High-resolution glycosylation site-engineering method identifies MICA epitope critical for shedding inhibition activity of anti-MICA antibodies

References

• Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA. 1999;96:6879–6884.
   PubMed Web of Science ®Google Scholar
• Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285:727–729.
   PubMed Web of Science ®Google Scholar
• Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol. 2002;169:4098–4102.
   PubMed Web of Science ®Google Scholar
• Jinushi M, Hodi FS, Dranoff G. Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc Natl Acad Sci USA. 2006;103:9190–9195. doi:10.1073/pnas.0603503103.
   PubMed Web of Science ®Google Scholar
• Ferrari de Andrade L, Tay RE, Pan D, Luoma AM, Ito Y, Badrinath S, Tsoucas D, Franz B, May KF Jr., Harvey CJ, et al. Antibody-mediated inhibition of MICA and MICB shedding promotes NK cell-driven tumor immunity. Science. 2018;359:1537–1542. doi:10.1126/science.aao0505.
   PubMed Web of Science ®Google Scholar
• Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, Stevanovic S, Rammensee HG, Steinle A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68:6368–6376. doi:10.1158/0008-5472.CAN-07-6768.
   PubMed Web of Science ®Google Scholar
• Wang X, Lundgren AD, Singh P, Goodlett DR, Plymate SR, Wu JD. An six-amino acid motif in the alpha3 domain of MICA is the cancer therapeutic target to inhibit shedding. Biochem Biophys Res Commun. 2009;387:476–481. doi:10.1016/j.bbrc.2009.07.062.
   PubMed Web of Science ®Google Scholar
• Xu G, Chance MR. Hydroxyl radical-mediated modification of proteins as probes for structural proteomics. Chem Rev. 2007;107:3514–3543. doi:10.1021/cr0682047.
   PubMed Web of Science ®Google Scholar
• Ciferri C, Chandramouli S, Leitner A, Donnarumma D, Cianfrocco MA, Gerrein R, Friedrich K, Aggarwal Y, Palladino G, Aebersold R, et al. Antigenic characterization of the HCMV gH/gL/gO and pentamer cell entry complexes reveals binding sites for potently neutralizing human antibodies. PLoS Pathogens. 2015;11:e1005230. doi:10.1371/journal.ppat.1005230.
   PubMed Web of Science ®Google Scholar
• Li P, Willie ST, Bauer S, Morris DL, Spies T, Strong RK. Crystal structure of the MHC class I homolog MIC-A, a gammadelta T cell ligand. Immunity. 1999;10:577–584.
   PubMed Web of Science ®Google Scholar
• Li P, Morris DL, Willcox BE, Steinle A, Spies T, Strong RK. Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA. Nat Immunol. 2001;2:443–451. doi:10.1038/87757.
   PubMed Web of Science ®Google Scholar
• Gao X, Single RM, Karacki P, Marti D, O’Brien SJ, Carrington M. Diversity of MICA and linkage disequilibrium with HLA-B in two North American populations. Hum Immunol. 2006;67:152–158. doi:10.1016/j.humimm.2006.02.009.
   PubMed Web of Science ®Google Scholar
• Petersdorf EW, Shuler KB, Longton GM, Spies T, Hansen JA. Population study of allelic diversity in the human MHC class I-related MIC-A gene. Immunogenetics. 1999;49:605–612.
   PubMed Web of Science ®Google Scholar
• Petrova G, Ferrante A, Gorski J. Cross-reactivity of T cells and its role in the immune system. Crit Rev Immunol. 2012;32:349–372.
   PubMed Web of Science ®Google Scholar
• Tian W, Cai JH, Wang F, Li LX. MICA polymorphism in a northern Chinese Han population: the identification of a new MICA allele, MICA*059. Hum Immunol. 2010;71:423–427. doi:10.1016/j.humimm.2010.01.025.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Han M, Vorhaben R, Giang C, Lavingia B, Stastny P. Study of MICA alleles in 201 African Americans by multiplexed single nucleotide extension (MSNE) typing. Hum Immunol. 2003;64:130–136.
   PubMed Web of Science ®Google Scholar
• Kirijas M, Spiroski M. MICA polymorphism, association with diseases and the role of anti-MICA antibodies in organ and stem cell transplantation. Macedonian J Med Sci. 2013;6:285–295.
   Google Scholar
• Cho HS, Mason K, Ramyar KX, Stanley AM, Gabelli SB, Denney DW Jr., Leahy DJ. Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature. 2003;421:756–760. doi:10.1038/nature01392.
   PubMed Web of Science ®Google Scholar
• Franklin MC, Carey KD, Vajdos FF, Leahy DJ, de Vos AM, Sliwkowski MX. Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex. Cancer Cell. 2004;5:317–328.
   PubMed Web of Science ®Google Scholar
• Junttila TT, Akita RW, Parsons K, Fields C, Lewis Phillips GD, Friedman LS, Sampath D, Sliwkowski MX. Ligand-independent HER2/HER3/PI3K complex is disrupted by trastuzumab and is effectively inhibited by the PI3K inhibitor GDC-0941. Cancer Cell. 2009;15:429–440. doi:10.1016/j.ccr.2009.03.020.
   PubMed Web of Science ®Google Scholar
• Lam PV, Goldman R, Karagiannis K, Narsule T, Simonyan V, Soika V, Mazumder R. Structure-based comparative analysis and prediction of N-linked glycosylation sites in evolutionarily distant eukaryotes. Genomics Proteomics Bioinformatics. 2013;11:96–104. doi:10.1016/j.gpb.2012.11.003.
   PubMedGoogle Scholar
• Kaiser BK, Yim D, Chow IT, Gonzalez S, Dai Z, Mann HH, Strong RK, Groh V, Spies T. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature. 2007;447:482–486. doi:10.1038/nature05768.
   PubMed Web of Science ®Google Scholar
• Wu JD, Atteridge CL, Wang X, Seya T, Plymate SR. Obstructing shedding of the immunostimulatory MHC class I chain-related gene B prevents tumor formation. Clin Cancer Res. 2009;15:632–640. doi:10.1158/1078-0432.CCR-08-1305.
   PubMed Web of Science ®Google Scholar
• Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 2002;419:734–738. doi:10.1038/nature01112.
   PubMed Web of Science ®Google Scholar
• Brinkmann U, Kontermann RE. The making of bispecific antibodies. mAbs. 2017;9:182–212. doi:10.1080/19420862.2016.1268307.
   PubMed Web of Science ®Google Scholar
• Spiess C, Zhai Q, Carter PJ. Alternative molecular formats and therapeutic applications for bispecific antibodies. Mol Immunol. 2015;67:95–106. doi:10.1016/j.molimm.2015.01.003.
   PubMed Web of Science ®Google Scholar
• Eitner K, Koch U, Gaweda T, Marciniak J. Statistical distribution of amino acid sequences: a proof of Darwinian evolution. Bioinformatics. 2010;26:2933–2935. doi:10.1093/bioinformatics/btq571.
   PubMed Web of Science ®Google Scholar
• Moelbert S, Emberly E, Tang C. Correlation between sequence hydrophobicity and surface-exposure pattern of database proteins. Protein Sci. 2004;13:752–762. doi:10.1110/ps.03431704.
   PubMed Web of Science ®Google Scholar
• Shental-Bechor D, Levy Y. Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc Natl Acad Sci USA. 2008;105:8256–8261. doi:10.1073/pnas.0801340105.
   PubMed Web of Science ®Google Scholar
• Sola RJ, Griebenow K. Effects of glycosylation on the stability of protein pharmaceuticals. J Pharm Sci. 2009;98:1223–1245. doi:10.1002/jps.21504.
   PubMed Web of Science ®Google Scholar
• Li J, Stagg NJ, Johnston J, Harris MJ, Menzies SA, DiCara D, Clark V, Hristopoulos M, Cook R, Slaga D, et al. Membrane-proximal epitope facilitates efficient T cell synapse formation by anti-FcRH5/CD3 and is a requirement for myeloma cell killing. Cancer Cell. 2017;31:383–395. doi:10.1016/j.ccell.2017.02.001.
   PubMed Web of Science ®Google Scholar
• Deng X, Storz U, Doranz BJ. Enhancing antibody patent protection using epitope mapping information. mAbs. 2018;10:204–209. doi:10.1080/19420862.2017.1402998.
   PubMed Web of Science ®Google Scholar
• Eaton DL, Wood WI, Eaton D, Hass PE, Hollingshead P, Wion K, Mather J, Lawn RM, Vehar GA, Gorman C. Construction and characterization of an active factor VIII variant lacking the central one-third of the molecule. Biochemistry. 1986;25:8343–8347.
   PubMed Web of Science ®Google Scholar
• Lombana TN, Dillon M, Bevers J 3rd, Spiess C. Optimizing antibody expression by using the naturally occurring framework diversity in a live bacterial antibody display system. Sci Rep. 2015;5:17488. doi:10.1038/srep17488.
   PubMed Web of Science ®Google Scholar
• Wong AW, Baginski TK, Reilly DE. Enhancement of DNA uptake in FUT8-deleted CHO cells for transient production of afucosylated antibodies. Biotechnol Bioeng. 2010;106:751–763. doi:10.1002/bit.22749.
   PubMed Web of Science ®Google Scholar
• Bos AB, Duque JN, Bhakta S, Farahi F, Chirdon LA, Junutula JR, Harms PD, Wong AW. Development of a semi-automated high throughput transient transfection system. J Biotechnol. 2014;180:10–16. doi:10.1016/j.jbiotec.2014.03.027.
   PubMed Web of Science ®Google Scholar
• Bos AB, Luan P, Duque JN, Reilly D, Harms PD, Wong AW. Optimization and automation of an end-to-end high throughput microscale transient protein production process. Biotechnol Bioeng. 2015;112:1832–1842. doi:10.1002/bit.25601.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Liu P, Gan Y, Sandoval W, Katakam AK, Reichelt M, Rangell L, Reilly D. Enhancing full-length antibody production by signal peptide engineering. Microb Cell Fact. 2016;15:47. doi:10.1186/s12934-016-0445-3.
   PubMed Web of Science ®Google Scholar
• Simmons LC, Reilly D, Klimowski L, Raju TS, Meng G, Sims P, Hong K, Shields RL, Damico LA, Rancatore P, et al. Expression of full-length immunoglobulins in Escherichia coli: rapid and efficient production of aglycosylated antibodies. J Immunol Methods. 2002;263:133–147.
   PubMed Web of Science ®Google Scholar
• Spiess C, Merchant M, Huang A, Zheng Z, Yang NY, Peng J, Ellerman D, Shatz W, Reilly D, Yansura DG, et al. Bispecific antibodies with natural architecture produced by co-culture of bacteria expressing two distinct half-antibodies. Nat Biotechnol. 2013;31:753–758. doi:10.1038/nbt.2621.
   PubMed Web of Science ®Google Scholar
• Spiess C, Bevers J 3rd, Jackman J, Chiang N, Nakamura G, Dillon M, Liu H, Molina P, Elliott JM, Shatz W, et al. Development of a human IgG4 bispecific antibody for dual targeting of interleukin-4 (IL-4) and interleukin-13 (IL-13) cytokines. J Biol Chem. 2013;288:26583–26593. doi:10.1074/jbc.M113.480483.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Rempel DL, Zhang H, Gross ML. An improved fast photochemical oxidation of proteins (FPOP) platform for protein therapeutics. J Am Soc Mass Spectrom. 2015;26:526–529. doi:10.1007/s13361-014-1055-0.
   PubMed Web of Science ®Google Scholar
• Oppikofer M, Bai T, Gan Y, Haley B, Liu P, Sandoval W, Ciferri C, Cochran AG. Expansion of the ISWI chromatin remodeler family with new active complexes. EMBO Rep. 2017;18:1697–1706. doi:10.15252/embr.201744011.
   PubMed Web of Science ®Google Scholar
• Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997;276:307–326.
   PubMed Web of Science ®Google Scholar
• Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66:213–221. doi:10.1107/S0907444909052925.
   PubMed Web of Science ®Google Scholar
• Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallogr D Biol Crystallogr. 2010;66:486–501. doi:10.1107/S0907444910007493.
   PubMed Web of Science ®Google Scholar
• Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53:240–255. doi:10.1107/S0907444996012255.
   PubMed Web of Science ®Google Scholar
• Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011;67:235–242. doi:10.1107/S0907444910045749.
   PubMed Web of Science ®Google Scholar