Britanova, G. V. Sharonov, D. B. Staroverov, D. A. Bolotin, A. N. Davydov, E. Barsova, Y. B. Lebedev, M. Shugay, D. M. Chudakov, Quantitative profiling of immune repertoires for minor lymphocyte counts using unique molecular identifiers. J. Immunol. 194, 6155-6163 (2015).
43. T. Kivioja, A. Vähärautio, K. Karlsson, M. Bonke, M. Enge, S. Linnarsson, J. Taipale, Counting absolute numbers of molecules using unique molecular identifiers. Nat. Methods 9, 72-74 (2011).
44. N. J. Gotelli, R. K. Colwell, Estimating species richness. Biological Diversity: Frontiers in Measurement and Assessment, A. E. Magurran, B. J. McGill, Eds. (Oxford Univ. Press, New York, 2011), pp. 39-54.
45. J. Zhu, G. Ofek, Y. Yang, B. Zhang, M. K. Louder, G. Lu, K. McKee, M. Pancera, J. Skinner, Z. Zhang, R. Parks, J. Eudailey, K. E. Lloyd, J. Blinn, S. M. Alam, B. F. Haynes, M. Simek, D. R. Burton, W. C. Koff; NISC Comparative Sequencing Program, J. C. Mullikin, J. R. Mascola, L. Shapiro, P. D. Kwong, Mining the antibodyome for HIV-1-neutralizing antibodies with next-generation sequencing and phylogenetic pairing of heavy/light chains. Proc. Natl. Acad. Sci. U.S.A. 110, 6470-6475 (2013).
46. H.-X. Liao, R. Lynch, T. Zhou, F. Gao, S. M. Alam, S. D. Boyd, A. Z. Fire, K. M. Roskin, C. A. Schramm, Z. Zhang, J. Zhu, L. Shapiro; NISC Comparative Sequencing Program, J. C. Mullikin, S. Gnanakaran, P. Hraber, K. Wiehe, G. Kelsoe, G. Yang, S.-M. Xia, D. C. Montefiori, R. Parks, K. E. Lloyd, R. M. Scearce, K. A. Soderberg, M. Cohen, G. Kamanga, M. K. Louder, L. M. Tran, Y. Chen, F. Cai, S. Chen, S. Moquin, X. Du, M. G. Joyce, S. Srivatsan, B. Zhang, A. Zheng, G. M. Shaw, B. H. Hahn, T. B. Kepler, B. T. M. Korber, P. D. Kwong, J. R. Mascola, B. F. Haynes, Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496, 469-476 (2013).
47. D. J. Woodsworth, M. Castellarin, R. A. Holt, Sequence analysis of T-cell repertoires in health and disease. Genome Med. 5, 98 (2013).
48. B. Wang, C. A. Kluwe, O. I. Lungu, B. J. DeKosky, S. A. Kerr, E. L. Johnson, J. Jung, A. B. Rezigh, S. M. Carroll, A. N. Reyes, J. R. Bentz, I. Villanueva, A. L. Altman, R. A. Davey, A. D. Ellington, G. Georgiou, Facile discovery of a diverse panel of anti-Ebola virus antibodies by immune repertoire mining. Sci. Rep. 5, 13926 (2015).
49. A. Jarasch, H. Koll, J. T. Regula, M. Bader, A. Papadimitriou, H. Kettenberger, Developability assessment during the selection of novel therapeutic antibodies. J. Pharm. Sci. 104, 1885-1898 (2015).
50. C. E. Busse, I. Czogiel, P. Braun, P. F. Arndt, H. Wardemann, Single-cell based highthroughput sequencing of full-length immunoglobulin heavy and light chain genes. Eur. J. Immunol. 44, 597-603 (2014).
51. M. A. Turchaninova, O. V. Britanova, D. A. Bolotin, M. Shugay, E. V. Putintseva, D. B. Staroverov, G. Sharonov, D. Shcherbo, I. V. Zvyagin, I. Z. Mamedov, C. Linnemann, T. N. Schumacher, D. M. Chudakov, Pairing of T-cell receptor chains via emulsion PCR. Eur. J. Immunol. 43, 2507-2515 (2013).
52. B. Howie, A. M. Sherwood, A. D. Berkebile, J. Berka, R. O. Emerson, D. W. Williamson, I. Kirsch, M. Vignali, M. J. Rieder, C. S. Carlson, H. S. Robins, High-throughput pairing of T cell receptor a and b sequences. Sci. Transl. Med. 7, 301ra131 (2015).
53. Y. Wine, D. R. Boutz, J. J. Lavinder, A. E. Miklos, R. A. Hughes, K. H. Hoi, S. T. Jung, A. P. Horton, E. M. Murrin, A. D. Ellington, E. M. Marcotte, G. Georgiou, Molecular deconvolution of the monoclonal antibodies that comprise the polyclonal serum response. Proc. Natl. Acad. Sci. U.S.A. 110, 2993-2998 (2013).
54. M. P. Lefranc, V. Giudicelli, C. Ginestoux, J. Jabado-Michaloud, G. Folch, F. Bellahcene, Y. Wu, E. Gemrot, X. Brochet, J. Lane, L. Regnier, F. Ehrenmann, G. Lefranc, P. Duroux, IMGT®, the international ImMunoGeneTics information system®. Nucleic Acids Res. 37, D1006-D1012 (2009).