Anti-dsDNA antibodies and resident renal cells — Their putative roles in pathogenesis of renal lesions in lupus nephritis

Clinical Immunology

Volumn 185, Issue , 2017, Pages 40-50

  Yung, Susan ^a   Chan, Tak Mao ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Anti dsDNA antibodies; Endothelial cells; Fibrosis; Inflammation; Lupus nephritis; Mesangial cells; Proximal renal tubular epithelial cells

Indexed keywords

CELL NUCLEUS ANTIGEN; DEOXYRIBONUCLEASE I; DOUBLE STRANDED DNA ANTIBODY; MYCOPHENOLATE MOFETIL; ANTIINFLAMMATORY AGENT; ANTINUCLEAR ANTIBODY; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLIC ACID;

ANTIBODY DETECTION; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; APOPTOSIS; ARTICLE; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CELL PROLIFERATION; CLEARANCE; DRUG EFFECT; ENDOTHELIUM CELL; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY CELL; KIDNEY FIBROSIS; KIDNEY INJURY; KIDNEY PARENCHYMA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; LUPUS ERYTHEMATOSUS NEPHRITIS; MESANGIUM CELL; PRIORITY JOURNAL; ANIMAL; FIBROSIS; HUMAN; IMMUNOLOGY; KIDNEY; PATHOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIBODIES, ANTINUCLEAR; ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; DEOXYRIBONUCLEASE I; FIBROSIS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; KIDNEY; LUPUS NEPHRITIS; MYCOPHENOLIC ACID;

EID: 85008957426     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.09.002     Document Type: Article

References (165)

1. Kurts, C., Panzer, U., Anders, H.J., Rees, A.J., The immune system and kidney disease: basic concepts and clinical implications. Nat. Rev. Immunol. 13 (2013), 738–753.
2. Scott, R.P., Quaggin, S.E., Review series: the cell biology of renal filtration. J. Cell Biol. 209 (2015), 199–210.
3. Miner, J.H., The glomerular basement membrane. Exp. Cell Res. 318 (2012), 973–978.
4. Cameron, J.S., Lupus nephritis. J. Am. Soc. Nephrol. 10 (1999), 413–424.
5. Mohan, C., Putterman, C., Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis. Nat. Rev. Nephrol. 11 (2015), 329–341.
6. Park, M.H., D'Agati, V., Appel, G.B., Pirani, C.L., Tubulointerstitial disease in lupus nephritis: relationship to immune deposits, interstitial inflammation, glomerular changes, renal function, and prognosis. Nephron 44 (1986), 309–319.
7. Magil, A.B., Tyler, M., Tubulo-interstitial disease in lupus nephritis. A morphometric study. Histopathology 8 (1984), 81–87.
8. Yung, S., Tsang, R.C., Sun, Y., Leung, J.K., Chan, T.M., Effect of human anti-DNA antibodies on proximal renal tubular epithelial cell cytokine expression: implications on tubulointerstitial inflammation in lupus nephritis. J. Am. Soc. Nephrol. 16 (2005), 3281–3294.
9. Weening, J.J., D'Agati, V.D., Schwartz, M.M., Seshan, S.V., Alpers, C.E., Appel, G.B., Balow, J.E., Bruijn, J.A., Cook, T., Ferrario, F., Fogo, A.B., Ginzler, E.M., Hebert, L., Hill, G., Hill, P., Jennette, J.C., Kong, N.C., Lesavre, P., Lockshin, M., Looi, L.M., Makino, H., Moura, L.A., Nagata, M., The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int. 65 (2004), 521–530.
10. Waldman, M., Madaio, M.P., Pathogenic autoantibodies in lupus nephritis. Lupus 14 (2005), 19–24.
11. Davidson, A., Berthier, C.C., Kretzler, M., Pathogenetic Mechanisms in Lupus Nephritis. Wallace, D.J., Hahn, B.H., (eds.) Dubois' Lupus Erythematosus and Related Syndromes, 2008, Elsevier Philadelphia, 237–255.
12. Hahn, B.H., The Pathogenesis of SLE. Wallace, D.J., Hahn, B.H., (eds.) Dubois' Lupus Erythematosus and Related Syndromes, 2013, Elsevier Saunders, Philadelphia, 25–34.
13. Lech, M., Anders, H.J., The pathogenesis of lupus nephritis. J. Am. Soc. Nephrol. 24 (2013), 1357–1366.
14. Allam, R., Anders, H.J., The role of innate immunity in autoimmune tissue injury. Curr. Opin. Rheumatol. 20 (2008), 538–544.
15. Fenton, K., Fismen, S., Hedberg, A., Seredkina, N., Fenton, C., Mortensen, E.S., Rekvig, O.P., 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.
16. Sherer, Y., Gorstein, A., Fritzler, M.J., Shoenfeld, Y., Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients. Semin. Arthritis Rheum. 34 (2004), 501–537.
17. 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. 175 (2009), 97–106.
18. Mevorach, D., Zhou, J.L., Song, X., Elkon, K.B., Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 188 (1998), 387–392.
19. Savill, J., Dransfield, I., Gregory, C., Haslett, C., A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2 (2002), 965–975.
20. Napirei, M., Karsunky, H., Zevnik, B., Stephan, H., Mannherz, H.G., Moroy, T., Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 25 (2000), 177–181.
21. Bickerstaff, M.C., Botto, M., Hutchinson, W.L., Herbert, J., Tennent, G.A., Bybee, A., Mitchell, D.A., Cook, H.T., Butler, P.J., Walport, M.J., Pepys, M.B., Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 5 (1999), 694–697.
22. Fismen, S., Thiyagarajan, D., Seredkina, N., Nielsen, H., Jacobsen, S., Elung-Jensen, T., Kamper, A.L., Johansen, S.D., Mortensen, E.S., Rekvig, O.P., Impact of the tumor necrosis factor receptor-associated protein 1 (Trap1) on renal DNaseI shutdown and on progression of murine and human lupus nephritis. Am. J. Pathol. 182 (2013), 688–700.
23. Thiyagarajan, D., Fismen, S., Seredkina, N., Jacobsen, S., Elung-Jensen, T., Kamper, A.L., Fenton, C.G., Rekvig, O.P., Mortensen, E.S., Silencing of renal DNaseI in murine lupus nephritis imposes exposure of large chromatin fragments and activation of toll like receptors and the Clec4e. PLoS One, 7, 2012, e34080.
24. Zykova, S.N., Tveita, A.A., Rekvig, O.P., Renal Dnase1 enzyme activity and protein expression is selectively shut down in murine and human membranoproliferative lupus nephritis. PLoS One, 5, 2010, e12096.
25. Madaio, M.P., Fabbi, M., Tiso, M., Daga, A., Puccetti, A., Spontaneously produced anti-DNA/DNase I autoantibodies modulate nuclear apoptosis in living cells. Eur. J. Immunol. 26 (1996), 3035–3041.
26. Chitrabamrung, S., Rubin, R.L., Tan, E.M., Serum deoxyribonuclease I and clinical activity in systemic lupus erythematosus. Rheumatol. Int. 1 (1981), 55–60.
27. Arbuckle, M.R., McClain, M.T., Rubertone, M.V., Scofield, R.H., Dennis, G.J., James, J.A., Harley, J.B., Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349 (2003), 1526–1533.
28. Tan, E.M., Cohen, A.S., Fries, J.F., Masi, A.T., McShane, D.J., Rothfield, N.F., Schaller, J.G., Talal, N., Winchester, R.J., The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25 (1982), 1271–1277.
29. Isenberg, D.A., Manson, J.J., Ehrenstein, M.R., Rahman, A., Fifty years of anti-ds DNA antibodies: are we approaching journey's end?. Rheumatology (Oxford) 46 (2007), 1052–1056.
30. Chan, T.M., Leung, J.K., Ho, S.K., Yung, S., Mesangial cell-binding anti-DNA antibodies in patients with systemic lupus erythematosus. J. Am. Soc. Nephrol. 13 (2002), 1219–1229.
31. Rahman, A., Isenberg, D.A., Systemic lupus erythematosus. N. Engl. J. Med. 358 (2008), 929–939.
32. Hahn, B.H., Antibodies to DNA. N. Engl. J. Med. 338 (1998), 1359–1368.
33. Foster, M.H., Cizman, B., Madaio, M.P., Nephritogenic autoantibodies in systemic lupus erythematosus: immunochemical properties, mechanisms of immune deposition, and genetic origins. Lab. Investig. 69 (1993), 494–507.
34. Yung, S., Chan, T.M., Anti-DNA antibodies in the pathogenesis of lupus nephritis — the emerging mechanisms. Autoimmun. Rev. 7 (2008), 317–321.
35. Radic, M.Z., Weigert, M., Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 12 (1994), 487–520.
36. Xia, Y., Pawar, R.D., Nakouzi, A.S., Herlitz, L., Broder, A., Liu, K., Goilav, B., Fan, M., Wang, L., Li, Q.Z., Casadevall, A., Putterman, C., The constant region contributes to the antigenic specificity and renal pathogenicity of murine anti-DNA antibodies. J. Autoimmun. 39 (2012), 398–411.
37. Smeenk, R.J., Methodological update detection of antibodies to dsDNA: current insights into its relevance. Clin. Exp. Rheumatol. 20 (2002), 294–300.
38. Aarden, L.A., de Groot, E.R., Feltkamp, T.E., Immunology of DNA. III. Crithidia luciliae, a simple substrate for the determination of anti-dsDNA with the immunofluorescence technique. Ann. N. Y. Acad. Sci. 254 (1975), 505–515.
39. Madaio, M.P., Hodder, S., Schwartz, R.S., Stollar, B.D., Responsiveness of autoimmune and normal mice to nucleic acid antigens. J. Immunol. 132 (1984), 872–876.
40. Tsao, B.P., Ohnishi, K., Cheroutre, H., Mitchell, B., Teitell, M., Mixter, P., Kronenberg, M., Hahn, B.H., Failed self-tolerance and autoimmunity in IgG anti-DNA transgenic mice. J. Immunol. 149 (1992), 350–358.
41. Vlahakos, D.V., Foster, M.H., Adams, S., Katz, M., Ucci, A.A., Barrett, K.J., Datta, S.K., Madaio, M.P., Anti-DNA antibodies form immune deposits at distinct glomerular and vascular sites. Kidney Int. 41 (1992), 1690–1700.
42. Raz, E., Brezis, M., Rosenmann, E., Eilat, D., Anti-DNA antibodies bind directly to renal antigens and induce kidney dysfunction in the isolated perfused rat kidney. J. Immunol. 142 (1989), 3076–3082.
43. Kramers, C., Hylkema, M.N., van Bruggen, M.C., van de Lagemaat, R., Dijkman, H.B., Assmann, K.J., Smeenk, R.J., Berden, J.H., Anti-nucleosome antibodies complexed to nucleosomal antigens show anti-DNA reactivity and bind to rat glomerular basement membrane in vivo. J. Clin. Invest. 94 (1994), 568–577.
44. D'Andrea, D.M., Coupaye-Gerard, B., Kleyman, T.R., Foster, M.H., Madaio, M.P., Lupus autoantibodies interact directly with distinct glomerular and vascular cell surface antigens. Kidney Int. 49 (1996), 1214–1221.
45. Blatt, N.B., Glick, G.D., Anti-DNA autoantibodies and systemic lupus erythematosus. Pharmacol. Ther. 83 (1999), 125–139.
46. Krishnan, M.R., Wang, C., Marion, T.N., Anti-DNA autoantibodies initiate experimental lupus nephritis by binding directly to the glomerular basement membrane in mice. Kidney Int. 82 (2012), 184–192.
47. Rosetti, F., Tsuboi, N., Chen, K., Nishi, H., Ernandez, T., Sethi, S., Croce, K., Stavrakis, G., Alcocer-Varela, J., Gomez-Martin, D., van Rooijen, N., Kyttaris, V.C., Lichtman, A.H., Tsokos, G.C., Mayadas, T.N., Human lupus serum induces neutrophil-mediated organ damage in mice that is enabled by Mac-1 deficiency. J. Immunol. 189 (2012), 3714–3723.
48. Deng, Y., Tsao, B.P., Genetics of Human SLE. Wallace, D.J., Hahn, B.H., (eds.) Dubois' Lupus Erythematosus and Related Syndromes, 2008, Elsevier Saunders, Philadelphia, 35–45.
49. Hepburn, A.L., Mason, J.C., Wang, S., Shepherd, C.J., Florey, O., Haskard, D.O., Davies, K.A., Both Fcgamma and complement receptors mediate transfer of immune complexes from erythrocytes to human macrophages under physiological flow conditions in vitro. Clin. Exp. Immunol. 146 (2006), 133–145.
50. Nath, S.K., Han, S., Kim-Howard, X., Kelly, J.A., Viswanathan, P., Gilkeson, G.S., Chen, W., Zhu, C., McEver, R.P., Kimberly, R.P., Alarcon-Riquelme, M.E., Vyse, T.J., Li, Q.Z., Wakeland, E.K., Merrill, J.T., James, J.A., Kaufman, K.M., Guthridge, J.M., Harley, J.B., A nonsynonymous functional variant in integrin-alpha(M) (encoded by ITGAM) is associated with systemic lupus erythematosus. Nat. Genet. 40 (2008), 152–154.
51. Liu, K., Li, Q.Z., Delgado-Vega, A.M., Abelson, A.K., Sanchez, E., Kelly, J.A., Li, L., Liu, Y., Zhou, J., Yan, M., Ye, Q., Liu, S., Xie, C., Zhou, X.J., Chung, S.A., Pons-Estel, B., Witte, T., de Ramon, E., Bae, S.C., Barizzone, N., Sebastiani, G.D., Merrill, J.T., Gregersen, P.K., Gilkeson, G.G., Kimberly, R.P., Vyse, T.J., Kim, I., D'Alfonso, S., Martin, J., Harley, J.B., Criswell, L.A., Wakeland, E.K., Alarcon-Riquelme, M.E., Mohan, C., Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. J. Clin. Invest. 119 (2009), 911–923.
52. Shao, X., Yang, R., Yan, M., Li, Y., Du, Y., Raman, I., Zhang, B., Wakeland, E.K., Igarashi, P., Mohan, C., Li, Q.Z., Inducible expression of kallikrein in renal tubular cells protects mice against spontaneous lupus nephritis. Arthritis Rheum. 65 (2013), 780–791.
53. Deocharan, B., Qing, X., Lichauco, J., Putterman, C., Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J. Immunol. 168 (2002), 3072–3078.
54. Mostoslavsky, G., Fischel, R., Yachimovich, N., Yarkoni, Y., Rosenmann, E., Monestier, M., Baniyash, M., Eilat, D., Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry. Eur. J. Immunol. 31 (2001), 1221–1227.
55. Yung, S., Cheung, K.F., Zhang, Q., Chan, T.M., Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis. J. Am. Soc. Nephrol. 21 (2010), 1912–1927.
56. Suzuki, N., Harada, T., Mizushima, Y., Sakane, T., Possible pathogenic role of cationic anti-DNA autoantibodies in the development of nephritis in patients with systemic lupus erythematosus. J. Immunol. 151 (1993), 1128–1136.
57. Yung, S., Chan, T.M., Autoantibodies and resident renal cells in the pathogenesis of lupus nephritis: getting to know the unknown. Clin. Dev. Immunol., 2012, 2012, 139365.
58. 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. 168 (2006), 1779–1792.
59. Mortensen, E.S., Rekvig, O.P., Nephritogenic potential of anti-DNA antibodies against necrotic nucleosomes. J. Am. Soc. Nephrol. 20 (2009), 696–704.
60. Putterman, C., New approaches to the renal pathogenicity of anti-DNA antibodies in systemic lupus erythematosus. Autoimmun. Rev. 3 (2004), 7–11.
61. Yung, S., Chan, T.M., Mechanisms of kidney injury in lupus nephritis — the role of anti-dsDNA antibodies. Front. Immunol., 6, 2015, 475.
62. Yung, S., Chan, T.M., Molecular and immunological basis of tubulo-interstitial injury in lupus nephritis: a comprehensive review. Clin. Rev. Allergy Immunol., 2016 In press.
63. Berden, J.H., Licht, R., van Bruggen, M.C., Tax, W.J., Role of nucleosomes for induction and glomerular binding of autoantibodies in lupus nephritis. Curr. Opin. Nephrol. Hypertens. 8 (1999), 299–306.
64. Rekvig, O.P., Nossent, J.C., Anti-double-stranded DNA antibodies, nucleosomes, and systemic lupus erythematosus: a time for new paradigms?. Arthritis Rheum. 48 (2003), 300–312.
65. Yung, S., Tsang, R.C., Leung, J.K., Chan, T.M., Increased mesangial cell hyaluronan expression in lupus nephritis is mediated by anti-DNA antibody-induced IL-1beta. Kidney Int. 69 (2006), 272–280.
66. Yung, S., Zhang, Q., Chau, M.K., Chan, T.M., Distinct effects of mycophenolate mofetil and cyclophosphamide on renal fibrosis in NZBWF1/J mice. Autoimmunity 48 (2015), 471–487.
67. Yung, S., Zhang, Q., Zhang, C.Z., Chan, K.W., Lui, S.L., Chan, T.M., Anti-DNA antibody induction of protein kinase C phosphorylation and fibronectin synthesis in human and murine lupus and the effect of mycophenolic acid. Arthritis Rheum. 60 (2009), 2071–2082.
68. Qing, X., Pitashny, M., Thomas, D.B., Barrat, F.J., Hogarth, M.P., Putterman, C., Pathogenic anti-DNA antibodies modulate gene expression in mesangial cells: involvement of HMGB1 in anti-DNA antibody-induced renal injury. Immunol. Lett. 121 (2008), 61–73.
69. Qing, X., Zavadil, J., Crosby, M.B., Hogarth, M.P., Hahn, B.H., Mohan, C., Gilkeson, G.S., Bottinger, E.P., Putterman, C., Nephritogenic anti-DNA antibodies regulate gene expression in MRL/lpr mouse glomerular mesangial cells. Arthritis Rheum. 54 (2006), 2198–2210.
70. Zhang, H., Zhao, C., Wang, S., Huang, Y., Wang, H., Zhao, J., Yang, N., Anti-dsDNA antibodies induce inflammation via endoplasmic reticulum stress in human mesangial cells. J. Transl. Med., 13, 2015, 178.
71. Yu, C.L., Huang, M.H., Tsai, C.Y., Tsai, Y.Y., Tsai, S.T., Sun, K.H., Han, S.H., Yu, H.S., The effect of human polyclonal anti-dsDNA autoantibodies on apoptotic gene expression in cultured rat glomerular mesangial cells. Scand. J. Rheumatol. 27 (1998), 54–60.
72. Yung, S., Ng, C.Y., Ho, S.K., Cheung, K.F., Chan, K.W., Zhang, Q., Chau, M.K., Chan, T.M., Anti-dsDNA antibody induces soluble fibronectin secretion by proximal renal tubular epithelial cells and downstream increase of TGF-beta1 and collagen synthesis. J. Autoimmun. 58 (2015), 111–122.
73. Fenton, K.A., Tommeras, B., Marion, T.N., Rekvig, O.P., Pure anti-dsDNA mAbs need chromatin structures to promote glomerular mesangial deposits in BALB/c mice. Autoimmunity 43 (2010), 179–188.
74. Chan, T.M., Frampton, G., Staines, N.A., Hobby, P., Perry, G.J., Cameron, J.S., Different mechanisms by which anti-DNA MoAbs bind to human endothelial cells and glomerular mesangial cells. Clin. Exp. Immunol. 88 (1992), 68–74.
75. Sun, K.H., Liu, W.T., Tang, S.J., Tsai, C.Y., Hsieh, S.C., Wu, T.H., Han, S.H., Yu, C.L., The expression of acidic ribosomal phosphoproteins on the surface membrane of different tissues in autoimmune and normal mice which are the target molecules for anti-double-stranded DNA antibodies. Immunology 87 (1996), 362–371.
76. Otey, C.A., Carpen, O., Alpha-actinin revisited: a fresh look at an old player. Cell Motil. Cytoskeleton 58 (2004), 104–111.
77. Edlund, M., Lotano, M.A., Otey, C.A., Dynamics of alpha-actinin in focal adhesions and stress fibers visualized with alpha-actinin-green fluorescent protein. Cell Motil. Cytoskeleton 48 (2001), 190–200.
78. Wehland, J., Osborn, M., Weber, K., Cell-to-substratum contacts in living cells: a direct correlation between interference-reflexion and indirect-immunofluorescence microscopy using antibodies against actin and alpha-actinin. J. Cell Sci. 37 (1979), 257–273.
79. Yung, S., Woods, A., Chan, T.M., Davies, M., Williams, J.D., Couchman, J.R., Syndecan-4 up-regulation in proliferative renal disease is related to microfilament organization. FASEB J. 15 (2001), 1631–1633.
80. Smoyer, W.E., Mundel, P., Gupta, A., Welsh, M.J., Podocyte alpha-actinin induction precedes foot process effacement in experimental nephrotic syndrome. Am. J. Phys. 273 (1997), F150–F157.
81. Beggs, A.H., Byers, T.J., Knoll, J.H., Boyce, F.M., Bruns, G.A., Kunkel, L.M., Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11. J. Biol. Chem. 267 (1992), 9281–9288.
82. Zhao, Z., Weinstein, E., Tuzova, M., Davidson, A., Mundel, P., Marambio, P., Putterman, C., Cross-reactivity of human lupus anti-DNA antibodies with alpha-actinin and nephritogenic potential. Arthritis Rheum. 52 (2005), 522–530.
83. Deocharan, B., Zhou, Z., Antar, K., Siconolfi-Baez, L., Angeletti, R.H., Hardin, J., Putterman, C., Alpha-actinin immunization elicits anti-chromatin autoimmunity in nonautoimmune mice. J. Immunol. 179 (2007), 1313–1321.
84. Zou, X., Cheng, H., Zhang, Y., Fang, C., Xia, Y., The antigen-binding fragment of anti-double-stranded DNA IgG enhances F-actin formation in mesangial cells by binding to alpha-actinin-4. Exp. Biol. Med. (Maywood) 237 (2012), 1023–1031.
85. Mason, L.J., Ravirajan, C.T., Rahman, A., Putterman, C., Isenberg, D.A., Is alpha-actinin a target for pathogenic anti-DNA antibodies in lupus nephritis?. Arthritis Rheum. 50 (2004), 866–870.
86. Renaudineau, Y., Croquefer, S., Jousse, S., Renaudineau, E., Devauchelle, V., Gueguen, P., Hanrotel, C., Gilburd, B., Saraux, A., Shoenfeld, Y., Putterman, C., Youinou, P., Association of alpha-actinin-binding anti-double-stranded DNA antibodies with lupus nephritis. Arthritis Rheum. 54 (2006), 2523–2532.
87. Seret, G., Canas, F., Pougnet-Di Costanzo, L., Hanrotel-Saliou, C., Jousse-Joulin, S., Le Meur, Y., Saraux, A., Valeri, A., Putterman, C., Youinou, P., Rojas-Villarraga, A., Anaya, J.M., Renaudineau, Y., Anti-alpha-actinin antibodies are part of the anti-cell membrane antibody spectrum that characterize patients with lupus nephritis. J. Autoimmun. 61 (2015), 54–61.
88. Manson, J.J., Ma, A., Rogers, P., Mason, L.J., Berden, J.H., van der Vlag, J., D'Cruz, D.P., Isenberg, D.A., Rahman, A., Relationship between anti-dsDNA, anti-nucleosome and anti-alpha-actinin antibodies and markers of renal disease in patients with lupus nephritis: a prospective longitudinal study. Arthritis Res. Ther., 11, 2009, R154.
89. 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. 54 (2006), 914–926.
90. Romay-Penabad, Z., Montiel-Manzano, M.G., Shilagard, T., Papalardo, E., Vargas, G., Deora, A.B., Wang, M., Jacovina, A.T., Garcia-Latorre, E., Reyes-Maldonado, E., Hajjar, K.A., Pierangeli, S.S., Annexin A2 is involved in antiphospholipid antibody-mediated pathogenic effects in vitro and in vivo. Blood 114 (2009), 3074–3083.
91. Ma, K., Simantov, R., Zhang, J.C., Silverstein, R., Hajjar, K.A., McCrae, K.R., High affinity binding of beta 2-glycoprotein I to human endothelial cells is mediated by annexin II. J. Biol. Chem. 275 (2000), 15541–15548.
92. Canas, F., Simonin, L., Couturaud, F., Renaudineau, Y., Annexin A2 autoantibodies in thrombosis and autoimmune diseases. Thromb. Res. 135 (2015), 226–230.
93. Zhou, H., Yan, Y., Xu, G., Zhou, B., Wen, H., Guo, D., Zhou, F., Wang, H., Toll-like receptor (TLR)-4 mediates anti-beta2GPI/beta2GPI-induced tissue factor expression in THP-1 cells. Clin. Exp. Immunol. 163 (2011), 189–198.
94. Martin, M., Leffler, J., Blom, A.M., Annexin A2 and A5 serve as new ligands for C1q on apoptotic cells. J. Biol. Chem. 287 (2012), 33733–33744.
95. Caster, D.J., Korte, E.A., Merchant, M.L., Klein, J.B., Wilkey, D.W., Rovin, B.H., Birmingham, D.J., Harley, J.B., Cobb, B.L., Namjou, B., McLeish, K.R., Powell, D.W., Autoantibodies targeting glomerular annexin A2 identify patients with proliferative lupus nephritis. Proteomics Clin. Appl. 9 (2015), 1012–1020.
96. Salle, V., Maziere, J.C., Smail, A., Cevallos, R., Maziere, C., Fuentes, V., Tramier, B., Makdassi, R., Choukroun, G., Vittecoq, O., Goeb, V., Ducroix, J.P., Anti-annexin II antibodies in systemic autoimmune diseases and antiphospholipid syndrome. J. Clin. Immunol. 28 (2008), 291–297.
97. Im, S.R., Im, S.W., Chung, H.Y., Pravinsagar, P., Jang, Y.J., Cell- and nuclear-penetrating anti-dsDNA autoantibodies have multiple arginines in CDR3 of VH and increase cellular level of pERK and Bcl-2 in mesangial cells. Mol. Immunol. 67 (2015), 377–387.
98. Alarcon-Segovia, D., Llorente, L., Antibody penetration into living cells. IV. Different effects of anti-native DNA and anti-ribonucleoprotein IgG on the cell cycle of activated T gamma cells. Clin. Exp. Immunol. 52 (1983), 365–371.
99. Yanase, K., Smith, R.M., Puccetti, A., Jarett, L., Madaio, M.P., Receptor-mediated cellular entry of nuclear localizing anti-DNA antibodies via myosin 1. J. Clin. Invest. 100 (1997), 25–31.
100. Alarcon-Segovia, D., Antinuclear antibodies: to penetrate or not to penetrate, that was the question. Lupus 10 (2001), 315–318.
101. Alarcon-Segovia, D., Ruiz-Arguelles, A., Fishbein, E., Antibody to nuclear ribonucleoprotein penetrates live human mononuclear cells through fc receptors. Nature 271 (1978), 67–69.
102. Lisi, S., Sisto, M., Soleti, R., Saponaro, C., Scagliusi, P., D'Amore, M., Saccia, M., Maffione, A.B., Mitolo, V., Fcgamma receptors mediate internalization of anti-Ro and anti-La autoantibodies from Sjogren's syndrome and apoptosis in human salivary gland cell line A-253. J. Oral Pathol. Med. 36 (2007), 511–523.
103. Koscec, M., Koren, E., Wolfson-Reichlin, M., Fugate, R.D., Trieu, E., Targoff, I.N., Reichlin, M., Autoantibodies to ribosomal P proteins penetrate into live hepatocytes and cause cellular dysfunction in culture. J. Immunol. 159 (1997), 2033–2041.
104. Hajjar, K.A., Jacovina, A.T., Chacko, J., An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. J. Biol. Chem. 269 (1994), 21191–21197.
105. Quigg, R.J., Complement and autoimmune glomerular diseases. Curr. Dir. Autoimmun. 7 (2004), 165–180.
106. Weening, J.J., D'Agati, V.D., Schwartz, M.M., Seshan, S.V., Alpers, C.E., Appel, G.B., Balow, J.E., Bruijn, J.A., Cook, T., Ferrario, F., Fogo, A.B., Ginzler, E.M., Hebert, L., Hill, G., Hill, P., Jennette, J.C., Kong, N.C., Lesavre, P., Lockshin, M., Looi, L.M., Makino, H., Moura, L.A., Nagata, M., The classification of glomerulonephritis in systemic lupus erythematosus revisited. J. Am. Soc. Nephrol. 15 (2004), 241–250.
107. Liu, M.F., Lei, H.Y., Anti-endothelial cell antibodies in patients with systemic lupus erythematosus. J. Formos. Med. Assoc. 90 (1991), 221–224.
108. Wang, M.X., Walker, R.G., Kincaid-Smith, P., Clinicopathologic associations of anti-endothelial cell antibodies in immunoglobulin a nephropathy and lupus nephritis. Am. J. Kidney Dis. 22 (1993), 378–386.
109. Chan, T.M., Cheng, I.K., A prospective study on anti-endothelial cell antibodies in patients with systemic lupus erythematosus. Clin. Immunol. Immunopathol. 78 (1996), 41–46.
110. Chan, T.M., Frampton, G., Jayne, D.R., Perry, G.J., Lockwood, C.M., Cameron, J.S., Clinical significance of anti-endothelial cell antibodies in systemic vasculitis: a longitudinal study comparing anti-endothelial cell antibodies and anti-neutrophil cytoplasm antibodies. Am. J. Kidney Dis. 22 (1993), 387–392.
111. D'Cruz, D.P., Houssiau, F.A., Ramirez, G., Baguley, E., McCutcheon, J., Vianna, J., Haga, H.J., Swana, G.T., Khamashta, M.A., Taylor, J.C., et al. Antibodies to endothelial cells in systemic lupus erythematosus: a potential marker for nephritis and vasculitis. Clin. Exp. Immunol. 85 (1991), 254–261.
112. Cines, D.B., Lyss, A.P., Reeber, M., Bina, M., DeHoratius, R.J., Presence of complement-fixing anti-endothelial cell antibodies in systemic lupus erythematosus. J. Clin. Invest. 73 (1984), 611–625.
113. Perry, G.J., Elston, T., Khouri, N.A., Chan, T.M., Cameron, J.S., Frampton, G., Antiendothelial cell antibodies in lupus: correlations with renal injury and circulating markers of endothelial damage. Q. J. Med. 86 (1993), 727–734.
114. Fujii, H., Nakatani, K., Arita, N., Ito, M.R., Terada, M., Miyazaki, T., Yoshida, M., Ono, M., Fujiwara, T., Saiga, K., Ota, T., Ohtani, H., Lockwood, M., Sasaki, T., Nose, M., Internalization of antibodies by endothelial cells via fibronectin implicating a novel mechanism in lupus nephritis. Kidney Int. 64 (2003), 1662–1670.
115. Frampton, G., Hobby, P., Morgan, A., Staines, N.A., Cameron, J.S., A role for DNA in anti-DNA antibodies binding to endothelial cells. J. Autoimmun. 4 (1991), 463–478.
116. Chan, T.M., Frampton, G., Cameron, J.S., Identification of DNA-binding proteins on human umbilical vein endothelial cell plasma membrane. Clin. Exp. Immunol. 91 (1993), 110–114.
117. Chan, T.M., Cheng, I.K., Identification of endothelial cell membrane proteins that bind anti-DNA antibodies from patients with systemic lupus erythematosus by direct or indirect mechanisms. J. Autoimmun. 10 (1997), 433–439.
118. Koren, E., Koscec, M., Wolfson-Reichlin, M., Ebling, F.M., Tsao, B., Hahn, B.H., Reichlin, M., Murine and human antibodies to native DNA that cross-react with the a and D SnRNP polypeptides cause direct injury of cultured kidney cells. J. Immunol. 154 (1995), 4857–4864.
119. Zack, D.J., Stempniak, M., Wong, A.L., Taylor, C., Weisbart, R.H., Mechanisms of cellular penetration and nuclear localization of an anti-double strand DNA autoantibody. J. Immunol. 157 (1996), 2082–2088.
120. Haberstroh, U., Zahner, G., Disser, M., Thaiss, F., Wolf, G., Stahl, R.A., TGF-beta stimulates rat mesangial cell proliferation in culture: role of PDGF beta-receptor expression. Am. J. Phys. 264 (1993), F199–F205.
121. Lovett, D.H., Ryan, J.L., Sterzel, R.B., Stimulation of rat mesangial cell proliferation by macrophage interleukin 1. J. Immunol. 131 (1983), 2830–2836.
122. Horii, Y., Muraguchi, A., Iwano, M., Matsuda, T., Hirayama, T., Yamada, H., Fujii, Y., Dohi, K., Ishikawa, H., Ohmoto, Y., et al. Involvement of IL-6 in mesangial proliferative glomerulonephritis. J. Immunol. 143 (1989), 3949–3955.
123. Feld, S.M., Hirschberg, R., Artishevsky, A., Nast, C., Adler, S.G., Insulin-like growth factor I induces mesangial proliferation and increases mRNA and secretion of collagen. Kidney Int. 48 (1995), 45–51.
124. Bera, A., Das, F., Ghosh-Choudhury, N., Li, X., Pal, S., Gorin, Y., Kasinath, B.S., Abboud, H.E., Ghosh Choudhury, G., A positive feedback loop involving Erk5 and Akt turns on mesangial cell proliferation in response to PDGF. Am. J. Phys. Cell Physiol. 306 (2014), C1089–C1100.
125. Roth, M., Nauck, M., Tamm, M., Perruchoud, A.P., Ziesche, R., Block, L.H., Intracellular interleukin 6 mediates platelet-derived growth factor-induced proliferation of nontransformed cells. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 1312–1316.
126. Shankland, S.J., Pippin, J., Flanagan, M., Coats, S.R., Nangaku, M., Gordon, K.L., Roberts, J.M., Couser, W.G., Johnson, R.J., Mesangial cell proliferation mediated by PDGF and bFGF is determined by levels of the cyclin kinase inhibitor p27Kip1. Kidney Int. 51 (1997), 1088–1099.
127. Munoz, L.E., Lauber, K., Schiller, M., Manfredi, A.A., Herrmann, M., The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 6 (2010), 280–289.
128. Shao, W.H., Cohen, P.L., Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis Res. Ther., 13, 2011, 202.
129. Makino, H., Sugiyama, H., Yamasaki, Y., Maeshima, Y., Wada, J., Kashihara, N., Glomerular cell apoptosis in human lupus nephritis. Virchows Arch. 443 (2003), 67–77.
130. Soto, H., Mosquera, J., Rodriguez-Iturbe, B., Henriquez La Roche, C., Pinto, A., Apoptosis in proliferative glomerulonephritis: decreased apoptosis expression in lupus nephritis. Nephrol. Dial. Transplant. 12 (1997), 273–280.
131. Zheng, L., Sinniah, R., Hsu, S.I., Renal cell apoptosis and proliferation may be linked to nuclear factor-kappaB activation and expression of inducible nitric oxide synthase in patients with lupus nephritis. Hum. Pathol. 37 (2006), 637–647.
132. Viau, A., El Karoui, K., Laouari, D., Burtin, M., Nguyen, C., Mori, K., Pillebout, E., Berger, T., Mak, T.W., Knebelmann, B., Friedlander, G., Barasch, J., Terzi, F., Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J. Clin. Invest. 120 (2010), 4065–4076.
133. El Karoui, K., Viau, A., Dellis, O., Bagattin, A., Nguyen, C., Baron, W., Burtin, M., Broueilh, M., Heidet, L., Mollet, G., Druilhe, A., Antignac, C., Knebelmann, B., Friedlander, G., Bienaime, F., Gallazzini, M., Terzi, F., Endoplasmic reticulum stress drives proteinuria-induced kidney lesions via lipocalin 2. Nat. Commun., 7, 2016, 10330.
134. Lai, K.N., Leung, J.C., Lai, K.B., Lai, C.K., Effect of anti-DNA autoantibodies on the gene expression of interleukin 8, transforming growth factor-beta, and nitric oxide synthase in cultured endothelial cells. Scand. J. Rheumatol. 26 (1997), 461–467.
135. Perez de Lema, G., Maier, H., Nieto, E., Vielhauer, V., Luckow, B., Mampaso, F., Schlondorff, D., Chemokine expression precedes inflammatory cell infiltration and chemokine receptor and cytokine expression during the initiation of murine lupus nephritis. J. Am. Soc. Nephrol. 12 (2001), 1369–1382.
136. Rovin, B.H., Tan, L.C., Role of protein kinase pathways in IL-1-induced chemoattractant expression by human mesangial cells. Kidney Int. 46 (1994), 1059–1068.
137. Kanapathippillai, P., Hedberg, A., Fenton, C.G., Fenton, K.A., Nucleosomes contribute to increase mesangial cell chemokine expression during the development of lupus nephritis. Cytokine 62 (2013), 244–252.
138. Tesch, G.H., Maifert, S., Schwarting, A., Rollins, B.J., Kelley, V.R., Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190 (1999), 1813–1824.
139. Peterson, K.S., Huang, J.F., Zhu, J., D'Agati, V., Liu, X., Miller, N., Erlander, M.G., Jackson, M.R., Winchester, R.J., Characterization of heterogeneity in the molecular pathogenesis of lupus nephritis from transcriptional profiles of laser-captured glomeruli. J. Clin. Invest. 113 (2004), 1722–1733.
140. Debets, J.M., Van der Linden, C.J., Dieteren, I.E., Leeuwenberg, J.F., Buurman, W.A., Fc-receptor cross-linking induces rapid secretion of tumor necrosis factor (cachectin) by human peripheral blood monocytes. J. Immunol. 141 (1988), 1197–1201.
141. Fielding, C.A., Jones, G.W., McLoughlin, R.M., McLeod, L., Hammond, V.J., Uceda, J., Williams, A.S., Lambie, M., Foster, T.L., Liao, C.T., Rice, C.M., Greenhill, C.J., Colmont, C.S., Hams, E., Coles, B., Kift-Morgan, A., Newton, Z., Craig, K.J., Williams, J.D., Williams, G.T., Davies, S.J., Humphreys, I.R., O'Donnell, V.B., Taylor, P.R., Jenkins, B.J., Topley, N., Jones, S.A., Interleukin-6 signaling drives fibrosis in unresolved inflammation. Immunity 40 (2014), 40–50.
142. Chan, T.M., Yu, P.M., Tsang, K.L., Cheng, I.K., Endothelial cell binding by human polyclonal anti-DNA antibodies: relationship to disease activity and endothelial functional alterations. Clin. Exp. Immunol. 100 (1995), 506–513.
143. Lai, K.N., Leung, J.C., Bik Lai, K., Li, P.K., Lai, C.K., Anti-DNA autoantibodies stimulate the release of interleukin-1 and interleukin-6 from endothelial cells. J. Pathol. 178 (1996), 451–457.
144. Lai, K.N., Leung, J.C., Lai, K.B., Lai, F.M., Wong, K.C., Increased release of von Willebrand factor antigen from endothelial cells by anti-DNA autoantibodies. Ann. Rheum. Dis. 55 (1996), 57–62.
145. McCarthy, E.M., Smith, S., Lee, R.Z., Cunnane, G., Doran, M.F., Donnelly, S., Howard, D., O'Connell, P., Kearns, G., Ni Gabhann, J., Jefferies, C.A., The association of cytokines with disease activity and damage scores in systemic lupus erythematosus patients. Rheumatology (Oxford) 53 (2014), 1586–1594.
146. Hansen, C., Otto, E., Kuhlemann, K., Forster, G., Kahaly, G.J., Glycosaminoglycans in autoimmunity. Clin. Exp. Rheumatol. 14:Suppl 15 (1996), S59–S67.
147. Faaber, P., Capel, P.J., Rijke, G.P., Vierwinden, G., van de Putte, L.B., Koene, R.A., Cross-reactivity of anti-DNA antibodies with proteoglycans. Clin. Exp. Immunol. 55 (1984), 502–508.
148. Pitashny, M., Schwartz, N., Qing, X., Hojaili, B., Aranow, C., Mackay, M., Putterman, C., Urinary lipocalin-2 is associated with renal disease activity in human lupus nephritis. Arthritis Rheum. 56 (2007), 1894–1903.
149. Vleming, L.J., Baelde, J.J., Westendorp, R.G., Daha, M.R., van Es, L.A., Bruijn, J.A., The glomerular deposition of PAS positive material correlates with renal function in human kidney diseases. Clin. Nephrol. 47 (1997), 158–167.
150. Nakapoulou, I., Stefanaki, K., Zeis, P.M., Papadakis, J., Boletis, J., Vosnidis, G., Davaris, P., The glomerular distribution of laminin and fibronectin in glomerulonephritis. Histol. Histopathol. 8 (1993), 521–526.
151. Zhang, Y., Yang, J., Jiang, S., Fang, C., Xiong, L., Cheng, H., Xia, Y., The lupus-derived anti-double-stranded DNA IgG contributes to myofibroblast-like phenotype in mesangial cells. J. Clin. Immunol. 32 (2012), 1270–1278.
152. Border, W.A., Noble, N.A., Transforming growth factor beta in tissue fibrosis. N. Engl. J. Med. 331 (1994), 1286–1292.
153. Liu, Y., Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int. 69 (2006), 213–217.
154. Oleksyn, D., Pulvino, M., Zhao, J., Misra, R., Vosoughi, A., Jenks, S., Tipton, C., Lund, F., Schwartz, G., Goldman, B., Mohan, C., Mehta, K., Mehta, M., Leitgets, M., Sanz, I., Chen, L., Protein kinase Cbeta is required for lupus development in Sle mice. Arthritis Rheum. 65 (2013), 1022–1031.
155. Rastaldi, M.P., Ferrario, F., Giardino, L., Dell'Antonio, G., Grillo, C., Grillo, P., Strutz, F., Muller, G.A., Colasanti, G., D'Amico, G., Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney Int. 62 (2002), 137–146.
156. Rastaldi, M.P., Epithelial-mesenchymal transition and its implications for the development of renal tubulointerstitial fibrosis. J. Nephrol. 19 (2006), 407–412.
157. Lovisa, S., LeBleu, V.S., Tampe, B., Sugimoto, H., Vadnagara, K., Carstens, J.L., Epithelial-To-Mesenchymal Transition Induces Cell Cycle Arrest and Parenchymal Damage in Renal Fibrosis. Vol. 21, 2015, 998–1009.
158. Yap, D.Y., Tang, C.S., Ma, M.K., Lam, M.F., Chan, T.M., Survival analysis and causes of mortality in patients with lupus nephritis. Nephrol. Dial. Transplant. 27 (2012), 3248–3254.
159. Chan, T.M., Li, F.K., Tang, C.S., Wong, R.W., Fang, G.X., Ji, Y.L., Lau, C.S., Wong, A.K., Tong, M.K., Chan, K.W., Lai, K.N., Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. Hong Kong-Guangzhou nephrology study group. N. Engl. J. Med. 343 (2000), 1156–1162.
160. Chan, T.M., Tse, K.C., Tang, C.S., Mok, M.Y., Li, F.K., Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis. J. Am. Soc. Nephrol. 16 (2005), 1076–1084.
161. Chan, T.M., Treatment of severe lupus nephritis: the new horizon. Nat. Rev. Nephrol. 11 (2015), 46–61.
162. Copeland, J.W., Beaumont, B.W., Merrilees, M.J., Pilmore, H.L., Epithelial-to-mesenchymal transition of human proximal tubular epithelial cells: effects of rapamycin, mycophenolate, cyclosporin, azathioprine, and methylprednisolone. Transplantation 83 (2007), 809–814.
163. Dubus, I., Vendrely, B., Christophe, I., Labouyrie, J.P., Delmas, Y., Bonnet, J., Combe, C., Mycophenolic acid antagonizes the activation of cultured human mesangial cells. Kidney Int. 62 (2002), 857–867.
164. Baer, P.C., Wegner, B., Geiger, H., Effects of mycophenolic acid on IL-6 expression of human renal proximal and distal tubular cells in vitro. Nephrol. Dial. Transplant. 19 (2004), 47–52.
165. Morath, C., Reuter, H., Simon, V., Krautkramer, E., Muranyi, W., Schwenger, V., Goulimari, P., Grosse, R., Hahn, M., Lichter, P., Zeier, M., Effects of mycophenolic acid on human fibroblast proliferation, migration and adhesion in vitro and in vivo. Am. J. Transplant. 8 (2008), 1786–1797.