The pathogenesis, diagnosis and treatment of lupus nephritis

Current Opinion in Rheumatology

Volumn 26, Issue 5, 2014, Pages 502-509

  Schwartz, Noa ^a   Goilav, Beatrice ^a   Putterman, Chaim ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

biomarkers; long lived plasma cells; lupus nephritis; microRNA

Indexed keywords

BELIMUMAB; BIOLOGICAL MARKER; BORTEZOMIB; CORTICOSTEROID; CYTOKINE; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PROTEASOME INHIBITOR; RITUXIMAB; AUTOANTIBODY; MICRORNA; MONOCLONAL ANTIBODY;

B LYMPHOCYTE; EARLY DIAGNOSIS; EPIGENETICS; HUMAN; IMMUNOCOMPETENT CELL; LUPUS ERYTHEMATOSUS NEPHRITIS; MACROPHAGE; NONHUMAN; PATHOGENESIS; PLACEBO EFFECT; PLASMA CELL; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; LUPUS NEPHRITIS; METABOLISM; MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; AUTOANTIBODIES; B-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNOSUPPRESSION; LUPUS NEPHRITIS; MACROPHAGES; MICE; MICRORNAS; PLASMA CELLS; RITUXIMAB;

EID: 84905459899     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0000000000000089     Document Type: Review

References (78)

1. Herrmann M, Voll RE, Zoller OM, et al. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 1998; 41:1241-1250.
2. Elkon KB, Stone VV. Type I interferon and systemic lupus erythematosus. J Interferon Cytokine Res 2011; 31:803-812.
3. Tucker LB, Menon S, Schaller JG, Isenberg DA. Adult- and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br J Rheumatol 1995; 34:866-872.
4. Giannico G, Fogo AB. Lupus nephritis: is the kidney biopsy currently necessary in the management of lupus nephritis? Clin J Am Soc Nephrol 2013; 8:138-145.
5. Lech M, Anders HJ. The pathogenesis of lupus nephritis. J Am Soc Nephrol 2013; 24:1357-1366.
6. Hiepe F, Dörner T, Hauser AE, et al. Long-lived autoreactive plasma cells drive persistent autoimmune inflammation. Nat Rev Rheumatol 2011; 7:170-178
7. Cheng Q, Mumtaz IM, Khodadadi L, et al. Autoantibodies from long-lived 'memory' plasma cells of NZB/W mice drive immune complex nephritis. Ann Rheum Dis 2013; 72:2011-2017.
8. Espeli M, Bökers S, Giannico G, et al. Local renal autoantibody production in lupus nephritis. J Am Soc Nephrol 2011; 22:296-305.
9. Andrews BS, Eisenberg RS, Theofilopoulos AN, et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med 1978; 148:1198-1215.
10. Ripoll E, Merino A, Goma M, et al. CD40 gene silencing reduces the progression of experimental lupus nephritis modulating local milieu and systemic mechanisms. PLoS ONE 2013; 8:e65068.
11. Moreth K, Brodbeck R, Babelova A, et al. The proteoglycan biglycan regulates expression of the B cell chemoattractant CXCL13 and aggravates murine lupus nephritis. J Clin Invest 2010; 120:4251-4272.
12. Sun C, Shen Y, Chen X, et al. The characteristics and significance of locally infiltrating B cells in lupus nephritis and their association with local BAFF expression. Int J Rheumatol 2013; 2013:954292.
13. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5:522-531.
14. Xiao C, Rajewsky K. MicroRNA control in the immune system: basic principles. Cell 2009; 136:26-36.
15. Pauley KM, Cha S, Chan EK. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 2009; 32:189-194.
16. Chafin CB, Reilly CM. MicroRNA implicated in the immunopathogenesis of lupus nephritis. Clinc Dev Immunol 2013; 2013:430239.
17. Liu Y, Dong J, Mu R, et al. MicroRNA-30a promotes B cell hyperactivity in patients with systemic lupus erythematosus by direct interaction with Lyn. Arthritis Rheum 2013; 65:1603-1611.
18. Yu CC, Yen TS, Lowell CA, DeFranco AL. Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases LYN and Fyn. Curr Biol 2001; 11:34-38.
19. Yuan Y, Kasar S, Underbayev C, et al. Role of microRNA-15a in autoantibody production in interferon-augmented murine model of lupus. Mol Immunol 2012; 52:61-70.
20. Klaas M, Oetke C, Lewis LE, et al. Sialoadhesin promotes rapid proinflammatory and type I IFN responses to a sialylated pathogen, Campylobacter jejuni. J Immunol 2012; 189:2414-2422.
21. Biesen R, Demir C, Barkhudarova F, et al. Sialic acid-binding Ig-like lectin 1 expression in inflammatory and resident monocytes is a potential biomarker for monitoring disease activity and success of therapy in systemic lupus erythematosus. Arthritis Rheum 2008; 58:1136-1145.
22. Ip CW, Kroner A, Crocker PR, et al. Sialoadhesin deficiency ameliorates myelin degeneration and axonopathic changes in the CNS of PLP overexpressing mice. Neurobiol Dis 2007; 25:105-111.
23. Kidder D, Richards HE, Lyons PA, Crocker PR. Sialoadhesin deficiency does not influence the severity of lupus nephritis in New Zealand Black x New Zealand White F1 mice. Arthritis Res Ther 2013; 15:R175.
24. Lu J, Kwan BC, Lai FM, et al. Gene expression of TWEAK/Fn14 and IP-10/ CXCR3 in glomerulus and tubulointerstitium of patient with lupus nephritis. Nephrology (Carlton) 2011; 16:426-432.
25. Campbell S, Burkly LC, Gao HX, et al. Proinflammatory effects of TWEAK/ Fn14 interactions in glomerular mesangial cells. J Immunol 2006; 176:1889-1898.
26. Michaelson JS, Wisniacki N, Burkly LC, Putterman C. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun 2012; 39:130-142.
27. Cheng E, Armstrong CL, Galisteo R, Winkles JA. TWEAK/Fn14 axis-targeted therapeutics: moving basic science discoveries to the clinic. Front Immunol 2013; 4:473.
28. Ward MM. Changes in the incidence of endstage renal disease due to lupus nephritis in the United States, 1996-2004. J Rheumatol 2009; 36:63-67.
29. Gunnarsson I, Sundelin B, Jonsdottir T, et al. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide- resistant proliferative lupus nephritis. Arthritis Rheum 2007; 56:1263-1272.
30. Lightstone L. Lupus nephritis: where are we now? Curr Opin Rheumatol 2010; 22:252-256.
31. Dolff S, Abdulahad WH, Arends S, et al. Urinary CD8+ T-cell counts discriminate between active and inactive lupus nephritis. Arthritis Res Ther 2013; 15:R36.
32. Yang XY, Wang HY, Zhao XY, et al. Th22, but not Th17 might be a good index to predict the tissue involvement of systemic lupus erythematosus. J Clinc Immunol 2013; 33:767-774.
33. Enghard P, Rieder C, Kopetschke K, et al. Urinary CD4 T cells identify SLE patients with proliferative lupus nephritis and can be used to monitor treatment response. Ann Rheum Dis 2014; 73:277-283.
34. Reyes-Thomas J, Blanco I, Putterman C. Urinary biomarkers in lupus nephritis. Clinc Rev Allergy Immunol 2011; 40:138-150.
35. Watson L, Beresford MW. Urine biomarkers in juvenile-onset SLE nephritis. Pediatr Nephrol 2013; 28:363-374.
36. Wang G, Tam LS, Li EKM, et al. Serum and urinary free microRNA level in patients with systemic lupus erythematosus. Lupus 2011; 20:493-500.
37. Wang G, Tam LS, Kwan BCH, et al. Expression of miRNA-146a and miRNA- 155 in the urinary sediment of systemic lupus erythematosus. Clin Rheumatol 2012; 31:435-440.
38. Dai Y, Sui W, Lan H, et al. Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int 2009; 29:749-754.
39. Te JL, Dozmorov IM, Guthridge JM, et al. Identification of unique microRNA signature associated with lupus nephritis. PLoS ONE 2010; 5:e10344.
40. Dai R, Zhang Y, Khan D, et al. Identification of a common lupus diseaseassociated microRNA expression pattern in three different murine models of lupus. PLoS ONE 2010; 5:e14302.
41. Wu T, Du Y, Han J, et al. Urinary angiostatin: a novel putative marker of renal pathology chronicity in lupus nephritis. Mol Cell Proteomics 2013; 12:1170-1179.
42. Brunner HI, Bennett MR, Mina R, et al. Association of noninvasively measured renal protein biomarkers with histologic features of lupus nephritis. Arthritis Rheum 2012; 64:2687-2697.
43. Zhang X, Nagaraja HN, Nadasdy T, et al. A composite urine biomarker reflects interstitial inflammation in lupus nephritis kidney biopsies. Kidney Int 2012; 81:401-406.
44. Sui M, Lin Q, Xu Z, et al. Simultaneous positivity for anti-DNA, anti-nucleosome and anti-histone antibodies is a marker for more severe lupus nephritis. J Clin Immunol 2013; 33:378-387.
45. BLISS-52 and BLISS-76 Study Groups. Petri M, van Vollenhoven RF, Buyon J, et al. Baseline predictors of systemic lupus erythematosus flares: data from the combined placebo groups in the phase III Belimumab trials. Arthritis Rheum 2013; 65:2143-2153.
46. Xuejing Z, Jiazhen T, Jun L, et al. Urinary TWEAK level as a marker of lupus nephritis activity in 46 cases. J Biomed Biotechnol 2012; 2012:359647.
47. El-shehaby A, Darweesh H, El-Khatib M, et al. Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. J Clin Immunol 2001; 31:848-856.
48. Schwartz N, Rubinstein T, Burkly LC, et al. Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther 2009; 11:R143.
49. Treamtrakanpon W, Tantivitayakul P, Benjachat T, et al. APRIL, a proliferationinducing ligand, as a potential marker of lupus nephritis. Arthritis Res Ther 2012; 14:R252.
50. Dai Y, Huang YS, Tang M, et al. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 2007; 16:939-946.
51. Zhao S, Wang Y, Liang Y, et al. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum 2011; 63:1376-1386.
52. Richardson B, Scheinbart L, Strahler J, et al. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 1990; 33:1665-1673.
53. Zhang Y, Zhao M, Sawalha AH, et al. Impaired DNA methylation and its mechanisms in CD4+T cells of systemic lupus erythematosus. J Autoimmun 2013; 41:92-99.
54. Liu Z, Davidson A. Taming lupus: a new understanding of pathogenesis is leading to clinical advances. Nat Med 2012; 18:871-882.
55. Paz Z, Tsokos GC. New therapeutics in systemic lupus erythematosus. Curr Opin Rheumatol 2013; 25:297-303.
56. Koutsokeras T, Healy T. Systemic lupus erythematosus and lupus nephritis. Nat Rev Drug Discov 2014; 13:173-174.
57. Xiong W, Lahita RG. Pragmatic approaches to therapy for systemic lupus erythematosus. Nat Rev Rheumatol 2014; 10:97-107.
58. MaloneyDG, Liles TM, Czerwinski DK, et al. Phase I clinical trial using escalating single-dose infusion of chimeric anti-CD20 monoclonal antibody (IDEC-C2B8) in patients with recurrent B-cell lymphoma. Blood 1994; 84:2457-2466.
59. Anolik JH. B cell biology: implications for treatment of systemic lupus erythematosus. Lupus 2013; 22:342-349.
60. Weidenbusch M, Rommele C, Schrottle A, Anders HJ. Beyond the LUNAR trial: efficacy of rituximab in refractory lupus nephritis. Nephrol Dial Transplant 2013; 28:106-111.
61. Merrill JT, Neuwelt CM, Wallace DJ, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum 2010; 62:222-233.
62. Rovin BH, Furie R, Latinis K, et al., LUNAR Investigator Group. 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.
63. Wofsy D, Hillson JL, Diamond B. Comparison of alternative primary outcome measures for use in lupus nephritis clinical trials. Arthritis Rheum 2013; 65:1586-1591.
64. Isenberg DA, Rahman A. Systemic lupus erythematosus in 2013.Taking a closer look at biologic therapy for SLE. Nat Rev Rheumatol 2014; 10:71-72.
65. Hahn BH, McMahon MA, Wilkinson A, et al. American College of Rheumatology guidelines for screening, case definition, treatment, and management of lupus nephritis. Arthritis Care Res (Hoboken) 2012; 64:797-808.
66. Bertsias GK, Tektonidou M, Amoura Z, et al. Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis 2012; 71:1771-1782.
67. Condon MB, Ashby D, Pepper RJ, et al. Prospective observational singlecentre cohort study to evaluate the effectiveness of treating lupus nephritis with rituximab and mycophenolate mofetil but no oral steroids. Ann Rheum Dis 2013; 72:1280-1286.
68. Chang A, Henderson SG, Brandt D, et al. In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J Immunol 2011; 186:1849-1860.
69. Wang W, Rangel-Moreno J, Owen T, et al. Long-term B cell depletion in murine lupus eliminates autoantibody-secreting cells and is associated with alterations in the kidney plasma cell niche. J Immunol 2014; 192:3011-3020.
70. Neubert K, Meister S, Moser K, et al. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat Med 2008; 14:748-755.
71. Hiepe F, Alexander T, Peukert R, et al. Refractory SLE patients respond to the proteasome inhibitor bortezomib. Ann Rheum Dis 2012; 71:A15-A16.
72. Murphy G, Lisnevskaia L, Isenberg D. Systemic lupus erythematosus and other autoimmune rheumatic diseases: challenges to treatment. Lancet 2013; 382:809-818.
73. Corthals SL, Kuiper R, Johnson DC, et al. Genetic factors underlying the risk of bortezomib induced peripheral neuropathy in multiple myeloma patients. Haematologica 2011; 96:1728-1732.
74. Stohl W. Therapeutic targeting of the BAFF/APRIL axis in systemic lupus erythematosus. Expert Opin Ther Targets 2014; 18:473-489.
75. Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo controlled, phase 3 trial. Lancet 2011; 377:721-731.
76. Furie R, Petri M, Zamani O, et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum 2011; 63:3918-6930.
77. Dooley MA, Houssiau F, Aranow C, et al. Effect of belimumab treatment on renal outcomes: results from the phase 3 belimumab clinical trials in patients with SLE. Lupus 2013; 22:63-72.
78. Rovin BH, Parikh SV. Lupus nephritis: the evolving role of novel therapeutics. Am J Kidney Dis 2014; 63:677-690.