Deposition of chromatin-IgG complexes in skin of nephritic MRL-lpr/lpr mice is associated with increased local matrix metalloprotease activities

Experimental Dermatology

Volumn 19, Issue 8, 2010, Pages

  Hedberg, Annica ^a   Fismen, Silje ^b   Fenton, Kristin A ^a   Mortensen, Elin S ^a,b   Rekvig, Ole P ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

Chromatin fragments; Lupus dermatitis; Lupus nephritis; Matrix metalloproteases; Renal Dnase1; Systemic lupus erythematosus

Indexed keywords

DEOXYRIBONUCLEASE I; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN G; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CHROMATIN; COMPLEX FORMATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GLOMERULUS; LUPUS ERYTHEMATOSUS NEPHRITIS; MOUSE; NONHUMAN; SKIN LUPUS ERYTHEMATOSUS; UPREGULATION;

ANIMALS; BASEMENT MEMBRANE; BIOPSY; CHROMATIN; DEOXYRIBONUCLEASE I; DERMATITIS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOGLOBULIN G; KIDNEY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED MRL LPR; NEPHRITIS; RNA, MESSENGER; SKIN;

EID: 77954838721     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2010.01064.x     Document Type: Article

References (50)

1. Mortensen E S, Fenton K A, Rekvig O P. Lupus nephritis: the central role of nucleosomes revealed. Am J Pathol 2008, 172:275-283.
2. Balow J E B D, Ausin H A. Systemic lupus erythematosus and the kidney. Systemic Lupus Erythematosus 1999, 657-685. Lahita R, ed, San diego, London, Boston, New York, Sydney, Tokyo, Toronto, Academic Press
3. Tan E M, Cohen A S, Fries J F. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271-1277.
4. Noel L H, Droz D, Rothfield N F. Clinical and serologic significance of cutaneous deposits of immunoglobulins, C3, and C1q in SLE patients with nephritis. Clin Immunol Immunopathol 1978, 10:381-388.
5. Burnham T K, Fine G. The immunofluorescent " band" test for lupus erythematosus. Br J Dermatol 1971, 84:176-177.
6. Caperton E M, Bean S F, Dick F R. Immunofluorescent skin test in systemic lupus erythematosus. Lack of relationship with renal disease. JAMA 1972, 222:935-937.
7. Fismen S, Rekvig O P, Mortensen E S. Pathogenesis of SLE dermatitis - a reflection of the process in SLE nephritis? Current Rheumatology Reviews 2007, 3:159-165. 157
8. Grootscholten C, van Bruggen M C, van der Pijl J W. Deposition of nucleosomal antigens (histones and DNA) in the epidermal basement membrane in human lupus nephritis. Arthritis Rheum 2003, 48:1355-1362.
9. Kalaaji M, Fenton K A, Mortensen E S. Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis. Kidney Int 2007, 71:664-672.
10. Kalaaji M, Sturfelt G, Mjelle J E, Nossent H, Rekvig O P. Critical comparative analyses of anti-alpha-actinin and glomerulus-bound antibodies in human and murine lupus nephritis. Arthritis Rheum 2006, 54:914-926.
11. Kalaaji M, Mortensen E, Jorgensen L, Olsen R, Rekvig O P. Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells. Am J Pathol 2006, 168:1779-1792.
12. Mjelle J E, Rekvig O P, Fenton K A. 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.
13. Fismen S, Hedberg A, Fenton K. Circulating chromatin-anti-chromatin antibody complexes bind with high affinity to dermo-epidermal structures in murine and human lupus nephritis. Lupus 2009, 18:597-607.
14. Tveita A A, Rekvig O P, Zykova S N. Increased glomerular matrix metalloproteinase activity in murine lupus nephritis. Kidney Int 2008, 74:1150-1158.
15. Kahari V M, Saarialho-Kere U. Matrix metalloproteinases in skin. Exp Dermatol 1997, 6:199-213.
16. Overall C M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002, 22:51-86.
17. Overall C M, Butler G S. Protease yoga: extreme flexibility of a matrix metalloproteinase. Structure 2007, 15:1159-1161.
18. Jarvinen T M, Kanninen P, Jeskanen L. Matrix metalloproteinases as mediators of tissue injury in different forms of cutaneous lupus erythematosus. Br J Dermatol 2007, 157:970-980.
19. Furukawa F, Tanaka H, Sekita K, Nakamura T, Horiguchi Y, Hamashima Y. Dermatopathological studies on skin lesions of MRL mice. Arch Dermatol Res 1984, 276:186-194.
20. Andrews B S, Eisenberg R A, Theofilopoulos A N. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med 1978, 148:1198-1215.
21. Dubois E L, Horowitz R E, Demopoulos H B, Teplitz R. NZB/NZW mice as a model of systemic lupus erythematosus. JAMA 1966, 195:285-289.
22. Haugbro K, Nossent J C, Winkler T, Figenschau Y, Rekvig O P. Anti-dsDNA antibodies and disease classification in antinuclear antibody positive patients: the role of analytical diversity. Ann Rheum Dis 2004, 63:386-394.
23. Rekvig O P, Moens U, Sundsfjord A. 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.
24. Detter J C, Nguyen Q A, Kingsmore S F. Identification of novel simple sequence length polymorphisms (SSLPs) in mouse by interspersed repetitive element (IRE)-PCR. Nucleic Acids Res 1998, 26:4091-4092.
25. Zykova S N, Seredkina N, Benjaminsen J, Rekvig O P. Reduced fragmentation of apoptotic chromatin is associated with nephritis in lupus-prone (NZB x NZW)F(1) mice. Arthritis Rheum 2008, 58:813-825.
26. Tokuyasu K T. A study of positive staining of ultrathin frozen sections. J Ultrastruct Res 1978, 63:287-307.
27. Woessner J F. Matrilysin. Methods Enzymol 1995, 248:485-495.
28. Andreassen K, Bredholt G, Moens U, Bendiksen S, Kauric G, Rekvig O P. T cell lines specific for polyomavirus T-antigen recognize T-antigen complexed with nucleosomes: a molecular basis for anti-DNA antibody production. Eur J Immunol 1999, 29:2715-2728.
29. Tillman D M, Jou N T, Hill R J, Marion T N. Both IgM and IgG anti-DNA antibodies are the products of clonally selective B cell stimulation in (NZB × NZW)F1 mice. J Exp Med 1992, 176:761-779.
30. Elenitsas R, Abell E, Lee Y Y, Huang J, Deng J S. Comparison of IgG subclass autoantibodies in patients with systemic lupus erythematosus and subacute cutaneous lupus erythematosus. J Dermatol Sci 1990, 1:207-215.
31. Bennion S D, Ferris C, Lieu T S, Reimer C B, Lee L A. IgG subclasses in the serum and skin in subacute cutaneous lupus erythematosus and neonatal lupus erythematosus. J Invest Dermatol 1990, 95:643-646.
32. Alahlafi A M, Wordsworth P, Wojnarowska F. The distribution of IgG subclasses in the lupus band suggests disease-specific alteration in subclass switching rather than polyclonal B-cell activation. Clin Exp Dermatol 2004, 29:288-292.
33. Bijl M, Dijstelbloem H M, Oost W W. IgG subclass distribution of autoantibodies differs between renal and extra-renal relapses in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2002, 41:62-67.
34. Kuroki A, Shibata T, Honda H, Totsuka D, Kobayashi K, Sugisaki T. Glomerular and serum IgG subclasses in diffuse proliferative lupus nephritis, membranous lupus nephritis, and idiopathic membranous nephropathy. Intern Med 2002, 41:936-942.
35. Ravirajan C T, Rowse L, MacGowan J R, Isenberg D A. An analysis of clinical disease activity and nephritis-associated serum autoantibody profiles in patients with systemic lupus erythematosus: a cross-sectional study. Rheumatology (Oxford) 2001, 40:1405-1412.
36. Grishman E, Churg J. Ultrastructure of dermal lesions in systemic lupus erythematosus. Lab Invest 1970, 22:189-197.
37. Horiguchi Y, Furukawa F, Hamashima Y, Imamura S. Ultrastructural observations of skin lesions in MRL mice - dermoepidermal junction. Arch Dermatol Res 1984, 276:229-234.
38. Williams R C, Malone C C, Meyers C, Decker P, Muller S. Detection of nucleosome particles in serum and plasma from patients with systemic lupus erythematosus using monoclonal antibody 4H7. J Rheumatol 2001, 28:81-94.
39. Licht R, van Bruggen M C, Oppers-Walgreen B, Rijke T P, Berden J H. Plasma levels of nucleosomes and nucleosome-autoantibody complexes in murine lupus: effects of disease progression and lipopolyssacharide administration. Arthritis Rheum 2001, 44:1320-1330.
40. Amoura Z, Piette J C, Bach J F, Koutouzov S. The key role of nucleosomes in lupus. Arthritis Rheum 1999, 42:833-843.
41. Hewicker M, Kromschroder E, Trautwein G. Detection of circulating immune complexes in MRL mice with different forms of glomerulonephritis. Z Versuchstierkd 1990, 33:149-156.
42. Merrell M A, Ilvesaro J M, Lehtonen N. Toll-like receptor 9 agonists promote cellular invasion by increasing matrix metalloproteinase activity. Mol Cancer Res 2006, 4:437-447.
43. Lim E J, Lee S H, Lee J G. Toll-like receptor 9 dependent activation of MAPK and NF-kB is required for the CpG ODN-induced matrix metalloproteinase-9 expression. Exp Mol Med 2007, 39:239-245.
44. Kuhn A, Herrmann M, Kleber S. Accumulation of apoptotic cells in the epidermis of patients with cutaneous lupus erythematosus after ultraviolet irradiation. Arthritis Rheum 2006, 54:939-950.
45. Baima B, Sticherling M. Apoptosis in different cutaneous manifestations of lupus erythematosus. Br J Dermatol 2001, 144:958-966.
46. Blazsek A, Sillo P, Ishii N. Searching for foreign antigens as possible triggering factors of autoimmunity: Torque Teno virus DNA prevalence is elevated in sera of patients with bullous pemphigoid. Exp Dermatol 2008, 17:446-454.
47. Rekvig O P, Bendiksen S, Moens U. Immunity and autoimmunity induced by polyomaviruses: clinical, experimental and theoretical aspects. Adv Exp Med Biol 2006, 577:117-147.
48. Niimi Y, Pawankar R, Kawana S. Increased expression of matrix metalloproteinase-2, matrix metalloproteinase-9 and matrix metalloproteinase-13 in lesional skin of bullous pemphigoid. Int Arch Allergy Immunol 2006, 139:104-113.
49. Seredkina N, Zykova S N, Rekvig O P. Progression of murine lupus nephritis is linked to acquired renal Dnase1 deficiency and not to up-regulated apoptosis. Am J Pathol 2009, 175:97-106.
50. Basnakian A G, Apostolov E O, Yin X, Napirei M, Mannherz H G, Shah S V. Cisplatin nephrotoxicity is mediated by deoxyribonuclease I. J Am Soc Nephrol 2005, 16:697-702.