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Published in: Journal of Clinical Immunology 2/2013

01-02-2013 | Original Research

Simultaneous Positivity for Anti-DNA, Anti-Nucleosome and Anti-Histone Antibodies is a Marker for More Severe Lupus Nephritis

Authors: Mansu Sui, Qingyuan Lin, Zhaozhen Xu, Xiaojing Han, Rujuan Xie, Xiuzhi Jia, Xiaofang Guo, Weihua Zhang, Xiuru Guan, Huan Ren

Published in: Journal of Clinical Immunology | Issue 2/2013

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Abstract

Objective

The purpose of this study is to examine autoantibody profile of systemic lupus erythematosus (SLE) patients with lupus nephritis (LN) and to establish the correlation between the antibody reactivity and disease activity of LN.

Methods

Autoantibodies and serological parameters were measured and analyzed in 589 SLE patients. The associations of the co-positivity of anti-dsDNA, -nucleosome and –histone antibodies (3-pos) with clinical, serological and outcome parameters were analyzed.

Results

At the study entry, the prevalence for anti-dsDNA (61.52 % vs. 34.11 %, P < 0.0001), anti-nucleosome (56.09 % vs. 37.21 %, P = 0.0002) and anti-histone (49.35 % vs. 33.33 %, P = 0.0013) antibodies in patients with LN were significantly higher than that in patients without LN. Patients with 3-pos had a higher proportion of proliferative renal lesions (class III + IV). The incidence of a poor renal outcome (7.14 % vs. 2.52 %, P = 0.0174) in LN patients with 3-pos was significantly higher than those without 3-pos. Moreover, the rate of remission (73.63 % vs. 82.37 %, P = 0.0245) was significantly reduced and recurrence increased (58.90 % vs. 23.44 %, P < 0.0001) in 3-pos patients as compared to that in non 3-pos within the LN group.

Conclusion

Our data indicate a strong association between the 3-pos and renal disease activities, especially proliferative glomerulonephritis. The ability of 3-pos to predict renal flares may lead to major additional benefits in the follow-up of these patients.
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Literature
1.
go back to reference Riemekasten G, Hahn BH. Key autoantigens in SLE. Rheumatology (Oxford). 2005;44(8):975–82.CrossRef Riemekasten G, Hahn BH. Key autoantigens in SLE. Rheumatology (Oxford). 2005;44(8):975–82.CrossRef
3.
go back to reference Koffler D, Agnello V, Thoburn R, Kunkel HG. Systemic lupus erythematosus: prototype of immune complex nephritis in man. J Exp Med. 1971;134(3):169–79.PubMed Koffler D, Agnello V, Thoburn R, Kunkel HG. Systemic lupus erythematosus: prototype of immune complex nephritis in man. J Exp Med. 1971;134(3):169–79.PubMed
4.
go back to reference Jakes RW, Bae SC, Louthrenoo W, Mok CC, Navarra SV, Kwon N. Systematic review of the epidemiology of systemic lupus erythematosus in the Asia-Pacific region: prevalence, incidence, clinical features, and mortality. Arthritis Care Res (Hoboken). 2012;64(2):159–68.CrossRef Jakes RW, Bae SC, Louthrenoo W, Mok CC, Navarra SV, Kwon N. Systematic review of the epidemiology of systemic lupus erythematosus in the Asia-Pacific region: prevalence, incidence, clinical features, and mortality. Arthritis Care Res (Hoboken). 2012;64(2):159–68.CrossRef
5.
go back to reference Shabana AA, El-Ghawet AE, Machaly SA, Abu Hashim EM, El-Kady BA, Shaat R. Anti-chromatin and anti-histone antibodies in Egyptian patients with systemic lupus erythematosus. Clin Rheumatol. 2009;28(6):673–8.PubMedCrossRef Shabana AA, El-Ghawet AE, Machaly SA, Abu Hashim EM, El-Kady BA, Shaat R. Anti-chromatin and anti-histone antibodies in Egyptian patients with systemic lupus erythematosus. Clin Rheumatol. 2009;28(6):673–8.PubMedCrossRef
6.
go back to reference Isenberg DA, Ravirajan CT, Rahman A, Kalsi J. The role of antibodies to DNA in systemic lupus erythematosus–a review and introduction to an international workshop on DNA antibodies held in London, May 1996. Lupus. 1997;6(3):290–304.PubMedCrossRef Isenberg DA, Ravirajan CT, Rahman A, Kalsi J. The role of antibodies to DNA in systemic lupus erythematosus–a review and introduction to an international workshop on DNA antibodies held in London, May 1996. Lupus. 1997;6(3):290–304.PubMedCrossRef
7.
go back to reference Sherer Y, Gorstein A, Fritzler MJ, Shoenfeld Y. Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients. Semin Arthritis Rheum. 2004;34(2):501–37.PubMedCrossRef Sherer Y, Gorstein A, Fritzler MJ, Shoenfeld Y. Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients. Semin Arthritis Rheum. 2004;34(2):501–37.PubMedCrossRef
8.
go back to reference Kiss E, Lakos G, Szegedi G, Poor G, Szodoray P. Anti-nuscleosome antibody, a reliable indicator for lupus nephritis. Autoimmunity. 2009;42(5):393–8.PubMedCrossRef Kiss E, Lakos G, Szegedi G, Poor G, Szodoray P. Anti-nuscleosome antibody, a reliable indicator for lupus nephritis. Autoimmunity. 2009;42(5):393–8.PubMedCrossRef
9.
go back to reference Bigler C, Lopez-Trascasa M, Potlukova E, Moll S, Danner D, Schaller M, et al. Antinucleosome antibodies as a marker of active proliferative lupus nephritis. Am J Kidney Dis. 2008;51(4):624–9.PubMedCrossRef Bigler C, Lopez-Trascasa M, Potlukova E, Moll S, Danner D, Schaller M, et al. Antinucleosome antibodies as a marker of active proliferative lupus nephritis. Am J Kidney Dis. 2008;51(4):624–9.PubMedCrossRef
10.
go back to reference Ahlin E, Mathsson L, Eloranta ML, Jonsdottir T, Gunnarsson I, Ronnblom L, et al. Autoantibodies associated with RNA are more enriched than anti-dsDNA antibodies in circulating immune complexes in SLE. Lupus. 2012;21(6):586–95.PubMedCrossRef Ahlin E, Mathsson L, Eloranta ML, Jonsdottir T, Gunnarsson I, Ronnblom L, et al. Autoantibodies associated with RNA are more enriched than anti-dsDNA antibodies in circulating immune complexes in SLE. Lupus. 2012;21(6):586–95.PubMedCrossRef
11.
go back to reference Jaekell HP, Trabandt A, Grobe N, Werle E. Anti-dsDNA antibody subtypes and anti-C1q antibodies: toward a more reliable diagnosis and monitoring of systemic lupus erythematosus and lupus nephritis. Lupus. 2006;15(6):335–45.PubMedCrossRef Jaekell HP, Trabandt A, Grobe N, Werle E. Anti-dsDNA antibody subtypes and anti-C1q antibodies: toward a more reliable diagnosis and monitoring of systemic lupus erythematosus and lupus nephritis. Lupus. 2006;15(6):335–45.PubMedCrossRef
12.
go back to reference Cortes-Hernandez J, Ordi-Ros J, Labrador M, Bujan S, Balada E, Segarra A, et al. Antihistone and anti-double-stranded deoxyribonucleic acid antibodies are associated with renal disease in systemic lupus erythematosus. Am J Med. 2004;116(3):165–73.PubMedCrossRef Cortes-Hernandez J, Ordi-Ros J, Labrador M, Bujan S, Balada E, Segarra A, et al. Antihistone and anti-double-stranded deoxyribonucleic acid antibodies are associated with renal disease in systemic lupus erythematosus. Am J Med. 2004;116(3):165–73.PubMedCrossRef
13.
go back to reference Isenberg DA, Manson JJ, Ehrenstein MR, Rahman A. Fifty years of anti-ds DNA antibodies: are we approaching journey’s end? Rheumatology (Oxford). 2007;46(7):1052–6.CrossRef Isenberg DA, Manson JJ, Ehrenstein MR, Rahman A. Fifty years of anti-ds DNA antibodies: are we approaching journey’s end? Rheumatology (Oxford). 2007;46(7):1052–6.CrossRef
14.
go back to reference Linnik MD, Hu JZ, Heilbrunn KR, Strand V, Hurley FL, Joh T. Relationship between anti-double-stranded DNA antibodies and exacerbation of renal disease in patients with systemic lupus erythematosus. Arthritis Rheum. 2005;52(4):1129–37.PubMedCrossRef Linnik MD, Hu JZ, Heilbrunn KR, Strand V, Hurley FL, Joh T. Relationship between anti-double-stranded DNA antibodies and exacerbation of renal disease in patients with systemic lupus erythematosus. Arthritis Rheum. 2005;52(4):1129–37.PubMedCrossRef
15.
go back to reference Ho A, Magder LS, Barr SG, Petri M. Decreases in anti-double-stranded DNA levels are associated with concurrent flares in patients with systemic lupus erythematosus. Arthritis Rheum. 2001;44(10):2342–9.PubMedCrossRef Ho A, Magder LS, Barr SG, Petri M. Decreases in anti-double-stranded DNA levels are associated with concurrent flares in patients with systemic lupus erythematosus. Arthritis Rheum. 2001;44(10):2342–9.PubMedCrossRef
16.
go back to reference Cairns AP, McMillan SA, Crockard AD, Meenagh GK, Duffy EM, Armstrong DJ, et al. Antinucleosome antibodies in the diagnosis of systemic lupus erythematosus. Ann Rheum Dis. 2003;62(3):272–3.PubMedCrossRef Cairns AP, McMillan SA, Crockard AD, Meenagh GK, Duffy EM, Armstrong DJ, et al. Antinucleosome antibodies in the diagnosis of systemic lupus erythematosus. Ann Rheum Dis. 2003;62(3):272–3.PubMedCrossRef
17.
go back to reference Ng KP, Manson JJ, Rahman A, Isenberg DA. Association of antinucleosome antibodies with disease flare in serologically active clinically quiescent patients with systemic lupus erythematosus. Arthritis Rheum. 2006;55(6):900–4.PubMedCrossRef Ng KP, Manson JJ, Rahman A, Isenberg DA. Association of antinucleosome antibodies with disease flare in serologically active clinically quiescent patients with systemic lupus erythematosus. Arthritis Rheum. 2006;55(6):900–4.PubMedCrossRef
18.
go back to reference Amoura Z, Chabre H, Koutouzov S, Lotton C, Cabrespines A, Bach JF, et al. Nucleosome-restricted antibodies are detected before anti-dsDNA and/or antihistone antibodies in serum of MRL-Mp lpr/lpr and +/+ mice, and are present in kidney eluates of lupus mice with proteinuria. Arthritis Rheum. 1994;37(11):1684–8.PubMedCrossRef Amoura Z, Chabre H, Koutouzov S, Lotton C, Cabrespines A, Bach JF, et al. Nucleosome-restricted antibodies are detected before anti-dsDNA and/or antihistone antibodies in serum of MRL-Mp lpr/lpr and +/+ mice, and are present in kidney eluates of lupus mice with proteinuria. Arthritis Rheum. 1994;37(11):1684–8.PubMedCrossRef
19.
go back to reference Gomez-Puerta JA, Burlingame RW, Cervera R. Anti-chromatin (anti-nucleosome) antibodies: diagnostic and clinical value. Autoimmun Rev. 2008;7(8):606–11.PubMedCrossRef Gomez-Puerta JA, Burlingame RW, Cervera R. Anti-chromatin (anti-nucleosome) antibodies: diagnostic and clinical value. Autoimmun Rev. 2008;7(8):606–11.PubMedCrossRef
20.
go back to reference Cervera R, Vinas O, Ramos-Casals M, Font J, Garcia-Carrasco M, Siso A, et al. Anti-chromatin antibodies in systemic lupus erythematosus: a useful marker for lupus nephropathy. Ann Rheum Dis. 2003;62(5):431–4.PubMedCrossRef Cervera R, Vinas O, Ramos-Casals M, Font J, Garcia-Carrasco M, Siso A, et al. Anti-chromatin antibodies in systemic lupus erythematosus: a useful marker for lupus nephropathy. Ann Rheum Dis. 2003;62(5):431–4.PubMedCrossRef
21.
go back to reference Hung W, Chen Y, Lan J, Chen H, Chen D, Hsieh C, et al. Antinucleosome antibodies as a potential biomarker for the evaluation of renal pathological activity in patients with proliferative lupus nephritis. Lupus. 2011;20(13):1404–10.PubMedCrossRef Hung W, Chen Y, Lan J, Chen H, Chen D, Hsieh C, et al. Antinucleosome antibodies as a potential biomarker for the evaluation of renal pathological activity in patients with proliferative lupus nephritis. Lupus. 2011;20(13):1404–10.PubMedCrossRef
22.
go back to reference van der Vlag J, Berden JH. Lupus nephritis: role of antinucleosome autoantibodies. Semin Nephrol. 2011;31(4):376–89.PubMedCrossRef van der Vlag J, Berden JH. Lupus nephritis: role of antinucleosome autoantibodies. Semin Nephrol. 2011;31(4):376–89.PubMedCrossRef
23.
go back to reference Marto N, Bertolaccini ML, Calabuig E, Hughes GR, Khamashta MA. Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis. 2005;64(3):444–8.PubMedCrossRef Marto N, Bertolaccini ML, Calabuig E, Hughes GR, Khamashta MA. Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis. 2005;64(3):444–8.PubMedCrossRef
24.
go back to reference Trendelenburg M, Lopez-Trascasa M, Potlukova E, Moll S, Regenass S, Fremeaux-Bacchi V, et al. High prevalence of anti-C1q antibodies in biopsy-proven active lupus nephritis. Nephrol Dial Transplant. 2006;21(11):3115–21.PubMedCrossRef Trendelenburg M, Lopez-Trascasa M, Potlukova E, Moll S, Regenass S, Fremeaux-Bacchi V, et al. High prevalence of anti-C1q antibodies in biopsy-proven active lupus nephritis. Nephrol Dial Transplant. 2006;21(11):3115–21.PubMedCrossRef
25.
go back to reference Seelen MA, Trouw LA, Daha MR. Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens. 2003;12(6):619–24.PubMedCrossRef Seelen MA, Trouw LA, Daha MR. Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens. 2003;12(6):619–24.PubMedCrossRef
26.
go back to reference Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, et al. Are laboratory tests useful for monitoring the activity of lupus nephritis? A 6-year prospective study in a cohort of 228 patients with lupus nephritis. Ann Rheum Dis. 2009;68(2):234–7.PubMedCrossRef Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, et al. Are laboratory tests useful for monitoring the activity of lupus nephritis? A 6-year prospective study in a cohort of 228 patients with lupus nephritis. Ann Rheum Dis. 2009;68(2):234–7.PubMedCrossRef
27.
go back to reference Katsumata Y, Miyake K, Kawaguchi Y, Okamoto Y, Kawamoto M, Gono T, et al. Anti-C1q antibodies are associated with systemic lupus erythematosus global activity but not specifically with nephritis: a controlled study of 126 consecutive patients. Arthritis Rheum. 2011;63(8):2436–44.PubMedCrossRef Katsumata Y, Miyake K, Kawaguchi Y, Okamoto Y, Kawamoto M, Gono T, et al. Anti-C1q antibodies are associated with systemic lupus erythematosus global activity but not specifically with nephritis: a controlled study of 126 consecutive patients. Arthritis Rheum. 2011;63(8):2436–44.PubMedCrossRef
28.
go back to reference Meyer OC, Nicaise-Roland P, Cadoudal N, Grootenboer-Mignot S, Palazzo E, Hayem G, et al. Anti-C1q antibodies antedate patent active glomerulonephritis in patients with systemic lupus erythematosus. Arthritis Res Ther. 2009;11(3):R87.PubMedCrossRef Meyer OC, Nicaise-Roland P, Cadoudal N, Grootenboer-Mignot S, Palazzo E, Hayem G, et al. Anti-C1q antibodies antedate patent active glomerulonephritis in patients with systemic lupus erythematosus. Arthritis Res Ther. 2009;11(3):R87.PubMedCrossRef
29.
go back to reference Becker-Merok A, Kalaaji M, Haugbro K, Nikolaisen C, Nilsen K, Rekvig OP, et al. Alpha-actinin-binding antibodies in relation to systemic lupus erythematosus and lupus nephritis. Arthritis Res Ther. 2006;8(6):R162.PubMedCrossRef Becker-Merok A, Kalaaji M, Haugbro K, Nikolaisen C, Nilsen K, Rekvig OP, et al. Alpha-actinin-binding antibodies in relation to systemic lupus erythematosus and lupus nephritis. Arthritis Res Ther. 2006;8(6):R162.PubMedCrossRef
30.
go back to reference Mason LJ, Ravirajan CT, Rahman A, Putterman C, Isenberg DA. Is alpha-actinin a target for pathogenic anti-DNA antibodies in lupus nephritis? Arthritis Rheum. 2004;50(3):866–70.PubMedCrossRef Mason LJ, Ravirajan CT, Rahman A, Putterman C, Isenberg DA. Is alpha-actinin a target for pathogenic anti-DNA antibodies in lupus nephritis? Arthritis Rheum. 2004;50(3):866–70.PubMedCrossRef
31.
go back to reference Matrat A, Veysseyre-Balter C, Trolliet P, Villar E, Dijoud F, Bienvenu J, et al. Simultaneous detection of anti-C1q and anti-double stranded DNA autoantibodies in lupus nephritis: predictive value for renal flares. Lupus. 2011;20(1):28–34.PubMedCrossRef Matrat A, Veysseyre-Balter C, Trolliet P, Villar E, Dijoud F, Bienvenu J, et al. Simultaneous detection of anti-C1q and anti-double stranded DNA autoantibodies in lupus nephritis: predictive value for renal flares. Lupus. 2011;20(1):28–34.PubMedCrossRef
32.
go back to reference Grootscholten C, van Bruggen MC, van der Pijl JW, de Jong EM, Ligtenberg G, Derksen RH, et al. Deposition of nucleosomal antigens (histones and DNA) in the epidermal basement membrane in human lupus nephritis. Arthritis Rheum. 2003;48(5):1355–62.PubMedCrossRef Grootscholten C, van Bruggen MC, van der Pijl JW, de Jong EM, Ligtenberg G, Derksen RH, et al. Deposition of nucleosomal antigens (histones and DNA) in the epidermal basement membrane in human lupus nephritis. Arthritis Rheum. 2003;48(5):1355–62.PubMedCrossRef
33.
go back to reference Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25(11):1271–7.PubMedCrossRef Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25(11):1271–7.PubMedCrossRef
34.
go back to reference Weening JJ, D’Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int. 2004;65(2):521–30.PubMedCrossRef Weening JJ, D’Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int. 2004;65(2):521–30.PubMedCrossRef
35.
go back to reference Mosca M, Pasquariello A, Tavoni A, Moriconi L, Moneta I, Innocenti M, et al. Predictors of renal outcome in diffuse proliferative glomerulonephritis in systemic lupus erythematosus. Lupus. 1997;6(4):371–8.PubMedCrossRef Mosca M, Pasquariello A, Tavoni A, Moriconi L, Moneta I, Innocenti M, et al. Predictors of renal outcome in diffuse proliferative glomerulonephritis in systemic lupus erythematosus. Lupus. 1997;6(4):371–8.PubMedCrossRef
36.
go back to reference Austin III HA, Muenz LR, Joyce KM, Antonovych TA, Kullick ME, Klippel JH, et al. Prognostic factors in lupus nephritis. Contribution of renal histologic data. Am J Med. 1983;75(3):382–91.PubMedCrossRef Austin III HA, Muenz LR, Joyce KM, Antonovych TA, Kullick ME, Klippel JH, et al. Prognostic factors in lupus nephritis. Contribution of renal histologic data. Am J Med. 1983;75(3):382–91.PubMedCrossRef
37.
go back to reference Bertsias G, Boumpas DT. Update on the management of lupus nephritis: let the treatment fit the patient. Nat Clin Pract Rheumatol. 2008;4(9):464–72.PubMedCrossRef Bertsias G, Boumpas DT. Update on the management of lupus nephritis: let the treatment fit the patient. Nat Clin Pract Rheumatol. 2008;4(9):464–72.PubMedCrossRef
38.
go back to reference Mosca M, Bencivelli W, Neri R, Pasquariello A, Batini V, Puccini R, et al. Renal flares in 91 SLE patients with diffuse proliferative glomerulonephritis. Kidney Int. 2002;61(4):1502–9.PubMedCrossRef Mosca M, Bencivelli W, Neri R, Pasquariello A, Batini V, Puccini R, et al. Renal flares in 91 SLE patients with diffuse proliferative glomerulonephritis. Kidney Int. 2002;61(4):1502–9.PubMedCrossRef
39.
go back to reference Strasser A, Huang DC, Vaux DL. The role of the bcl-2/ced-9 gene family in cancer and general implications of defects in cell death control for tumourigenesis and resistance to chemotherapy. Biochim Biophys Acta. 1997;1333(2):F151–78.PubMed Strasser A, Huang DC, Vaux DL. The role of the bcl-2/ced-9 gene family in cancer and general implications of defects in cell death control for tumourigenesis and resistance to chemotherapy. Biochim Biophys Acta. 1997;1333(2):F151–78.PubMed
40.
go back to reference Dieker JW, Fransen JH, van Bavel CC, Briand JP, Jacobs CW, Muller S, et al. Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum. 2007;56(6):1921–33.PubMedCrossRef Dieker JW, Fransen JH, van Bavel CC, Briand JP, Jacobs CW, Muller S, et al. Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum. 2007;56(6):1921–33.PubMedCrossRef
41.
go back to reference van Bavel CC, Fenton KA, Rekvig OP, van der Vlag J, Berden JH. Glomerular targets of nephritogenic autoantibodies in systemic lupus erythematosus. Arthritis Rheum. 2008;58(7):1892–9.PubMedCrossRef van Bavel CC, Fenton KA, Rekvig OP, van der Vlag J, Berden JH. Glomerular targets of nephritogenic autoantibodies in systemic lupus erythematosus. Arthritis Rheum. 2008;58(7):1892–9.PubMedCrossRef
42.
go back to reference Jorgensen MH, Rekvig OP, Jacobsen RS, Jacobsen S, Fenton KA. Circulating levels of chromatin fragments are inversely correlated with anti-dsDNA antibody levels in human and murine systemic lupus erythematosus. Immunol Lett. 2011;138(2):179–86.PubMedCrossRef Jorgensen MH, Rekvig OP, Jacobsen RS, Jacobsen S, Fenton KA. Circulating levels of chromatin fragments are inversely correlated with anti-dsDNA antibody levels in human and murine systemic lupus erythematosus. Immunol Lett. 2011;138(2):179–86.PubMedCrossRef
43.
go back to reference Fismen S, Hedberg A, Fenton KA, Jacobsen S, Krarup E, Kamper AL, et al. Circulating chromatin-anti-chromatin antibody complexes bind with high affinity to dermo-epidermal structures in murine and human lupus nephritis. Lupus. 2009;18(7):597–607.PubMedCrossRef Fismen S, Hedberg A, Fenton KA, Jacobsen S, Krarup E, Kamper AL, et al. Circulating chromatin-anti-chromatin antibody complexes bind with high affinity to dermo-epidermal structures in murine and human lupus nephritis. Lupus. 2009;18(7):597–607.PubMedCrossRef
44.
go back to reference Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16):1526–33.PubMedCrossRef Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16):1526–33.PubMedCrossRef
Metadata
Title
Simultaneous Positivity for Anti-DNA, Anti-Nucleosome and Anti-Histone Antibodies is a Marker for More Severe Lupus Nephritis
Authors
Mansu Sui
Qingyuan Lin
Zhaozhen Xu
Xiaojing Han
Rujuan Xie
Xiuzhi Jia
Xiaofang Guo
Weihua Zhang
Xiuru Guan
Huan Ren
Publication date
01-02-2013
Publisher
Springer US
Published in
Journal of Clinical Immunology / Issue 2/2013
Print ISSN: 0271-9142
Electronic ISSN: 1573-2592
DOI
https://doi.org/10.1007/s10875-012-9825-6

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