Acquired loss of renal nuclease activity is restricted to DNaseI and is an organ-selective feature in murine lupus nephritis

American Journal of Pathology

Volumn 179, Issue 3, 2011, Pages 1120-1128

  Seredkina, Natalya ^a   Rekvig, Ole P ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CASPASE ACTIVATED DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE 2A; DEOXYRIBONUCLEASE I; DEOXYRIBONUCLEASE II; ENDONUCLEASE G; KIDNEY ENZYME; MAGNESIUM ION; MESSENGER RNA; NUCLEASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CIRCULATION; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME DEFICIENCY; FEMALE; GENE SILENCING; KIDNEY FAILURE; LIVER; LUPUS ERYTHEMATOSUS NEPHRITIS; MALE; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MESANGIUM; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN;

ANIMALS; DEOXYRIBONUCLEASE I; DOWN-REGULATION; FEMALE; GENE EXPRESSION; GENE SILENCING; KIDNEY; LIVER; LUPUS NEPHRITIS; MICE; MICE, INBRED BALB C; RNA, MESSENGER; SPLEEN;

EID: 80052841986     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.05.011     Document Type: Article

References (48)

1. E.M. Tan Autoantibodies to nuclear antigens (ANA): their immunobiology and medicine Adv Immunol 33 1982 167 240
2. M. Herrmann, T. Winkler, U. Gaipl, H. Lorenz, T. Geiler, and J.R. Kalden Etiopathogenesis of systemic lupus erythematosus Int Arch Allergy Immunol 123 2000 28 35
3. J.C. Nossent, W. Bronsveld, and A.J. Swaak Systemic lupus erythematosus, III: observations on clinical renal involvement and follow up of renal function: Dutch experience with 110 patients studied prospectively Ann Rheum Dis 48 1989 810 816 (Pubitemid 19258533)
4. R. Clynes, C. Dumitru, and J.V. Ravetch Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis Science 279 1998 1052 1054 (Pubitemid 28113310)
5. A. Davidson, and C. Aranow Lupus nephritis: lessons from murine models Nat Rev Rheumatol 6 2010 13 20
6. G.B. Appel, and A. Valeri The course and treatment of lupus nephritis Annu Rev Med 45 1994 525 537 (Pubitemid 24158179)
7. J.H. Berden Lupus nephritis Kidney Int 52 1997 538 558 (Pubitemid 27359601)
8. K. Fenton, S. Fismen, A. Hedberg, N. Seredkina, C. Fenton, E.S. Mortensen, and O.P. Rekvig Anti-dsDNA antibodies promote initiation, and acquired loss of renal Dnase1 promotes progression of lupus nephritis in autoimmune (NZBxNZW)F1 mice PLoS One 4 2009 e8474
9. A.G. Basnakian, E.O. Apostolov, X. Yin, M. Napirei, H.G. Mannherz, and S.V. Shah Cisplatin nephrotoxicity is mediated by deoxyribonuclease I J Am Soc Nephrol 16 2005 697 702 (Pubitemid 41725106)
10. N. Seredkina, S.N. Zykova, and O.P. Rekvig Progression of murine lupus nephritis is linked to acquired renal Dnase1 deficiency and not to up-regulated apoptosis Am J Pathol 175 2009 97 106
11. S.N. Zykova, N. Seredkina, J. Benjaminsen, and O.P. Rekvig Reduced fragmentation of apoptotic chromatin is associated with nephritis in lupus-prone (NZB x NZW)F(1) mice Arthritis Rheum 58 2008 813 825 (Pubitemid 351364879)
12. Y. Ogawa, T. Yoshinaga, K. Yasuda, M. Nishikawa, and Y. Takakura The uptake and degradation of DNA is impaired in macrophages and dendritic cells from NZB/W F(1) mice Immunol Lett 101 2005 32 40 (Pubitemid 41297496)
13. A.A. Tveita, O.P. Rekvig, and S.N. Zykova Increased glomerular matrix metalloproteinase activity in murine lupus nephritis Kidney Int 74 2008 1150 1158
14. M. Macanovic, and P.J. Lachmann Measurement of deoxyribonuclease I (DNase) in the serum and urine of systemic lupus erythematosus (SLE)-prone NZB/NZW mice by a new radial enzyme diffusion assay Clin Exp Immunol 108 1997 220 226 (Pubitemid 27223457)
15. S.N. Zykova, A.A. Tveita, and O.P. Rekvig Renal Dnase1 enzyme activity and protein expression is selectively shut down in murine and human membranoproliferative lupus nephritis PLoS One 5 2010 e12096
16. S. Ludwig, H.G. Mannherz, S. Schmitt, M. Schaffer, H. Zentgraf, and M. Napirei Murine serum deoxyribonuclease 1 (Dnase1) activity partly originates from the liver Int J Biochem Cell Biol 41 2009 1079 1093
17. M. Napirei, A. Ricken, D. Eulitz, H. Knoop, and H.G. Mannherz Expression pattern of the deoxyribonuclease 1 gene: lessons from the Dnase1 knockout mouse Biochem J 380 2004 929 937 (Pubitemid 38850536)
18. H. Takeshita, K. Mogi, T. Yasuda, T. Nakajima, Y. Nakashima, S. Mori, T. Hoshino, and K. Kishi Mammalian deoxyribonucleases I are classified into three types: pancreas, parotid, and pancreas-parotid (mixed), based on differences in their tissue concentrations Biochem Biophys Res Commun 269 2000 481 484 (Pubitemid 30440326)
19. K.A. Davies, K. Erlendsson, H.L. Beynon, A.M. Peters, K. Steinsson, H. Valdimarsson, and M.J. Walport Splenic uptake of immune complexes in man is complement-dependent J Immunol 151 1993 3866 3873 (Pubitemid 23282698)
20. T. Skogh, R. Blomhoff, W. Eskild, and T. Berg Hepatic uptake of circulating IgG immune complexes Immunology 55 1985 585 594 (Pubitemid 15237665)
21. M. Kalaaji, E. Mortensen, L. Jorgensen, R. Olsen, and O.P. Rekvig Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells Am J Pathol 168 2006 1779 1792 (Pubitemid 43825300)
22. O.P. Rekvig, U. Moens, A. Sundsfjord, G. Bredholt, A. Osei, H. Haaheim, T. Traavik, E. Arnesen, and H.J. Haga 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 99 1997 2045 2054 (Pubitemid 27175953)
23. E. Richardsen, T. Ukkonen, T. Bjornsen, E. Mortensen, L. Egevad, and C. Busch Overexpression of IGBFB2 is a marker for malignant transformation in prostate epithelium Virchows Arch 442 2003 329 335 (Pubitemid 36561089)
24. S. Chitrabamrung, J.S. Bannett, R.L. Rubin, and E.M. Tan A radial diffusion assay for plasma and serum deoxyribonuclease I Rheumatol Int 1 1981 49 53 (Pubitemid 11038704)
25. A.L. Rosenthal, and S.A. Lacks Nuclease detection in SDS-polyacrylamide gel electrophoresis Anal Biochem 80 1977 76 90 (Pubitemid 8123718)
26. M. Macanovic, D. Sinicropi, S. Shak, S. Baughman, S. Thiru, and P.J. Lachmann The treatment of systemic lupus erythematosus (SLE) in NZB/W F1 hybrid mice: studies with recombinant murine DNase and with dexamethasone Clin Exp Immunol 106 1996 243 252 (Pubitemid 26359889)
27. J.C. Davis Jr, S. Manzi, C. Yarboro, J. Rairie, I. Mcinnes, D. Averthelyi, D. Sinicropi, V.G. Hale, J. Balow, H. Austin, D.T. Boumpas, and J.H. Klippel Recombinant human Dnase I (rhDNase) in patients with lupus nephritis Lupus 8 1999 68 76 (Pubitemid 29050221)
28. D. Verthelyi, N. Dybdal, K.A. Elias, and D.M. Klinman DNAse treatment does not improve the survival of lupus prone (NZB x NZW)F1 mice Lupus 7 1998 223 230 (Pubitemid 28263999)
29. K. Samejima, and W.C. Earnshaw Trashing the genome: the role of nucleases during apoptosis Nat Rev Mol Cell Biol 6 2005 677 688 (Pubitemid 41748063)
30. T. Buzder, X. Yin, X. Wang, G. Banfalvi, and A.G. Basnakian Uptake of foreign nucleic acids in kidney tubular epithelial cells deficient in proapoptotic endonucleases DNA Cell Biol 28 2009 435 442
31. S. Chitrabamrung, R.L. Rubin, and E.M. Tan Serum deoxyribonuclease I and clinical activity in systemic lupus erythematosus Rheumatol Int 1 1981 55 60 (Pubitemid 11038705)
32. F. Martinez-Valle, E. Balada, J. Ordi-Ros, S. Bujan-Rivas, A. Sellas-Fernandez, and M. Vilardell-Tarres DNase1 activity in systemic lupus erythematosus patients with and without nephropathy Rheumatol Int 30 2010 1601 1604
33. K. Sallai, E. Nagy, B. Derfalvy, G. Muzes, and P. Gergely Antinucleosome antibodies and decreased deoxyribonuclease activity in sera of patients with systemic lupus erythematosus Clin Diagn Lab Immunol 12 2005 56 59
34. F. Martinez-Valle, E. Balada, J. Ordi-Ros, S. Bujan-Rivas, A. Sellas-Fernandez, and M. Vilardell-Tarres DNase 1 activity in patients with systemic lupus erythematosus: relationship with epidemiological, clinical, immunological and therapeutical features Lupus 18 2009 418 423
35. J.W. Dieker, J. van der Vlag, and J.H. Berden Deranged removal of apoptotic cells: its role in the genesis of lupus Nephrol Dial Transplant 19 2004 282 285 (Pubitemid 38195970)
36. U.S. Gaipl, A. Kuhn, A. Sheriff, L.E. Munoz, S. Franz, R.E. Voll, J.R. Kalden, and M. Herrmann Clearance of apoptotic cells in human SLE Curr Dir Autoimmun 9 2006 173 187
37. R. Licht, J.W. Dieker, C.W. Jacobs, W.J. Tax, and J.H. Berden Decreased phagocytosis of apoptotic cells in diseased SLE mice J Autoimmun 22 2004 139 145 (Pubitemid 38252970)
38. L.E. Munoz, C. Janko, C. Schulze, C. Schorn, K. Sarter, G. Schett, and M. Herrmann Autoimmunity and chronic inflammation: two clearance-related steps in the etiopathogenesis of SLE Autoimmun Rev 10 2010 38 42
39. S. Fismen, E.S. Mortensen, and O.P. Rekvig Nuclease deficiencies promote end-stage lupus nephritis but not nephritogenic autoimmunity in (NZB x NZW) F1 mice Immunol Cell Biol 89 2011 90 99
40. M. Kalaaji, K.A. Fenton, E.S. Mortensen, R. Olsen, G. Sturfelt, P. Alm, and O.P. Rekvig Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis Kidney Int 71 2007 664 672 (Pubitemid 46494570)
41. D. Malide, I. Londono, P. Russo, and M. Bendayan Ultrastructural localization of DNA in immune deposits of human lupus nephritis Am J Pathol 143 1993 304 311 (Pubitemid 24058184)
42. J.E. Mjelle, O.P. Rekvig, and K.A. Fenton Nucleosomes possess a high affinity for glomerular laminin and collagen IV and bind nephritogenic antibodies in murine lupus-like nephritis Ann Rheum Dis 66 2007 1661 1668 (Pubitemid 350205458)
43. S. Fismen, A. Hedberg, K.A. Fenton, S. Jacobsen, E. Krarup, A.L. Kamper, O.P. Rekvig, and E.S. Mortensen Circulating chromatin-anti-chromatin antibody complexes bind with high affinity to dermo-epidermal structures in murine and human lupus nephritis Lupus 18 2009 597 607
44. A. Hedberg, S. Fismen, K.A. Fenton, E.S. Mortensen, and O.P. Rekvig Deposition of chromatin-IgG complexes in skin of nephritic MRL-lpr/lpr mice is associated with increased local matrix metalloprotease activities Exp Dermatol 19 2010 e265 e274
45. G.N. Montesano, G. Chirico, G. Pirozzi, E. Costantino, M. Landriscina, and F. Esposito Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis Stress 10 2007 342 350 (Pubitemid 350125789)
46. K. Takemoto, S. Miyata, H. Takamura, T. Katayama, and M. Tohyama Mitochondrial TRAP1 regulates the unfolded protein response in the endoplasmic reticulum Neurochem Int 58 2011 880 887
47. T. Ohse, R. Inagi, T. Tanaka, T. Ota, T. Miyata, I. Kojima, J.R. Ingelfinger, S. Ogawa, T. Fujita, and M. Nangaku Albumin induces endoplasmic reticulum stress and apoptosis in renal proximal tubular cells Kidney Int 70 2006 1447 1455 (Pubitemid 44527314)
48. X. Wu, Y. He, Y. Jing, K. Li, and J. Zhang Albumin overload induces apoptosis in renal tubular epithelial cells through a CHOP-dependent pathway OMICS 14 2010 61 73