Polyclonal Immunoglobulin G N-Glycosylation in the Pathogenesis of Plasma Cell Disorders

Journal of Proteome Research

Volumn 16, Issue 2, 2017, Pages 748-762

  Mittermayr, Stefan ^a   Lê, Giao N ^a,b,c   Clarke, Colin ^a   Millán Martín, Silvia ^a   Larkin, Anne Marie ^c   O'Gorman, Peter ^b   Bones, Jonathan ^a  

^a NATIONAL INSTITUTE FOR BIOPROCESSING RESEARCH AND TRAINING   (Ireland)

^b MATER MISERICORDIAE UNIVERSITY HOSPITAL   (Ireland)

^c DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

glycan analysis; IgG N glycosylation; multiple myeloma; plasma cell disorders; polyclonal IgG

Indexed keywords

GALACTOSE; GLYCAN; IMMUNOGLOBULIN G; N ACETYLGLUCOSAMINE; PROTEIN; PROTEIN B4GALT1; PROTEIN BACH2; PROTEIN FUT8; PROTEIN RECK; PROTEIN ST6GAL1; UNCLASSIFIED DRUG; GLYCOSYLATED IGG; POLYSACCHARIDE;

ADULT; AGED; ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; MALE; MASS SPECTROMETRY; MONOCLONAL IMMUNOGLOBULINEMIA; MULTIPLE MYELOMA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; RELAPSE; SIALYLATION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; BLOOD; GLYCOSYLATION; MIDDLE AGED; PATHOLOGY; TUMOR RECURRENCE;

AGED; FEMALE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; MALE; MIDDLE AGED; MULTIPLE MYELOMA; NEOPLASM RECURRENCE, LOCAL; POLYSACCHARIDES;

EID: 85011636327     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00768     Document Type: Article

References (59)

1. National Cancer Institute, Surveillance and End Results Program. SEER Cancer Statistics Factsheets: Myeloma; National Cancer Institute: Bethesda, MD, 2016. http://seer.cancer.gov/statfacts/html/mulmy.html (accessed May 2016).
2. Kyle, R. A.; Therneau, T. M.; Rajkumar, S. V.; Offord, J. R.; Larson, D. R.; Plevak, M. F.; Melton, L. J. A Long-Term Study of Prognosis in Monoclonal Gammopathy of Undetermined Significance N. Engl. J. Med. 2002, 346 (8) 564-569 10.1056/NEJMoa01133202
3. Kyle, R. A.; Durie, B. G.; Rajkumar, S. V.; Landgren, O.; Blade, J.; Merlini, G.; Kroger, N.; Einsele, H.; Vesole, D. H.; Dimopoulos, M.; San Miguel, J.; Avet-Loiseau, H.; Hajek, R.; Chen, W. M.; Anderson, K. C.; Ludwig, H.; Sonneveld, P.; Pavlovsky, S.; Palumbo, A.; Richardson, P. G.; Barlogie, B.; Greipp, P.; Vescio, R.; Turesson, I.; Westin, J.; Boccadoro, M. International Myeloma Working, G., Monoclonal gammopathy of undetermined significance (MGUS) and smoldering (asymptomatic) multiple myeloma: IMWG consensus perspectives risk factors for progression and guidelines for monitoring and management Leukemia 2010, 24 (6) 1121-7 10.1038/leu.2010.60
4. Kyle, R. A.; Remstein, E. D.; Therneau, T. M.; Dispenzieri, A.; Kurtin, P. J.; Hodnefield, J. M.; Larson, D. R.; Plevak, M. F.; Jelinek, D. F.; Fonseca, R.; Melton, L. J.; Rajkumar, S. V. Clinical Course and Prognosis of Smoldering (Asymptomatic) Multiple Myeloma N. Engl. J. Med. 2007, 356 (25) 2582-2590 10.1056/NEJMoa070389
5. Vidarsson, G.; Dekkers, G.; Rispens, T. IgG Subclasses and Allotypes: From Structure to Effector Functions Front. Immunol. 2014, 5, 520 10.3389/fimmu.2014.00520
6. Bowden, T. A.; Baruah, K.; Coles, C. H.; Harvey, D. J.; Yu, X.; Song, B.-D.; Stuart, D. I.; Aricescu, A. R.; Scanlan, C. N.; Jones, E. Y.; Crispin, M. Chemical and Structural Analysis of an Antibody Folding Intermediate Trapped during Glycan Biosynthesis J. Am. Chem. Soc. 2012, 134 (42) 17554-17563 10.1021/ja306068g
7. Fleming, S. C.; Smith, S.; Knowles, D.; Skillen, A.; Self, C. H. Increased sialylation of oligosaccharides on IgG paraproteins - a potential new tumour marker in multiple myeloma J. Clin. Pathol. 1998, 51 (11) 825-830 10.1136/jcp.51.11.825
8. Moehler, T. M.; Seckinger, A.; Hose, D.; Andrulis, M.; Moreaux, J.; Hielscher, T.; Willhauck-Fleckenstein, M.; Merling, A.; Bertsch, U.; Jauch, A.; Goldschmidt, H.; Klein, B.; Schwartz-Albiez, R. The glycome of normal and malignant plasma cells PLoS One 2013, 8 (12) e83719 10.1371/journal.pone.0083719
9. Lauc, G.; Huffman, J. E.; Pucic, M.; Zgaga, L.; Adamczyk, B.; Muzinic, A.; Novokmet, M.; Polasek, O.; Gornik, O.; Kristic, J.; Keser, T.; Vitart, V.; Scheijen, B.; Uh, H. W.; Molokhia, M.; Patrick, A. L.; McKeigue, P.; Kolcic, I.; Lukic, I. K.; Swann, O.; van Leeuwen, F. N.; Ruhaak, L. R.; Houwing-Duistermaat, J. J.; Slagboom, P. E.; Beekman, M.; de Craen, A. J.; Deelder, A. M.; Zeng, Q.; Wang, W.; Hastie, N. D.; Gyllensten, U.; Wilson, J. F.; Wuhrer, M.; Wright, A. F.; Rudd, P. M.; Hayward, C.; Aulchenko, Y.; Campbell, H.; Rudan, I. Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers PLoS Genet. 2013, 9 (1) e1003225 10.1371/journal.pgen.1003225
10. Glavey, S. V.; Manier, S.; Natoni, A.; Sacco, A.; Moschetta, M.; Reagan, M. R.; Murillo, L. S.; Sahin, I.; Wu, P.; Mishima, Y.; Zhang, Y.; Zhang, W.; Zhang, Y.; Morgan, G.; Joshi, L.; Roccaro, A. M.; Ghobrial, I. M.; O'Dwyer, M. E. The sialyltransferase ST3GAL6 influences homing and survival in multiple myeloma Blood 2014, 124 (11) 1765 10.1182/blood-2014-03-560862
11. Rajkumar, S. V.; Dimopoulos, M. A.; Palumbo, A.; Blade, J.; Merlini, G.; Mateos, M.-V.; Kumar, S.; Hillengass, J.; Kastritis, E.; Richardson, P.; Landgren, O.; Paiva, B.; Dispenzieri, A.; Weiss, B.; LeLeu, X.; Zweegman, S.; Lonial, S.; Rosinol, L.; Zamagni, E.; Jagannath, S.; Sezer, O.; Kristinsson, S. Y.; Caers, J.; Usmani, S. Z.; Lahuerta, J. J.; Johnsen, H. E.; Beksac, M.; Cavo, M.; Goldschmidt, H.; Terpos, E.; Kyle, R. A.; Anderson, K. C.; Durie, B. G. M.; Miguel, J. F. S. International Myeloma Working Group updated criteria for the diagnosis of multiple myeloma Lancet Oncol. 2014, 15 (12) e538-e548 10.1016/S1470-2045(14)70442-5
12. Kyle, R. A.; Rajkumar, S. V. Criteria for diagnosis, staging, risk stratification and response assessment of multiple myeloma Leukemia 2009, 23 (1) 3-9 10.1038/leu.2008.291
13. Bones, J.; Mittermayr, S.; O'Donoghue, N.; Guttman, A.; Rudd, P. M. Ultra Performance Liquid Chromatographic Profiling of Serum N-Glycans for Fast and Efficient Identification of Cancer Associated Alterations in Glycosylation Anal. Chem. 2010, 82 (24) 10208-10215 10.1021/ac102860w
14. Varki, A.; Cummings, R. D.; Aebi, M.; Packer, N. H.; Seeberger, P. H.; Esko, J. D.; Stanley, P.; Hart, G.; Darvill, A.; Kinoshita, T.; Prestegard, J. J.; Schnaar, R. L.; Freeze, H. H.; Marth, J. D.; Bertozzi, C. R.; Etzler, M. E.; Frank, M.; Vliegenthart, J. F.; Lutteke, T.; Perez, S.; Bolton, E.; Rudd, P.; Paulson, J.; Kanehisa, M.; Toukach, P.; Aoki-Kinoshita, K. F.; Dell, A.; Narimatsu, H.; York, W.; Taniguchi, N.; Kornfeld, S. Symbol Nomenclature for Graphical Representations of Glycans Glycobiology 2015, 25 (12) 1323-4 10.1093/glycob/cwv091
15. Royle, L.; Campbell, M. P.; Radcliffe, C. M.; White, D. M.; Harvey, D. J.; Abrahams, J. L.; Kim, Y.-G.; Henry, G. W.; Shadick, N. A.; Weinblatt, M. E.; Lee, D. M.; Rudd, P. M.; Dwek, R. A. HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software Anal. Biochem. 2008, 376 (1) 1-12 10.1016/j.ab.2007.12.012
16. Tousi, F.; Bones, J.; Hancock, W. S.; Hincapie, M. Differential chemical derivatization integrated with chromatographic separation for analysis of isomeric sialylated N-glycans: a nano-hydrophilic interaction liquid chromatography-MS platform Anal. Chem. 2013, 85 (17) 8421-8 10.1021/ac4018007
17. Mattioli, M.; Agnelli, L.; Fabris, S.; Baldini, L.; Morabito, F.; Bicciato, S.; Verdelli, D.; Intini, D.; Nobili, L.; Cro, L.; Pruneri, G.; Callea, V.; Stelitano, C.; Maiolo, A. T.; Lombardi, L.; Neri, A. Oncogene 2005, 24 (15) 2461-2473 10.1038/sj.onc.1208447
18. Zhan, F.; Barlogie, B.; Arzoumanian, V.; Huang, Y.; Williams, D. R.; Hollmig, K.; Pineda-Roman, M.; Tricot, G.; van Rhee, F.; Zangari, M.; Dhodapkar, M.; Shaughnessy, J. D. Gene-expression signature of benign monoclonal gammopathy evident in multiple myeloma is linked to good prognosis Blood 2007, 109 (4) 1692-1700 10.1182/blood-2006-07-037077
19. Agnelli, L.; Mosca, L.; Fabris, S.; Lionetti, M.; Andronache, A.; Kwee, I.; Todoerti, K.; Verdelli, D.; Battaglia, C.; Bertoni, F.; Deliliers, G. L.; Neri, A. A SNP microarray and FISH-based procedure to detect allelic imbalances in multiple myeloma: An integrated genomics approach reveals a wide gene dosage effect Genes, Chromosomes Cancer 2009, 48 (7) 603-614 10.1002/gcc.20668
20. Chauhan, D.; Tian, Z.; Nicholson, B.; Kumar, K. G. S.; Zhou, B.; Carrasco, R.; McDermott, J. L.; Leach, C. A.; Fulcinniti, M.; Kodrasov, M. P.; Weinstock, J.; Kingsbury, W. D.; Hideshima, T.; Shah, P. K.; Minvielle, S.; Altun, M.; Kessler, B. M.; Orlowski, R.; Richardson, P.; Munshi, N.; Anderson, K. C. A Small Molecule Inhibitor of Ubiquitin-Specific Protease-7 Induces Apoptosis in Multiple Myeloma Cells and Overcomes Bortezomib Resistance Cancer Cell 2012, 22 (3) 345-358 10.1016/j.ccr.2012.08.007
21. López-Corral, L.; Corchete, L. A.; Sarasquete, M. E.; Mateos, M. V.; García-Sanz, R.; Ferminán, E.; Lahuerta, J.-J.; Bladé, J.; Oriol, A.; Teruel, A. I.; Martino, M. L.; Hernández, J.; Hernández-Rivas, J. M.; Burguillo, F. J.; San Miguel, J. F.; Gutiérrez, N. C. Transcriptome analysis reveals molecular profiles associated with evolving steps of monoclonal gammopathies Haematologica 2014, 99 (8) 1365-1372 10.3324/haematol.2013.087809
22. Irizarry, R. A.; Hobbs, B.; Collin, F.; Beazer-Barclay, Y. D.; Antonellis, K. J.; Scherf, U.; Speed, T. P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4 (2) 249-264 10.1093/biostatistics/4.2.249
23. Gautier, L.; Cope, L.; Bolstad, B. M.; Irizarry, R. A. affy-analysis of Affymetrix GeneChip data at the probe level Bioinformatics 2004, 20 (3) 307-315 10.1093/bioinformatics/btg405
24. Ritchie, M. E.; Phipson, B.; Wu, D.; Hu, Y.; Law, C. W.; Shi, W.; Smyth, G. K. limma powers differential expression analyses for RNA-sequencing and microarray studies Nucleic Acids Res. 2015, 43 (7) e47 10.1093/nar/gkv007
25. Carvalho, B. S.; Irizarry, R. A. A framework for oligonucleotide microarray preprocessing Bioinformatics 2010, 26 (19) 2363-2367 10.1093/bioinformatics/btq431
26. Rouillard, A. D.; Gundersen, G. W.; Fernandez, N. F.; Wang, Z.; Monteiro, C. D.; McDermott, M. G.; Ma'ayan, A. The harmonizome: a collection of processed datasets gathered to serve and mine knowledge about genes and proteins Database 2016, 2016, 1-16 10.1093/database/baw100
27. Mittermayr, S.; Bones, J.; Doherty, M.; Guttman, A.; Rudd, P. M. Multiplexed analytical glycomics: rapid and confident IgG N-glycan structural elucidation J. Proteome Res. 2011, 10 (8) 3820-9 10.1021/pr200371s
28. Huffman, J. E.; Pucic Bakovic, M.; Klaric, L.; Hennig, R.; Selman, M. H.; Vuckovic, F.; Novokmet, M.; Kristic, J.; Borowiak, M.; Muth, T.; Polasek, O.; Razdorov, G.; Gornik, O.; Plomp, R.; Theodoratou, E.; Wright, A. F.; Rudan, I.; Hayward, C.; Campbell, H.; Deelder, A. M.; Reichl, U.; Aulchenko, Y.; Rapp, E.; Wuhrer, M.; Lauc, G. Comparative Performance of Four Methods for High-throughput Glycosylation Analysis of Immunoglobulin G in Genetic and Epidemiological Research Mol. Cell. Proteomics 2014, 13, 1598-1610 10.1074/mcp.M113.037465
29. Mahan, A. E.; Tedesco, J.; Dionne, K.; Baruah, K.; Cheng, H. D.; De Jager, P. L.; Barouch, D. H.; Suscovich, T.; Ackerman, M.; Crispin, M.; Alter, G. A method for high-throughput, sensitive analysis of IgG Fc and Fab glycosylation by capillary electrophoresis J. Immunol. Methods 2015, 417, 34-44 10.1016/j.jim.2014.12.004
30. Anthony, R. M.; Nimmerjahn, F.; Ashline, D. J.; Reinhold, V. N.; Paulson, J.; Ravetch, J. V. A RECOMBINANT IgG Fc THAT RECAPITULATES THE ANTI-INFLAMMATORY ACTIVITY OF IVIG Science 2008, 320 (5874) 373-376 10.1126/science.1154315
31. Bondt, A.; Rombouts, Y.; Selman, M. H.; Hensbergen, P. J.; Reiding, K. R.; Hazes, J. M. W.; Dolhain, R.; Wuhrer, M. Immunoglobulin G (IgG) Fab Glycosylation Analysis Using a New Mass Spectrometric High-throughput Profiling Method Reveals Pregnancy-associated Changes Mol. Cell. Proteomics 2014, 13, 3029-3039 10.1074/mcp.M114.039537
32. Reusch, D.; Tejada, M. L. Fc glycans of therapeutic antibodies as critical quality attributes Glycobiology 2015, 25 (12) 1325-34 10.1093/glycob/cwv065
33. Zheng, K.; Yarmarkovich, M.; Bantog, C.; Bayer, R.; Patapoff, T. W. Influence of glycosylation pattern on the molecular properties of monoclonal antibodies mAbs 2014, 6 (3) 649-58 10.4161/mabs.28588
34. Thomann, M.; Reckermann, K.; Reusch, D.; Prasser, J.; Tejada, M. L. Fc-galactosylation modulates antibody-dependent cellular cytotoxicity of therapeutic antibodies Mol. Immunol. 2016, 73, 69-75 10.1016/j.molimm.2016.03.002
35. Thomann, M.; Schlothauer, T.; Dashivets, T.; Malik, S.; Avenal, C.; Bulau, P.; Ruger, P.; Reusch, D. In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity PLoS One 2015, 10 (8) e0134949 10.1371/journal.pone.0134949
36. Bakovic, M. P.; Selman, M. H.; Hoffmann, M.; Rudan, I.; Campbell, H.; Deelder, A. M.; Lauc, G.; Wuhrer, M. High-throughput IgG Fc N-glycosylation profiling by mass spectrometry of glycopeptides J. Proteome Res. 2013, 12 (2) 821-31 10.1021/pr300887z
37. Bolli, N.; Avet-Loiseau, H.; Wedge, D. C.; Van Loo, P.; Alexandrov, L. B.; Martincorena, I.; Dawson, K. J.; Iorio, F.; Nik-Zainal, S.; Bignell, G. R.; Hinton, J. W.; Li, Y.; Tubio, J. M. C.; McLaren, S.; O' Meara, S.; Butler, A. P.; Teague, J. W.; Mudie, L.; Anderson, E.; Rashid, N.; Tai, Y.-T.; Shammas, M. A.; Sperling, A. S.; Fulciniti, M.; Richardson, P. G.; Parmigiani, G.; Magrangeas, F.; Minvielle, S.; Moreau, P.; Attal, M.; Facon, T.; Futreal, P. A.; Anderson, K. C.; Campbell, P. J.; Munshi, N. C. Heterogeneity of genomic evolution and mutational profiles in multiple myeloma Nat. Commun. 2014, 5 (2997) 1-13 10.1038/ncomms3997
38. Aurer, I.; Lauc, G.; Dumic, J.; Rendic, D.; Matisic, D.; Milos, M.; Heffer-Lauc, M.; Flogel, M.; Labar, B. Aberrant Glycosylation of Igg Heavy Chain in Multiple Myeloma Coll. Antropol. 2007, 31 (1) 247-251
39. Farooq, M.; Takahashi, N.; Arrol, H.; Drayson, M.; Jefferis, R. Glycosylation of polyclonal and paraprotein IgG in multiple myeloma Glycoconjugate J. 1997, 14, 489-492 10.1023/A:1018555619519
40. Jefferis, R.; Lund, J.; Mizutani, H.; Nakagawa, H.; Kawazoe, Y.; Arata, Y.; Takahashi, N. A comparative study of the N-linked oligosaccharide structures of human IgG subclass proteins Biochem. J. 1990, 268, 529 10.1042/bj2680529
41. Mimura, Y.; Ashton, P. R.; Takahashi, N.; Harvey, D. J.; Jefferis, R. Contrasting glycosylation profiles between Fab and Fc of a human IgG protein studied by electrospray ionization mass spectrometry J. Immunol. Methods 2007, 326 (1-2) 116-126 10.1016/j.jim.2007.07.014
42. Hashimoto, R.; Toda, T.; Tsutsumi, H.; Ohta, M.; Mori, M. AbnormalN-Glycosylation of the Immunoglobulin G κ Chain in a Multiple Myeloma Patient with Crystalglobulinemia: Case Report Int. J. Hematol. 2007, 85 (3) 203 10.1532/IJH97.06074
43. Toda, T.; Nakamura, M.; Yamada, M.; Nishine, T.; Torii, T.; Ikenaka, K.; Hashimoto, R.; Mori, M. Glycoproteomic analysis of abnormal N-glycosylation on the kappa chain of cryocrystalglobulin in a patient of multiple myeloma J. Electrophor. 2009, 53, 1-6 10.2198/jelectroph.53.1
44. Roopenian, D. C.; Akilesh, S. FcRn: the neonatal Fc receptor comes of age Nat. Rev. Immunol. 2007, 7 (9) 715-725 10.1038/nri2155
45. Hobbs, S. M.; Jackson, L. E.; Hoadley, J. Interaction of aglycosyl immunoglobulins with the IgG Fc transport receptor from neonatal rat gut: Comparison of deglycosylation by tunicamycim treatment and genetic engineering Mol. Immunol. 1992, 29, 949-956 10.1016/0161-5890(92)90133-I
46. Liu, L. Antibody Glycosylation and Its Impact on the Pharmacokinetics and Pharmacodynamics of Monoclonal Antibodies and Fc-Fusion Proteins J. Pharm. Sci. 2015, 104, 1866-1884 10.1002/jps.24444
47. van de Bovenkamp, F. S.; Hafkenscheid, L.; Rispens, T.; Rombouts, Y. The Emerging Importance of IgG Fab Glycosylation in Immunity J. Immunol. 2016, 196 (4) 1435-41 10.4049/jimmunol.1502136
48. Bork, K.; Horstkorte, R.; Weidemann, W. Increasing the sialylation of therapeutic glycoproteins: the potential of the sialic acid biosynthetic pathyway J. Pharm. Sci. 2009, 98, 3499-3508 10.1002/jps.21684
49. Shields, R. L.; Lai, J.; Keck, R.; O'Connell, L. Y.; Hong, K.; Meng, Y. G.; Weikert, S. H. A.; Presta, L. G. Lack of Fucose on Human IgG1 N-Linked Oligosaccharide Improves Binding to Human FcγRIII and Antibody-dependent Cellular Toxicity J. Biol. Chem. 2002, 277 (30) 26733-26740 10.1074/jbc.M202069200
50. Masuda, K.; Kubota, T.; Kaneko, E.; Iida, S.; Wakitani, M.; Kobayashi-Natsume, Y.; Kubota, A.; Shitara, K.; Nakamura, K. Enhanced binding affinity for FcγRIIIa of fucose-negative antibody is sufficient to induce maximal antibody-dependent cellular cytotoxicity Mol. Immunol. 2007, 44 (12) 3122-3131 10.1016/j.molimm.2007.02.005
51. Pučić, M.; Knežević, A.; Vidič, J.; Adamczyk, B.; Novokmet, M.; Polašek, O.; Gornik, O.; Šupraha-Goreta, S.; Wormald, M. R.; Redžić, I.; Campbell, H.; Wright, A.; Hastie, N. D.; Wilson, J. F.; Rudan, I.; Wuhrer, M.; Rudd, P. M.; Josić, D.; Lauc, G. 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 (10) 1-15 10.1074/mcp.M111.010090
52. Preithner, S.; Elm, S.; Lippold, S.; Locher, M.; Wolf, A.; Silva, A. J. d.; Baeuerle, P. A.; Prang, N. S. High concentrations of therapeutic IgG1 antibodies are needed to compensate for inhibition of antibody-dependent cellular cytotoxicity by excess endogenous immunoglobulin G Mol. Immunol. 2006, 43 (8) 1183-1193 10.1016/j.molimm.2005.07.010
53. Iida, S.; Misaka, H.; Inoue, M.; Shibata, M.; Nakano, R.; Yamane-Ohnuki, N.; Wakitani, M.; Yano, K.; Shitara, K.; Satoh, M. Nonfucosylated Therapeutic IgG1 Antibody Can Evade the Inhibitory Effect of Serum Immunoglobulin G on Antibody-Dependent Cellular Cytotoxicity through its High Binding to FcγRIIIa Clin. Cancer Res. 2006, 12 (9) 2879-2887 10.1158/1078-0432.CCR-05-2619
54. Vuckovic, F.; Kristic, J.; Gudelj, I.; Teruel, M.; Keser, T.; Pezer, M.; Pucic-Bakovic, M.; Stambuk, J.; Trbojevic-Akmacic, I.; Barrios, C.; Pavic, T.; Menni, C.; Wang, Y.; Zhou, Y.; Cui, L.; Song, H.; Zeng, Q.; Guo, X.; Pons-Estel, B. A.; McKeigue, P.; Leslie Patrick, A.; Gornik, O.; Spector, T. D.; Harjacek, M.; Alarcon-Riquelme, M.; Molokhia, M.; Wang, W.; Lauc, G. Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome Arthritis Rheumatol. 2015, 67 (11) 2978-89 10.1002/art.39273
55. Mihai, S.; Nimmerjahn, F. The role of Fc receptors and complement in autoimmunity Autoimmun. Rev. 2013, 12 (6) 657-660 10.1016/j.autrev.2012.10.008
56. Zheng, M. M.; Zhang, Z.; Bemis, K.; Belch, A. R.; Pilarski, L. M.; Shively, J. E.; Kirshner, J. The Systemic Cytokine Environment Is Permanently Altered in Multiple Myeloma PLoS One 2013, 8 (3) e58504 10.1371/journal.pone.0058504
57. Nishiura, T.; Fujii, S.; Kanayama, Y.; Nishikawa, A.; Tomiyama, Y.; Iida, M.; Karasuno, T.; Nakao, H.; Yonezawa, T.; Taniguchi, N.; Tarui, S. Carbohydrate Analysis of Immunoglobulin G Myeloma Proteins by Lectin and High Performance Liquid Chromatography: Role of Glycosyltransferases in the Structures Cancer Res. 1990, 50, 5345-5350
58. Trbojevic Akmacic, I.; Ventham, N. T.; Theodoratou, E.; Vuckovic, F.; Kennedy, N. A.; Kristic, J.; Nimmo, E. R.; Kalla, R.; Drummond, H.; Stambuk, J.; Dunlop, M. G.; Novokmet, M.; Aulchenko, Y.; Gornik, O.; Campbell, H.; Pucic Bakovic, M.; Satsangi, J.; Lauc, G. Inflammatory bowel disease associates with proinflammatory potential of the immunoglobulin G glycome Inflammatory bowel diseases 2015, 21 (6) 1237-47 10.1097/MIB.0000000000000372
59. Vuckovic, F.; Theodoratou, E.; Thaci, K.; Timofeeva, M.; Vojta, A.; Stambuk, J.; Pucic-Bakovic, M.; Rudd, P. M.; Derek, L.; Servis, D.; Wennerstrom, A.; Farrington, S. M.; Perola, M.; Aulchenko, Y.; Dunlop, M. G.; Campbell, H.; Lauc, G. IgG Glycome in Colorectal Cancer Clin. Cancer Res. 2016, 22 (12) 3078-3086 10.1158/1078-0432.CCR-15-1867