Development of immunoglobulin A nephropathy-like disease in β-1,4-galactosyltransferase-I-deficient mice

American Journal of Pathology

Volumn 170, Issue 2, 2007, Pages 447-456

  Nishie, Toshikazu ^a   Miyaishi, Osamu ^b   Azuma, Haruhito ^c   Kameyama, Akihiko ^d   Naruse, Chie ^a   Hashimoto, Noriyoshi ^a   Yokoyama, Hitoshi ^a   Narimatsu, Hisashi ^d   Wada, Takashi ^a   Asano, Masahide ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c OSAKA MEDICAL COLLEGE   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,4 GALACTOSYLTRANSFERASE 1; COMPLEMENT COMPONENT C3; GALACTOSAMINE; GALACTOSE; GALACTOSYLTRANSFERASE; GLYCAN DERIVATIVE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; N GLYCAN; O GLYCAN; POLYMER; UNCLASSIFIED DRUG; BETA 1,4 GALACTOSYLTRANSFERASE I; BETA-1,4-GALACTOSYLTRANSFERASE I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEXOSE TRANSPORT; IMMUNOGLOBULIN A NEPHROPATHY; IMMUNOGLOBULIN BLOOD LEVEL; KIDNEY DYSFUNCTION; MESANGIUM; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; ANIMAL; ENZYMOLOGY; GENETICS; GLYCOSYLATION; HUMAN; KIDNEY FAILURE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN PROCESSING;

ANIMALS; GALACTOSYLTRANSFERASES; GLOMERULONEPHRITIS, IGA; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN A; KIDNEY FAILURE; MICE; MICE, KNOCKOUT; PROTEIN MODIFICATION, TRANSLATIONAL;

EID: 33947538270     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.060559     Document Type: Article

References (52)

1. Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW: Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat Med 2000, 6:306-312
2. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M, Inazu T, Mitsuhashi H, Takahashi S, Takeuchi M, Herrmann R, Straub V, Talim B, Voit T, Topaloglu H, Toda T, Endo T: Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 2001, 1:717-724
3. Chui D, Oh-Eda M, Liao YF, Panneerselvam K, Lal A, Marek KW, Freeze HH, Moremen KW, Fukuda MN, Marth JD: Alpha-mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 1997, 90:157-167
4. Wagner R, Matrosovich M, Klenk HD: Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 2002, 12:159-166
5. Kawakubo M, Ito Y, Okimura Y, Kobayashi M, Sakura K, Kasama S, Fukuda MN, Fukuda M, Katsuyama T, Nakayama J: Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 2004, 305:1003-1006
6. Nagamune K, Acosta-Serrano A, Uemura H, Brun R, Kunz-Renggli C, Maeda Y, Ferguson MA, Kinoshita T: Surface sialic acids taken from the host allow trypanosome survival in tsetse fly vectors. J Exp Med 2004, 199:1445-1450
7. Aebi M, Helenius A, Schenk B, Barone R, Fiumara A, Berger EG, Hennet T, Imbach T, Stutz A, Bjursell C, Uller A, Wahlstrom JG, Briones P, Cardo E, Clayton P, Winchester B, Cormier-Dalre V, de Lonlay P, Cuer M, Dupre T, Seta N, de Koning T, Dorland L, de Loos F, Kupers L, Fabritz L, Hasilik M, Marquardt T, Niehues R, Freeze H, Grünewald S, Heykants L, Jaeken J, Matthijs G, Schollen E, Keir xKeir G, Kjaergaard S, Schwartz M, Skovby F, Klein A, Roussel P, Körner C, Lübke T, Thiel C, von Figura K, Koscielak J, Krasnewich D, Lehle L, Peters V, Raab M, Saether O, Schachter H, Van Schaftingen E, Verbert A, Vilaseca A, Wevers R, Yamashita K: Carbohydrate-deficient glycoprotein syndromes become congenital disorders of glycosylation: an updated nomenclature for CDG. First International Workshop on CDGS. Glycoconj J 1999, 16:669-671
8. Hennet T: The galactosyltransferase family. Cell Mol Life Sci 2002, 59:1081-1095
9. Narimatsu H, Sinha S, Brew K, Okayama H, Qasba PK: Cloning and sequencing of cDNA of bovine N-acetylglucosamine (beta 1-4)galactosyltransferase. Proc Natl Acad Sci USA 1986, 83:4720-4724
10. Humphreys-Beher MG, Bunnell B, vanTuinen P, Ledbetter DH, Kidd VJ: Molecular cloning and chromosomal localization of human 4-beta- galactosyltransferase. Proc Natl Acad Sci USA 1986, 83:8918-8922
11. Shaper NL, Hollis GF, Douglas JG, Kirsch IR, Shaper JH: Characterization of the full length cDNA for murine beta-1,4-galactosyltransferase. Novel features at the 5′-end predict two translations start sites at two in-frame AUGs. J Biol Chem 1988, 263:10420-10428
12. Asano M, Furukawa K, Kido M, Matsumoto S, Umesaki Y, Kochibe N, Iwakura Y: Growth retardation and early death of beta-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO J 1997, 16:1850-1857
13. Lu Q, Hasty P, Shur BD: Targeted mutation in beta1,4- galactosyltransferase leads to pituitary insufficiency and neonatal lethality. Dev Biol 1997, 181:257-267
14. Asano M, Nakae S, Kotani N, Shirafuji N, Nambu A, Hashimoto N, Kawashima H, Hirose M, Miyasaka M, Takasaki S, Iwakura Y: Impaired selectin-ligand biosynthesis and reduced inflammatory responses in beta-1,4- galactosyltransferase-I-deficient mice. Blood 2003, 102:1678-1685
15. Mori R, Kondo T, Nishie T, Ohshima T, Asano M: Impairment of skin wound healing in beta-1,4-galactosyltransferase-deficient mice with reduced leukocyte recruitment. Am J Pathol 2004, 164:1303-1314
16. D'Amico G: The commonest glomerulonephritis in the world: IgA nephropathy. Q J Med 1987, 64:709-727
17. Galla JH: IgA nephropathy. Kidney Int 1995, 47:377-387
18. Russell MW, Mestecky J, Julian BA, Galla JH: IgA-associated renal diseases: antibodies to environmental antigens in sera and deposition of immunoglobulins and antigens in glomeruli. J Clin Immunol 1986, 6:74-86
19. Floege J, Feehally J: IgA nephropathy: recent developments. J Am Soc Nephrol 2000, 11:2395-2403
20. Mestecky J, Tomana M, Crowley-Nowick PA, Moldoveanu Z, Julian BA, Jackson S: Defective galactosylation and clearance of IgA1 molecules as a possible etiopathogenic factor in IgA nephropathy. Contrib Nephrol 1993, 104:172-182
21. Allen AC, Bailey EM, Barratt J, Buck KS, Feehally J: Analysis of IgA1 O-glycans in IgA nephropathy by fluorophore-assisted carbohydrate electrophoresis. J Am Soc Nephrol 1999, 10:1763-1771
22. 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 2001, 60:969-973
23. 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 2001, 59:1077-1085
24. Odani H, Hiki Y, Takahashi M, Nishimoto A, Yasuda Y, Iwase H, Shinzato T, Maeda K: 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 2000, 271:268-274
25. Ando Y, Moriyama T, Miyazaki M, Akagi Y, Kawada N, Isaka Y, Izumi M, Yokoyama K, Yamauchi A, Horio M, Ando A, Ueda N, Sobue K, Imai E, Hori M: Enhanced glomerular expression of caldesmon in IgA nephropathy and its suppression by glucocorticoid-heparin therapy. Nephrol Dial Transplant 1998, 13:1168-1175
26. Wada T, Tomosugi N, Naito T, Yokoyama H, Kobayashi K, Harada A, Mukaida N, Matsushima K: Prevention of proteinuria by the administration of anti-interleukin 8 antibody in experimental acute immune complex-induced glomerulonephritis. J Exp Med 1994, 180:1135-1140
27. Klein-Schneegans AS, Gaveriaux C, Fonteneau P, Loor F: Indirect double sandwich ELISA for the specific and quantitative measurement of mouse IgM, IgA and IgG subclasses. J Immunol Methods 1989, 119:117-125
28. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685
29. Suzuki N, Khoo KH, Chen CM, Chen HC, Lee YC: N-glycan structures of pigeon IgG: a major serum glycoprotein containing Galalpha1-4 Gal termini. J Biol Chem 2003, 278:46293-46306
30. Maeda A, Gohda T, Funabiki K, Horikoshi S, Shirato I, Tomino Y: Significance of serum IgA levels and serum IgA/C3 ratio in diagnostic analysis of patients with IgA nephropathy. J Clin Lab Anal 2003, 17:73-76
31. Lipniunas P, Gronberg 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 1993, 300:335-345
32. Harvey DJ: Matrix-assisted laser desorption/ionization mass spectrometry of carbohydrates. Mass Spectrom Rev 1999, 18:349-450
33. Wada T, Yokoyama H, Tomosugi N, Hisada Y, Ohta S, Naito T, Kobayashi K, Mukaida N, Matsushima K: Detection of urinary interleukin-8 in glomerular diseases. Kidney Int 1994, 46:455-460
34. Zheng F, Kundu GC, Zhang Z, Ward J, DeMayo F, Mukherjee AB: Uteroglobin is essential in preventing immunoglobulin A nephropathy in mice. Nat Med 1999, 5:1018-1025
35. Launay P, Grossetete B, Arcos-Fajardo M, Gaudin E, Torres SP, Beaudoin L, Patey-Mariaud de Serre N, Lehuen A, Monteiro RC: Fcalpha receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease). Evidence for pathogenic soluble receptor-IgA complexes in patients and CD89 transgenic mice. J Exp Med 2000, 191:1999-2009
36. Wang J, Anders RA, Wu Q, Peng D, Cho JH, Sun Y, Karaliukas R, Kang HS, Turner JR, Fu YX: Dysregulated LIGHT expression on T cells mediates intestinal inflammation and contributes to IgA nephropathy. J Clin Invest 2004, 113:826-835
37. Chui D, Sellakumar G, Green R, Sutton-Smith M, McQuistan T, Marek K, Morris H, Dell A, Marth J: Genetic remodeling of protein glycosylation in vivo induces autoimmune disease. Proc Natl Acad Sci USA 2001, 98:1142-1147
38. Chuang PD, Morrison SL: Elimination of N-linked glycosylation sites from the human IgA1 constant region: effects on structure and function. J Immunol 1997, 158:724-732
39. Royle L, Roos A, Harvey DJ, Wormald MR, van Gijlswijk-Janssen D, Redwan el RM, Wilson IA, Daha MR, Dwek RA, Rudd PM: Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J Biol Chem 2003, 278:20140-20153
40. Rifai A, Small Jr PA, Teague PO, Ayoub EM: Experimental IgA nephropathy. J Exp Med 1979, 150:1161-1173
41. Miyawaki S, Muso E, Takeuchi E, Matsushima H, Shibata Y, Sasayama S, Yoshida H: Selective breeding for high serum IgA levels from noninbred ddY mice: isolation of a strain with an early onset of glomerular IgA deposition. Nephron 1997, 76:201-207
42. 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 2002, 17:2108-2116
43. Marquina R, Diez MA, Lopez-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)F(1)-bcl-2 transgenic mice. J Immunol 2004, 172:7177-7185
44. Smith AC, Feehally J: New insights into the pathogenesis of IgA nephropathy. Pathogenesis of IgA nephropathy. Springer Semin Immunopathol 2003, 24:477-493
45. 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 and the role of N-glycosylation on Fc alpha receptor interactions. J Biol Chem 1998, 273:2260-2272
46. Kokubo T, Hiki Y, Iwase H, Tanaka A, Toma K, Hotta K, Kobayashi Y: Protective role of IgA1 glycans against IgA1 self-aggregation and adhesion to extracellular matrix proteins. J Am Soc Nephrol 1998, 9:2048-2054
47. Sano T, Hiki Y, Kokubo T, Iwase H, Shigematsu H, Kobayashi Y: Enzymatically deglycosylated human IgA1 molecules accumulate and induce inflammatory cell reaction in rat glomeruli. Nephrol Dial Transplant 2002, 17:50-56
48. 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 1999, 104:73-81
49. Young NM, Jackson GE, Brisson JR: The glycopeptides of the mouse immunoglobulin A T15. Mol Immunol 1990, 27:1083-1090
50. Baharaki D, Dueymes M, Perrichot R, Basset C, Le Corre R, Cledes J, Youinou P: Aberrant glycosylation of IgA from patients with IgA nephropathy. Glycoconj J 1996, 13:505-511
51. Amore A, Cirina P, Conti G, Brusa P, Peruzzi L, Coppo R: Glycosylation of circulating IgA in patients with IgA nephropathy modulates proliferation and apoptosis of mesangial cells. J Am Soc Nephrol 2001, 12:1862-1871
52. Hansske B, Thiel C, Lubke T, Hasilik M, Honing S, Peters V, Heidemann PH, Hoffmann GF, Berger EG, von Figura K, Korner C: Deficiency of UDP-galactose:N-acetylglucosamine beta-1,4-galactosyltransferase I causes the congenital disorder of glycosylation type IId. J Clin Invest 2002, 109:725-733