Genetics of Lupus Nephritis: Clinical Implications

Seminars in Nephrology

Volumn 35, Issue 5, 2015, Pages 396-409

  Munroe, Melissa E ^a   James, Judith A ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Genetics; Immune response; Lupus nephritis; SLE

Indexed keywords

AUTOANTIGEN; AUTOPHAGY PROTEIN 5; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DEOXYRIBONUCLEASE I; INTERFERON REGULATORY FACTOR 5; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; PATTERN RECOGNITION RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; ANTIGEN ANTIBODY COMPLEX; AUTOANTIBODY;

ADAPTIVE IMMUNITY; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; ATG5 GENE; B LYMPHOCYTE ACTIVATION; CTLA4 GENE; CYTOKINE RELEASE; DNASE1 GENE; ENZYME ACTIVITY; FCGR3A GENE; FCGR3B GENE; GENE; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEREDITY; HUMAN; IFIH1 GENE; IMMUNOPATHOGENESIS; IMMUNOREGULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; IRF5 GENE; IRF7 GENE; ITGAM GENE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAVS GENE; MTMR3 GENE; NECROPTOSIS; NONHUMAN; PDCD1 GENE; PERSONALIZED MEDICINE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; TNFAIP3 GENE; TNIP1 GENE; TRANSCRIPTION REGULATION; TREX1 GENE; UBE2L3 GENE; ANTIGEN ANTIBODY COMPLEX; CHRONIC KIDNEY FAILURE; DISEASE COURSE; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADAPTIVE IMMUNITY; ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; AUTOANTIBODIES; DISEASE PROGRESSION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNITY, INNATE; KIDNEY FAILURE, CHRONIC; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; POLYMORPHISM, GENETIC;

EID: 84945905054     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2015.08.002     Document Type: Review

References (129)

1. Borchers A.T., Leibushor N., Naguwa S.M., Cheema G.S., Shoenfeld Y., Gershwin M.E. Lupus nephritis: a critical review. Autoimmun Rev 2012, 12:174-194.
2. Richman I.B., Taylor K.E., Chung S.A., et al. European genetic ancestry is associated with a decreased risk of lupus nephritis. Arthritis Rheum 2012, 64:3374-3382.
3. Rullo O.J., Tsao B.P. Recent insights into the genetic basis of systemic lupus erythematosus. Ann Rheum Dis 2013, 72(Suppl 2):ii56-ii61.
4. Fenton K. The effect of cell death in the initiation of lupus nephritis. Clin Exp Immunol 2015, 179:11-16.
5. 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 2010, 6:280-289.
6. Bollain YGJJ, Arellano-Rodriguez M., Torres-Del-Muro Fde J, et al. Soluble fas and the -670 polymorphism of fas in lupus nephritis. Int J Nephrol 2014, 2014:780406.
7. Moudi B., Salimi S., Farajian Mashhadi F., Sandoughi M., Zakeri Z. Association of FAS and FAS ligand genes polymorphism and risk of systemic lupus erythematosus. Sci World J 2013, 2013:176741.
8. Martinez-Valle F., Balada E., Ordi-Ros J., Bujan-Rivas S., Sellas-Fernandez A., Vilardell-Tarres M. DNase1 activity in systemic lupus erythematosus patients with and without nephropathy. Rheumatol Int 2010, 30:1601-1604.
9. Panneer D., Antony P.T., Negi V.S. Q222R polymorphism in DNAse I gene is a risk factor for nephritis in South Indian SLE patients. Lupus 2013, 22:996-1000.
10. Harley J.B., Alarcon-Riquelme M.E., Criswell L.A., et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008, 40:204-210.
11. Zhou X.J., Nath S.K., Qi Y.Y., et al. Brief report: identification of MTMR3 as a novel susceptibility gene for lupus nephritis in northern Han Chinese by shared-gene analysis with IgA nephropathy. Arthritis Rheum 2014, 66:2842-2848.
12. Kelley J.M., Edberg J.C., Kimberly R.P. Pathways: strategies for susceptibility genes in SLE. Autoimmun Rev 2010, 9:473-476.
13. Robinson T., Kariuki S.N., Franek B.S., et al. Autoimmune disease risk variant of IFIH1 is associated with increased sensitivity to IFN-alpha and serologic autoimmunity in lupus patients. J Immunol 2011, 187:1298-1303.
14. Imaizumi T., Aizawa-Yashiro T., Tsuruga K., et al. Melanoma differentiation-associated gene 5 regulates the expression of a chemokine CXCL10 in human mesangial cells: implications for chronic inflammatory renal diseases. Tohoku J Exp Med 2012, 228:17-26.
15. Enevold C., Kjaer L., Nielsen C.H., et al. Genetic polymorphisms of dsRNA ligating pattern recognition receptors TLR3, MDA5, and RIG-I. Association with systemic lupus erythematosus and clinical phenotypes. Rheumatol Int 2014, 34:1401-1408.
16. Pothlichet J., Niewold T.B., Vitour D., Solhonne B., Crow M.K., Si-Tahar M. A loss-of-function variant of the antiviral molecule MAVS is associated with a subset of systemic lupus patients. EMBO Mol Med 2011, 3:142-152.
17. Namjou B., Kothari P.H., Kelly J.A., et al. Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort. Genes Immun 2011, 12:270-279.
18. Imaizumi T., Aizawa T., Segawa C., et al. Toll-like receptor 3 signaling contributes to the expression of a neutrophil chemoattractant, CXCL1 in human mesangial cells. Clin Exp Nephrol 2014, Epub ahead of print.
19. Tian J., Ma Y., Li J., et al. The TLR7 7926A>G polymorphism is associated with susceptibility to systemic lupus erythematosus. Mol Med Rep 2012, 6:105-110.
20. Ramachandran R., Sharma V., Rathi M., et al. Association between -1486 T>C and +1174 G>A single nucleotide polymorphisms in TLR9 gene and severity of lupus nephritis. Indian J Nephrol 2012, 22:125-129.
21. Teichmann L.L., Schenten D., Medzhitov R., Kashgarian M., Shlomchik M.J. Signals via the adaptor MyD88 in B cells and DCs make distinct and synergistic contributions to immune activation and tissue damage in lupus. Immunity 2013, 38:528-540.
22. Namjou B., Choi C.B., Harley I.T., et al. Evaluation of TRAF6 in a large multiancestral lupus cohort. Arthritis Rheum 2012, 64:1960-1969.
23. Jacob C.O., Zhu J., Armstrong D.L., et al. Identification of IRAK1 as a risk gene with critical role in the pathogenesis of systemic lupus erythematosus. Proc Natl Acad Sci U S A 2009, 106:6256-6261.
24. Kaufman K.M., Zhao J., Kelly J.A., et al. Fine mapping of Xq28: both MECP2 and IRAK1 contribute to risk for systemic lupus erythematosus in multiple ancestral groups. Ann Rheum Dis 2013, 72:437-444.
25. Li P., Cao C., Luan H., et al. Association of genetic variations in the STAT4 and IRF7/KIAA1542 regions with systemic lupus erythematosus in a Northern Han Chinese population. Hum Immunol 2011, 72:249-255.
26. Bolin K., Sandling J.K., Zickert A., et al. Association of STAT4 polymorphism with severe renal insufficiency in lupus nephritis. PLoS One 2013, 8:e84450.
27. Salloum R., Franek B.S., Kariuki S.N., et al. Genetic variation at the IRF7/PHRF1 locus is associated with autoantibody profile and serum interferon-alpha activity in lupus patients. Arthritis Rheum 2010, 62:553-561.
28. Niewold T.B., Kelly J.A., Flesch M.H., Espinoza L.R., Harley J.B., Crow M.K. Association of the IRF5 risk haplotype with high serum interferon-alpha activity in systemic lupus erythematosus patients. Arthritis Rheum 2008, 58:2481-2487.
29. Bates J.S., Lessard C.J., Leon J.M., et al. Meta-analysis and imputation identifies a 109 kb risk haplotype spanning TNFAIP3 associated with lupus nephritis and hematologic manifestations. Genes Immun 2009, 10:470-477.
30. Tavares R.M., Turer E.E., Liu C.L., et al. The ubiquitin modifying enzyme A20 restricts B cell survival and prevents autoimmunity. Immunity 2010, 33:181-191.
31. Verstrepen L., Carpentier I., Beyaert R. The biology of A20-binding inhibitors of NF-kappaB activation (ABINs). Adv Exp Med Biol 2014, 809:13-31.
32. Caster D.J., Korte E.A., Nanda S.K., et al. ABIN1 dysfunction as a genetic basis for lupus nephritis. J Am Soc Nephrol 2013, 24:1743-1754.
33. Zhou X.J., Cheng F.J., Zhu L., et al. Association of systemic lupus erythematosus susceptibility genes with IgA nephropathy in a Chinese cohort. Clin J Am Soc Nephrol 2014, 9:788-797.
34. Lewis M.J., Vyse S., Shields A.M., et al. UBE2L3 polymorphism amplifies NF-kappaB activation and promotes plasma cell development, linking linear ubiquitination to multiple autoimmune diseases. Am J Hum Genet 2015, 96:221-234.
35. Chung S.A., Taylor K.E., Graham R.R., et al. Differential genetic associations for systemic lupus erythematosus based on anti-dsDNA autoantibody production. PLoS Genet 2011, 7:e1001323.
36. Jonsen A., Gunnarsson I., Gullstrand B., et al. Association between SLE nephritis and polymorphic variants of the CRP and FcgammaRIIIa genes. Rheumatology (Oxford) 2007, 46:1417-1421.
37. Floto R.A., Clatworthy M.R., Heilbronn K.R., et al. Loss of function of a lupus-associated FcgammaRIIb polymorphism through exclusion from lipid rafts. Nat Med 2005, 11:1056-1058.
38. Karassa F.B., Trikalinos T.A., Ioannidis J.P. FcgammaRIIa-SLE Meta-Analysis Investigators. Role of the Fcgamma receptor IIa polymorphism in susceptibility to systemic lupus erythematosus and lupus nephritis: a meta-analysis. Arthritis Rheum 2002, 46:1563-1571.
39. Karassa F.B., Trikalinos T.A., Ioannidis J.P. FcgammaRIIIa-SLE Meta-Analysis Investigators. The Fc gamma RIIIA-F158 allele is a risk factor for the development of lupus nephritis: a meta-analysis. Kidney Int 2003, 63:1475-1482.
40. Gelmetti A.P., Freitas A.C., Woronik V., Barros R.T., Bonfa E., Monteiro R.C. Polymorphism of the FcgammaRIIalpha IgG receptor in patients with lupus nephritis and glomerulopathy. J Rheumatol 2006, 33:523-530.
41. Zuniga R., Markowitz G.S., Arkachaisri T., Imperatore E.A., D'Agati V.D., Salmon J.E. Identification of IgG subclasses and C-reactive protein in lupus nephritis: the relationship between the composition of immune deposits and FCgamma receptor type IIA alleles. Arthritis Rheum 2003, 48:460-470.
42. Salmon J.E., Millard S., Schachter L.A., et al. Fc gamma RIIA alleles are heritable risk factors for lupus nephritis in African Americans. J Clin Invest 1996, 97:1348-1354.
43. Haseley L.A., Wisnieski J.J., Denburg M.R., et al. Antibodies to C1q in systemic lupus erythematosus: characteristics and relation to Fc gamma RIIA alleles. Kidney Int 1997, 52:1375-1380.
44. Wu J., Edberg J.C., Redecha P.B., et al. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest 1997, 100:1059-1070.
45. Alarcon G.S., McGwin G., Petri M., et al. Time to renal disease and end-stage renal disease in PROFILE: a multiethnic lupus cohort. PLoS Med 2006, 3:e396.
46. Salmon J.E., Edberg J.C., Kimberly R.P. Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin Invest 1990, 85:1287-1295.
47. Lee Y.H., Bae S.C. Association between the functional ITGAM rs1143679 G/A polymorphism and systemic lupus erythematosus/lupus nephritis or rheumatoid arthritis: an update meta-analysis. Rheumatol Int 2015, 35:815-823.
48. Kim-Howard X., Maiti A.K., Anaya J.M., et al. ITGAM coding variant (rs1143679) influences the risk of renal disease, discoid rash and immunological manifestations in patients with systemic lupus erythematosus with European ancestry. Ann Rheum Dis 2010, 69:1329-1332.
49. Aitman T.J., Dong R., Vyse T.J., et al. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 2006, 439:851-855.
50. Nossent JC, Becker-Merok A, Rischmueller M, Lester S. Susceptibility for lupus nephritis by low copy number of the FCGR3B gene is linked to increased levels of pathogenic autoantibodies. Autoimmune Dis. 2013;2013:750814.
51. Leffler J., Bengtsson A.A., Blom A.M. The complement system in systemic lupus erythematosus: an update. Ann Rheum Dis 2014, 73:1601-1606.
52. Villarreal J., Crosdale D., Ollier W., et al. Mannose binding lectin and FcgammaRIIa (CD32) polymorphism in Spanish systemic lupus erythematosus patients. Rheumatology (Oxford) 2001, 40:1009-1012.
53. Seelen M.A., van der Bijl E.A., Trouw L.A., et al. A role for mannose-binding lectin dysfunction in generation of autoantibodies in systemic lupus erythematosus. Rheumatology (Oxford) 2005, 44:111-119.
54. MacPherson M., Lek H.S., Prescott A., Fagerholm S.C. A systemic lupus erythematosus-associated R77H substitution in the CD11b chain of the Mac-1 integrin compromises leukocyte adhesion and phagocytosis. J Biol Chem 2011, 286:17303-17310.
55. Sanchez E., Nadig A., Richardson B.C., et al. Phenotypic associations of genetic susceptibility loci in systemic lupus erythematosus. Ann Rheum Dis 2011, 70:1752-1757.
56. Rhodes B., Furnrohr B.G., Roberts A.L., et al. The rs1143679 (R77H) lupus associated variant of ITGAM (CD11b) impairs complement receptor 3 mediated functions in human monocytes. Ann Rheum Dis 2012, 71:2028-2034.
57. Verma J., Arora V., Marwaha V., Kumar A., Das N. Association of leukocyte CR1 gene transcription with the disease severity and renal involvement in systemic lupus erythematosus. Lupus 2005, 14:273-279.
58. Ivashkiv L.B. A signal-switch hypothesis for cross-regulation of cytokine and TLR signalling pathways. Nat Rev Immunol 2008, 8:816-822.
59. Hervas-Stubbs S., Perez-Gracia J.L., Rouzaut A., Sanmamed M.F., Le Bon A., Melero I. Direct effects of type I interferons on cells of the immune system. Clin Cancer Res 2011, 17:2619-2627.
60. Sigurdsson S., Nordmark G., Goring H.H., et al. Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am J Hum Genet 2005, 76:528-537.
61. He C.F., Liu Y.S., Cheng Y.L., et al. TNIP1, SLC15A4, ETS1, RasGRP3 and IKZF1 are associated with clinical features of systemic lupus erythematosus in a Chinese Han population. Lupus 2010, 19:1181-1186.
62. Couser W.G. Basic and translational concepts of immune-mediated glomerular diseases. J Am Soc Nephrol 2012, 23:381-399.
63. Chung S.A., Brown E.E., Williams A.H., et al. Lupus nephritis susceptibility loci in women with systemic lupus erythematosus. J Am Soc Nephrol 2014, 25:2859-2870.
64. Niu Z., Zhang P., Tong Y. Value of HLA-DR genotype in systemic lupus erythematosus and lupus nephritis: a meta-analysis. Int J Rheum Dis 2015, 18:17-28.
65. Masutani K., Akahoshi M., Tsuruya K., et al. Predominance of Th1 immune response in diffuse proliferative lupus nephritis. Arthritis Rheum 2001, 44:2097-2106.
66. Vang T., Landskron J., Viken M.K., et al. The autoimmune-predisposing variant of lymphoid tyrosine phosphatase favors T helper 1 responses. Hum Immunol 2013, 74:574-585.
67. Vang T., Congia M., Macis M.D., et al. Autoimmune-associated lymphoid tyrosine phosphatase is a gain-of-function variant. Nat Genet 2005, 37:1317-1319.
68. Prokunina L., Gunnarsson I., Sturfelt G., et al. The systemic lupus erythematosus-associated PDCD1 polymorphism PD1.3A in lupus nephritis. Arthritis Rheum 2004, 50:327-328.
69. Bertsias G.K., Nakou M., Choulaki C., et al. Genetic, immunologic, and immunohistochemical analysis of the programmed death 1/programmed death ligand 1 pathway in human systemic lupus erythematosus. Arthritis Rheum 2009, 60:207-218.
70. Joo Y.B., Park B.L., Shin H.D., Park S.Y., Kim I., Bae S.C. Association of genetic polymorphisms in CD40 with susceptibility to SLE in the Korean population. Rheumatology (Oxford) 2013, 52:623-630.
71. Citores M.J., Rua-Figueroa I., Rodriguez-Gallego C., et al. The dinucleotide repeat polymorphism in the 3'UTR of the CD154 gene has a functional role on protein expression and is associated with systemic lupus erythematosus. Ann Rheum Dis 2004, 63:310-317.
72. Zhou XJ, Cheng FJ, Qi YY, Zhao MH, Zhang H. A replication study from Chinese supports association between lupus-risk allele in TNFSF4 and renal disorder. Biomed Res Int. 2013;2013:597921.
73. Patschan S., Dolff S., Kribben A., et al. CD134 expression on CD4+ T cells is associated with nephritis and disease activity in patients with systemic lupus erythematosus. Clin Exp Immunol 2006, 145:235-242.
74. Yap D.Y., Lai K.N. Pathogenesis of renal disease in systemic lupus erythematosus-the role of autoantibodies and lymphocytes subset abnormalities. Int J Mol Sci 2015, 16:7917-7931.
75. Liarski V.M., Kaverina N., Chang A., et al. Cell distance mapping identifies functional T follicular helper cells in inflamed human renal tissue. Sci Transl Med 2014, 6:230ra246.
76. Lee S.K., Silva D.G., Martin J.L., et al. Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 2012, 37:880-892.
77. Miyake K., Nakashima H., Akahoshi M., et al. Genetically determined interferon-gamma production influences the histological phenotype of lupus nephritis. Rheumatology (Oxford) 2002, 41:518-524.
78. Namjou B., Sestak A.L., Armstrong D.L., et al. High-density genotyping of STAT4 reveals multiple haplotypic associations with systemic lupus erythematosus in different racial groups. Arthritis Rheum 2009, 60:1085-1095.
79. Lessard C.J., Adrianto I., Ice J.A., et al. Identification of IRF8, TMEM39A, and IKZF3-ZPBP2 as susceptibility loci for systemic lupus erythematosus in a large-scale multiracial replication study. Am J Hum Genet 2012, 90:648-660.
80. Tucci M., Stucci S., Strippoli S., Silvestris F. Cytokine overproduction, T cell activation, and defective T-regulatory functions promote nephritis in systemic lupus erythematosus. J Biomed Biotechnol 2010, 2010:457146.
81. Susianti H., Handono K., Purnomo B.B., Widodo N., Gunawan A., Kalim H. Changes to signal peptide and the level of transforming growth factor- beta1 due to T869C polymorphism of TGF beta1 associated with lupus renal fibrosis. Springerplus 2014, 3:514.
82. Zhu L.J., Liu Z.H., Zeng C.H., Chen Z.H., Yu C., Li L.S. Association of interleukin-10 gene -592 A/C polymorphism with the clinical and pathological diversity of lupus nephritis. Clin Exp Rheumatol 2005, 23:854-860.
83. Hermann J., Gruber S., Neufeld J.B., et al. IL10R1 loss-of-function alleles in rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Rheumatol 2009, 27:603-608.
84. Sung Y.K., Park B.L., Shin H.D., Kim L.H., Kim S.Y., Bae S.C. Interleukin-10 gene polymorphisms are associated with the SLICC/ACR damage index in systemic lupus erythematosus. Rheumatology (Oxford) 2006, 45:400-404.
85. Packard T.A., Cambier J.C. B lymphocyte antigen receptor signaling: initiation, amplification, and regulation. F1000prime reports 2013, 5:40.
86. Manjarrez-Orduno N., Marasco E., Chung S.A., et al. CSK regulatory polymorphism is associated with systemic lupus erythematosus and influences B-cell signaling and activation. Nat Genet 2012, 44:1227-1230.
87. Lu R., Vidal G.S., Kelly J.A., et al. Genetic associations of LYN with systemic lupus erythematosus. Genes Immun 2009, 10:397-403.
88. Culton D.A., Nicholas M.W., Bunch D.O., et al. Similar CD19 dysregulation in two autoantibody-associated autoimmune diseases suggests a shared mechanism of B-cell tolerance loss. J Clin Immunol 2007, 27:53-68.
89. Guo L., Deshmukh H., Lu R., et al. Replication of the BANK1 genetic association with systemic lupus erythematosus in a European-derived population. Genes Immun 2009, 10:531-538.
90. Kozyrev S.V., Bernal-Quiros M., Alarcon-Riquelme M.E., Castillejo-Lopez C. The dual effect of the lupus-associated polymorphism rs10516487 on BANK1 gene expression and protein localization. Genes Immun 2012, 13:129-138.
91. Guthridge J.M., Lu R., Sun H., et al. Two functional lupus-associated BLK promoter variants control cell-type- and developmental-stage-specific transcription. Am J Hum Genet 2014, 94:586-598.
92. Buchta C.M., Bishop G.A. Toll-like receptors and B cells: functions and mechanisms. Immunol Res 2014, 59:12-22.
93. Peters A.L., Plenge R.M., Graham R.R., et al. A novel polymorphism of the human CD40 receptor with enhanced function. Blood 2008, 112:1863-1871.
94. Peters A.L., Bishop G.A. Differential TRAF3 utilization by a variant human CD40 receptor with enhanced signaling. J Immunol 2010, 185:6555-6562.
95. Poovassery J.S., Bishop G.A. Type I IFN receptor and the B cell antigen receptor regulate TLR7 responses via distinct molecular mechanisms. J Immunol 2012, 189:1757-1764.
96. Cervera R., Khamashta M.A., Font J., et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine 2003, 82:299-308.
97. Clynes R., Dumitru C., Ravetch J.V. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 1998, 279:1052-1054.
98. Sanchez-Nino M.D., Benito-Martin A., Goncalves S., et al. TNF superfamily: a growing saga of kidney injury modulators. Mediators Inflamm 2010, 2010. Article ID 182958.
99. Aten J., Roos A., Claessen N., Schilder-Tol E.J., Ten Berge I.J., Weening J.J. Strong and selective glomerular localization of CD134 ligand and TNF receptor-1 in proliferative lupus nephritis. J Am Soc Nephrol 2000, 11:1426-1438.
100. Richter C., Messerschmidt S., Holeiter G., et al. The tumor necrosis factor receptor stalk regions define responsiveness to soluble versus membrane-bound ligand. Mol Cell Biol 2012, 32:2515-2529.
101. Vielhauer V., Stavrakis G., Mayadas T.N. Renal cell-expressed TNF receptor 2, not receptor 1, is essential for the development of glomerulonephritis. J Clin Invest 2005, 115:1199-1209.
102. Tsuchiya N., Komata T., Matsushita M., Ohashi J., Tokunaga K. New single nucleotide polymorphisms in the coding region of human TNFR2: association with systemic lupus erythematosus. Genes Immun 2000, 1:501-503.
103. Lu J., Kwan B.C., Lai F.M., et al. Gene expression of TWEAK/Fn14 and IP-10/CXCR3 in glomerulus and tubulointerstitium of patients with lupus nephritis. Nephrology (Carlton) 2011, 16:426-432.
104. Tucci M., Barnes E.V., Sobel E.S., et al. Strong association of a functional polymorphism in the monocyte chemoattractant protein 1 promoter gene with lupus nephritis. Arthritis Rheum 2004, 50:1842-1849.
105. Rovin B.H., Lu L., Zhang X. A novel interleukin-8 polymorphism is associated with severe systemic lupus erythematosus nephritis. Kidney Int 2002, 62:261-265.
106. Zhang J., Zhang Y., Yang J., et al. Three SNPs in chromosome 11q23.3 are independently associated with systemic lupus erythematosus in Asians. Human Mol Genet 2014, 23:524-533.
107. Warchol T., Lianeri M., Lacki J.K., Jagodzinski P.P. SDF1-3' G801A polymorphisms in Polish patients with systemic lupus erythematosus. Mol Biol Rep 2010, 37:3121-3125.
108. Wu F.X., Luo X.Y., Wu L.J., et al. Association of chemokine CXCL12-3'G801A polymorphism with systemic lupus erythematosus in a Han Chinese population. Lupus 2012, 21:604-610.
109. Sela U., Hershkoviz R., Cahalon L., Lider O., Mozes E. Down-regulation of stromal cell-derived factor-1alpha-induced T cell chemotaxis by a peptide based on the complementarity-determining region 1 of an anti-DNA autoantibody via up-regulation of TGF-beta secretion. J Immunol 2005, 174:302-309.
110. Liu K., Li Q.Z., Delgado-Vega A.M., et al. Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. J Clin Invest 2009, 119:911-923.
111. Li Q.Z., Zhou J., Yang R., et al. The lupus-susceptibility gene kallikrein downmodulates antibody-mediated glomerulonephritis. Genes Immun 2009, 10:503-508.
112. Pogorevici A., Gluhovschi C., Gluhovschi G., Velciov S.M., Trandafirescu V., Secrii R.V. Hypertension in lupus nephritis. Rom J Intern Med 2006, 44:295-316.
113. Kammoun K., Jarraya F., Bouhamed L., et al. Poor prognostic factors of lupus nephritis. Saudi J Kidney Dis Transpl 2011, 22:727-732.
114. Sprovieri S.R., Sens Y.A., Martini Filho D. Association between polymorphisms of the renin-angiotensin system and more severe histological forms of lupus nephritis. Clin Nephrol 2005, 64:20-27.
115. Parsa A., Lovett D.H., Peden E.A., Zhu L., Seldin M.F., Criswell L.A. Renin-angiotensin system gene polymorphisms predict the progression to renal insufficiency among Asians with lupus nephritis. Genes Immun 2005, 6:217-224.
116. Lin C.P., Adrianto I., Lessard C.J., et al. Role of MYH9 and APOL1 in African and non-African populations with lupus nephritis. Genes Immun 2012, 13:232-238.
117. Kruzel-Davila E., Wasser W.G., Aviram S., Skorecki K. APOL1 nephropathy: from gene to mechanisms of kidney injury. Nephrol Dial Transplant 2015, Epub ahead of print.
118. Rhodes B., Vyse T.J. Using genetics to deliver personalized SLE therapy-a realistic prospect?. Nat Rev Rheumatol 2010, 6:373-377.
119. Rovin BH, McKinley AM, Birmingham DJ. Can we personalize treatment for kidney diseases? Clin J Am Soc Nephrol. 2009;4:1670-6.
120. Filipski K.K., Mechanic L.E., Long R., Freedman A.N. Pharmacogenomics in oncology care. Front Genet 2014, 5:73.
121. Koutsokeras T., Healy T. Systemic lupus erythematosus and lupus nephritis. Nat Rev Drug Discov 2014, 13:173-174.
122. Rovin B.H., Parikh S.V. Lupus nephritis: the evolving role of novel therapeutics. Am J Kidney Dis 2014, 63:677-690.
123. Diaz-Lagares C., Croca S., Sangle S., et al. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun Rev 2012, 11:357-364.
124. Vigna-Perez M., Hernandez-Castro B., Paredes-Saharopulos O., et al. Clinical and immunological effects of rituximab in patients with lupus nephritis refractory to conventional therapy: a pilot study. Arthritis Res Ther 2006, 8:R83.
125. Rovin B.H., Furie R., Latinis K., et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum 2012, 64:1215-1226.
126. Manzi S., Sanchez-Guerrero J., Merrill J.T., et al. Effects of belimumab, a B-lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis 2012, 71:1833-1838.
127. Michaelson J.S., Wisniacki N., Burkly L.C., Putterman C. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun 2012, 39:130-142.
128. Li Y., Fang X., Li Q.Z. Biomarker profiling for lupus nephritis. Genomics Proteomics Bioinformatics 2013, 11:158-165.
129. Sarzi-Puttini P., Atzeni F., Iaccarino L., Doria A. Environment and systemic lupus erythematosus: an overview. Autoimmunity 2005, 38:465-472.