Pathogenesis of immunoglobulin A nephropathy

Current Opinion in Nephrology and Hypertension

Volumn 22, Issue 3, 2013, Pages 287-294

  Novak, Jan ^a   Renfrow, Matthew B ^a   Gharavi, Ali G ^b   Julian, Bruce A ^a  

^a UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^b Columbia University ^*  (United States)

Author keywords

Genome wide association studies; High resolution mass spectrometry; Immunoglobulin A nephropathy; Immunoglobulin A1; O glycans

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; GALACTOSE; IMMUNOGLOBULIN A1;

ANTIGEN ANTIBODY COMPLEX; DISEASE COURSE; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETICS; GEOGRAPHIC DISTRIBUTION; GLYCOSYLATION; HUMAN; IGA IGG IMMUNE COMPLEX DISEASE; IMMUNE COMPLEX DISEASE; IMMUNOGLOBULIN A NEPHROPATHY; IMMUNOPATHOGENESIS; KIDNEY INJURY; MASS SPECTROMETRY; MESANGIUM; NONHUMAN; PATIENT MONITORING; PRIORITY JOURNAL; PROGNOSIS; RACE DIFFERENCE; REVIEW; RISK ASSESSMENT;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; BIOLOGICAL MARKERS; GENETIC PREDISPOSITION TO DISEASE; GENOMICS; GLOMERULONEPHRITIS, IGA; HUMANS; IMMUNOGLOBULIN A; KIDNEY GLOMERULUS; PHENOTYPE; PREDICTIVE VALUE OF TESTS; RISK FACTORS;

EID: 84878879876     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0b013e32835fef54     Document Type: Review

References (100)

1. Berger J, Hinglais N. Intercapillary deposits of IgA-IgG [in French]. J Urol Nephrol 1968; 74:694-695.
2. D'Amico G. The commonest glomerulonephritis in the world: IgA nephropathy. Q J Med 1987; 64:709-727.
3. Julian BA, Waldo FB, Rifai A, Mestecky J. IgA nephropathy, the most common glomerulonephritis worldwide. A neglected disease in the United States? Am J Med 1988; 84:129-132.
4. D'Amico G. Natural history of idiopathic IgA nephropathy and factors predictive of disease outcome. Semin Nephrol 2004; 24:179-196.
5. Julian BA, Suzuki H, Suzuki Y, et al. Sources of urinary proteins and their analysis by urinary proteomics for the detection of biomarkers of disease. Proteomics Clin Appl 2009; 3:1029-1043.
6. Allen AC, Bailey EM, Brenchley PEC, et al. Mesangial IgA1 in IgA nephropathy exhibits aberrant O-glycosylation: observations in three patients. Kidney Int 2001; 60:969-973.
7. Hiki Y, Odani H, Takahashi M, et al. Mass spectrometry proves under-Oglycosylation of glomerular IgA1 in IgA nephropathy. Kidney Int 2001; 59:1077-1085.
8. Haas M, Reich HN. Morphologic markers of progressive immunoglobulin A nephropathy. Adv Chronic Kidney Dis 2012; 19:107-113.
9. Floege J, Eitner F. Current therapy for IgA nephropathy. J Am Soc Nephrol 2011; 22:1785-1794.
10. Suzuki H, Kiryluk K, Novak J, et al. The pathophysiology of IgA nephropathy. J Am Soc Nephrol 2011; 22:1795-1803.
11. Lai KN, Leung JC, Chan LY, et al. Activation of podocytes by mesangialderived TNF-α: glomerulo-podocytic communication in IgA nephropathy. Am J Physiol Renal Physiol 2008; 294:F945-F955.
12. LaiKN, Leung JC,Chan LY, et al.Podocyte injury induced bymesangial-derived cytokines in IgA nephropathy. Nephrol Dial Transplant 2009; 24:62-72.
13. Lai KN. Pathogenesis of IgA nephropathy. Nat Rev Nephrol 2012; 8:275-283.
14. Kiryluk K, Julian BA, Wyatt RJ, et al.Genetic studies of IgA nephropathy: past, present, and future. Pediatr Nephrol 2010; 25:2257-2268.
15. Takahashi K, Wall SB, Suzuki H, et al. Clustered O-glycans of IgA1: Defining macro- and micro-heterogeneity by use of electron capture/transfer dissociation. Mol Cell Proteomics 2010; 9:2545-2557.
16. Takahashi K, Smith AD, Poulsen K, et al. Identification of structural isomers in IgA1 hinge-region O-glycosylation using high-resolution mass spectrometry. J Proteome Res 2012; 11:692-702.
17. Tarelli E, Smith AC, Hendry BM, et al. 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 2004; 339:2329-2335.
18. Iwase H, Tanaka A, Hiki Y, et al. Application of matrix-assisted laser desorption ionization time-of-flight mass spectrometry to the analysis of glycopeptide-containing multiple O-linked oligosaccharides. J Chromatogr Biomed Sci Appl 1998; 709:145-149.
19. Mattu TS, Pleass RJ, Willis AC, et al. 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 1998; 273:2260-2272.
20. Renfrow MB, Cooper HJ, Tomana M, et al. Determination of aberrant O-glycosylation in the IgA1 hinge region by electron capture dissociation Fourier transform-ion cyclotron resonance mass spectrometry. J Biol Chem 2005; 280:19136-19145.
21. Renfrow MB, MacKay CL, Chalmers MJ, et al. Analysis of O-glycan heterogeneity in IgA1 myeloma proteins by Fourier transform ion cyclotron resonance mass spectrometry: Implications for IgA nephropathy. Anal Bioanal Chem 2007; 389:1397-1407.
22. Wada Y, Dell A, Haslam SM, et al. Comparison of methods for profiling O-glycosylation: Human Proteome Organisation Human Disease Glycomics/Proteome Initiative multiinstitutional study of IgA1. Mol Cell Proteomics 2010; 9:719-727.
23. Baenziger J, Kornfeld S. Structure of the carbohydrate units of IgA1 immunoglobulin II. Structure of the O-glycosidically linked oligosaccharide units. J Biol Chem 1974; 249:7270-7281.
24. Field MC, Dwek RA, Edge CJ, Rademacher TW. O-linked oligosaccharides from human serum immunoglobulin A1. Biochem Soc Trans 1989; 17:1034-1035.
25. Tomana M, Niedermeier W, Mestecky J, Hammack WJ. The carbohydrate composition of human myeloma IgA. Immunochemistry 1972; 9:933-940.
26. Tomana M, Niedermeier W, Mestecky J, Skvaril F. The differences in carbohydrate composition between the subclasses of IgA immunoglobulins. Immunochemistry 1976; 13:325-328.
27. Tomana M, Niedermeier W, Spivey C. Microdetermination of monosaccharide in glycoproteins. Anal Biochem 1978; 89:110-118.
28. Andre PM, Le Pogamp P, Chevet D. Impairment of jacalin binding to serum IgA in IgA nephropathy. J Clin Lab Anal 1990; 4:115-119.
29. Mestecky J, Tomana M, Crowley-Nowick PA, et al. Defective galactosylation and clearance of IgA1 molecules as a possible etiopathogenic factor in IgA nephropathy. Contrib Nephrol 1993; 104:172-182.
30. Allen AC, Harper SJ, Feehally J. Galactosylation of N- and O-linked carbohydrate moieties of IgA1 and IgG in IgA nephropathy. Clin Exp Immunol 1995; 100:470-474.
31. Moldoveanu Z, Wyatt RJ, Lee J, et al. Patients with IgA nephropathy have increased serum galactose-deficient IgA1 levels. Kidney Int 2007; 71:1148-1154.
32. Tomana M, Matousovic K, Julian BA, et al. Galactose-deficient IgA1 in sera of IgA nephropathy patients is present in complexes with IgG. Kidney Int 1997; 52:509-516.
33. Smith AC, de Wolff JF, Molyneux K, et al. O-Glycosylation of serum IgD in IgA nephropathy. J Am Soc Nephrol 2006; 17:1192-1199.
34. Wada Y, Tajiri M, Ohshima S. Quantitation of saccharide compositions of O-glycans by mass spectrometry of glycopeptides and its application to rheumatoid arthritis. J Proteome Res 2010; 9:1367-1373.
35. Tomana M, Novak J, Julian BA, et al. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J Clin Invest 1999; 104:73-81.
36. Berthoux F, Suzuki H, Thibaudin L, et al. Autoantibodies targeting galactosedeficient IgA1 associate with progression of IgA nephropathy. J Am Soc Nephrol 2012; 23:1579-1587.
37. Suzuki H, Moldoveanu Z, Hall S, et al. IgA1-secreting cell lines from patients with IgA nephropathy produce aberrantly glycosylated IgA1. J Clin Invest 2008; 118:629-639.
38. Suzuki H, Fun R, Zhang Z, et al. Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J Clin Invest 2009; 119:1668-1677.
39. Novak J, Julian BA, Mestecky J, Renfrow MB. Glycosylation of IgA1 and pathogenesis of IgA nephropathy. Semin Immunopathol 2012; 34:365-382.
40. Moore JS, Kulhavy R, Tomana M, et al. Reactivities of N-acetylgalactosaminespecific lectins with human IgA1 proteins. Mol Immunol 2007; 44:2598-2604.
41. Novak J, Tomana M, Kilian M, et al. Heterogeneity of O-glycosylation in the hinge region of human IgA1. Mol Immunol 2000; 37:1047-1056.
42. Rebecchi KR, Wenke JL, Go EP, Desaire H. Label-free quantitation: a new glycoproteomics approach. J Am Soc Mass Spectrom 2009; 20:1048-1059.
43. Novak J, Vu HL, Novak L, et al. Interactions of human mesangial cells with IgA and IgA-containing circulating immune complexes. Kidney Int 2002; 62:465-475.
44. Novak J, Tomana M, Matousovic K, et al. IgA1-containing immune complexes in IgA nephropathy differentially affect proliferation of mesangial cells. Kidney Int 2005; 67:504-513.
45. Novak J, Moldoveanu Z, Renfrow MB, et al. IgA nephropathy and Henoch-Schoenlein purpura nephritis: aberrant glycosylation of IgA1, formation of IgA1-containing immune complexes, and activation of mesangial cells. Contrib Nephrol 2007; 157:134-138.
46. Novak J, Mestecky J. IgA Immune-complex. In: Lai KN, editor. Recent advances in IgA nephropathy. London, UK: Imperial College Press and the World Scientific Publisher; 2009. pp. 177-191.
47. Novak J, Raskova Kafkova L, Suzuki H, et al. IgA1 immune complexes from pediatric patients with IgA nephropathy activate cultured mesangial cells. Nephrol Dial Transplant 2011; 26:3451-3457.
48. Moura IC, Arcos-Fajardo M, Sadaka C, et al. Glycosylation and size of IgA1 are essential for interaction with mesangial transferrin receptor in IgA nephropathy. J Am Soc Nephrol 2004; 15:622-634.
49. Leung JC, Tsang AW, Chan LY, et al. Size-dependent binding of IgA to HepG2, U937, and human mesangial cells. J Lab Clin Med 2002; 140:398-406.
50. Leung JC, Tang SC, Chan LY, et al. Synthesis of TNF-α by mesangial cells cultured with polymeric anionic IgA: role of MAPK and NF-κB. Nephrol Dial Transplant 2008; 23:72-81.
51. Bene MC, Faure GC. Mesangial IgA in IgA nephropathy arises from the mucosa. Am J Kidney Dis 1988; 12:406-409.
52. Bene MC, Hurault De Ligny B, Kessler M, Faure GC. Confirmation of tonsillar anomalies in IgA nephropathy: a multicenter study. Nephron 1991; 58:425-428.
53. Smith AC, Molyneux K, Feehally J, Barratt J. O-Glycosylation of serum IgA1 antibodies against mucosal and systemic antigens in IgA nephropathy. J Am Soc Nephrol 2006; 17:3520-3528.
54. Suzuki H, Suzuki Y, Narita I, et al. Toll-like receptor 9 affects severity of IgA nephropathy. J Am Soc Nephrol 2008; 19:2384-2395.
55. Feehally J, Farrall M, Boland A, et al. HLA has strongest association with IgA nephropathy in genome-wide analysis. J Am Soc Nephrol 2010; 21:1791-1797.
56. Gharavi AG, Kiryluk K, Choi M, et al. Genome-wide association study identifies susceptibility loci for IgA nephropathy. Nat Genet 2011; 43:321-327.
57. Beerman I, Novak J, Wyatt RJ, et al. Genetics of IgA nephropathy. Nat Clin Pract Nephrol 2007; 3:325-338.
58. Gharavi AG, Yan Y, Scolari F, et al. IgA nephropathy, the most common cause of glomerulonephritis, is linked to 6q22-23. Nature Genet 2000; 26:354-357.
59. Gharavi AG, Moldoveanu Z, Wyatt RJ, et al. Aberrant IgA1 glycosylation is inherited in familial and sporadic IgA nephropathy. J Am Soc Nephrol 2008; 19:1008-1014.
60. Izzi C, Sanna-Cherchi S, Prati E, et al. Familial aggregation of primary glomerulonephritis in an Italian population isolate: Valtrompia study. Kidney Int 2006; 69:1033-1040.
61. Karnib HH, Sanna-Cherchi S, Zalloua PA, et al. Characterization of a large Lebanese family segregating IgA nephropathy. Nephrol Dial Transplant 2007; 22:772-777.
62. Kiryluk K, Moldoveanu Z, Sanders JT, et al. Aberrant glycosylation of IgA1 is inherited in both pediatric IgA nephropathy and Henoch-Schö nlein purpura nephritis. Kidney Int 2011; 80:79-87.
63. Lavigne KA, Woodford SY, Barker CV, et al. Familial IgA nephropathy in southeastern Kentucky. Clin Nephrol 2010; 73:115-121.
64. Novak J, Julian BA, Tomana M, Mestecky J. Progress in molecular and genetic studies of IgA nephropathy. J Clin Immunol 2001; 21:310-327.
65. Gomez-Guerrero C, Alonso J, Lopez-Armada MJ, et al. Potential factors governing extracellular matrix production by mesangial cells: their relevance for the pathogenesis of IgA nephropathy. Contrib Nephrol 1995; 111:45-54.
66. Yanagihara T, Brown R, Hall S, et al. In vitro-formed immune complexes containing galactose-deficient IgA1 stimulate proliferation of mesangial cells. Results Immunol 2012; 2:166-172.
67. Moura IC, Centelles MN, Arcos-Fajardo M, et al. Identification of the transferrin receptor as a novel immunoglobulin (Ig)A1 receptor and its enhanced expression on mesangial cells in IgA nephropathy. J Exp Med 2001; 194:417-425.
68. Matysiak-Budnik T, Moura IC, Arcos-Fajardo M, et al. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J Exp Med 2008; 205:143-154.
69. Kanamaru Y, Arcos-Fajardo M, Moura IC, et al. Fca receptor I activation induces leukocyte recruitment and promotes aggravation of glomerulonephritis through the FcRg adaptor. Eur J Immunol 2007; 37:1116-1128.
70. Moura IC, Arcos-Fajardo M, Gdoura A, et al. Engagement of transferrin receptor by polymeric IgA1: evidence for a positive feedback loop involving increased receptor expression and mesangial cell proliferation in IgA nephropathy. J Am Soc Nephrol 2005; 16:2667-2676.
71. Kaneko Y, Otsuka T, Tsuchida Y, et al. Integrin a1/b1 and a2/b1 as a receptor for IgA1 in human glomerular mesangial cells in IgA nephropathy. Int Immunol 2012; 24:219-232.
72. Tamouza H, Chemouny J, Raskova Kafkova L, et al. IgA1 immune complexmediated activation of MAPK/ERK kinase pathway in mesangial cells is associated with glomerular damage in IgA nephropathy. Kidney Int 2012; 82:1284-1296.
73. Huang ZQ, Anderson J, Rohrbach TD, et al. Characterization of signaling pathways in cultured human mesangial cells induced by IgA1-containing immune complexes from patients with IgA nephropathy. J Am Soc Nephrol 2012; 23:824A.
74. Julian BA, Quiggins PA, Thompson JS, et al. Familial IgA nephropathy. Evidence of an inherited mechanism of disease. N Engl J Med 1985; 312:202-208.
75. Yamada K, Raska M, Moldoveanu Z, et al. Effect of gp130 cytokines on IgA1-producing cells from patients with IgA nephropathy. J Am Soc Nephrol 2011; 22:625A.
76. Kiryluk K, Li Y, Sanna-Cherchi S, et al. Geographic differences in genetic susceptibility to IgA nephropathy: GWAS replication study and geospatial risk analysis. PLoS Genet 2012; 8:e1002765.
77. Yu XQ, Li M, Zhang H, et al. A genome-wide association study in Han Chinese identifies multiple susceptibility loci for IgA nephropathy. Nat Genet 2011; 44:178-182.
78. McCarthy DD, Kujawa J, Wilson C, et al. Mice overexpressing BAFF develop a commensal flora-dependent, IgA-associated nephropathy. J Clin Invest 2011; 121:3991-4002.
79. Cattran DC, Coppo R, Cook HT, et al. The Oxford classification of IgA nephropathy: rationale, clinicopathological correlations, and classification. Kidney Int 2009; 76:534-545.
80. Coppo R, Troyanov S, Camilla R, et al. The Oxford IgA nephropathy clinicopathological classification is valid for children as well as adults. Kidney Int 2010; 77:921-927.
81. Herzenberg AM, Fogo AB, Reich HN, et al. Validation of the Oxford classification of IgA nephropathy. Kidney Int 2011; 80:310-317.
82. Roberts IS, Cook HT, Troyanov S, et al. The Oxford classification of IgA nephropathy: pathology definitions, correlations, and reproducibility. Kidney Int 2009; 76:546-556.
83. Berthoux F, Mohey H, Laurent B, et al. Predicting the risk for dialysis or death in IgA nephropathy. J Am Soc Nephrol 2011; 22:752-761.
84. Muda AO, Feriozzi S, Rahimi S, Faraggiana T. Spatial arrangement of IgA and C3 as a prognostic indicator of IgA nephropathy. J Pathol 1995; 177:201-208.
85. Bellur SS, Troyanov S, Cook HT, Roberts IS. Immunostaining findings in IgA nephropathy: correlation with histology and clinical outcome in the Oxford classification patient cohort. Nephrol Dial Transplant 2011; 26:2533-2536.
86. Wada Y, Ogata H, Takeshige Y, et al. Clinical significance of IgG deposition in the glomerular mesangial area in patients with IgA nephropathy. Clin Exp Nephrol 2013; 17:73-82.
87. Nieuwhof C, Kruytzer M, Frederiks P, van Breda Vriesman PJC. Chronicity index and mesangial IgG deposition are risk factors for hypertension and renal failure in early IgA nephropathy. Am J Kidney Dis 1998; 31:962-970.
88. Gomes MM, Suzuki H, Brooks MT, et al. Recognition of galactose-deficient O-glycans in the hinge region of IgA1 by N-acetylgalactosamine-specific snail lectins: a comparative binding study. Biochemistry 2010; 49:5671-5682.
89. Zhao N, Hou P, Lv J, et al. The level of galactose-deficient IgA1 in the sera of patients with IgA nephropathy is associated with disease progression. Kidney Int 2012; 82:790-796.
90. Eison TM, Hastings MC, Moldoveanu Z, et al. Association of IgG codeposition with serum levels of galactose-deficient IgA1 in pediatric IgA nephropathy. Clin Nephrol 2012; 78:465-469.
91. Fliser D, Novak J, Thongboonkerd V, et al. Advances in urinary proteome analysis and biomarker discovery. J Am Soc Nephrol 2007; 18:1057-1071.
92. Mischak H, Coon JJ, Novak J, et al. Capillary electrophoresis-mass spectrometry as a powerful tool in biomarker discovery and clinical diagnosis: an update of recent developments. Mass Spectrom Rev 2009; 28:703-724.
93. Julian BA, Suzuki H, Spasovski G, et al. Application of proteomic analysis to renal disease in the clinic. Proteomics Clin Appl 2009; 3:1023-1028.
94. Good DM, Zurbig P, Argiles A, et al. Naturally occurring human urinary peptides for use in diagnosis of chronic kidney disease. Mol Cell Proteomics 2010; 9:2424-2437.
95. Haubitz M, Mischak H, Julian BA, Novak J. Urinary protein patterns as a diagnostic tool in patients with IgA nephropathy. In European Renal Disease - Touch Briefings 2007. European Renal Disease; 2007 pp. 12-13.
96. Julian BA, Wittke S, Novak J, et al. Electrophoretic methods for analysis of urinary polypeptides in IgA-associated renal diseases. Electrophoresis 2007; 28:4469-4483.
97. Mischak H, Allmaier G, Apweiler R, et al. Recommendations for biomarker identification and qualification in clinical proteomics. Sci Transl Med 2010; 2:46s42.
98. Mischak H, Kolch W, Aivaliotis M, et al. Comprehensive human urine standards for comparability and standardization in clinical proteome analysis. Proteomics Clin Appl 2010; 4:464-478.
99. Mischak H, Ioannidis JP, Argiles A, et al. Implementation of proteomic biomarkers: making it work. Eur J Clin Invest 2012; 42:1027-1036.
100. Rossing K, Mischak H, Dakna M, et al. Urinary proteomics in diabetes and CKD. J Am Soc Nephrol 2008; 19:1283-1290.