Enzymatic sialylation of IgA1 O-glycans: Implications for studies of IgA nephropathy

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Takahashi, Kazuo ^a,d   Raska, Milan ^a,e   Horynova, Milada Stuchlova ^a,e   Hall, Stacy D ^a   Poulsen, Knud ^f   Kilian, Mogens ^f   Hiki, Yoshiyuki ^g   Yuzawa, Yukio ^d   Moldoveanu, Zina ^a   Julian, Bruce A ^a,b   Renfrow, Matthew B ^c   Novak, Jan ^a  

^a University of Alabama at Birmingham   (United States)

^b and Clinical Center   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e PALACKÝ UNIVERSITY   (Czech Republic)

^f AARHUS UNIVERSITY   (Denmark)

^g FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLUTININ; ALPHA 2,3 SIALYLTRANSFERASE; ALPHA 2,6 SIALYLTRANSFERASE; GALACTOSE; GLYCAN; IGA1 O GLYCAN; IMMUNOGLOBULIN A1; LECTIN; N ACETYLNEURAMINIC ACID; PARAPROTEIN; SIALIDASE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; GLYCOSYLTRANSFERASE; IMMUNOGLOBULIN A; POLYSACCHARIDE; RECOMBINANT PROTEIN; SIALIC ACID DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ENZYMATIC SIALYLATION; ENZYME ACTIVITY; HELIX ASPERSA; HUMAN; IMMUNOGLOBULIN A NEPHROPATHY; PROTEIN BINDING; PROTEIN GLYCOSYLATION; SIALYLATION; AMINO ACID SEQUENCE; ANIMAL; CARBOHYDRATE ANALYSIS; CHEMISTRY; HEK293 CELL LINE; HELIX (SNAIL); METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANIMALS; CARBOHYDRATE SEQUENCE; GLOMERULONEPHRITIS, IGA; GLYCOSYLTRANSFERASES; HEK293 CELLS; HELIX (SNAILS); HUMANS; IMMUNOGLOBULIN A; LECTINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; RECOMBINANT PROTEINS; SIALIC ACIDS;

EID: 84903372718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099026     Document Type: Article

References (85)

1. Mestecky J, Tomana M, Crowley-Nowick PA, Moldoveanu Z, Julian BA, et al. (1993) Defective galactosylation and clearance of IgA1 molecules as a possible etiopathogenic factor in IgA nephropathy. Contrib Nephrol 104: 172-182.
2. Moore JS, Wu X, Kulhavy R, Tomana M, Novak J, et al. (2005) Increased levels of galactose-deficient IgG in sera of HIV-1-infected individuals. AIDS 19: 381-389. (Pubitemid 40446184)
3. Rademacher TW, Williams P, Dwek RA (1994) Agalactosyl glycoforms of IgG autoantibodies are pathogenic. Proc Natl Acad Sci U S A 91: 6123-6127. (Pubitemid 24188295)
4. Springer GF (1984) T and Tn, general carcinoma autoantigens. Science 224: 1198-1206.
5. Troelsen LN, Garred P, Madsen HO, Jacobsen S (2007) Genetically determined high serum levels of mannose-binding lectin and agalactosyl IgG are associated with ischemic heart disease in rheumatoid arthritis. Arthritis Rheum 56: 21-29. (Pubitemid 46106175)
6. Mestecky J, Raska M, Julian BA, Gharavi AG, Renfrow MB, et al. (2013) IgA Nephropathy: Molecular Mechanisms of the Disease. Annu Rev Pathol Mech Dis 8: 217-240.
7. Xue J, Zhu LP, Wei Q (2013) IgG-Fc N-glycosylation at Asn297 and IgA O-glycosylation in the hinge region in health and disease. Glycoconj J 30: 735-745.
8. Novak J, Renfrow MB, Gharavi AG, Julian BA (2013) Pathogenesis of immunoglobulin A nephropathy. Curr Opin Nephrol Hypertens 22: 287-294.
9. Scott DW, Patel RP (2013) Endothelial heterogeneity and adhesion molecules N-glycosylation: implications in leukocyte trafficking in inflammation. Glycobiology 23: 622-633.
10. Stuchlova Horynova M, Raska M, Clausen H, Novak J (2013) Aberrant O-glycosylation and anti-glycan antibodies in an autoimmune disease IgA nephropathy and breast adenocarcinoma. Cell Mol Life Sci 70: 829-839.
11. Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA (2001) Glycosylation and the immune system. Science 291: 2370-2376. (Pubitemid 32231792)
12. Varki A (2008) Sialic acids in human health and disease. Trends Mol Med 14: 351-360.
13. Varki A and Gagneux P (2012) Multifarious roles of sialic acids in immunity. Ann N Y Acad Sci 1253: 16-36.
14. Schmitt FC, Figueiredo P, Lacerda M (1995) Simple mucin-type carbohydrate antigens (T, sialosyl-T, Tn and sialosyl-Tn) in breast carcinogenesis. Virchows Archiv 427: 251-258.
15. Sewell R, Backstrom M, Dalziel M, Gschmeissner S, Karlsson H, et al. (2006) The ST6GalNAc-I sialyltransferase localizes throughout the Golgi and is responsible for the synthesis of the tumor-associated sialyl-Tn O-glycan in human breast cancer. J Biol Chem 281: 3586-3594. (Pubitemid 43845976)
16. Brockhausen I (2006) Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep 7: 599-604.
17. Pinho S, Marcos NT, Ferreira B, Carvalho AS, Oliveira MJ, et al. (2007) Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett 249: 157-170. (Pubitemid 46452924)
18. Storr SJ, Royle L, Chapman CJ, Hamid UM, Robertson JF, et al. (2008) The O-linked glycosylation of secretory/shed MUC1 from an advanced breast cancer patient's serum. Glycobiology 18: 456-462. (Pubitemid 351753549)
19. Picco G, Julien S, Brockhausen I, Beatson R, Antonopoulos A, et al. (2010) Over-expression of ST3Gal-I promotes mammary tumorigenesis. Glycobiology 20: 1241-1250.
20. Mungul A, Cooper L, Brockhausen I, Ryder K, Mandel U, et al. (2004) Sialylated core 1 based O-linked glycans enhance the growth rate of mammary carcinoma cells in MUC1 transgenic mice. Int J Oncol 25: 937-943.
21. Bresalier RS, Ho SB, Schoeppner HL, Kim YS, Sleisenger MH, et al. (1996) Enhanced sialylation of mucin-associated carbohydrate structures in human colon cancer metastasis. Gastroenterology 110: 1354-1367. (Pubitemid 26134066)
22. Schindlbeck C, Jeschke U, Schulze S, Karsten U, Janni W, et al. (2005) Characterisation of disseminated tumor cells in the bone marrow of breast cancer patients by the Thomsen-Friedenreich tumor antigen. Histochem Cell Biol 123: 631-637. (Pubitemid 41126082)
23. Julien S, Lagadec C, Krzewinski-Recchi MA, Courtand G, Le Bourhis X, et al. (2005) Stable expression of sialyl-Tn antigen in T47-D cells induces a decrease of cell adhesion and an increase of cell migration. Breast Cancer Res Treat 90: 77-84. (Pubitemid 40487005)
24. Mestecky J, Russell MW (1986) IgA subclasses. Monogr Allergy 19: 277-301.
25. Baenziger J, Kornfeld S (1974) Structure of the carbohydrate units of IgA1 immunoglobulin. II. Structure of the O-glycosidically linked oligosaccharide units. J Biol Chem 249: 7270-7281.
26. Mattu TS, Pleass RJ, Willis AC, Kilian M, Wormald MR, et al. (1998) The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N-glycosylation on Fca receptor interactions. J Biol Chem 273: 2260-2272. (Pubitemid 28069279)
27. Tarelli E, Smith AC, Hendry BM, Challacombe SJ, Pouria S (2004) Human serum IgA1 is substituted with up to six O-glycans as shown by matrix assisted laser desorption ionisation time-of-flight mass spectrometry. Carbohydr Res 339: 2329-2335. (Pubitemid 39165126)
28. Renfrow MB, Cooper HJ, Tomana M, Kulhavy R, Hiki Y, et al. (2005) Determination of aberrant O-glycosylation in the IgA1 hinge region by electron capture dissociation Fourier transform-ion cyclotron resonance mass spectrometry. J Biol Chem 280: 19136-19145. (Pubitemid 41379620)
29. Renfrow MB, Mackay CL, Chalmers MJ, Julian BA, Mestecky J, et al. (2007) Analysis of O-glycan heterogeneity in IgA1 myeloma proteins by Fourier transform ion cyclotron resonance mass spectrometry: implications for IgA nephropathy. Anal Bioanal Chem 389: 1397-1407. (Pubitemid 350023664)
30. Takahashi K, Wall SB, Suzuki H, Smith AD, Hall S, et al. (2010) Clustered O-glycans of IgA1: Defining macro- and micro-heterogeneity by use of electron capture/transfer dissociation. Mol Cell Proteomics 9: 2545-2557.
31. Takahashi K, Smith AD, Poulsen K, Kilian M, Julian BA, et al. (2012) Naturally occurring structural isomers in serum IgA1 O-glycosylation. J Proteome Res 11: 692-702.
32. Berger J and Hinglais N (1968) [Intercapillary deposits of IgA-IgG]. Urol Nephrol (Paris) 74: 694-695.
33. Conley ME, Cooper MD, Michael AF (1980) Selective deposition of immunoglobulin A1 in immunoglobulin A nephropathy, anaphylactoid purpura nephritis, and systemic lupus erythematosus. J Clin Invest 66: 1432-1436. (Pubitemid 11205607)
34. Julian BA, Waldo FB, Rifai A, Mestecky J (1988) IgA nephropathy, the most common glomerulonephritis worldwide. A neglected disease in the United States? Am J Med 84: 129-132.
35. Donadio JV, Grande JP (2002) IgA nephropathy. N Engl J Med 347: 738-748. (Pubitemid 35203906)
36. Wyatt RJ, Julian BA (2013) IgA nephropathy. N Engl J Med 368: 2402-2414.
37. Czerkinsky C, Koopman WJ, Jackson S, Collins JE, Crago SS, et al. (1986) Circulating immune complexes and immunoglobulin A rheumatoid factor in patients with mesangial immunoglobulin A nephropathies. J Clin Invest 77: 1931-1938. (Pubitemid 16062650)
38. Coppo R, Basolo B, Piccoli G, Mazzucco G, Bulzomi MR, et al. (1984) IgA1 and IgA2 immune complexes in primary IgA nephropathy and Henoch-Schonlein nephritis. Clin Exp Immunol 57: 583-590. (Pubitemid 14057714)
39. 2 antibodies in patients with primary IgA nephropathy. Clin Exp Immunol 77: 15-20.
40. Tomana M, Matousovic K, Julian BA, Radl J, Konecny K, et al. (1997) Galactose-deficient IgA1 in sera of IgA nephropathy patients is present in complexes with IgG. Kidney Int 52: 509-516. (Pubitemid 27359597)
41. Tomana M, Novak J, Julian BA, Matousovic K, Konecny K, et al. (1999) Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J Clin Invest 104: 73-81. (Pubitemid 29534347)
42. Novak J, Tomana M, Matousovic K, Brown R, Hall S, et al. (2005) IgA1-containing immune complexes in IgA nephropathy differentially affect proliferation of mesangial cells. Kidney Int 67: 504-513. (Pubitemid 40139842)
43. Suzuki H, Fan R, Zhang Z, Brown R, Hall S, et al. (2009) Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J Clin Invest 119: 1668-1677.
44. Suzuki H, Kiryluk K, Novak J, Moldoveanu Z, Herr AB, et al. (2011) The pathophysiology of IgA nephropathy. J Am Soc Nephrol 22: 1795-1803.
45. Berthoux F, Suzuki H, Thibaudin L, Yanagawa H, Maillard N, et al. (2012) Autoantibodies targeting galactose-deficient IgA1 associate with progression of IgA nephropathy. J Am Soc Nephrol 23: 1579-1587.
46. Novak J, Julian BA, Tomana M, Mestecky J (2001) Progress in molecular and genetic studies of IgA nephropathy. J Clin Immunol 21: 310-327. (Pubitemid 33015802)
47. Suzuki H, Moldoveanu Z, Hall S, Brown R, Vu HL, et al. (2008) IgA1-secreting cell lines from patients with IgA nephropathy produce aberrantly glycosylated IgA1. J Clin Invest 118: 629-639. (Pubitemid 351206552)
48. Suzuki H, Raska M, Yamada K, Moldoveanu Z, Julian BA, et al. (2014) Cytokines alter IgA1 O-glycosylation by dysregulating C1GalT1 and ST6Gal-NAc-II enzymes. J Biol Chem 289: 5330-5339.
49. Leung JC, Poon PY, Lai KN (1999) Increased sialylation of polymeric immunoglobulin A1: mechanism of selective glomerular deposition in immunoglobulin A nephropathy? J Lab Clin Med 133: 152-160. (Pubitemid 29073239)
50. Amore A, Cirina P, Conti G, Brusa P, Peruzzi L, et al. (2001) Glycosylation of circulating IgA in patients with IgA nephropathy modulates proliferation and apoptosis of mesangial cells. J Am Soc Nephrol 12: 1862-1871. (Pubitemid 32801361)
51. Leung JC, Tang SC, Chan DT, Lui SL, Lai KN (2002) Increased sialylation of polymeric lambda-IgA1 in patients with IgA nephropathy. J Clin Lab Anal 16: 11-19.
52. Odani H, Hiki Y, Takahashi M, Nishimoto A, Yasuda Y, et al. (2000) Direct evidence for decreased sialylation and galactosylation of human serum IgA1 Fc O-glycosylated hinge peptides in IgA nephropathy by mass spectrometry. Biochem Biophys Res Commun 271: 268-274. (Pubitemid 30444888)
53. Horie A, Hiki Y, Odani H, Yasuda Y, Takahashi M, et al. (2003) IgA1 molecules produced by tonsillar lymphocytes are under-O-glycosylated in IgA nephropathy. Am J Kidney Dis 42: 486-496. (Pubitemid 37048124)
54. Xu LX, Zhao MH (2005) Aberrantly glycosylated serum IgA1 are closely associated with pathologic phenotypes of IgA nephropathy. Kidney Int 68: 167-172.
55. Ding JX, Xu LX, Lv JC, Zhao MH, Zhang H, et al. (2007) Aberrant sialylation of serum IgA1 was associated with prognosis of patients with IgA nephropathy. Clin Immunol 125: 268-274. (Pubitemid 350116717)
56. Maenuma K, Yim M, Komatsu K, Hoshino M, Tachiki-Fujioka A, et al. (2009) A library of mutated Maackia amurensis hemagglutinin distinguishes putative glycoforms of immunoglobulin A1 from IgA nephropathy patients. J Proteome Res 8: 3617-3624.
57. Leung JC, Tang SC, Lam MF, Chan TM, Lai KN (2001) Charge-dependent binding of polymeric IgA1 to human mesangial cells in IgA nephropathy. Kidney Int 59: 277-285. (Pubitemid 32055236)
58. Coppo R, Amore A, Gianoglio B, Reyna A, Peruzzi L, et al. (1993) Serum IgA and macromolecular IgA reacting with mesangial matrix components. Contrib Nephrol 104: 162-171.
59. Kokubo T, Hiki Y, Iwase H, Tanaka A, Toma K, et al. (1998) Protective role of IgA1 glycans against IgA1 self-aggregation and adhesion to extracellular matrix proteins. J Am Soc Nephrol 9: 2048-2054. (Pubitemid 28482152)
60. Sano T, Hiki Y, Kokubo T, Iwase H, Shigematsu H, et al. (2002) Enzymatically deglycosylated human IgA1 molecules accumulate and induce inflammatory cell reaction in rat glomeruli. Nephrol Dial Transplant 17: 50-56. (Pubitemid 34093009)
61. Hiki Y (2009) O-linked oligosaccharides of the IgA1 hinge region: roles of its aberrant structure in the occurrence and/or progression of IgA nephropathy. Clin Exp Nephrol 13: 415-423.
62. Hiki Y, Odani H, Takahashi M, Yasuda Y, Nishimoto A, et al. (2001) Mass spectrometry proves under-O-glycosylation of glomerular IgA1 in IgA nephropathy. Kidney Int 59: 1077-1085. (Pubitemid 32206870)
63. Allen AC, Bailey EM, Brenchley PE, Buck KS, Barratt J, et al. (2001) Mesangial IgA1 in IgA nephropathy exhibits aberrant O-glycosylation: observations in three patients. Kidney Int 60: 969-973. (Pubitemid 34205796)
64. Moldoveanu Z, Wyatt RJ, Lee JY, Tomana M, Julian BA, et al. (2007) Patients with IgA nephropathy have increased serum galactose-deficient IgA1 levels. Kidney Int 71: 1148-1154. (Pubitemid 46809135)
65. Horynova M, Takahashi K, Hall S, Renfrow MB, Novak J, et al. (2012) Production of N-acetylgalactosaminyl-transferase 2 (GalNAc-T2) fused with secretory signal Igk in insect cells. Protein Expr Purif 81: 175-180.
66. Moore JS, Kulhavy R, Tomana M, Moldoveanu Z, Suzuki H, et al. (2007) Reactivities of N-acetylgalactosamine-specific lectins with human IgA1 proteins. Mol Immunol 44: 2598-2604. (Pubitemid 46240321)
67. Raska M, Moldoveanu Z, Suzuki H, Brown R, Kulhavy R, et al. (2007) Identification and characterization of CMP-NeuAc:GalNAc-IgA1 α2,6-sialyltransferase in IgA1-producing cells. J Mol Biol 369: 69-78. (Pubitemid 46635435)
68. Monteiro RC, Halbwachs-Mecarelli L, Roque-Barreira MC, Noel LH, Berger J, et al. (1985) Charge and size of mesangial IgA in IgA nephropathy. Kidney Int 28: 666-671. (Pubitemid 16205803)
69. Lai KN, Chui SH, Lewis WH, Poon AS, Lam CW (1994) Charge distribution of IgA-lambda in IgA nephropathy. Nephron 66: 38-44. (Pubitemid 23355574)
70. Tomana M, Kulhavy R, Mestecky J (1988) Receptor-mediated binding and uptake of immunoglobulin A by human liver. Gastroenterology 94: 762-770. (Pubitemid 18073541)
71. Stockert RJ (1995) The asialoglycoprotein receptor: relationships between structure, function, and expression. Physiol Rev 75: 591-609.
72. Basset C, Devauchelle V, Durand V, Jamin C, Pennec YL, et al. (1999) Glycosylation of immunoglobulin A influences its receptor binding. Scand J Immunol 50: 572-579.
73. Steirer LM, Park EI, Townsend RR, Baenziger JU (2009) The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid α2,6-galactose. J Biol Chem 284: 3777-3783.
74. Moldoveanu Z, Epps JM, Thorpe SR, Mestecky J (1988) The sites of catabolism of murine monomeric IgA. J Immunol 141: 208-213.
75. Mestecky J, Moldoveanu Z, Tomana M, Epps JM, Thorpe SR, et al. (1989) The role of the liver in catabolism of mouse and human IgA. Immunol Invest 18: 313-324. (Pubitemid 19120804)
76. Novak J, Julian BA, Tomana M, Mestecky J (2008) IgA glycosylation and IgA immune complexes in the pathogenesis of IgA nephropathy. Semin Nephrol 28: 78-87.
77. Stephenson AE, Wu H, Novak J, Tomana M, Mintz K, et al. (2002) The Fap1 fimbrial adhesin is a glycoprotein: antibodies specific for the glycan moiety block the adhesion of Streptococcus parasanguis in an in vitro tooth model. Mol Microbiol 43: 147-157. (Pubitemid 34212197)
78. Mistry D, Stockley RA (2006) IgA1 protease. Int J Biochem Cell Biol 38: 1244-1248.
79. Kilian M, Reinholdt J, Lomholt H, Poulsen K and Frandsen EV (1996) Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. APMIS 104: 321-338. (Pubitemid 26226034)
80. Reinholdt J, Tomana M, Mortensen SB, Kilian M (1990) Molecular aspects of immunoglobulin A1 degradation by oral streptococci. Infect Immun 58: 1186-1194. (Pubitemid 20151776)
81. Corfield T (1992) Bacterial sialidases-roles in pathogenicity and nutrition. Glycobiology 2: 509-521.
82. Severi E, Hood DW, Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822. (Pubitemid 47517045)
83. King SJ (2010) Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 25: 15-24.
84. Lewis AL, Lewis WG (2012) Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14: 1174-1182.
85. Hastings MC, Moldoveanu Z, Suzuki H, Berthoux F, Julian BA, et al. (2013) Biomarkers in IgA nephropathy: relationship to pathogenetic hits. Expert Opin Med Diagn 7: 615-627.