Abstract
The expressions of some terminal glycotopes of synovial immunoglobulins G, A, and M were analysed in relation to rheumatoid arthritis (RA) progression defined according to early and advanced radiological changes in patients’ hands. The relative amounts of terminal monosaccharides were determined by lectin-immunoblotting of immunoglobulin preparations using appropriate lectins able to recognize α2,6-linked (Sambucus nigra agglutinin) and α2,3-linked (Maackia amurensis agglutinin) sialic acid, galactose (Ricinus communis agglutinin I), N-acetylglucosamine (Griffonia simplicifolia agglutinin II) as well as α1,6-linked (Aleuria aurantia lectin), α1,3-linked (Lotus tetragonolobus agglutinin), and α1,2-linked (Ulex europaeus agglutinin) fucose. The results indicate differences between early and advanced RA stages in the terminal sugar exposition of synovial IgG and IgA, but not IgM. The galactose-deficient glycotope with exposed N-acetylglucosamine of the synovial 33.1-kDa IgG fragment appeared exclusively in the early stage of RA. In contrast, this glycotope of intact synovial IgG and IgA was present in both groups, although with higher proportions in advanced RA. The proportions of the sialyl and fucosyl determinants of intact synovial A and G immunoglobulins were clearly lower in the early RA group than in the advanced. The analysis of terminal oligosaccharide exposition in IgG, IgG fragments, and IgA present in the synovial fluid of RA patients might be applicable as a stage-specific marker in the diagnosis and therapy of RA patients.
Similar content being viewed by others
Abbreviations
- RA:
-
Rheumatoid arthritis
- SNA:
-
Lectin from Sambucus nigra
- MAA:
-
Lectin from Maackia amurensis
- RCA I:
-
Lectin from Ricinus communis
- GSL II:
-
Lectin from Griffonia simplicifolia
- AAL:
-
Lectin from Aleuria aurantia
- LTA:
-
Lectin from Lotus tetragonolobus
- UEA:
-
Lectin from Ulex europaeus
References
Tak P (2001) Is early rheumatoid arthritis the same disease process as late rheumatoid arthritis? Best Pract Res Clin Rheumatol 15:17–26
Nijenhuis S, Zendman AJ, Vossenaar ER, Pruijn GJ, vanVenrooij WJ (2004) Autoantibodies to citrullinated proteins in rheumatoid arthritis: clinical performance and biochemical aspects of an RA-specific marker. Clin Chim Acta 350:17–34
Axford JS (1999) Glycosylation and rheumatic disease. Biochem Biophys Acta 1455:219–229
Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA (2007) The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 25:21–50
Alavi A, Axford JS (2008) Sweet and sour: the impact of sugars on disease. Rheumatology (Oxford) 47:760–770
Gindzieńska-Sieśkiewicz E, Klimiuk PA, Kisiel DG, Gindzieński A, Sierakowski S (2007) The changes in monosaccharide composition of immunoglobulin G in the course of rheumatoid arthritis. Clin Rheumatol 26:685–690
Krotkiewski H (1999) Carbohydrate moiety of immunoglobulins in health and pathology. Acta Biochim Pol 46:341–350
Pasek M, Duk M, Podbielska M, Sokolik R, Szechiński J, Lisowska E, Krotkiewski H (2006) Galactosylation of IgG from rheumatoid arthritis (RA) patients—changes during therapy. Glycoconj J 23:463–471
Croce A, Firuzi O, Altieri F, Eufemi M, Agostino R, Priori R, Bombardieri M, Alessandri C, Valesini G, Saso L (2007) Effect of infliximab on the glycosylation of IgG of patients with rheumatoid arthritis. J Clin Lab Anal 21:303–314
Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324
Renton P (1998) Imaging in rheumatoid arthritis. In: Maddison PJ, Isenberg DA, Woo P, Glass DN (eds) Oxford textbook of rheumatology. Oxford University Press, Oxford, pp 24–51
Przybysz M, Borysewicz K, Szechiński J, Kątnik-Prastowska I (2007) Synovial fibronectin fragmentation and domain expressions in relation to rheumatoid arthritis progression. Rheumatology 46:1071–1075
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354
Kratz EM, Borysewicz K, Krotkiewski H, Kątnik-Prastowska I (2007) Expression of IgG glycoforms in different stages of rheumatoid arthritis. In: 2nd European Conference on Chemistry and Life Sciences, Wrocław, Poland; September 4–8, 2007. Medimond International Proceedings, pp 103–106
Shibuya N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ (1987) The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2–6)Gal/GalNAc sequence. J Biol Chem 262:1596–1601
Knibbs RN, Goldstein IJ, Ratcliffe RM, Shibuya N (1991) Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J Biol Chem 266:83–88
Wu AM, Song SC, Sugii S, Herp A (1997) Differential binding properties of Gal/GalNAc specific lectins available for characterization of glycoreceptors. Indian J Biochem Biophys 34:61–71
Nakamura-Tsuruta S, Kominami J, Kamei M, Koyama Y, Suzuki T, Isemura M, Hirabayashi J (2006) Comparative analysis by frontal affinity chromatography of oligosaccharide specificity of GlcNAc-binding lectins, Griffonia simplicifolia lectin-II (GSL-II) and Boletopsis leucomelas lectin (BLL). J Biochem 140:285–291
Yamashita K, Kochibe N, Ohkura T, Ueda I, Kobata A (1985) Fractionation of l-fucose-containing oligosaccharides on immobilized Aleuria aurantia lectin. J Biol Chem 260:4688–4693
Yan L, Wilkins PP, Alvarez-Manilla G, Do SI, Smith DF, Cummings RD (1997) Immobilized Lotus tetragonolobus agglutinin binds oligosaccharides containing the Le(x) determinant. Glycoconj J 14:45–55
Audette GF, Vandonselaar M, Delbaere LT (2000) The 2.2 A resolution structure of the O(H) blood-group-specific lectin I from Ulex europaeus. J Mol Biol 304:423–433
Zerfaoui M, Fukuda M, Sbarra V, Lombardo D, El-Battari A (2000) Alpha(1, 2)-fucosylation prevents sialyl Lewis x expression and E-selectin-mediated adhesion of fucosyltransferase VII-transfected cells. Eur J Biochem 267:53–61
Kątnik I, Jadach J, Krotkiewski H, Gerber J (1994) Investigating the glycosylation of normal and ovarian cancer haptoglobins using digoxigenin-labeled lectins. Glycosyl Dis 1:97–104
Raza K, Falciani F, Curnow SJ, Ross EJ, Lee C, Akbar AN, Lord JM, Gordon C, Buckley CD, Salmon M (2005) Early rheumatoid arthritis is characterized by a distinct and transient synovial fluid cytokine profile of T cell and stromal cell origin. Arthritis Res Ther 7:784–795
Yasuda T (2006) Cartilage destruction by matrix degradation products. Mod Rheumatol 16:197–205
Popko J, Marciniak J, Ilendo E, Knas M, Guszczyn T, Stasiak-Barmuta A, Moniuszko T, Zwierz K, Wysocka J (2008) Profile of exoglycosidases in synovial cell cultures derived from human synovial membrane. Cell Biochem Biophys 51:89–95
Homandberg GA (2001) Cartilage damage by matrix degradation products: fibronectin fragments. Clin Orthop Relat Res 391:100–107
Przybysz M, Maszczak D, Borysewicz K, Szechinski J, Katnik-Prastowska I (2007) Relative sialylation and fucosylation of synovial and plasma fibronectins in relation to the progression and activity of rheumatoid arthritis. Glycoconj J 24:543–550
Alavi A, Axford JS, Pool AJ (2004) Serum galactosyltransferase isoform changes in rheumatoid arthritis. J Rheumatol 31:1513–1520
Albert H, Collin M, Dudziak D, Ravetch JV, Nimmerjahn F (2008) In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner. Proc Natl Acad Sci USA 39:15005–15009
Nimmerjahn F, Ravetch JV (2004) The antiinflammatory activity of IgG: the intravenous IgG paradox. J Exp Med 1:11–15
Author information
Authors and Affiliations
Corresponding author
Additional information
Some preliminary experiments described in this work were presented during the 2nd European Conference on Chemistry and Life Sciences, 2007, Wrocław, Poland.
Rights and permissions
About this article
Cite this article
Kratz, E.M., Borysewicz, K. & Kątnik-Prastowska, I. Terminal monosaccharide screening of synovial immunoglobulins G and A for the early detection of rheumatoid arthritis. Rheumatol Int 30, 1285–1292 (2010). https://doi.org/10.1007/s00296-009-1139-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00296-009-1139-5