4,467
Views
2
CrossRef citations to date
0
Altmetric
Report

Direct mass spectrometric characterization of disulfide linkages

, &
Pages 572-582 | Received 04 Nov 2017, Accepted 14 Feb 2018, Published online: 14 Mar 2018

References

  • Dillon TM, Ricci MS, Vezina C, Flynn GC, Liu YD, Rehder DS, Plant M, Henkle B, Li Y, Deechongkit S, et al. Structural and functional characterization of disulfide Isoforms of the human IgG2 subclass. J Biol Chem. 2008;283:16206–15. doi:10.1074/jbc.M709988200. PMID:18339626
  • Mamathambika BS, Bardwell JC. Disulfide-linked protein folding pathways. Annu Rev Cell Dev Biol. 2008;24:211–35. doi:10.1146/annurev.cellbio.24.110707.175333. PMID:18588487
  • Wypych J, Li M, Guo A, Zhang Z, Martinez T, Allen MJ, Fodor S, Kelner DN, Flynn GC, Liu YD, et al. Human IgG2 antibodies display disulfide-mediated structural isoforms. J Biol Chem. 2008;283:16194–205. doi:10.1074/jbc.M709987200. PMID:18339624
  • Liu YD, Chen X, Enk JZ-v, Plant M, Dillon TM, Flynn GC. Human IgG2 antibody disulfide rearrangement in Vivo. J Biol Chem. 2008;283:29266–72. doi:10.1074/jbc.M804787200. PMID:18713741
  • Machino Y, Ohta H, Suzuki E, Higurashi S, Tezuka T, Nagashima H, Kohroki J, Masuho Y. Effect of immunoglobulin G (IgG) interchain disulfide bond cleavage on efficacy of intravenous immunoglobulin for immune thrombocytopenic purpura (ITP). Clin Exp Immunol. 2010;162:415–24. doi:10.1111/j.1365-2249.2010.04255.x. PMID:21029072
  • McAuley A, Jacob J, Kolvenbach CG, Westland K, Lee HJ, Brych SR, Rehder D, Kleemann GR, Brems DN, Matsumura M. Contributions of a disulfide bond to the structure, stability, and dimerization of human IgG1 antibody C(H)3 domain. Protein Sci. 2008;17:95–106. doi:10.1110/ps.073134408. PMID:18156469
  • van der Neut Kolfschoten M, Schuurman J, Losen M, Bleeker WK, Martínez-Martínez P, Vermeulen E, den Bleker TH, Wiegman L, Vink T, Aarden LA, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic fab arm exchange. Science. 2007;317:1554–7. doi:10.1126/science.1144603. PMID:17872445
  • Labrijn AF, Buijsse AO, van den Bremer ETJ, Verwilligen AYW, Bleeker WK, Thorpe SJ, Killestein J, Polman CH, Aalberse RC, Schuurman J, et al. Therapeutic IgG4 antibodies engage in Fab-arm exchange with endogenous human IgG4 in vivo. Nat Biotech. 2009;27:767–71. doi:10.1038/nbt.1553.
  • Kao Y-H, Hewitt DP, Trexler-Schmidt M, Laird MW. Mechanism of antibody reduction in cell culture production processes. Biotechnol Bioeng. 2010;107:622–32. doi:10.1002/bit.22848. PMID:20589844
  • Mullan B, Dravis B, Lim A, Clarke A, Janes S, Lambooy P, Olson D, O'Riordan T, Ricart B, Tulloch AG. Disulphide bond reduction of a therapeutic monoclonal antibody during cell culture manufacturing operations. BMC Proc. 2011;5:P110–P. doi:10.1186/1753-6561-5-S8-P110. PMID:22373255
  • Ruaudel J, Bertschinger M, Letestu S, Giovannini R, Wassmann P, Moretti P. Antibody disulfide bond reduction during process development: insights using a scale-down model process. BMC Proc. 2015;9:P24–P. doi:10.1186/1753-6561-9-S9-P24.
  • Trexler-Schmidt M, Sargis S, Chiu J, Sze-Khoo S, Mun M, Kao Y-H, Laird MW. Identification and prevention of antibody disulfide bond reduction during cell culture manufacturing. Biotechnol Bioeng. 2010;106:452–61. PMID:20178122
  • Edelman GM, Poulik MD. Studies on structural units of the γ-Globulins. J Exp Med. 1961;113:861–84. doi:10.1084/jem.113.5.861. PMID:13725659
  • Pink JRL, Milstein C. Inter heavy–light chain disulphide bridge in Immune Globulins. Nature. 1967;214:92. doi:10.1038/214092a0. PMID:4166384
  • Liu H, May K. Disulfide bond structures of IgG molecules. mAbs. 2012;4:17–23. doi:10.4161/mabs.4.1.18347. PMID:22327427
  • Kikuchi H, Goto Y, Hamaguchi K. Reduction of the buried intrachain disulfide bond of the constant fragment of the immunoglobulin light chain: global unfolding under physiological conditions. Biochemistry. 1986;25:2009–13. doi:10.1021/bi00356a026. PMID:3085710
  • Amzel a LM, Poljak RJ. Three-dimensional structure of immunoglobulins. Annu Rev Biochem. 1979;48:961–97. doi:10.1146/annurev.bi.48.070179.004525. PMID:89832
  • Lefranc M-P, Pommié C, Kaas Q, Duprat E, Bosc N, Guiraudou D, Jean C, Ruiz M, Da Piédade I, Rouard M, et al. IMGT unique numbering for immunoglobulin and T cell receptor constant domains and Ig superfamily C-like domains. Dev Comp Immunol. 2005;29:185–203. doi:10.1016/j.dci.2004.07.003. PMID:15572068
  • Lefranc M-P, Pommié C, Ruiz M, Giudicelli V, Foulquier E, Truong L, Thouvenin-Contet V, Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev Comp Immunol. 2003;27:55–77. doi:10.1016/S0145-305X(02)00039-3. PMID:12477501
  • Chaderjian WB, Chin ET, Harris RJ, Etcheverry TM. Effect of copper sulfate on performance of a serum-free cho cell culture process and the level of free thiol in the recombinant antibody expressed. Biotechnol Progr. 2005;21:550–3. doi:10.1021/bp0497029.
  • Harris RJ. Heterogeneity of recombinant antibodies: linking structure to function. Dev Biol. 2005;122:117–27.
  • Harris RJ, Chin ET, Macchi F, Keck RG, Shyong B-J, Ling VT, Cordoba AJ, Marian M, Sinclair D, Battersby JE, et al. Analytical characterization of monoclonal antibodies: linking structure to function. In: Shire SJ, Gombotz W, Bechtold-Peters K, Andya J, eds. Current trends in monoclonal antibody development and manufacturing. New York (NY): Springer New York; 2010, pp. 193–205.
  • Remmele RL, Callahan WJ, Krishnan S, Zhou L, Bondarenko PV, Nichols AC, Kleemann GR, Pipes GD, Park S, Fodor S, et al. Active dimer of Epratuzumab provides insight into the complex nature of an antibody aggregate. J Pharm Sci. 2006;95:126–45. doi:10.1002/jps.20515. PMID:16315222
  • Brych SR, Gokarn YR, Hultgen H, Stevenson RJ, Rajan R, Matsumura M. Characterization of antibody aggregation: role of buried, unpaired cysteines in particle formation. J Pharm Sci. 2010;99:764–81. doi:10.1002/jps.21868. PMID:19691118
  • Van Buren N, Rehder D, Gadgil H, Matsumura M, Jacob J. Elucidation of two major aggregation pathways in an IgG2 antibody. J Pharm Sci. 2009;98:3013–30. doi:10.1002/jps.21514. PMID:18680168
  • Bloom JW, Madanat MS, Marriott D, Wong T, Chan S-Y. Intrachain disulfide bond in the core hinge region of human IgG4. Protein Sci. 1997;6:407–15. doi:10.1002/pro.5560060217. PMID:9041643
  • Gorman JJ, Wallis TP, Pitt JJ. Protein disulfide bond determination by mass spectrometry. Mass Spectrom Rev. 2002;21:183–216. doi:10.1002/mas.10025. PMID:12476442
  • Haniu M, Acklin C, Kenney WC, Rohde MF. Direct assignment of disulfide bonds by Edman degradation of selected peptide fragments. Int J Pept Protein Res. 1994;43:81–6. doi:10.1111/j.1399-3011.1994.tb00378.x. PMID:8138354
  • Lu S, Fan S-B, Yang B, Li Y-X, Meng J-M, Wu L, Li P, Zhang K, Zhang M-J, Fu Y, et al. Mapping native disulfide bonds at a proteome scale. Nat Methods. 2015;12:329. doi:10.1038/nmeth.3283. PMID:25664544
  • Zhang Z, Pan H, Chen X. Mass spectrometry for structural characterization of therapeutic antibodies. Mass Spectrom Rev. 2009;28:147–76. doi:10.1002/mas.20190. PMID:18720354
  • Srebalus Barnes CA, Lim A. Applications of mass spectrometry for the structural characterization of recombinant protein pharmaceuticals. Mass Spectrom Rev. 2007;26:370–88. doi:10.1002/mas.20129. PMID:17410555
  • Mikesh LM, Ueberheide B, Chi A, Coon JJ, Syka JEP, Shabanowitz J, Hunt DF. The utility of ETD mass spectrometry in proteomic analysis. Biochim Biophys Acta. 2006;1764:1811–22. doi:10.1016/j.bbapap.2006.10.003. PMID:17118725
  • Clark DF, Go EP, Desaire H. Simple approach to assign disulfide connectivity using extracted ion chromatograms of electron transfer dissociation spectra. Anal Chem. 2013;85:1192–9. doi:10.1021/ac303124w. PMID:23210856
  • Zubarev RA, Kruger NA, Fridriksson EK, Lewis MA, Horn DM, Carpenter BK, McLafferty FW. Electron capture dissociation of gaseous multiply-charged proteins is favored at disulfide bonds and other sites of high hydrogen atom affinity. J Am Chem Soc. 1999;121:2857–62. doi:10.1021/ja981948k.
  • Sobczyk M, Anusiewicz I, Berdys-Kochanska J, Sawicka A, Skurski P, Simons J. Coulomb-assisted dissociative electron attachment:  application to a model peptide. J Phys Chem A. 2005;109:250–8. doi:10.1021/jp0463114. PMID:16839114
  • Syrstad EA, Turecček F. Toward a general mechanism of electron capture dissociation. J Am Soc Mass Spectrom 2005;16:208–24. doi:10.1016/j.jasms.2004.11.001. PMID:15694771
  • Neff D, Smuczynska S, Simons J. Electron shuttling in electron transfer dissociation. Int J Mass Spectrom. 2009;283:122–34. doi:10.1016/j.ijms.2009.02.021.
  • Wu S-L, Jiang H, Lu Q, Dai S, Hancock WS, Karger BL. Mass spectrometric determination of disulfide linkages in recombinant therapeutic proteins using online LC−MS with electron-transfer dissociation. Anal Chem. 2009;81:112–22. doi:10.1021/ac801560k. PMID:19117448
  • Cole SR, Ma X, Zhang X, Xia Y. Electron Transfer Dissociation (ETD) of peptides containing intrachain disulfide bonds. J Am Soc Mass Spectrom. 2012;23:310–20. doi:10.1007/s13361-011-0300-z. PMID:22161508
  • Wang Y, Lu Q, Wu S-L, Karger BL, Hancock WS. Characterization and comparison of disulfide linkages and scrambling patterns in therapeutic monoclonal antibodies: using LC-MS with electron transfer dissociation. Anal Chem. 2011;83:3133–40. doi:10.1021/ac200128d. PMID:21428412
  • Liu YD, Chou RYT, Dillon TM, Poppe L, Spahr C, Shi SDH, Flynn GC. Protected hinge in the immunoglobulin G2-A2 disulfide isoform. Protein Sci. 2014;23:1753–64. doi:10.1002/pro.2557. PMID:25264323
  • Shukla AA, Hubbard B, Tressel T, Guhan S, Low D. Downstream processing of monoclonal antibodies—application of platform approaches. J Chromatogr B. 2007;848:28–39. doi:10.1016/j.jchromb.2006.09.026.
  • Chrisman PA, Pitteri SJ, Hogan JM, McLuckey SA. SO 2 −· electron transfer ion/ion reactions with disulfide linked polypeptide ions. J Am Soc Mass Spectrom. 2005;16:1020–30. doi:10.1016/j.jasms.2005.02.010. PMID:15914021
  • Valdivieso-Torres L, Sarangi A, Whidby J, Marcotrigiano J, Roth MJ. Role of cysteines in stabilizing the randomized receptor binding domains within feline leukemia virus envelope proteins. J Virol. 2016;90:2971–80. doi:10.1128/JVI.02544-15.
  • Zhang Z. Prediction of low-energy collision-induced dissociation spectra of peptides. Anal Chem. 2004;76:3908–22. doi:10.1021/ac049951b. PMID:15253624
  • Good DM, Wenger CD, Coon JJ. The effect of interfering ions on search algorithm performance for ETD data. Proteomics. 2010;10:164–7. doi:10.1002/pmic.200900570. PMID:19899080
  • Good DM, Wenger CD, McAlister GC, Coon JJ. Post-acquisition ETD spectral processing for increased peptide identifications. J Am Soc Mass Spectrom. 2009;20:1435–40. doi:10.1016/j.jasms.2009.03.006. PMID:19362853