Renal participation of myeloperoxidase in antineutrophil cytoplasmic antibody (ANCA)-associated glomerulonephritis

Kidney International

Volumn 88, Issue 5, 2015, Pages 1030-1046

  O'Sullivan, Kim M ^a   Lo, Camden Y ^a   Summers, Shaun A ^a,b   Elgass, Kirstin D ^a   McMillan, Paul J ^c,d   Longano, Anthony ^b   Ford, Sharon L ^a,b   Gan, Poh Yi ^a   Kerr, Peter G ^b   Kitching, A Richard ^a,b   Holdsworth, Stephen R ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b SOUTHERN HEALTH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

ANCA; Glomerulonephritis; Inflammation; Macrophages; Renal biopsy; Vasculitis

Indexed keywords

FIBRIN; MYELOPEROXIDASE; NEUTROPHIL CYTOPLASMIC ANTIBODY; PEROXIDASE;

AGED; ANCA ASSOCIATED VASCULITIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LOCALIZATION; ENZYME RELEASE; EXTRACELLULAR TRAP; FEMALE; GLOMERULONEPHRITIS; GLOMERULUS FILTRATION RATE; HUMAN; HUMAN TISSUE; LEUKOCYTE; MALE; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; AUTOIMMUNE DISEASE; CD4 LYMPHOCYTE COUNT; DENDRITIC CELL; ENDOTHELIUM CELL; ENZYMOLOGY; EXTRACELLULAR FLUID; GLOMERULUS; IMMUNOLOGY; MACROPHAGE; METABOLISM; NEUTROPHIL; PATHOLOGY; PODOCYTE;

AGED; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; AUTOIMMUNE DISEASES; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; ENDOTHELIAL CELLS; EXTRACELLULAR FLUID; EXTRACELLULAR TRAPS; FEMALE; GLOMERULAR FILTRATION RATE; GLOMERULONEPHRITIS; HUMANS; KIDNEY GLOMERULUS; MACROPHAGES; MALE; NEUTROPHILS; PEROXIDASE; PODOCYTES;

EID: 84947602409     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.202     Document Type: Article

References (55)

1. Gatenby PA. Anti-neutrophil cytoplasmic antibody-associated systemic vasculitis: nature or nurture? Intern Med J 2012; 42: 1066-1067.
2. Coughlan AM, Freeley SJ, Robson MG. Animal models of anti-neutrophil cytoplasmic antibody-associated vasculitis. Clin Exp Immunol 2012; 169: 229-237.
3. Odobasic D, Kitching AR, Yang Y et al. Neutrophil myeloperoxidase regulates T-cell-driven tissue inflammation in mice by inhibiting dendritic cell function. Blood 2013; 121: 4195-4204.
4. Kessenbrock K, Krumbholz M, Schonermarck U et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15: 623-625.
5. Brinkmann V, Reichard U, Goosmann C et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
6. Nakazawa D, Shida H, Tomaru U et al. Enhanced formation and disordered regulation of NETs in myeloperoxidase-ANCA-associated microscopic polyangiitis. J Am Soc Nephrol 2014; 25: 990-997.
7. Liu P, Wu X, Liao C et al. Escherichia coli and Candida albicans induced macrophage extracellular trap-like structures with limited microbicidal activity. PLoS One 2014; 9: e90042.
8. Wong KW, Jacobs WR Jr. Mycobacterium tuberculosis exploits human interferon gamma to stimulate macrophage extracellular trap formation and necrosis. J Infect Dis 2013; 208: 109-119.
9. Mohanan S, Horibata S, McElwee JL et al. Identification of macrophage extracellular trap-like structures in mammary gland adipose tissue: a preliminary study. Front Immunol 2013; 4: 67.
10. Hellenbrand KM, Forsythe KM, Rivera-Rivas JJ et al. Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microb Pathog 2013; 54: 67-75.
11. Aulik NA, Hellenbrand KM, Kisiela D et al. Mannheimia haemolytica leukotoxin binds cyclophilin D on bovine neutrophil mitochondria. Microb Pathog 2011; 50: 168-178.
12. Grattendick K, Stuart R, Roberts E et al. Alveolar macrophage activation by myeloperoxidase: a model for exacerbation of lung inflammation. Am J Respir Cell Mol Biol 2002; 26: 716-722.
13. Brouwer E, Huitema MG, Mulder AH et al. Neutrophil activation in vitro and in vivo in Wegener's granulomatosis. Kidney Int 1994; 45: 1120-1131.
14. 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.
15. Ruth AJ, Kitching AR, Kwan RY et al. Anti-neutrophil cytoplasmic antibodies and effector CD4+ cells play nonredundant roles in antimyeloperoxidase crescentic glomerulonephritis. J Am Soc Nephrol 2006; 17: 1940-1949.
16. Gan PY, Holdsworth SR, Kitching AR et al. Myeloperoxidase (MPO)-specific CD4+ T cells contribute to MPO-anti-neutrophil cytoplasmic antibody (ANCA) associated glomerulonephritis. Cell Immunol 2013; 282: 21-27.
17. Ooi JD, Chang J, Hickey MJ et al. The immunodominant myeloperoxidase T-cell epitope induces local cell-mediated injury in antimyeloperoxidase glomerulonephritis. Proc Natl Acad Sci USA 2012; 109: E2615-E2624.
18. Berden AE, Ferrario F, Hagen EC et al. Histopathologic classification of ANCA-associated glomerulonephritis. J Am Soc Nephrol 2010; 21: 1628-1636.
19. Ford SL, Polkinghorne KR, Longano A et al. Histopathologic and clinical predictors of kidney outcomes in ANCA-associated vasculitis. Am J Kidney Dis 2014; 63: 227-235.
20. Weidner S, Carl M, Riess R et al. Histologic analysis of renal leukocyte infiltration in antineutrophil cytoplasmic antibody-associated vasculitis: importance of monocyte and neutrophil infiltration in tissue damage. Arthritis Rheum 2004; 50: 3651-3657.
21. Cunningham MA, Huang XR, Dowling JP et al. Prominence of cellmediated immunity effectors in "pauci-immune" glomerulonephritis. J Am Soc Nephrol 1999; 10: 499-506.
22. Jennette JC, Falk RJ, Hu P et al. Pathogenesis of antineutrophil cytoplasmic autoantibody-associated small-vessel vasculitis. Annu Rev Pathol 2013; 8: 139-160.
23. Aulik NA, Hellenbrand KM, Czuprynski CJ. Mannheimia haemolytica and its leukotoxin cause macrophage extracellular trap formation by bovine macrophages. Infect Immun 2012; 80: 1923-1933.
24. Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895-1902.
25. Rohrbach AS, Slade DJ, Thompson PR et al. Activation of PAD4 in NET formation. Front Immunol 2012; 3: 360.
26. Li P, Li M, Lindberg MR et al. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010; 207: 1853-1862.
27. Leshner M, Wang S, Lewis C et al. PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front Immunol 2012; 3: 307.
28. Wang Y, Li M, Stadler S et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009; 184: 205-213.
29. Dwivedi N, Radic M. Citrullination of autoantigens implicates NETosis in the induction of autoimmunity. Ann Rheum Dis 2014; 73: 483-491.
30. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013; 5: 178ra140.
31. Couser WG. Glomerulonephritis. Lancet 1999; 353: 1509-1515.
32. Kawashima S, Arimura Y, Sano K et al. Immunopathologic co-localization of MPO, IgG, and C3 in glomeruli in human MPO-ANCA-associated glomerulonephritis. Clin Nephrol 2013; 79: 292-301.
33. McKinney EF, Lyons PA, Carr EJ et al. A CD8+ T cell transcription signature predicts prognosis in autoimmune disease. Nat Med 2010; 16: 586-591 581p following 591.
34. Saeki T, Kuroda T, Morita T et al. Significance of myeloperoxidase in rapidly progressive glomerulonephritis. Am J Kidney Dis 1995; 26: 13-21.
35. Niemir ZI, Kubiak A, Olejniczak P et al. Can von Willebrand factor, plateletendothelial cell adhesion molecule-1 and thrombomodulin be used as alternative markers of endothelial cell injury in human glomerulonephritis? Rocz Akad Med Bialymst 2004; 49: 213-218.
36. Yang JJ, Preston GA, Pendergraft WF et al. Internalization of proteinase 3 is concomitant with endothelial cell apoptosis and internalization of myeloperoxidase with generation of intracellular oxidants. Am J Pathol 2001; 158: 581-592.
37. Jerke U, Rolle S, Purfurst B et al. beta2 integrin-mediated cell-cell contact transfers active myeloperoxidase from neutrophils to endothelial cells. J Biol Chem 2013; 288: 12910-12919.
38. Goldwich A, Burkard M, Olke M et al. Podocytes are nonhematopoietic professional antigen-presenting cells. J Am Soc Nephrol 2013; 24: 906-916.
39. Coers W, Brouwer E, Vos JT et al. Podocyte expression of MHC class I and II and intercellular adhesion molecule-1 (ICAM-1) in experimental pauci-immune crescentic glomerulonephritis. Clin Exp Immunol 1994; 98: 279-286.
40. Eiserich JP, Baldus S, Brennan ML et al. Myeloperoxidase, a leukocytederived vascular NO oxidase. Science 2002; 296: 2391-2394.
41. Muczynski KA, Ekle DM, Coder DM et al. Normal human kidney HLA-DRexpressing renal microvascular endothelial cells: characterization, isolation, and regulation of MHC class II expression. J Am Soc Nephrol 2003; 14: 1336-1348.
42. Chadban SJ, Tesch GH, Foti R et al. Interleukin-10 differentially modulates MHC class II expression by mesangial cells and macrophages in vitro and in vivo. Immunology 1998; 94: 72-78.
43. Kitching AR. Dendritic cells in progressive renal disease: some answers, many questions. Nephrol Dial Transplant 2014; 29: 2185-2193.
44. Rastaldi MP, Ferrario F, Crippa A et al. Glomerular monocyte-macrophage features in ANCA-positive renal vasculitis and cryoglobulinemic nephritis. J Am Soc Nephrol 2000; 11: 2036-2043.
45. McMillen TS, Heinecke JW, LeBoeuf RC. Expression of human myeloperoxidase by macrophages promotes atherosclerosis in mice. Circulation 2005; 111: 2798-2804.
46. Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol 2013; 191: 2647-2656.
47. Silva MT. Macrophage phagocytosis of neutrophils at inflammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation. J Leukoc Biol 2011; 89: 675-683.
48. Locati M, Mantovani A, Sica A. Macrophage activation and polarization as an adaptive component of innate immunity. Adv Immunol 2013; 120: 163-184.
49. Gan PY, Steinmetz OM, Tan DS et al. Th17 cells promote autoimmune anti-myeloperoxidase glomerulonephritis. J Am Soc Nephrol 2010; 21: 925-931.
50. Velden J, Paust HJ, Hoxha E et al. Renal IL-17 expression in human ANCAassociated glomerulonephritis. Am J Physiol Renal Physiol 2012; 302: F1663-F1673.
51. Nogueira E, Hamour S, Sawant D et al. Serum IL-17 and IL-23 levels and autoantigen-specific Th17 cells are elevated in patients with ANCA-associated vasculitis. Nephrol Dial Transplant 2010; 25: 2209-2217.
52. Heeringa P, Brouwer E, Klok PA et al. Autoantibodies to myeloperoxidase aggravate mild anti-glomerular-basement-membrane-mediated glomerular injury in the rat. Am J Pathol 1996; 149: 1695-1706.
53. Johnson RJ, Couser WG, Chi EY et al. New mechanism for glomerular injury. Myeloperoxidase-hydrogen peroxide-halide system. J Clin Invest 1987; 79: 1379-1387.
54. Bradley PP, Christensen RD, Rothstein G. Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood 1982; 60: 618-622.
55. Xu PC, Hao J, Chen M et al. Influence of myeloperoxidase-catalyzing reaction on the binding between myeloperoxidase and antimyeloperoxidase antibodies. Hum Immunol 2012; 73: 364-369.