De Novo MS/MS Sequencing of Native Human Antibodies

Journal of Proteome Research

Volumn 16, Issue 1, 2017, Pages 45-54

  Guthals, Adrian ^a   Gan, Yutian ^b   Murray, Laura ^b   Chen, Yongmei ^b   Stinson, Jeremy ^b   Nakamura, Gerald ^b   Lill, Jennie R ^b   Sandoval, Wendy ^b   Bandeira, Nuno ^c,d  

^a Mapp Biopharmaceutical Inc   (United States)

^b GENENTECH INC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

antibody discovery; B cell; de novo sequencing; mass spectrometry; monoclonal antibody; polyclonal antibody; shotgun protein sequencing

Indexed keywords

GLYCOPROTEIN B; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; ANTISERUM; GLYCOPROTEIN B, SIMPLEXVIRUS; IMMUNOGLOBULIN G; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANTIBODY BLOOD LEVEL; ARTICLE; BINDING AFFINITY; CYTOMEGALOVIRUS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEASIBILITY STUDY; HUMAN; MEMORY CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; B LYMPHOCYTE; BIOSYNTHESIS; BLOOD; CHEMISTRY; CYTOLOGY; CYTOMEGALOVIRUS INFECTION; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; IMMUNOGLOBULIN PRODUCING CELL; IMMUNOLOGY; ISOLATION AND PURIFICATION; PROCEDURES; VIROLOGY;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIBODY-PRODUCING CELLS; B-LYMPHOCYTES; CHROMATOGRAPHY, AFFINITY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEK293 CELLS; HUMANS; IMMUNE SERA; IMMUNOGLOBULIN G; SEQUENCE ANALYSIS, PROTEIN; TANDEM MASS SPECTROMETRY; VIRAL ENVELOPE PROTEINS;

EID: 85017575241     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00608     Document Type: Article

References (40)

1. Reichert, J. M.; Rosensweig, C. J.; Faden, L. B.; Dewitz, M. C. Monoclonal antibody successes in the clinic Nat. Biotechnol. 2005, 23 (9) 1073-1078 10.1038/nbt0905-1073
2. Reichert, J. M. Trends in the development and approval of monoclonal antibodies for viral infections BioDrugs 2007, 21 (1) 1-7 10.2165/00063030-200721010-00001
3. Drake, C. G.; Lipson, E. J.; Brahmer, J. R. Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer Nat. Rev. Clin. Oncol. 2013, 11 (1) 24-37 10.1038/nrclinonc.2013.208
4. Qiu, X.; Wong, G.; Audet, J.; Bello, A.; Fernando, L.; Alimonti, J. B.; Fausther-Bovendo, H.; Wei, H.; Aviles, J.; Hiatt, E. et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp Nature 2014, 514 (7520) 47-53 10.1038/nature13777
5. Furuyama, W.; Marzi, A.; Nanbo, A.; Haddock, E.; Maruyama, J.; Miyamoto, H.; Igarashi, M.; Yoshida, R.; Noyori, O.; Feldmann, H. et al. Discovery of an antibody for pan-ebolavirus therapy Sci. Rep. 2016, 6, 20514 10.1038/srep20514
6. Bornholdt, Z. A.; Turner, H. L.; Murin, C. D.; Li, W.; Sok, D.; Souders, C. A.; Piper, A. E.; Goff, A.; Shamblin, J. D.; Wollen, S. E. et al. Isolation of potent neutralizing antibodies from a survivor of the 2014 Ebola virus outbreak Science (Washington, DC, U. S.) 2016, 351 (6277) 1078-1083 10.1126/science.aad5788
7. Smith, S. A.; de Alwis, R.; Kose, N.; Durbin, A. P.; Whitehead, S. S.; de Silva, A. M.; Crowe, J. E. Human monoclonal antibodies derived from memory B cells following live attenuated dengue virus vaccination or natural infection exhibit similar characteristics J. Infect. Dis. 2013, 207 (12) 1898-1908 10.1093/infdis/jit119
8. Zhou, T.; Georgiev, I.; Wu, X.; Yang, Z.-Y.; Dai, K.; Finzi, A.; Do Kwon, Y.; Scheid, J. F.; Shi, W.; Xu, L. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01 Science 2010, 329 (5993) 811-817 10.1126/science.1192819
9. 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. Biotechnol. 2014, 32 (2) 158-168 10.1038/nbt.2782
10. Hibi, T.; Dosch, H.-M. Limiting dilution analysis of the B cell compartment in human bone marrow Eur. J. Immunol. 1986, 16 (2) 139-145 10.1002/eji.1830160206
11. Apostoaei, I. A.; Trabalka, J. R. Review, Synthesis, and Application of Information on the Human Lymphatic System to Radiation Dosimetry for Chronic Lymphocytic Leukemia; SENES Oak Ridge, Inc.: Oak Ridge, TN, 2010.
12. Brekke, O. H.; Sandlie, I. Therapeutic antibodies for human diseases at the dawn of the twenty-first century Nat. Rev. Drug Discovery 2003, 2 (1) 52-62 10.1038/nrd984
13. 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. et al. A proteomics approach for the identification and cloning of monoclonal antibodies from serum Nat. Biotechnol. 2012, 30, 447-452 10.1038/nbt.2167
14. 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 (11) 1039-1043 10.1038/nbt.2406
15. Duncan, M. W.; Aebersold, R.; Caprioli, R. M. The pros and cons of peptide-centric proteomics Nat. Biotechnol. 2010, 28 (7) 659-664 10.1038/nbt0710-659
16. Guthals, A.; Clauser, K. R.; Frank, A. M.; Bandeira, N. Sequencing-Grade De novo Analysis of MS/MS Triplets (CID/HCD/ETD) From Overlapping Peptides J. Proteome Res. 2013, 12 (6) 2846-2857 10.1021/pr400173d
17. Bandeira, N.; Pham, V.; Pevzner, P.; Arnott, D.; Lill, J. R. Automated de novo protein sequencing of monoclonal antibodies Nat. Biotechnol. 2008, 26 (12) 1336-1338 10.1038/nbt1208-1336
18. Castellana, N. E.; Pham, V.; Arnott, D.; Lill, J. R.; Bafna, V. Template proteogenomics: sequencing whole proteins using an imperfect database Mol. Cell. Proteomics 2010, 9 (6) 1260-1270 10.1074/mcp.M900504-MCP200
19. Liu, X.; Han, Y.; Yuen, D.; Ma, B. Automated protein (re)sequencing with MS/MS and a homologous database yields almost full coverage and accuracy Bioinformatics 2009, 25 (17) 2174-2180 10.1093/bioinformatics/btp366
20. Guthals, A.; Clauser, K. R.; Bandeira, N. Shotgun protein sequencing with meta-contig assembly Mol. Cell. Proteomics 2012, 11 (10) 1084-1096 10.1074/mcp.M111.015768
21. MassIVE. ftp://massive.ucsd.edu/MSV000080039.
22. Kessner, D.; Chambers, M.; Burke, R.; Agus, D.; Mallick, P. ProteoWizard: open source software for rapid proteomics tools development Bioinformatics 2008, 24 (21) 2534-2536 10.1093/bioinformatics/btn323
23. Frank, A. M. Predicting intensity ranks of peptide fragment ions J. Proteome Res. 2009, 8 (5) 2226-2240 10.1021/pr800677f
24. Dancík, V.; Addona, T. A.; Clauser, K. R.; Vath, J. E.; Pevzner, P. A. De novo peptide sequencing via tandem mass spectrometry J. Comput. Biol. 1999, 6 (3-4) 327-342 10.1089/106652799318300
25. Datta, R.; Bern, M. Spectrum Fusion: Using Multiple Mass Spectra for De Novo Peptide Sequencing J. Comput. Biol. 2009, 16 (8) 1169-1182 10.1089/cmb.2009.0122
26. Guthals, A.; Bandeira, N. Peptide identification by tandem mass spectrometry with alternate fragmentation modes Mol. Cell. Proteomics 2012, 11 (9) 550-557 10.1074/mcp.R112.018556
27. Bandeira, N.; Tsur, D.; Frank, A.; Pevzner, P. A. Protein identification by spectral networks analysis Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (15) 6140-6145 10.1073/pnas.0701130104
28. Bandeira, N.; Clauser, K. R.; Pevzner, P. A. Shotgun protein sequencing: assembly of peptide tandem mass spectra from mixtures of modified proteins Mol. Cell. Proteomics 2007, 6 (7) 1123-1134 10.1074/mcp.M700001-MCP200
29. Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215 (3) 403-410 10.1016/S0022-2836(05)80360-2
30. Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T. L. BLAST+: architecture and applications BMC Bioinf. 2009, 10, 421 10.1186/1471-2105-10-421
31. The Global Proteome Machine. cRAP protein sequences http://www.thegpm.org/crap/.
32. Kim, S.; Mischerikow, N.; Bandeira, N.; Navarro, J. D.; Wich, L.; Mohammed, S.; Heck, A. J. R.; Pevzner, P. A. The generating function of CID, ETD, and CID/ETD pairs of tandem mass spectra: applications to database search Mol. Cell. Proteomics 2010, 9 (12) 2840-2852 10.1074/mcp.M110.003731
33. Shields, R. L.; Namenuk, A. K.; Hong, K.; Meng, Y. G.; Rae, J.; Briggs, J.; Xie, D.; Lai, J.; Stadlen, A.; Li, B. et al. High Resolution Mapping of the Binding Site on Human IgG1 for Fcgamma RI, Fcgamma RII, Fcgamma RIII, and FcRn and Design of IgG1 Variants with Improved Binding to the Fcgamma R J. Biol. Chem. 2001, 276 (9) 6591-6604 10.1074/jbc.M009483200
34. Altschul, S.; Madden, T. L.; Schäffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25 (17) 3389-3402 10.1093/nar/25.17.3389
35. Safonova, Y.; Bonissone, S.; Kurpilyansky, E.; Starostina, E.; Lapidus, A.; Stinson, J.; DePalatis, L.; Sandoval, W.; Lill, J.; Pevzner, P. A. IgRepertoireConstructor: a novel algorithm for antibody repertoire construction and immunoproteogenomics analysis Bioinformatics 2015, 31 (12) i53-61 10.1093/bioinformatics/btv238
36. von Pawel-Rammingen, U.; Johansson, B. P.; Björck, L. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G EMBO J. 2002, 21 (7) 1607-1615 10.1093/emboj/21.7.1607
37. Frank, A. M.; Pesavento, J. J.; Mizzen, C. A.; Kelleher, N. L.; Pevzner, P. A. Interpreting top-down mass spectra using spectral alignment Anal. Chem. 2008, 80 (7) 2499-2505 10.1021/ac702324u
38. Zabrouskov, V.; Senko, M. W.; Du, Y.; Leduc, R. D.; Kelleher, N. L. New and automated MSn approaches for top-down identification of modified proteins J. Am. Soc. Mass Spectrom. 2005, 16 (12) 2027-2038 10.1016/j.jasms.2005.08.004
39. Dekker, L.; Wu, S.; Vanduijn, M.; Tolić, N.; Stingl, C.; Zhao, R.; Luider, T.; Paša-Tolić, L. An integrated top-down and bottom-up proteomic approach to characterize the antigen-binding fragment of antibodies Proteomics 2014, 14, 1239-1248 10.1002/pmic.201300366
40. Durbin, K. R.; Fornelli, L.; Fellers, R. T.; Doubleday, P. F.; Narita, M.; Kelleher, N. L. Quantitation and Identification of Thousands of Human Proteoforms below 30 kDa J. Proteome Res. 2016, 15 (3) 976-982 10.1021/acs.jproteome.5b00997