Progression of murine lupus nephritis is linked to acquired renal Dnase1 deficiency and not to up-regulated apoptosis

American Journal of Pathology

Volumn 175, Issue 1, 2009, Pages 97-106

  Seredkina, Natalya ^a   Zykova, Svetlana N ^a   Rekvig, Ole P ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DEOXYRIBONUCLEASE I; DNA ANTIBODY;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEOXYRIBONUCLEASE 1 DEFICIENCY; ENZYME DEFICIENCY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNE COMPLEX DEPOSITION; LUPUS ERYTHEMATOSUS NEPHRITIS; MALE; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 67650000223     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080943     Document Type: Article

References (34)

1. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M: The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol 2004, 15:241-250
2. Berden JH, Licht R, van Bruggen MC, Tax WJ: Role of nucleosomes for induction and glomerular binding of autoantibodies in lupus nephritis. Curr Opin Nephrol Hypertens 1999, 8:299-306
3. Mjelle JE, Rekvig OP, Fenton KA: Nucleosomes possess a high affinity for glomerular laminin and collagen IV and bind nephritogenic antibodies in murine lupus-like nephritis. Ann Rheum Dis 2007, 66:1661-1668
4. Mohan C, Adams S, Stanik V, Datta SK: Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J Exp Med 1993, 177:1367-1381
5. Kalaaji M, Mortensen E, Jorgensen L, Olsen R, Rekvig OP: Nephritogenic lupus antibodies recognize glomerular basement membraneassociated chromatin fragments released from apoptotic intraglomerular cells. Am J Pathol 2006, 168:1779-1792
6. Kalaaji M, Fenton KA, Mortensen ES, Olsen R, Sturfelt G, Alm P, Rekvig OP: Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis. Kidney Int 2007, 71:664-672
7. Tax WJ, Kramers C, van Bruggen MC, Berden JH: Apoptosis, nucleosomes, and nephritis in systemic lupus erythematosus. Kidney Int 1995, 48:666-673
8. Kaplan MJ: Apoptosis in systemic lupus erythematosus. Clin Immunol 2004, 112:210-218
9. Mortensen ES, Fenton KA, Rekvig OP: Lupus nephritis: the central role of nucleosomes revealed. Am J Pathol 2008, 172:275-283
10. Casciola-Rosen LA, Anhalt G, Rosen A: Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 1994, 179:1317-1330
11. Dieker JW, van der Vlag J, Berden JH: Deranged removal of apoptotic cells: its role in the genesis of lupus. Nephrol Dial Transplant 2004, 19:282-285
12. Berden JH, Grootscholten C, Jurgen WC, van der Vlag J: Lupus nephritis: a nucleosome waste disposal defect? J Nephrol 2002, 15 Suppl 6:S1-S10
13. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, Sarter K, Voll RE, Winkler T, Kuhn A, Kalden J, Kern P, Herrmann M: Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 2007, 28:114-121
14. Courtney PA, Williamson K, Crockard AD, Bell AL: Apoptotic lymphocytes in SLE. Lupus 1998, 7:498
15. Emlen W, Niebur J, Kadera R: Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol 1994, 152:3685-3692
16. Ren Y, Tang J, Mok MY, Chan AW, Wu A, Lau CS: Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum 2003, 48:2888-2897
17. Courtney PA, Crockard AD, Williamson K, Irvine AE, Kennedy RJ, Bell AL: Increased apoptotic peripheral blood neutrophils in systemic lupus erythematosus: relations with disease activity, antibodies to double stranded DNA, and neutropenia. Ann Rheum Dis 1999, 58:309-314
18. Makino H, Sugiyama H, Yamasaki Y, Maeshima Y, Wada J, Kashihara N: Glomerular cell apoptosis in human lupus nephritis. Virchows Arch 2003, 443:67-77
19. Munoz LE, Gaipl US, Franz S, Sheriff A, Voll RE, Kalden JR, Herrmann M: SLE-a disease of clearance deficiency? Rheumatology (Oxford) 2005, 44:1101-1107
20. Gaipl US, Franz S, Voll RE, Sheriff A, Kalden JR, Herrmann M: Defects in the disposal of dying cells lead to autoimmunity. Curr Rheumatol Rep 2004, 6:401-407
21. Kuenkele S, Beyer TD, Voll RE, Kalden JR, Herrmann M: Impaired clearance of apoptotic cells in systemic lupus erythematosus: challenge of T and B cell tolerance. Curr Rheumatol Rep 2003, 5:175-177
22. Nagata S: Apoptosis by death factor. Cell 1997, 88:355-365
23. Hengartner MO: The biochemistry of apoptosis. Nature 2000, 407:770-776
24. Ehrenstein MR, Katz DR, Griffiths MH, Papadaki L, Winkler TH, Kalden JR, Isenberg DA: Human IgG anti-DNA antibodies deposit in kidneys and induce proteinuria in SCID mice. Kidney Int 1995, 48:705-711
25. Kramers C, Hylkema MN, van Bruggen MC, van de Lagemaat R, Dijkman HB, Assmann KJ, Smeenk RJ, Berden JH: Anti-nucleosome antibodies complexed to nucleosomal antigens show anti-DNA reactivity and bind to rat glomerular basement membrane in vivo. J Clin Invest 1994, 94:568-577
26. Rekvig OP, Moens U, Sundsfjord A, Bredholt G, Osei A, Haaheim H, Traavik T, Arnesen E, Haga HJ: Experimental expression in mice and spontaneous expression in human SLE of polyomavirus T-antigen. A molecular basis for induction of antibodies to DNA and eukaryotic transcription factors. J Clin Invest 1997, 99:2045-2054
27. Zykova SN, Seredkina N, Benjaminsen J, Rekvig OP: Reduced fragmentation of apoptotic chromatin is associated with nephritis in lupusprone (NZB x NZW)F(1) mice. Arthritis Rheum 2008, 58:813-825
28. Jeruc J, Vizjak A, Rozman B, Ferluga D: Immunohistochemical expression of activated caspase-3 as a marker of apoptosis in glomeruli of human lupus nephritis. Am J Kidney Dis 2006, 48:410-418
29. Baima B, Sticherling M: How specific is the TUNEL reaction? An account of a histochemical study on human skin. Am J Dermatopathol 2002, 24:130-134
30. Basnakian AG, Apostolov EO, Yin X, Napirei M, Mannherz HG, Shah SV: Cisplatin nephrotoxicity is mediated by deoxyribonuclease I. J Am Soc Nephrol 2005, 16:697-702
31. Papadaki HA, Boumpas DT, Gibson FM, Jayne DR, Axford JS, Gordon-Smith EC, Marsh JC, Eliopoulos GD: Increased apoptosis of bone marrow CD34(+) cells and impaired function of bone marrow stromal cells in patients with systemic lupus erythematosus. Br J Haematol 2001, 115:167-174
32. Floros KV, Thomadaki H, Florou D, Talieri M, Scorilas A: Alterations in mRNA expression of apoptosis-related genes BCL2. BAX, FAS, caspase-3, and the novel member BCL2L12 after treatment of human leukemic cell line HL60 with the antineoplastic agent etoposide Ann NY Acad Sci 2006, 1090:89-97
33. Eulitz D, Mannherz HG: Inhibition of deoxyribonuclease I by actin is to protect cells from premature cell death. Apoptosis 2007, 12:1511-1521
34. Mannherz HG, Peitsch MC, Zanotti S, Paddenberg R, Polzar B: A new function for an old enzyme: the role of DNase I in apoptosis. Curr Top Microbiol Immunol 1995, 198:161-174