178
Views
4
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

The Alterations of Serum IgG Fucosylation as a Potential Additional New Diagnostic Marker in Advanced Endometriosis

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 251-266 | Published online: 13 Jan 2022

References

  • Agarwal SK, Chapron C, Giudice LC, et al. Clinical diagnosis of endometriosis: a call to action. Am J Obstet Gynecol. 2019;220(4):354. doi:10.1016/j.ajog.2018.12.039
  • Johnson NP, Hummelsho L. Consensus on current management of endometriosis. Hum Reprod. 2013;28:1552–1568. doi:10.1093/humrep/det050
  • Dunselman G, Vermeulen N, Becker C, et al. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014;29:400–412. doi:10.1093/humrep/det457
  • Practice Committee of the American Society for Reproductive Medicine. Treatment of pelvic pain associated with endometriosis: a committee opinion. Fertil Steril. 2014;101(4):927–935. doi:10.1016/j.fertnstert.2014.02.012
  • Andrews WC, Buttram VC, Behrman SJ. Revised American fertility society classification of endometriosis: 1985. Fertil Steril. 1985;44:7–8.
  • Canis M, Donnez JG, Guzick DS, et al. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67:817–821. doi:10.1016/S0015-0282(97)81391-X
  • Kyama CM, Debrock S, Mwenda JM, D’Hooghe TM. Potential involvement of the immune system in the development of endometriosis. Reprod Biol Endocrinol. 2003;2(1):123. doi:10.1186/1477-7827-1-123
  • Hyun Ahn S, Monsanto SP, Miller C, Singh SS, Thomas R, Tayade C. Pathophysiology and immune dysfunction in endometriosis. Biomed Res Int. 2015;2015:795976. doi:10.1155/2015/795976
  • Vlahos NF, Kalampokas T, Fotiou S. Endometriosis and ovarian cancer: a review. Gynecol Endocrinol. 2010;26(3):213–219. doi:10.1080/09513590903184050
  • Czyzyk A, Podfigurna A, Szeliga A, Meczekalski B. Update on endometriosis pathogenesis. Minerva Ginecol. 2017;69(5):447–464. doi:10.23736/S0026-4784.17.04048-5
  • Ruderman R, Pavone ME. Ovarian cancer in endometriosis: an update on the clinical and molecular aspects. Minerva Ginecol. 2017;69(3):286–294. doi:10.23736/S0026-4784.17.04042-4
  • Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR. The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril. 1992;58(2):290–295. doi:10.1016/s0015-0282(16)55224-8
  • Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001;75(1):1–10. doi:10.1016/s0015-0282(00)01630-7
  • Patel BG, Lenk EE, Lebovic DI, Shu Y, Yu J, Taylor RN. Pathogenesis of endometriosis: interaction between endocrine and inflammatory pathways. Best Pract Res Clin Obstet Gynaecol. 2018;50:50–60. doi:10.1016/j.bpobgyn.2018.01.006
  • Routier FH, Hounsell EF, Rudd PM, et al. Quantitation of the oligosaccharides of human serum IgG from patients with rheumatoid arthritis: a critical evaluation of different methods. J Immunol Methods. 1998;213:113–130. doi:10.1016/s0022-1759(98)00032-5
  • Borrok MJ, Jung ST, Kang TH, Monzingo AF, Georgiou G. Revisiting the role of glycosylation in the structure of human IgG Fc. ACS Chem Biol. 2012;7:1596–1602. doi:10.1021/cb300130k
  • Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol. 2003;325:979–989. doi:10.1016/s0022-2836(02)01250-0
  • Shields RL, Lai J, Keck R, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem. 2002;277:26733–26740. doi:10.1074/jbc.M202069200
  • Sondermann P, Huber R, Oosthuizen V, Jacob U. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature. 2000;406(6793):267–273. doi:10.1038/35018508
  • Ferrara C, Grau S, Jager C, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A. 2011;108:12669–12674. doi:10.1073/pnas.1108455108
  • Parekh RB, Dwek RA, Sutton BJ, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316:52–457. doi:10.1038/316452a0
  • Ramakrishna C, Newo AN, Shen YW, Cantin E. Passively administered pooled human immunoglobulins exert IL-10 dependent anti-inflammatory effects that protect against fatal HSV encephalitis. PLoS Pathog. 2011;7:e1002071. doi:10.1371/journal.ppat.1002071
  • Mizuochi T, Taniguchi T, Shimizu A, Kobata A. Structural and numerical variations of the carbohydrate moiety of immunoglobulin G. J Immunol. 1982;129:2016–2020.
  • Shibata-Koyama M, Iida S, Okazaki A, et al. The N-linked oligosaccharide at Fc gamma RIIIa Asn-45: an inhibitory element for high Fc gammaRIIIa binding affinity to IgG glycoforms lacking core fucosylation. Glycobiology. 2009;19:126–134. doi:10.1093/glycob/cwn110
  • Mizushima T, Yagi H, Takemoto E, et al. Structural basis for improved efficacy of therapeutic antibodies on defucosylation of their Fc glycans. Genes Cells. 2011;16(11):1071–1080. doi:10.1111/j.1365-2443.2011.01552.x
  • Li J, Hsu HC, Mountz JD, Allen JG. Unmasking fucosylation: from cell adhesion to immune system regulation and diseases. Cell Chem Biol. 2018;25(5):499–512. doi:10.1016/j.chembiol.2018.02.005
  • Miyoshi E, Moriwaki K, Nakagawa T. Biological function of fucosylation in cancer biology. J Biochem. 2008;143:725–729. doi:10.1093/jb/mvn011
  • Ma B, Simala-Grant JL, Taylor DE. Fucosylation in prokaryotes and eukaryotes. Glycobiology. 2006;16:158–184. doi:10.1093/glycob/cwl040
  • Brinkman-van der Linden EC, de Haan PF, Havenaar EC, van Dijk W. Inflammation-induced expression of sialyl LewisX is not restricted to alpha1-acid glycoprotein but also occurs to a lesser extent on alpha1-antichymotrypsin and haptoglobin. Glycoconjugate J. 1998;15:177–182. doi:10.1023/a:1006972307166
  • Goodarzi MT, Axford JS, Varanasi SS, et al. Sialyl Lewis(x) expression on IgG in rheumatoid arthritis and other arthritic conditions: a preliminary study. Glycoconj J. 1998;15:1149–1154. doi:10.1023/a:1006920007227
  • Li J, Hsu HC, Ding Y, et al. Inhibition of fucosylation reshapes inflammatory macrophages and suppresses type II collagen-induced arthritis. Arthritis Rheumatol. 2014;66:2368–2379. doi:10.1002/art.38711
  • Ryden I, Pahlsson P, Lundblad A, Skogh T. Fucosylation of α1-acid glycoprotein (orosomucoid) compared with traditional biochemical markers of inflammation in recent onset rheumatoid arthritis. Clin Chim Acta. 2002;317:221–229. doi:10.1016/s0009-8981(01)00803-8
  • Thompson S, Kelly CA, Griffiths ID, Turner GA. Abnormally-fucosylated serum haptoglobins in patients with inflammatory joint disease. Clin Chim Acta. 1989;184:251–258. doi:10.1016/0009-8981(89)90058-2
  • Sarrats A, Saldova R, Pla E, et al. Glycosylation of liver acute phase proteins in pancreatic cancer and chronic pancreatitis. Proteomics Clin Appl. 2010;4:432–448. doi:10.1002/prca.200900150
  • Miyoshi J, Yajima T, Okamoto S, et al. Ectopic expression of blood type antigens in inflamed mucosa with higher incidence of FUT2 secretor status in colonic Crohn’s disease. J Gastroenterol. 2011;46:1056–1063. doi:10.1007/s00535-011-0425-7
  • Maroni L, van de Graaf SFJ, Hohenester SD, et al. Fucosyltransferase 2: a genetic risk factor for primary sclerosing cholangitis and Crohn’s disease–a comprehensive review. Clin Rev Allergy Immunol. 2015;48:182–191. doi:10.1007/s12016-014-8423-1
  • Kapur R, Kustiawan I, Vestrheim A, et al. A prominent lack of IgG1-Fc fucosylation of platelet alloantibodies in pregnancy. Blood. 2014;123:471–480. doi:10.1182/blood-2013-09-527978
  • Yamashita K, Kochibe N, Ohkura T, Ueda I, Kobata A. Fractionation of L-fucose-containing oligosaccharides on immobilized Aleuria aurantia lectin. J Biol Chem. 1985;260:4688–4693. doi:10.1016/S0021-9258(18)89125-6
  • Yan L, Wilkins PP, Alvarez-Manilla G, Do SI, Smith DF, Cummings RD. Immobilized Lotus tetragonolobus agglutinin binds oligosaccharides containing the Le(x) determinant. Glycoconj J. 1997;14:45–55. doi:10.1023/a:1018508914551
  • Loris R, De Greve H, Dao-Thi MH, Messens J, Imberty A, Wyns L. Structural basis of carbohydrate recognition by lectin II from Ulex europaeus, a protein with a promiscuous carbohydrate binding site. J Mol Biol. 2000;301:987–1002. doi:10.1006/jmbi.2000.4016
  • Sołkiewicz K, Krotkiewski H, Jędryka M, Kratz EM. Variability of serum IgG sialylation and galactosylation degree in women with advanced endometriosis. Sci Rep. 2021;11:5586. doi:10.1038/s41598-021-85200-x
  • Kokot I, Piwowar A, Jędryka M, Sołkiewicz K, Kratz EM. Diagnostic significance of selected serum inflammatory markers in women with advanced. Int J Mol Sci. 2021;22(5):2295. doi:10.3390/ijms22052295
  • Ey PL, Prowse SJ, Jenkin CR. Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-sepharose. Immunochemistry. 1978;15:429–436. doi:10.1016/0161-5890(78)90070-6
  • Bossuyt X. Clinical performance characteristics of a laboratory test. A practical approach in the autoimmune laboratory. Autoimmun Rev. 2009;8:543–548. doi:10.1016/j.autrev.2009.01.013
  • Eisenberg VH, Zolti M, Soriano D. Is there an association between autoimmunity and endometriosis? Autoimmun Rev. 2012;11:806–814. doi:10.1016/j.autrev.2012.01.005
  • Berkes E, Muzinic A, Rigo J, Tinneberg HR, Oehmke F. The analysis of the human plasma N-glycome in endometriosis patients. Eur J Obstet Gynecol Reprod Biol. 2013;171:107–115. doi:10.1016/j.ejogrb.2013.08.008
  • Corzo C, Barrientos Santillan N, Westin SN, Ramirez PT. Updates on Conservative Management of Endometrial Cancer. J Minim Invasive Gynecol. 2018;25(2):308–313. doi:10.1016/j.jmig.2017.07.022
  • Heong V, Ngoi N, Tan DS. Update on immune checkpoint inhibitors in gynecological cancers. J GynecolOncol. 2017;28(2):e20. doi:10.3802/jgo.2017.28.e20
  • Menderes G, Hicks C, Black JD, Schwab CL, Santin AD. Immune checkpoint inhibitors in gynecologic cancers with lessons learned from non-gynecologic cancers. Expert Opin Biol Ther. 2016;16(8):989–1004. doi:10.1080/14712598.2016.1177018
  • Saldova R, Royle L, Radcliffe CM, et al. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology. 2007;17:1344–1356. doi:10.1093/glycob/cwm100
  • Ohmi Y, Ise W, Harazono A, et al. Sialylation converts arthritogenic IgG into inhibitors of collagen-induced arthritis. Nat Commun. 2016;7:11205. doi:10.1038/ncomms11205
  • Komaromy A, Reider B, Jarvas G, Guttman A. Glycoprotein biomarkers and analysis in chronic obstructive pulmonary disease and lung cancer with special focus on serum immunoglobulin G. Clin Chim Acta. 2020;506:204–213. doi:10.1016/j.cca.2020.03.041
  • Halme J, Becker S, Haskill S. Altered maturation and function of peritoneal macrophages: possible role in pathogenesis of endometriosis. Am J Obstet Gynecol. 1987;156:783189. doi:10.1016/0002-9378(87)90333-4
  • Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril. 2004;81:652–661. doi:10.1016/j.fertnstert.2003.07.037
  • Khan KN, Masuzaki H, Fujishita A, et al. Regulation of hepatocyte growth factor by basal and stimulated macrophages in women with endometriosis. Hum Reprod. 2005;20:49–60. doi:10.1093/humrep/deh525
  • Khan KN, Kitajima M, Hiraki H, et al. Immunopathogenesis of pelvic endometriosis: role of hepatocyte growth factor, macrophages and ovarian steroids. Am J Reprod Immunol. 2008;60:383–404. doi:10.1111/j.1600-0897.2008.00643.x
  • Okazaki A, Shoji-Hosaka E, Nakamura K, et al. Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and FcgammaRIIIa. J Mol Biol. 2004;336:1239–1249. doi:10.1016/j.jmb.2004.01.007
  • Ferrara C, Stuart F, Sondermann P, Brünker P, Umaña P. The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem. 2006;281:5032. doi:10.1074/jbc.M510171200
  • Shibata-Koyama M, Iida S, Misaka H, et al. Nonfucosylated rituximab potentiates human neutrophil phagocytosis through its high binding for FcγRIIIb and MHC class II expression on the phagocytotic neutrophils. Exp Hematol. 2009;37(3):309–321. doi:10.1016/j.exphem.2008.11.006
  • Becker DJ, Lowe JB. Fucose: biosynthesis and biological function in mammals. Glycobiology. 2003;13:41–53. doi:10.1093/glycob/cwg054
  • Chen HL. Lewis glyco-epitopes: structure, biosynthesis, and functions. In: Wu AM, editor. The Molecular Immunology of Complex Carbohydrates-3. New York, Dordrecht, Heidelberg, London: Springer; 2011:53–80.
  • Castilho A, Gruber C, Thader A, et al. Processing of complex N-glycans in IgG Fc-region is affected by core fucosylation. MAbs. 2015;7:863–870. doi:10.1080/19420862.2015.1053683
  • Kratz EM, Borysewicz K, Katnik-Prastowska I. Terminal monosaccharide screening of synovial immunoglobulins G and A for the early detection of rheumatoid arthritis. Rheumatol Int. 2010;30(10):1285–1292. doi:10.1007/s00296-009-1139-5
  • Kratz EM, Ferens-Sieczkowska M, Faundez R, Kątnik-Prastowska I. Changes in fucosylation of human seminal IgG and secretory component of IgA in leukocytospermic patients. Glycoconj J. 2014;31(1):51–60. doi:10.1007/s10719-013-9501-y
  • Flögel M, Lauc G, Gornik I, Macek B. Fucosylation and galactosylation of IgG heavy chains differ between acute and remission phases of juvenile chronic arthritis. Clin Chem Lab Med. 1998;36(2):99–102. doi:10.1515/CCLM.1998.018
  • Gornik I, Maravić G, Dumić J, Flögel M, Lauc G. Fucosylation of IgG heavy chains is increased in rheumatoid arthritis. Clin Biochem. 1999;32(8):605–608. doi:10.1016/s0009-9120(99)00060-0
  • Zauner G, Selman MH, Bondt A, et al. Glycoproteomic analysis of antibodies. Mol Cell Proteomics. 2013;12:856–865. doi:10.1074/mcp.R112.026005
  • Niwa R, Shoji-Hosaka E, Sakurada M, et al. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res. 2004;64(6):2127–2133. doi:10.1158/0008-5472.can-03-2068
  • Niwa R, Natsume A, Uehara A, et al. IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J Immunol Methods. 2005;306(1–2):151–160. doi:10.1016/j.jim.2005.08.009
  • Masuda K, Kubota T, Kaneko E, et al. Enhanced binding affinity for FcgammaRIIIa of fucose-negative antibody is sufficient to induce maximal antibody-dependent cellular cytotoxicity. Mol Immunol. 2007;44(12):3122–3131. doi:10.1016/j.molimm.2007.02.005
  • Peipp M, Lammerts van Bueren JJ, Schneider-Merck T, et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood. 2008;112(6):2390–2399. doi:10.1182/blood-2008-03-144600
  • Van de Bovenkamp FS, Hafkenscheid L, Rispens T, Rombouts Y. The emerging importance of IgG Fab glycosylation in immunity. J Immunol. 2016;196:1435–1441. doi:10.4049/jimmunol.1502136
  • Van Damme EJM. Lectins as tools to select for glycosylated proteins. In: Gevaert K, Vandekerckhove J, editors. Gel-Free Proteomics. Springer Protocols; 2011:289–297.