Transglutaminase is essential for IgA nephropathy development acting through IgA receptors

Journal of Experimental Medicine

Volumn 209, Issue 4, 2012, Pages 793-806

  Berthelot, Laureline ^a,b   Papista, Christina ^a,b   Maciel, Thiago T ^a,b   Biarnes Pelicot, Martine ^a,b   Tissandie, Emilie ^a,b   Wang, Pamela H M ^a,b   Tamouza, Houda ^a,b   Jamin, Agnès ^a,b   Bex Coudrat, Julie ^a,b   Gestin, Aurelie ^a,b   Boumediene, Ahmed ^c   Arcos Fajardo, Michelle ^a,b   England, Patrick ^d   Pillebout, Evangéline ^a,b,e   Walker, Francine ^f   Daugas, Eric ^a,b,f   Vrtovsnik, François ^a,b,f   Flamant, Martin ^a,b,f   Benhamou, Marc ^a,b   Cogné, Michel ^c   Moura, Ivan C ^a,b   Monteiro, Renato C ^a,b,f   more..

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF LIMOGES   (France)

^d INSTITUT PASTEUR   (France)

^e SAINT LOUIS HOSPITAL   (France)

^f BICHAT HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD71 ANTIGEN; IMMUNOGLOBULIN A1; IMMUNOGLOBULIN RECEPTOR; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; SOLUBLE CD89 ANTIGEN; UNCLASSIFIED DRUG; FC RECEPTOR; FC(ALPHA) RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; IGA RECEPTOR; IMMUNOGLOBULIN A; LEUKOCYTE ANTIGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TFRC PROTEIN, MOUSE; TRANSFERRIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME INDUCTION; HEMATURIA; HUMAN; HUMAN TISSUE; IMMUNOGLOBULIN A NEPHROPATHY; MESANGIUM; MESANGIUM CELL; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEINURIA; UPREGULATION; ANIMAL; C57BL MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD; GLOMERULONEPHRITIS, IGA; GTP-BINDING PROTEINS; HUMANS; IMMUNOGLOBULIN A; MICE; MICE, INBRED C57BL; RECEPTORS, FC; RECEPTORS, TRANSFERRIN; TRANSGLUTAMINASES;

EID: 84861756076     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112005     Document Type: Article

References (42)

1. Berger, J., H. Yaneva, B. Nabarra, and C. Barbanel. 1975. Recurrence of mesangial deposition of IgA after renal transplantation. Kidney Int. 7:232-241. http://dx.doi.org/10.1038/ki.1975.35
2. Boyd, J.K., and J. Barratt. 2010. Immune complex formation in IgA nephropathy: CD89 a 'saint' or a 'sinner'? Kidney Int. 78:1211-1213. http:// dx.doi.org/10.1038/ki.2010.365
3. Coulon, S., M. Dussiot, D. Grapton, T.T. Maciel, P.H. Wang, C. Callens, M.K. Tiwari, S. Agarwal, A. Fricot, J. Vandekerckhove, et al. 2011. Polymeric IgA1 controls erythroblast proliferation and accelerates erythropoiesis recovery in anemia. Nat. Med. 17:1456-1465. http://dx.doi.org/10.1038/nm .2462
4. De Laurenzi, V., and G. Melino. 2001. Gene disruption of tissue transglutaminase. Mol. Cell. Biol. 21:148-155. http://dx.doi.org/10.1128/MCB.21 .1.148-155.2001
5. Donadio, J.V., and J.P. Grande. 2002. IgA nephropathy. N. Engl. J. Med. 347:738-748. http://dx.doi.org/10.1056/NEJMra020109
6. Duchez, S., R. Amin, N. Cogné, L. Delpy, C. Sirac, V. Pascal, B. Corthésy, and M. Cogné. 2010. Premature replacement of mu with alpha immunoglobulin chains impairs lymphopoiesis and mucosal homing but promotes plasma cell maturation. Proc. Natl. Acad. Sci. USA. 107:3064-3069. http://dx .doi.org/10.1073/pnas.0912393107
7. Fesus, L., and M. Piacentini. 2002. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 27:534-539. http://dx.doi.org/10.1016/S0968-0004(02)02182-5
8. Ganz, T. 2008. Iron homeostasis: fitting the puzzle pieces together. Cell Metab. 7:288-290. http://dx.doi.org/10.1016/j.cmet.2008.03.008
9. Glassock, R.J. 2011. The pathogenesis of IgA nephropathy. Curr. Opin. Nephrol. Hypertens. 20:153-160. http://dx.doi.org/10.1097/MNH .0b013e3283436f5c
10. Grossetête, B., P. Launay, A. Lehuen, P. Jungers, J.F. Bach, and R.C. Monteiro. 1998. Down-regulation of Fc alpha receptors on blood cells of IgA nephropathy patients: evidence for a negative regulatory role of serum IgA. Kidney Int. 53:1321-1335. http://dx.doi.org/10.1046/ j.1523-1755.1998.00885.x
11. Haddad, E., I.C. Moura, M. Arcos-Fajardo, M.A. Macher, V. Baudouin, C. Alberti, C. Loirat, R.C. Monteiro, and M. Peuchmaur. 2003. Enhanced expression of the CD71 mesangial IgA1 receptor in Berger disease and Henoch-Schönlein nephritis: association between CD71 expression and IgA deposits. J. Am. Soc. Nephrol. 14:327-337. http://dx.doi.org/10 .1097/01.ASN.0000046961.04917.83
12. Ikee, R., S. Kobayashi, N. Hemmi, T. Saigusa, T. Namikoshi, M. Yamada, T. Imakiire, Y. Kikuchi, S. Suzuki, and S. Miura. 2007. Involvement of transglutaminase-2 in pathological changes in renal disease. Nephron Clin. Pract. 105:c139-c146. http://dx.doi.org/10.1159/000098646
13. Jacob, L., M.A. Lety, R.C. Monteiro, F. Jacob, J.F. Bach, and D. Louvard. 1987. Altered cell-surface protein(s), crossreactive with DNA, on spleen cells of autoimmune lupic mice. Proc. Natl. Acad. Sci. USA. 84:1361-1363. http://dx.doi.org/10.1073/pnas.84.5.1361
14. Kerr, M.A. 1990. The structure and function of human IgA. Biochem. J. 271:285-296.
15. Launay, P., B. Grossetête, M. Arcos-Fajardo, E. Gaudin, S.P. Torres, L. Beaudoin, N. Patey-Mariaud de Serre, A. Lehuen, and R.C. Monteiro. 2000. Fcα 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. 191:1999-2009. http://dx.doi.org/10.1084/jem.191.11.1999
16. Lebrón, J.A., M.J. Bennett, D.E. Vaughn, A.J. Chirino, P.M. Snow, G.A. Mintier, J.N. Feder, and P.J. Bjorkman. 1998. Crystal structure of the hemochromatosis protein HFE and characterization of its interaction with transferrin receptor. Cell. 93:111-123. http://dx.doi.org/10.1016/ S0092-8674(00)81151-4
17. Lorand, L., and R.M. Graham. 2003. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4:140-156. http://dx.doi.org/10.1038/nrm1014
18. Matysiak-Budnik, T., I.C. Moura, M. Arcos-Fajardo, C. Lebreton, S. Ménard, C. Candalh, K. Ben-Khalifa, C. Dugave, H. Tamouza, G. van Niel, et al. 2008. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J. Exp. Med. 205:143-154. http://dx.doi.org/10.1084/jem.20071204
19. Mestecky, J. 1988. Immunobiology of IgA. Am. J. Kidney Dis. 12:378-383.
20. Monteiro, R.C., and J.G. Van De Winkel. 2003. IgA Fc receptors. Annu. Rev. Immunol. 21:177-204. http://dx.doi.org/10.1146/annurev.immunol.21 .120601.141011
21. Monteiro, R.C., L. Halbwachs-Mecarelli, M.C. Roque-Barreira, L.H. Noel, J. Berger, and P. Lesavre. 1985. Charge and size of mesangial IgA in IgA nephropathy. Kidney Int. 28:666-671. http://dx.doi.org/10.1038/ki.1985.181
22. Monteiro, R.C., I.C. Moura, P. Launay, T. Tsuge, E. Haddad, M. Benhamou, M.D. Cooper, and M. Arcos-Fajardo. 2002. Pathogenic significance of IgA receptor interactions in IgA nephropathy. Trends Mol. Med. 8:464-468. http://dx.doi.org/10.1016/S1471-4914(02)02405-X
23. Moura, I.C., M.N. Centelles, M. Arcos-Fajardo, D.M. Malheiros, J.F. Collawn, M.D. Cooper, and R.C. Monteiro. 2001. 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. 194:417-425. http://dx.doi.org/10.1084/jem.194.4.417
24. Moura, I.C., M. Arcos-Fajardo, C. Sadaka, V. Leroy, M. Benhamou, J. Novak, F. Vrtovsnik, E. Haddad, K.R. Chintalacharuvu, and R.C. Monteiro. 2004a. Glycosylation and size of IgA1 are essential for interaction with mesangial transferrin receptor in IgA nephropathy. J. Am. Soc. Nephrol. 15:622-634. http://dx.doi.org/10.1097/01.ASN.0000115401.07980.0C
25. Moura, I.C., Y. Lepelletier, B. Arnulf, P. England, C. Baude, C. Beaumont, A. Bazarbachi, M. Benhamou, R.C. Monteiro, and O. Hermine. 2004b. A neutralizing monoclonal antibody (mAb A24) directed against the transferrin receptor induces apoptosis of tumor T lymphocytes from ATL patients. Blood. 103:1838-1845. http://dx.doi.org/10.1182/ blood-2003-07-2440
26. Moura, I.C., M. Arcos-Fajardo, A. Gdoura, V. Leroy, C. Sadaka, N. Mahlaoui, Y. Lepelletier, F. Vrtovsnik, E. Haddad, M. Benhamou, and R.C. Monteiro. 2005. 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. 16:2667-2676. http://dx.doi.org/10.1681/ASN.2004111006
27. Novak, J., B.A. Julian, M. Tomana, and J. Mestecky. 2008. IgA glycosylation and IgA immune complexes in the pathogenesis of IgA nephropathy. Semin. Nephrol. 28:78-87. http://dx.doi.org/10.1016/j.semnephrol.2007.10.009
28. Pleass, R.J., J.I. Dunlop, C.M. Anderson, and J.M. Woof. 1999. Identification of residues in the CH2/CH3 domain interface of IgA essential for interaction with the human fcalpha receptor (FcalphaR) CD89. J. Biol. Chem. 274:23508-23514. http://dx.doi.org/10.1074/jbc.274.33.23508
29. Ponticelli, C., and R.J. Glassock. 2010. Posttransplant recurrence of primary glomerulonephritis. Clin. J. Am. Soc. Nephrol. 5:2363-2372. http://dx.doi.org/10.2215/CJN.06720810
30. Radoshitzky, S.R., J. Abraham, C.F. Spiropoulou, J.H. Kuhn, D. Nguyen, W. Li, J. Nagel, P.J. Schmidt, J.H. Nunberg, N.C. Andrews, et al. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature. 446:92-96. http://dx.doi.org/10.1038/nature05539
31. Roos, A., M.P. Rastaldi, N. Calvaresi, B.D. Oortwijn, N. Schlagwein, D.J. van Gijlswijk-Janssen, G.L. Stahl, M. Matsushita, T. Fujita, C. van Kooten, and M.R. Daha. 2006. Glomerular activation of the lectin pathway of complement in IgA nephropathy is associated with more severe renal disease. J. Am. Soc. Nephrol. 17:1724-1734. http://dx.doi.org/10.1681/ ASN.2005090923
32. Schmidt, P.J., P.T. Toran, A.M. Giannetti, P.J. Bjorkman, and N.C. Andrews. 2008. The transferrin receptor modulates Hfe-dependent regulation of hepcidin expression. Cell Metab. 7:205-214. http://dx.doi.org/10.1016/j.cmet.2007.11.016
33. Shweke, N., N. Boulos, C. Jouanneau, S. Vandermeersch, G. Melino, J.C. Dussaule, C. Chatziantoniou, P. Ronco, and J.J. Boffa. 2008. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am. J. Pathol. 173:631-642. http://dx.doi.org/10.2353/ ajpath.2008.080025
34. Suzuki, H., R. Fan, Z. Zhang, R. Brown, S. Hall, B.A. Julian, W.W. Chatham, Y. Suzuki, R.J. Wyatt, Z. Moldoveanu, et al. 2009. Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J. Clin. Invest. 119:1668-1677.
35. Tissandié, E., W. Morelle, L. Berthelot, F. Vrtovsnik, E. Daugas, F. Walker, D. Lebrec, J.M. Trawalé, C. Francoz, F. Durand, et al. 2011. Both IgA nephropathy and alcoholic cirrhosis feature abnormally glycosylated IgA1 and soluble CD89-IgA and IgG-IgA complexes: common mechanisms for distinct diseases. Kidney Int. 80:1352-1363. http://dx.doi.org/10.1038/ ki.2011.276
36. Tomana, M., J. Novak, B.A. Julian, K. Matousovic, K. Konecny, and J. Mestecky. 1999. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J. Clin. Invest. 104:73-81. http://dx.doi.org/10.1172/JCI5535
37. van der Boog, P.J., G. van Zandbergen, J.W. de Fijter, N. Klar-Mohamad, A. van Seggelen, P. Brandtzaeg, M.R. Daha, and C. van Kooten. 2002. Fc alpha RI/CD89 circulates in human serum covalently linked to IgA in a polymeric state. J. Immunol. 168:1252-1258.
38. van der Boog, P.J., C. van Kooten, G. van Zandbergen, N. Klar-Mohamad, B. Oortwijn, N.A. Bos, A. van Remoortere, C.H. Hokke, J.W. de Fijter, and M.R. Daha. 2004. Injection of recombinant FcalphaRI/ CD89 in mice does not induce mesangial IgA deposition. Nephrol. Dial. Transplant. 19:2729-2736. http://dx.doi.org/10.1093/ndt/gfh459
39. Varis, J., I. Rantala, A. Pasternack, H. Oksa, M. Jäntti, E.S. Paunu, and R. Pirhonen. 1993. Immunoglobulin and complement deposition in glomeruli of 756 subjects who had committed suicide or met with a violent death. J. Clin. Pathol. 46:607-610. http://dx.doi.org/10.1136/jcp.46.7.607
40. Vuong, M.T., M. Hahn-Zoric, S. Lundberg, I. Gunnarsson, C. van Kooten, L. Wramner, M. Seddighzadeh, A. Fernström, L.A. Hanson, L.T. Do, et al. 2010. Association of soluble CD89 levels with disease progression but not susceptibility in IgA nephropathy. Kidney Int. 78:1281-1287. http://dx.doi.org/10.1038/ki.2010.314
41. Woodroffe, A.J., and C.B. Wilson. 1977. An evaluation of elution techniques in the study of immune complex glomerulonephritis. J. Immunol. 118:1788-1794.
42. Zhang, W., B. Bi, R.G. Oldroyd, and P.J. Lachmann. 2000. Neutrophil lactoferrin release induced by IgA immune complexes differed from that induced by cross-linking of fcalpha receptors (FcalphaR) with a monoclonal antibody, MIP8a. Clin. Exp. Immunol. 121:106-111. http:// dx.doi.org/10.1046/j.1365-2249.2000.01254.x