Tissue deposits of IgA-binding streptococcal M proteins in IgA nephropathy and Henoch-Schönlein purpura

American Journal of Pathology

Volumn 176, Issue 2, 2010, Pages 608-618

  Schmitt, Roland ^a   Carlsson, Fredric ^b,c   Mörgelin, Matthias ^a   Tati, Ramesh ^a   Lindahl, Gunnar ^b   Karpman, Diana ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN A; M PROTEIN;

ADOLESCENT; ADULT; ANAPHYLACTOID PURPURA; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOGLOBULIN A NEPHROPATHY; IMMUNOHISTOCHEMISTRY; KIDNEY BIOPSY; MALE; MASS SPECTROMETRY; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN BINDING; SCHOOL CHILD; SKIN BIOPSY; STREPTOCOCCUS GROUP A;

EID: 76149095207     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090428     Document Type: Article

References (60)

1. Habib R: Schönlein-Henoch purpura nephritis and IgA-nephropathy. Edited by Tisher C BB. Philadelphia, JB Lippincott, 1994, pp. 472-523
2. Donadio JV, Grande JP: IgA nephropathy. N Engl J Med 2002, 347:738-748
3. Tizard EJ, Hamilton-Ayres MJ: Henoch Schönlein purpura. Arch Dis Child Educ Pract Ed 2008, 93:1-8
4. Halling SF, Söderberg MP, Berg UB: Henoch Schönlein nephritis: clinical findings related to renal function and morphology. Pediatr Nephrol 2005, 20:46-51
5. 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
6. Novak J, Moldoveanu Z, Renfrow MB, Yanagihara T, Suzuki H, Raska M, Hall S, Brown R, Huang WQ, Goepfert A, Kilian M, Poulsen K, Tomana M, Wyatt RJ, Julian BA, Mestecky J: 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
7. Lau KK, Suzuki H, Novak J, Wyatt RJ: Pathogenesis of Henoch- Schönlein purpura nephritis, Pediatr Nephrol 2010, 25:19-26
8. 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 2009, 119:1668-1677
9. Allen AC, Feehally J: IgA1 glycosylation and the pathogenesis of IgA nephropathy. Am J Kidney Dis 2000, 35:551-556
10. al-Sheyyab M, Batieha A, el-Shanti H, Daoud A: Henoch-Schönlein purpura and streptococcal infection: a prospective case-control study. Ann Trop Paediatr 1999, 19:253-255
11. Eisenstein EM, Navon-Elkan P: Acute rheumatic fever associated with Henoch-Schönlein purpura: report of three cases and review of the literature. Acta Paediatr 2002, 91:1265-1267
12. Masuda M, Nakanishi K, Yoshizawa N, Iijima K, Yoshikawa N: Group A streptococcal antigen in the glomeruli of children with Henoch-Schönlein nephritis. Am J Kidney Dis 2003, 41:366-370
13. Kukuminato Y, Hamamoto M, Kataura A: Role of serum antibodies to streptococci in patients with IgA nephropathy. Acta Otolaryngol Suppl 1993, 508:6-10
14. Nakatsuka K: Serum anti-streptococcal IgA. IgG and IgM antibodies in IgA-associated diseases, Acta Paediatr Jpn 1993, 35:118-123
15. Kikuchi Y, Yoshizawa N, Oda T, Imakiire T, Suzuki S, Miura S: Streptococcal origin of a case of Henoch-Schoenlein purpura nephritis. Clin Nephrol 2006, 65:124-128
16. Suzuki S, Nakatomi Y, Sato H, Tsukada H, Arakawa M: Haemophilus parainfluenzae antigen and antibody in renal biopsy samples and serum of patients with IgA nephropathy, Lancet 1994, 343:12-16
17. Koyama A, Sharmin S, Sakurai H, Shimizu Y, Hirayama K, Usui J, Nagata M, Yoh K, Yamagata K, Muro K, Kobayashi M, Ohtani K, Shimizu T: Staphylococcus aureus cell envelope antigen is a new candidate for the induction of IgA nephropathy, Kidney Int 2004, 66:121-132
18. Takahashi A, Kawasaki Y, Yoshida K, Mochizuki K, Isome M, Honzumi K, Nozawa R, Suzuki S, Hosoya M, Suzuki J, Suzuki H: Detection of enteroviruses in renal biopsies from patients with immunoglobulin A nephropathy. Pediatr Nephrol 2005, 20:1578-1582
19. Lindahl G, Stenberg L: Binding of IgA and/or IgG is a common property among clinical isolates of group A streptococci. Epidemiol Infect 1990, 105:87-93
20. Frithz E, Heden LO, Lindahl G: Extensive sequence homology between IgA receptor and M proteins in Streptococcus pyogenes. Mol Microbiol 1989, 3:1111-1119
21. Bessen DE, Fischetti VA: Nucleotide sequences of two adjacent M or M-like protein genes of group A streptococci: different RNA transcript levels and identification of a unique immunoglobulin A-binding protein. Infect Immun 1992, 60:124-135
22. Johnsson E, Andersson G, Lindahl G, Heden LO: Identification of the IgA-binding region in streptococcal protein. Arp. J Immunol 1994, 153:3557-3564
23. Bessen DE: Localization of immunoglobulin A-binding sites within M or M-like proteins of group A streptococci. Infect Immun 1994, 62:1968-1974
24. Fischetti VA: Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev 1989, 2:285-314
25. Facklam RF, Martin DR, Lovgren M, Johnson DR, Efstratiou A, Thompson TA, Gowan S, Kriz P, Tyrrell GJ, Kaplan E, Beall B: Extension of the Lancefield classification for group A streptococci by addition of 22 new M protein gene sequence types from clinical isolates: emm103 to emm124. Clin Infect Dis 2002, 34:28-38
26. Carlsson F, Berggård K, Stålhammar-Carlemalm M, Lindahl G: Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J Exp Med 2003, 198:1057-1068
27. Sandin C, Linse S, Areschoug T, Woof JM, Reinholdt J, Lindahl G: Isolation and detection of human IgA using a streptococcal IgAbinding peptide. J Immunol 2002, 169:1357-1364
28. Johnsson E, Areschoug T, Mestecky J, Lindahl G: An IgA-binding peptide derived from a streptococcal surface protein. J Biol Chem 1999, 274:14521-14524
29. Colman G, Tanna A, Efstratiou A, Gaworzewska ET: The serotypes of Streptococcus pyogenes present in Britain during 1980-1990 and their association with disease. J Med Microbiol 1993, 39:165-178
30. Stenberg L, O'Toole P, Lindahl G: Many group A streptococcal strains express two different immunoglobulin-binding proteins, encoded by closely linked genes: characterization of the proteins expressed by four strains of different M-type. Mol Microbiol 1992, 6:1185-1194
31. Stenberg L, O'Toole PW, Mestecky J, Lindahl G: Molecular characterization of protein Sir, a streptococcal cell surface protein that binds both immunoglobulin A and immunoglobulin G. J Biol Chem 1994, 269:13458-13464
32. Morfeldt E, Berggård K, Persson J, Drakenberg T, Johnsson E, Lindahl E, Linse S, Lindahl G: Isolated hypervariable regions derived from streptococcal M proteins specifically bind human C4b-binding protein: implications for antigenic variation. J Immunol 2001, 167: 3870-3877
33. Mills JA, Michel BA, Bloch DA, Calabrese LH, Hunder GG, Arend WP, Edworthy SM, Fauci AS, Leavitt RY, Lie JT, et al.: The American College of Rheumatology 1990 criteria for the classification of Henoch-Schönlein purpura. Arthritis Rheum 1990, 33:1114-1121
34. Beall B, Facklam R, Thompson T: Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol 1996, 34:953-958
35. Manea M, Tati R, Karlsson J, Bekassy ZD, Karpman D: Biologically active ADAMTS13 is expressed in renal tubular epithelial cells. Pediatr Nephrol 2010, 25:87-96.
36. Roth J: Post-embedding cytochemistry with gold-labelled reagents: a review. J Microsc 1986, 143:125-137
37. Bengtson SH, Phagoo SB, Norrby-Teglund A, Påhlman L, Mörgelin M, Zuraw BL, Leeb-Lundberg LM, Herwald H: Kinin receptor expression during Staphylococcus aureus infection. Blood 2006, 108:2055-2063
38. Kim JH, Cramer L, Mueller H, Wilson B, Vilen BJ: Independent trafficking of Ig-alpha/Ig-beta and mu-heavy chain is facilitated by dissociation of the B cell antigen receptor complex. J Immunol 2005, 175:147-154
39. Sarma VR, Davies DR, Labaw LW, Silverton EW, Terry WD: Crystal structure of an immunoglobulin molecule by x-ray diffraction and electron microscopy. Cold Spring Harb Symp Quant Biol 1972, 36:413-419
40. Picotti P, Lam H, Campbell D, Deutsch EW, Mirzaei H, Ranish J, Domon B, Aebersold R: A database of mass spectrometric assays for the yeast proteome. Nat Methods 2008, 5:913-914
41. Dysart NK Jr, Sisson S, Vernier RL: Immunoelectron microscopy of IgA nephropathy. Clin Immunol Immunopathol 1983, 29:254-270
42. Yoshiara S, Yoshikawa N, Matsuo T: Immunoelectron microscopic study of childhood IgA nephropathy and Henoch-Schönlein nephritis. Virchows Arch A Pathol Anat Histopathol 1987, 412:95-102
43. Westerhuis R, Van Zandbergen G, Verhagen NA, Klar-Mohamad N, Daha MR, van Kooten C: Human mesangial cells in culture and in kidney sections fail to express Fc alpha receptor (CD89). J Am Soc Nephrol 1999, 10:770-778
44. Moura IC, Centelles MN, Arcos-Fajardo M, Malheiros DM, Collawn JF, Cooper MD, Monteiro RC: 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
45. McDonald KJ, Cameron AJ, Allen JM, Jardine AG: Expression of Fc alpha/mu receptor by human mesangial cells: a candidate receptor for immune complex deposition in IgA nephropathy. Biochem Biophys Res Commun 2002, 290:438-442
46. Herwald H, Cramer H, Mörgelin M, Russell W, Sollenberg U, Norrby-Teglund A, Flodgaard H, Lindbom L, Björck L: M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 2004, 116:367-379
47. Berge A, Björck L: Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J Biol Chem 1995, 270:9862-9867
48. Åkerström B, Lindqvist A, Lindahl G: Binding properties of protein Arp, a bacterial IgA-receptor. Mol Immunol 1991, 28:349-357
49. Navas-Palacios JJ, Gutierrez-Millet V, Usera-Sarrage G, Garzon-Martin A: IgA nephropathy: an ultrastructural study. Ultrastruct Pathol 1981, 2:151-161
50. Smith AC, Feehally J: New insights into the pathogenesis of IgA nephropathy. Pathogenesis of IgA nephropathy, Springer Semin Immunopathol 2003, 24:477-493
51. Nangaku M, Couser WG: Mechanisms of immune-deposit formation and the mediation of immune renal injury. Clin Exp Nephrol 2005, 9:183-191
52. Barratt J, Smith AC, Molyneux K, Feehally J: Immunopathogenesis of IgAN. Semin Immunopathol 2007, 29:427-443
53. Mestecky J, Tomana M, Moldoveanu Z, Julian BA, Suzuki H, Matousovic K, Renfrow MB, Novak L, Wyatt RJ, Novak J: Role of aberrant glycosylation of IgA1 molecules in the pathogenesis of IgA nephropathy. Kidney Blood Press Res 2008, 31:29-37
54. Allen AC, Willis FR, Beattie TJ, Feehally J: Abnormal IgA glycosylation in Henoch-Schönlein purpura restricted to patients with clinical nephritis. Nephrol Dial Transplant 1998, 13:930-934
55. Chintalacharuvu SR, Nagy NU, Sigmund N, Nedrud JG, Amm ME, Emancipator SN: T cell cytokines determine the severity of experimental IgA nephropathy by regulating IgA glycosylation. Clin Exp Immunol 2001, 126:326-333
56. Horie A, Hiki Y, Odani H, Yasuda Y, Takahashi M, Kato M, Iwase H, Kobayashi Y, Nakashima I, Maeda K: IgA1 molecules produced by tonsillar lymphocytes are under-O-glycosylated in IgA nephropathy. Am J Kidney Dis 2003, 42:486-496
57. Nishikawa Y, Shibata R, Ozono Y, Ichinose H, Miyazaki M, Harada T, Kohno S: Streptococcal M protein enhances TGF-beta production and increases surface IgA-positive B cells in vitro in IgA nephropathy. Nephrol Dial Transplant 2000, 15:772-777
58. Cunningham MW: Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000, 13:470-511
59. Treser G, Semar M, Ty A, Agel I, Franklin MA, Lange K: Partial characterization of antigenic streptococcal plasma membrane components in acute glomerulonephritis. J Clin Invest 1970, 49:762-768
60. Rodriguez-Iturbe B, Batsford S: Pathogenesis of poststreptococcal glomerulonephritis a century after Clemens von Pirquet. Kidney Int 2007, 71:1094-1104