Anti-PR3 immune responses induce segmental and necrotizing glomerulonephritis

Clinical and Experimental Immunology

Volumn 159, Issue 3, 2010, Pages 327-337

  Primo, V C ^a   Marusic, S ^b   Franklin, C C ^a   Goldmann, W H ^c   Achaval, C G ^d   Smith, R N ^a   Arnaout, M A ^a   Nikolic, B ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Hooke Laboratories Inc   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d Laboratory of Pathology   (Argentina)

Author keywords

Animal models mice rats; Anti neutrophil cytoplasmic antibodies anti PR3 myeloperoxidase; Autoimmunity; Glomerulonephritis; Wegener's granulomatosis

Indexed keywords

ENZYME ANTIBODY; FREUND ADJUVANT; NEUTROPHIL CYTOPLASMIC ANTIBODY; PROTEINASE 3 ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; FOCAL GLOMERULOSCLEROSIS; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNIZATION; KIDNEY FAILURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEVERE COMBINED IMMUNODEFICIENCY; SPLEEN CELL; VASCULITIS;

ANIMALS; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; ANTIBODY SPECIFICITY; AUTOIMMUNE DISEASES; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MYELOBLASTIN; SPECIES SPECIFICITY; WEGENER GRANULOMATOSIS;

EID: 74549179173     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.04072.x     Document Type: Article

References (43)

1. Fahey JL, Leonard E, Churg J, Godman G. Wegener's granulomatosis. Am J Med 1954 17 : 168 179.
2. Hewins P, Tervaert JW, Savage CO, Kallenberg CG. Is Wegener's granulomatosis an autoimmune disease? Curr Opin Rheumatol 2000 12 : 3 10.
3. Franssen CF, Stegeman CA, Kallenberg CG et al. Antiproteinase 3-and antimyeloperoxidase-associated vasculitis. Kidney Int 2000 57 : 2195 2206.
4. Ewert BH, Jennette JC, Falk RJ. The pathogenic role of antineutrophil cytoplasmic autoantibodies. Am J Kidney Dis 1991 18 : 188 195.
5. Han WK, Choi HK, Roth RM, McCluskey RT, Niles JL. Serial ANCA titers: useful tool for prevention of relapses in ANCA-associated vasculitis. Kidney Int 2003 63 : 1079 1085.
6. Falk RJ, Jennette JC. ANCA are pathogenic - oh yes they are! J Am Soc Nephrol 2000 13 : 1977 1979.
7. Niles JL, McCluskey RT, Ahmad MF, Arnaout MA. Wegener's granulomatosis autoantigen is a novel neutrophil serine proteinase. Blood 1989 74 : 1888 1893.
8. Fujinaga M, Chernaia MM, Halenbeck R, Koths K, James MN. The crystal structure of PR3, a neutrophil serine proteinase antigen of Wegener's granulomatosis antibodies. J Mol Biol 1996 261 : 267 278.
9. Wiesner O, Litwiller RD, Hummel AM et al. Differences between human proteinase 3 and neutrophil elastase and their murine homologues are relevant for murine model experiments. FEBS Lett 2005 579 : 5305 5312.
10. Rao NV, Wehner NG, Marshall BC et al. Proteinase-3 (PR-3): a polymorphonuclear leukocyte serine proteinase. Ann NY Acad Sci 1991 624 : 60 8.
11. Campbell EJ, Campbell MA, Owen CA. Bioactive proteinase 3 on the cell surface of human neutrophils: quantification, catalytic activity, and susceptibility to inhibition. J Immunol 2000 165 : 3366 3374.
12. Schreiber A, Luft FC, Kettritz R. Membrane proteinase 3 expression and ANCA-induced neutrophil activation. Kidney Int 2004 65 : 2172 2183.
13. Csernok E, Lüdemann J, Gross WL, Bainton DF. Ultrastructural localization of proteinase 3, the target antigen of anti-cytoplasmic antibodies circulating in Wegener's granulomatosis. Am J Pathol 1990 137 : 1113 1120.
14. Harper L, Cockwell P, Adu D, Savage CO. Neutrophil priming and apoptosis in anti-neutrophil cytoplasmic autoantibody-associated vasculitis. Kidney Int 2001 59 : 1729 1738.
15. Csernok E, Ernst M, Schmitt W, Bainton DF, Gross WL. Activated neutrophils express proteinase 3 on their plasma membrane in vitro and in vivo. Clin Exp Immunol 1994 95 : 244 250.
16. Pankhurst T, Savage CO. Pathogenic role of anti-neutrophil cytoplasmic antibodies in vasculitis. Curr Opin Pharmacol 2006 6 : 190 196.
17. Goldmann WH, Niles JL, Arnaout MA. Interaction of purified human proteinase 3 (PR3) with reconstituted lipid bilayers. Eur J Biochem 1999 261 : 155 162.
18. Pfister H, Ollert M, Fröhlich LF et al. Antineutrophil cytoplasmic autoantibodies against the murine homolog of proteinase 3 (Wegener autoantigen) are pathogenic in vivo. Blood 2004 104 : 1411 1418.
19. Daouk GH, Palsson R, Arnaout MA. Inhibition of proteinase 3 by ANCA and its correlation with disease activity in Wegener's granulomatosis. Kidney Int 1995 47 : 1528 1536.
20. Finkielman JD, Merkel PA, Schroeder D et al. Antiproteinase 3 antineutrophil cytoplasmic antibodies and disease activity in Wegener granulomatosis. Ann Intern Med 2007 147 : 611 619.
21. Kinjoh K, Kyogoku M, Good RA. Genetic selection for crescent formation yields mouse strain with rapidly progressive glomerulonephritis and small vessel vasculitis. Proc Natl Acad Sci USA 1993 90 : 3413 3417.
22. Harper JM, Thiru S, Lockwood MC, Cooke A. Myeloperoxidase autoantibodies distinguish vasculitis mediated by anti-neutrophil cytoplasm antibodies from immune complex disease in MRL/Mp-lpr/lpr mice: a spontaneous model for human microscopic angiitis. Eur J Immunol 1998 28 : 2217 2226.
23. Mathieson PW, Thiru S, Oliveira DB. Mercuric chloride-treated Brown Norway rats develop widespread tissue injury including necrotizing vasculitis. Lab Invest 1992 67 : 121 129.
24. Brouwer E, Huitema MG, Klok PA et al. Antimyeloperoxidase-associated proliferative glomerulonephritis: an animal model. J Exp Med 1993 177 : 905 914.
25. Heeringa P, Foucher P, Klok PA et al. Systemic injection of products of activated neutrophils and H2O2 in myeloperoxidase-immunized rats leads to necrotizing vasculitis in the lungs and gut. Am J Pathol 1997 151 : 131 140.
26. Rauova L, Gilburd B, Zurgil N et al. Induction of biologically active antineutrophil cytoplasmic antibodies by immunization with human apoptotic polymorphonuclear leukocytes. Clin Immunol 2002 103 : 69 78.
27. Xiao H, Heeringa P, Hu P et al. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest 2002 110 : 955 963.
28. Pendergraft WF, Preston GA, Shah RR et al. Autoimmunity is triggered by cPR-3 (105-201), a protein complementary to human autoantigen proteinase-3. Nat Med 2004 10 : 72 9.
29. Little MA, Smyth CL, Yadav R et al. Anti-neutrophil cytoplasm antibodies directed against myeloperoxidase augment leukocyte-microvascular interactions in vivo. Blood 2005 106 : 2050 2058.
30. Blank M, Tomer Y, Stein M et al. Immunization with anti-neutrophil cytoplasmic antibody (ANCA) induces the production of mouse ANCA and perivascular lymphocyte infiltration. Clin Exp Immunol 1995 102 : 120 130.
31. Jenne DE, Frohlinch L, Hummel AM, Specks U. Cloning and functional expression of the murine homologue of proteinase 3: implication for the design of murine models of vasculitis. FEBS Lett 1997 408 : 187 190.
32. van der Geld YM, Hellmark T, Selga D et al. Rats and mice immunized with chimeric human/mouse proteinase 3 produce autoantibodies to mouse Pr3 and rat granulocytes. Ann Rheum Dis 2007 66 : 1679 1682.
33. Harmsen MC, Heeringa P, van der Geld YM et al. Recombinant proteinase 3 (Wegener's antigen) expressed in Pichia pastoris is functionally active and is recognized by patient sera. Clin Exp Immunol 1997 110 : 257 264.
34. van der Geld YM, Smooka MLF, Huitemaa MG, Harmsenb MC, Limburga PC, Kallenberg CGM. Expression of recombinant proteinase 3, the autoantigen in Wegener's granulomatosis, in insect cells. J Immunol Methods 2002 264 : 195 205.
35. Sadelain MW, Qin HY, Lauzon J, Singh B. Prevention of type I diabetes in NOD mice by adjuvant immunotherapy. Diabetes 1990 39 : 583.
36. Aoki CA, Borchers AT, Ridgway WM, Keen CL, Ansari AA, Gershwin ME. NOD mice and autoimmunity. Autoimmun Rev 2005 4 : 373 379.
37. Ikawa K, Nishioka T, Yu Z et al. Involvement of neutrophil recruitment and protease-activated receptor 2 activation in the induction of IL-18 in mice. J Leukoc Biol 2005 78 : 1118 1126.
38. Powrie F, Mason D. OX-22high CD4+ T cells induce wasting disease with multiple organ pathology: prevention by the OX-22low subset. J Exp Med 1990 172 : 1701 1708.
39. Powrie F, Leach MW, Mauze S, Caddle LB, Coffman RL. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 1993 5 : 1461 1471.
40. Scheerens H, Hessel E, de Waal-Malefyt R, Leach MW, Rennick D. Characterization of chemokines and chemokine receptors in two murine models of inflammatory bowel disease: IL-10-/- mice and Rag-2-/- mice reconstituted with CD4+CD45RBhigh T cells. Eur J Immunol 2001 31 : 1465 1474.
41. Lafaille JJ, Nagashima K, Katsuki M, Tonegawa S. High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 1994 78 : 399 408.
42. Olivares-Villagómez D, Wang Y, Lafaille JJ. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J Exp Med 1998 188 : 1883 1894.
43. van de Keere F, Tonegawa S. CD4(+) T cells prevent spontaneous experimental autoimmune encephalomyelitis in anti-myelin basic protein T cell receptor transgenic mice. J Exp Med 1998 188 : 1875 1882.