O-glycosylated IgA rheumatoid factor induces IgA deposits and glomerulonephritis

Journal of the American Society of Nephrology

Volumn 23, Issue 3, 2012, Pages 438-446

  Otani, Masako ^a   Nakata, Junichiro ^b   Kihara, Masao ^b   Leroy, Valérie ^a   Moll, Solange ^a   Wada, Yoshinao ^c   Izui, Shozo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN A1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2A RHEUMATOID FACTOR; RHEUMATOID FACTOR; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; BINDING AFFINITY; GLOMERULONEPHRITIS; HYBRIDOMA; IMMUNOGLOBULIN BLOOD LEVEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION;

EID: 84857972884     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2011070701     Document Type: Article

References (39)

1. Donadio JV, Grande JP: IgA nephropathy. N Engl J Med 347: 738-748, 2002 (Pubitemid 35203906)
2. Czerkinsky C, Koopman WJ, Jackson S, Collins JE, Crago SS, Schrohenloher RE, Julian BA, Galla JH, Mestecky J: Circulating immune complexes and IgA rheumatoid factor in patients with mesangial IgA nephropathies. J Clin Invest 77: 1931-1938, 1986 (Pubitemid 16062650)
3. Baenziger J, Kornfeld S: Structure of the carbohydrate units of IgA1 immunoglobulin. II. Structure of the O-glycosidically linked oligosaccharide units. J Biol Chem 249: 7270-7281, 1974
4. Tomana M, Novak J, Julian BA, Matousovic K, Konecny K, Mestecky J: Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J Clin Invest 104: 73-81, 1999 (Pubitemid 29534347)
5. Allen AC, Bailey EM, Barratt J, Buck KS, Feehally J: Analysis of IgA1 Oglycans in IgA nephropathy by fluorophore-assisted carbohydrate electrophoresis. J Am Soc Nephrol 10: 1763-1771, 1999 (Pubitemid 29364675)
6. Hiki Y, Odani H, Takahashi M, Yasuda Y, Nishimoto A, Iwase H, Shinzato T, Kobayashi Y, Maeda K: Mass spectrometry proves under-O-glycosylation of glomerular IgA1 in IgA nephropathy. Kidney Int 59: 1077-1085, 2001 (Pubitemid 32206870)
7. Allen AC, Bailey EM, Brenchley PE, Buck KS, Barratt J, Feehally J: Mesangial IgA1 in IgA nephropathy exhibits aberrant O-glycosylation: Observations in three patients. Kidney Int 60: 969-973, 2001 (Pubitemid 34205796)
8. Young NM, Jackson GE, Brisson JR: The glycopeptides of the mouse immunoglobulin A T15. Mol Immunol 27: 1083-1090, 1990 (Pubitemid 20382045)
9. Lipniunas P, Grönberg G, Krotkiewski H, Angel AS, Nilsson B: Investigation of the structural heterogeneity in the carbohydrate portion of a mouse monoclonal immunoglobulin A antibody. Arch Biochem Biophys 300: 335-345, 1993 (Pubitemid 23225755)
10. Mattu TS, Pleass RJ, Willis AC, Kilian M, Wormald MR, Lellouch AC, Rudd PM, Woof JM, Dwek RA: The glycosylation and structure of human serum IgA1, Fab, and Fc regions andthe role of N-glycosylation on Fc a receptor interactions. J Biol Chem273: 2260-2272, 1998 (Pubitemid 28069279)
11. Wada Y, Tajiri M, Ohshima S: Quantitation of saccharide compositions of O-glycans bymass spectrometry of glycopeptides and its application to rheumatoid arthritis. J Proteome Res 9: 1367-1373, 2010
12. Phillips-Quagliata JM: Mouse IgA allotypes have major differences in their hinge regions. Immunogenetics 53: 1033-1038, 2002
13. Robinson EA, Appella E: Complete amino acid sequence of a mouse immunoglobulin a chain (MOPC 511). Proc Natl Acad Sci U S A 77: 4909-4913, 1980
14. Kobayashi I, Nogaki F, Kusano H, Ono T, Miyawaki S, Yoshida H, Muso E: Interleukin-12 alters the physicochemical characteristics of serum and glomerular IgA and modifies glycosylation in a ddY mouse strain having high IgA levels. Nephrol Dial Transplant 17: 2108-2116, 2002 (Pubitemid 35446665)
15. Marquina R, Díez MA, López-Hoyos M, Buelta L, Kuroki A, Kikuchi S, Villegas J, Pihlgren M, Siegrist CA, Arias M, Izui S, Merino J, Merino R: Inhibition of B cell death causes the development of an IgA nephropathy in (New Zealand white x C57BL/6)F1-bcl-2 transgenic mice. J Immunol 172: 7177-7185, 2004 (Pubitemid 38669162)
16. Nishie T, Miyaishi O, Azuma H, Kameyama A, Naruse C, Hashimoto N, Yokoyama H, Narimatsu H, Wada T, Asano M: Development of immunoglobulin A nephropathy-like disease in b-1,4-galactosyltransferase- I-deficient mice. Am J Pathol 170: 447-456, 2007 (Pubitemid 47339382)
17. Lemoine R, Berney T, Shibata T, Fulpius T, Gyotoku Y, Shimada H, Sawada S, Izui S: Induction of "wire-loop" lesions by murine monoclonal IgG3 cryoglobulins. Kidney Int 41: 65-72, 1992
18. Fulpius T, Spertini F, Reininger L, Izui S: Immunoglobulin heavy chain constant region determines the pathogenicity and the antigen-binding activity of rheumatoid factor. Proc Natl Acad Sci U S A 90: 2345-2349, 1993 (Pubitemid 23078623)
19. Abdelmoula M, Spertini F, Shibata T, Gyotoku Y, Luzuy S, Lambert PH, Izui S: IgG3 is themajor source of cryoglobulins inmice. J Immunol 143: 526-532, 1989 (Pubitemid 19191547)
20. Oida E, Nogaki F, Kobayashi I, Kamata T, Ono T, Miyawaki S, Serikawa T, Yoshida H, Kita T, Muso E: Quantitative trait loci (QTL) analysis reveals a close linkage between the hinge region and trimeric IgA dominancy in a high IgA strain (HIGA) of ddY mice. Eur J Immunol 34: 2200-2208, 2004 (Pubitemid 39256101)
21. Kornfeld R, Kornfeld S: Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54: 631-664, 1985 (Pubitemid 15073660)
22. Baudino L, Fossati-Jimack L, Chevalley C, Martinez-Soria E, Shulman MJ, Izui S: IgM and IgA anti-erythrocyte autoantibodies induce anemia in a mouse model through multivalency-dependent hemagglutination but not through complement activation. Blood 109: 5355-5362, 2007 (Pubitemid 46890557)
23. Sinico RA, Fornasieri A, Oreni N, Benuzzi S, D'Amico G: Polymeric IgA rheumatoid factor in idiopathic IgA mesangial nephropathy (Berger's disease). J Immunol 137: 536-541, 1986 (Pubitemid 16045079)
24. Suzuki H, Suzuki Y, Aizawa M, Yamanaka T, Kihara M, Pang H, Horikoshi S, Tomino Y: Th1 polarization in murine IgA nephropathy directed by bone marrow-derived cells. Kidney Int 72: 319-327, 2007 (Pubitemid 47172373)
25. Suzuki H, Fan R, Zhang Z, Brown R, Hall S, Julian BA, Chatham WW, Suzuki Y, Wyatt RJ, Moldoveanu Z, Lee JY, Robinson J, Tomana M, Tomino Y, Mestecky J, Novak J: Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J Clin Invest 119: 1668-1677, 2009
26. Iwasaki H, Zhang Y, Tachibana K, Gotoh M, Kikuchi N, Kwon YD, Togayachi A, Kudo T, Kubota T, Narimatsu H: Initiation of O-glycan synthesis in IgA1 hinge region is determined by a single enzyme, UDP-N-acetyl-α-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase 2. J Biol Chem 278: 5613-5621, 2003 (Pubitemid 36800803)
27. Ronet C, Hauyon-La Torre Y, Revaz-Breton M, Mastelic B, Tacchini- Cottier F, Louis J, Launois P: Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J Immunol 184: 886-894, 2010
28. Wessels MR, Butko P, Ma M, Warren HB, Lage AL, Carroll MC: Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci U S A 92: 11490-11494, 1995 (Pubitemid 26014139)
29. Reininger L, Berney T, Shibata T, Spertini F, Merino R, Izui S: Cryoglobulinemia induced by a murine IgG3 rheumatoid factor: Skin vasculitis and glomerulonephritis arise from distinct pathogenic mechanisms. Proc Natl Acad Sci U S A 87: 10038-10042, 1990 (Pubitemid 120016580)
30. Neuberger MS: Expression and regulation of immunoglobulin heavy chain gene transfected into lymphoid cells. EMBO J 2: 1373-1378, 1983
31. Simon T, Rajewsky K: 'Enhancer-constitutive' vectors for the expression of recombinant antibodies. Nucleic Acids Res 16: 354, 1988
32. Nishida Y, Kataoka T, Ishida N, Nakai S, Kishimoto T, Böttcher I, Honjo T: Cloning ofmouse immunoglobulin " gene and its location within the heavy chain gene cluster. Proc NatlAcad Sci USA78: 1581-1585, 1981 (Pubitemid 11112168)
33. Gyotoku Y, Abdelmoula M, Spertini F, Izui S, Lambert PH: Cryoglobulinemia induced by monoclonal immunoglobulin G rheumatoid factors derived from autoimmune MRL/MpJ-lpr/lpr mice. J Immunol 138: 3785-3792, 1987 (Pubitemid 17078251)
34. Wolfowicz CB, Sakorafas P, Rothstein TL, Marshak-Rothstein A: Oligoclonality of rheumatoid factors arising spontaneously in lpr/lpr mice. Clin Immunol Immunopathol 46: 382-395, 1988 (Pubitemid 18081932)
35. Fossati-Jimack L, Reininger L, Chicheportiche Y, Clynes R, Ravetch JV, Honjo T, Izui S: High pathogenic potential of low-affinity autoantibodies in experimental autoimmune hemolytic anemia. J Exp Med 190: 1689-1696, 1999 (Pubitemid 30002350)
36. Trendelenburg M, Fossati-Jimack L, Cortes-Hernandez J, Turnberg D, Lewis M, Izui S, Cook HT, Botto M: The role of complement in cryoglobulin-induced immune complex glomerulonephritis. J Immunol 175: 6909-6914, 2005 (Pubitemid 41598936)
37. Berney T, Fulpius T, Shibata T, Reininger L, Van Snick J, Shan H, Weigert M, Marshak-Rothstein A, Izui S: Selective pathogenicity of murine rheumatoid factors of the cryoprecipitable IgG3 subclass. Int Immunol 4: 93-99, 1992
38. Orlandi R, Güssow DH, Jones PT, Winter G: Cloning immunoglobulin variable domains for expression by the polymerase chain reaction. Proc Natl Acad Sci U S A 86: 3833-3837, 1989 (Pubitemid 19141839)
39. Wada Y, Dell A, Haslam SM, Tissot B, Canis K, Azadi P, Bäckström M, Costello CE, Hansson GC, Hiki Y, Ishihara M, Ito H, Kakehi K, Karlsson N, Hayes CE, Kato K, Kawasaki N, Khoo KH, Kobayashi K, Kolarich D, Kondo A, Lebrilla C, Nakano M, Narimatsu H, Novak J, Novotny MV, Ohno E, Packer NH, Palaima E, Renfrow MB, Tajiri M, Thomsson KA, Yagi H, Yu SY, Taniguchi N: Comparison of methods for profiling O-glycosylation: Human Proteome Organisation Human Disease Glycomics/Proteome Initiative multi-institutional study of IgA1. Mol Cell Proteomics 9: 719-727, 2010