Lupus nephritis: Pathologic features, epidemiology and a guide to therapeutic decisions

Lupus

Volumn 19, Issue 5, 2010, Pages 557-574

  Ortega, L M ^a   Schultz, D R ^a   Lenz, O ^a   Pardo, V ^b   Contreras, G N ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Drug therapy; Epidemiology; Lupus nephritis; Pathogenesis; Systemic lupus erythematosus

Indexed keywords

ABATACEPT; ABETIMUS; ALDOSTERONE ANTAGONIST; ALPHA ACTININ ANTIBODY; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTICOAGULANT AGENT; AUTOANTIBODY; AZATHIOPRINE; BASILIXIMAB; BISPHOSPHONIC ACID DERIVATIVE; CALCINEURIN INHIBITOR; CALCIUM; COMPLEMENT COMPONENT C1Q ANTIBODY; CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYCLOSPORIN; CYTOKINE ANTIBODY; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DOUBLE STRANDED DNA ANTIBODY; FLUDARABINE; METHYLPREDNISOLONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NUCLEOSOME ANTIBODY; OCRELIZUMAB; PREDNISONE; RAPAMYCIN; RITUXIMAB; TACROLIMUS; UNCLASSIFIED DRUG; UNINDEXED DRUG; VITAMIN D;

AMENORRHEA; ANTIBODY BLOOD LEVEL; ANTIPHOSPHOLIPID SYNDROME; BACTERIAL INFECTION; CHRONIC KIDNEY FAILURE; CLINICAL DECISION MAKING; CLINICAL FEATURE; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CROSS REACTION; DISEASE CLASSIFICATION; DOSE RESPONSE; DRUG DOSAGE FORM COMPARISON; DRUG DOSE SEQUENCE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG POTENTIATION; DRUG PULSE THERAPY; DRUG SAFETY; DRUG TOLERABILITY; GLOMERULUS FILTRATION RATE; GRAFT FAILURE; HEMODIALYSIS; HEMORRHAGIC CYSTITIS; HERPES ZOSTER; HIGH RISK PATIENT; HISTOPATHOLOGY; HUMAN; HYPERTENSION; IMMUNOPATHOGENESIS; INFECTION; KIDNEY BIOPSY; KIDNEY FAILURE; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; LEUKOPENIA; LONG TERM CARE; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAINTENANCE THERAPY; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; NEPHROTOXICITY; NONHUMAN; OSTEOPENIA; OSTEOPOROSIS; PATIENT CARE; PRACTICE GUIDELINE; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; RECURRENCE RISK; REMISSION; REVIEW; SURVIVAL RATE; SYSTEMIC LUPUS ERYTHEMATOSUS; URINALYSIS; CLASSIFICATION; PATHOLOGY;

HUMANS; LUPUS NEPHRITIS; PRACTICE GUIDELINES AS TOPIC; PROGNOSIS;

EID: 77951242133     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1177/0961203309358187     Document Type: Review

References (157)

1. Churg J., Sobin LH Renal disease: classification and atlas of glomerular disease. Tokyo: Igaku-Shoin ; 1982.
2. Churg J., Bernstein J., Glassock RJ Renal disease. Tokyo: Igaku-Shoin ; 1995. pp. 151-179.
3. Weening JJ, DAgati VD, Schwartz MM, et al. Classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 2004 ; 65: 521-530. (Pubitemid 38130646)
4. Weening JJ, DAgati VD, Schwartz MM, et al. Classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol 2004 ; 15: 241-250. (Pubitemid 38140764)
5. Najafi CC, Korbert SM, Lewis EJ, et al. Significance of histologic patterns of glomerular injury upon long-term prognosis in severe lupus glomerulonephritis. Kidney Int 2001 ; 59: 2156-2163.
6. Appel GB, Cohen DJ, Pirani CL, et al. Long-term follow-up of lupus nephritis: a study based on the WHO classification. Am J Med 1987 ; 83: 877-885.
7. Radhakrishnan I., Szaboks M., DAgati V., Nicolaides M., Wharton R., Appel GB Lupus membranous nephropathy (LMN): course and prognosis in 50 patients. J Am Soc Nephrol 1993 ; meeting/abs 284.
8. Austin HA, Boumpas DT, Vaughan EM, Balow JE High-risk features of lupus nephritis: importance of race and clinical and histologic factors in 166 patients. Nephrol Dial Transplant 1995 ; 10: 1620-1628.
9. Contreras G., Pardo V., Cely C., et al. Factors associated with poor outcomes in patients with lupus nephritis. Lupus 2005 ; 14: 890-895. (Pubitemid 41736370)
10. Schwartz MM, Korbet SM, Lewis EJ for the Collaborative Study Group. The prognosis and pathogenesis of severe lupus glomerulonephritis. Nephrol Dial Transplant 2008 ; 23: 1298-1306.
11. Mittal B., Hurwitz S., Rennke H., et al. New subcategories of class IV lupus nephritis: are there clinical, histologic and outcome differences? Am J Kidney Dis 2004 ; 44: 1050-1059. (Pubitemid 39556485)
12. Hill GS, Delahousse M., Nochy D., et al. Class IV-S versus class IV-G lupus nephritis: clinical and morphological differences suggesting different pathogenesis. Kidney Int 2005 ; 68: 2382-2388. (Pubitemid 43117806)
13. Rahman A., Isenberg DA Systemic lupus erythematosus. N Eng J Med 2008 ; 358: 929-939. (Pubitemid 351397092)
14. Marshak-Rothstein A., Ohashi PS Intricate connections between innate and adaptive autoimmunity. Curr Opin Immunol 2007 ; 19: 603-605. (Pubitemid 50014681)
15. Zarember KA, Godowski PJ Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products and cytokines. J Immunol 2002 ; 168: 554-561.
16. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol 2006 ; 6: 823-835. (Pubitemid 44631651)
17. Von Landenberg P., Bauer S. Nucleic acid recognizing Toll-like receptors and autoimmunity. Curr Opin Immunol 2007 ; 19: 606-610. (Pubitemid 350236814)
18. Lang KS, Recher M., Junt T., et al. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med 2005 ; 11: 138-145. (Pubitemid 40321348)
19. Nangaku M., Couser WG Mechanisms of immune deposit formation and the mediation of immune renal injury. Clin Exp Nephrol 2005 ; 9: 183-191. (Pubitemid 41414116)
20. Cook HT, Botto M. Mechanisms of disease: the complement system and the pathogenesis of systemic lupus erythematosus. Nat Clin Pract Rheumatol 2006 ; 2: 330-337. (Pubitemid 43842262)
21. Cohen RA, Bayliss G., Crispin JC, et al. T cells and in situ cryoglobulin deposition in the pathogenesis of lupus nephritis. Clin Immunol 2008 ; 128: 1-7. (Pubitemid 351815199)
22. Markiewski MM, Nilsson B., Ekdahl KN, et al. Complement and coagulation: strangers or partners in crime? Trends Immunol 2007 ; 28: 184-192. (Pubitemid 46476881)
23. Loos M., Colomb M., Petry F., Reid KBM. Early phases of complement activation and innate immunity. Immunobiology 2002 ; 205: 337-339. (Pubitemid 35153951)
24. Guo RF, Ward PA Role of C5a in inflammatory responses. Annu Rev Immunol 2005 ; 23: 821-852.
25. Korb LC, Ahearn JM C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes. Complement deficiency and systemic lupus erythematosus revisited. J Immunol 1997 ; 158: 4525-4528.
26. Walport MJ, Davies KA, Morley BJ, et al. Complement deficiency and autoimmunity. Ann N Y Acad Sci 1997 ; 815: 267-281.
27. Pickering MC, Botto M., Taylor PR, et al. Systemic lupus erythematosus, complement deficiency and apoptosis. Adv Immunol 2000 ; 76: 227-324.
28. Rosen A., Casciola-Rosen L., Ahearn J. Novel packages of viral and self-antigens are generated during apoptosis. J Exp Med 1995 ; 181: 1557-1561.
29. Herrmann M., Voll RE, Zoller OM, et al. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosis. Arthritis Rheum 1998 ; 41: 1241-1250. (Pubitemid 28313427)
30. Baumann I., Kolowos W., Voll RE, et al. Impaired uptake of apoptotic cells into body macrophages in germinal centers of patients with systemic lupus erythematosis. Arthritis Rheum 2002 ; 46: 191-201. (Pubitemid 34121664)
31. Reid KBM. Chemistry and molecular genetics of C1q. Behring Inst Mitt 1989 ; 84: 8-19.
32. Knobel HR, Villiger W., Isliker H. Chemical analysis and electron microscopy studies of human C1q prepared by different methods. Eur J Immunol 1975 ; 5: 78-82.
33. Schultz DR, Perez GO, Volanakis JE, et al. Glomerular disease in two patients with urticaria-cutaneous vasculitis and hypocomplementemia. Am J Kidney Dis 1981 ; 1: 157-165.
34. Antes U., Heinz H-P., Loos M. Detection of C1q-bearing complexes by a monoclonal anti-C1q ELISA system. J Immunol Methods 1988 ; 102: 149-156. (Pubitemid 17141458)
35. Agnello V., Koffler D., Eisenberg JW, et al. C1q precipitins in the sera of patients with SLE and other hypocomplementemic states: characterization of high and low molecular weight types. J Exp Med 1971 ; 134 (Suppl): 228S - 241S.
36. Golan MO, Burger R., Loos M. Conformational changes in C1q after binding to immune complexes: detection of neoantigens with monoclonal antibodies. J Immunol 1982 ; 129: 445-447. (Pubitemid 12039356)
37. Heinz H-P., Rubin K., Laurell A-B., et al. Common epitopes in C1q and collagen type II. Mol Immunol 1989 ; 26: 163-169. (Pubitemid 19031181)
38. Wener MH, Mannik M., Schwartz MM, et al. Relationship between renal pathology and the size of circulating immune complexes in patients with systemic lupus erythematosus. Medicine 1987 ; 66: 85-97. (Pubitemid 17059639)
39. Uwatoko S., Mannik MM Low molecular weight C1q-binding immunoglobulin G in patients with systemic lupus erythematosus consist of autoantibodies to the collagen-like region of C1q. J Clin Invest 1988 ; 82: 816-824.
40. Antes U., Heinz H-P., Loos M. Evidence for the presence of autoantibodies to the collagen-like portion of C1q in systemic lupus erythematosus. Arthritis Rheum 1988 ; 31: 457-464.
41. Siegert CEH, Breedveld FC, Daha MR Autoantibodies against C1q in systemic lupus erythematosus. Behring Inst Mitt 1993 ; 93: 279-286.
42. Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology 1998 ; 199: 265-285. (Pubitemid 28404347)
43. Schultz DR, Loos M., Bub F., et al. Differentiation of hemolytically active fluid-phase and cell-bound human C1q by an ant venom-derived polysaccharide. J Immunol 1980 ; 124: 1251-1257. (Pubitemid 10139221)
44. Gewurz H., Ying S-C., Jiang H., et al. Nonimmune activation of the classical complement pathway. Behring Inst Mitt 1993 ; 93: 138-147.
45. Siegert C., Daha M., Westedt ML, et al. IgG autoantibodies against C1q are correlated with nephritis, hypocomplementemia and dsDNA antibodies in systemic lupus erythematosus. J Rheumatol 1991 ; 18: 230-234.
46. Gunnarsson I., Ronnelid J., Huang YH, et al. Association between ongoing anti-C1q antibody production in peripheral blood and proliferative nephritis in patients with active systemic lupus erythematosus. Br J Rheumatol 1997 ; 36: 32-37. (Pubitemid 27351220)
47. Trendelenburg M., Marfurt J., Gerbger I., et al. Lack of occurrence of severe lupus nephritis among anti-C1q autoantibody-negative patients. Arthritis Rheum 1999 ; 42: 187-188. (Pubitemid 29042588)
48. Norsworthy PE, Theodoridis E., Botto M., et al. Overrepresentation of the Fc gamma receptor type IIA R131/ R131 genotype in caucasoid systemic lupus erythematosus patients with autoantibodies to C1q and glomerulonephritis. Arthritis Rheum 1999 ; 42: 1828-1832. (Pubitemid 30257746)
49. Moroni G., Trendelenburg M., Del Papa N., et al. Anti-C1q antibodies may help in diagnosing a renal flare in lupus nephritis. Am J Kidney Dis 2001 ; 37: 490-498. (Pubitemid 32195287)
50. Siegert CE, Kazatchkine MD, Sjohölm A., et al. Autoantibodies against C1q: view on clinical relevance and pathogenic role. Clin Exp Immunol 1999 ; 116: 4-8. (Pubitemid 29169997)
51. Siegert CE, Daha MR, Tseng CM, et al. Predictive value of IgG autoantibodies against C1q for nephritis in systemic lupus erythematosus. Ann Rheum Dis 1993 ; 52: 851-856.
52. Coremans IE, Spronk PE, Bootsma H., et al. Changes in antibodies to C1q predict renal relapses in systemic lupus erythematosus. Am J Kidney Dis 1995 ; 26: 595-601.
53. Trinder PK, Maeurer MJ, Schorlemmer HU, et al. Autoreactivity of mouse C1q in a murine model of SLE. Rheumatol Int 1995 ; 15: 117-121.
54. Millake DB, Blanchard AD, Patel B., et al. The cDNA sequence of a human placental-actinin. Nucleic Acids Res 1989 ; 17: 6725.
55. Honda K., Yamada T., Endo R., et al. Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion. J Cell Biol 1998 ; 140: 1383-1393. (Pubitemid 28152987)
56. Beggs AH, Byers TJ, Knoll JH, et al. Cloning and characterization of two skeletal muscle α-actinin genes located on chromosomes one and eleven. J Biol Chem 1992 ; 267: 9281-9288.
57. Yang C., Glass WF II. Expression of α-actinin-1 in human glomerular mesangial cells in vivo and in vitro. Exp Biol Med 2008 ; 233: 689-693.
58. Mostoslavsky G., Fishchel R., Yachimovich N., et al. Lupus anti-DNA antibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry. Eur J Immunol 2001 ; 31: 1221-1227.
59. Deocharan B., Qing X., Lichauco J., et al. α-Actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J Immunol 2002 ; 168: 3072-3078. (Pubitemid 34211690)
60. Kaplan JM, Kim KN, North N., et al. Mutations in ACTN4, encoding ∝́-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 2000 ; 24: 251-256.
61. Kos CH, Le TC, Sinha S., Henderson JM, et al. Mice deficient in α-actinin-4 have severe glomerular disease. J Clin Invest 2003 ; 111: 1683-1690. (Pubitemid 38057750)
62. Mason LJ, Ravirajan CT, Rahman A., et al. Is alpha-actinin a target for pathogenic anti-DNA antibodies in lupus nephritis? Arthritis Rheum 2004 ; 50: 866-870. (Pubitemid 38326187)
63. Conquefers S., Renaudineau Y., Jousse S., et al. The anti-alpha-actinin test completes anti-DNA determination in systemic lupus erythematosus. Ann N Y Acad Sci 2005 ; 1050: 170-175. (Pubitemid 41129433)
64. Zhao Z., Weinstein E., Tuzova M., et al. Cross-reactivity of human lupus anti-DNA antibodies with alpha-actinin and nephritogenic potential. Arthritis Rheum 2005 ; 52: 522-530. (Pubitemid 40216316)
65. Zhao Z., Deocharan B., Scherer PE, et al. Differential binding of cross-reactive anti-DNA antibodies to mesangial cells: the role of alpha-actinin. J Immunol 2006 ; 176: 7704-7714. (Pubitemid 43849071)
66. Becker-Merok A., Kalaaji M., Haugbro K., et al. Alpha-actinin-binding antibodies in relation to systemic lupus erythematosus and lupus nephritis. Arthritis Res Therapy 2006 ; 8: R162. (Pubitemid 44168829)
67. Kalaaji M., Mortensen E., Jørgensen L., et al. Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells. Am J Path 2006 ; 168: 1779-1792. (Pubitemid 43825300)
68. Schultz DR, Diego JM Antineutrophil cytoplasmic antibodies (ANCA) and systemic vasculitis: update of assays, immunopathogenesis, controversies and report of a novel de novo ANCAassociated vasculitis after kidney transplantation. Sem Arthritis Rheum 2000 ; 29: 267-285.
69. Jennette JC, Falk RJ New insight into the pathogenesis of vasculitis associated with antineutrophil cytoplasmic autoantibodies. Curr Opin Rheumatol 2008 ; 20: 55-60.
70. Hill GS, Delahousse M., Nochy D., et al. Class IV-S versus class IV-G lupus nephritis: clinical and morphological differences suggesting different pathogenesis. Kidney Int 2005 ; 68: 2382-2388. (Pubitemid 43117806)
71. Schwartz MM, Korbet SM, Lewis EJ for the Collaborative Study Group. The prognosis and pathogenesis of severe lupus glomerulonephritis. Nephrol Dial Transplant 2008 ; 23: 1298-1306.
72. Feng YU, Ying TAN, Gang LIU, et al. Clinicopathological characteristics and outcomes of patients with crescentic lupus nephritis. Kidney Int 2009 ; 76: 307-317.
73. Davis JC, Tassiulas LO, Boumpas DT Lupus nephritis. Curr Opin Rheum 1996 ; 8: 415-423.
74. Danchenko N., Satia JA, Anthony MS Epidemiology of systemic lupus erythematosus: a comparison of World wide disease burden. Lupus 2006 ; 15: 308-318. (Pubitemid 43828810)
75. Seligman VA, Lum RF, Olson JL, et al. Demographic differences in the development of lupus nephritis: a retrospective analysis. Am J Med 2002 ; 112: 726-729.
76. Bastian HM, Roseman JM, McGwin G. Jr, et al. Systemic lupus erythematosus in three ethnic groups. XII. Risk factors for lupus nephritis after diagnosis. Lupus 2002 ; 11: 152-160.
77. Alarcon GS, McGwin G. Jr, Petri M., et al. Baseline characteristics of a multiethnic lupus cohort: PROFILE. Lupus 2002 ; 11: 95-101. (Pubitemid 34259439)
78. Adler M., Chambers S., Edwards C., et al. An assessment of renal failure in an SLE cohort with special reference to ethnicity, over a 25-year period. Rheumatology 2006 ; 45: 1144-1147. (Pubitemid 44542106)
79. Contreras G., Lenz O., Pardo V., et al. Outcomes in African Americans and Hispanics with lupus nephritis. Kidney Int 2006 ; 69: 1846-1851. (Pubitemid 43739214)
80. Korbet SM, Schwartz MM, Evans G., et al. Severe lupus nephritis: racial differences in presentation and outcome. J Am Soc Nephrol 2007 ; 18: 244-254.
81. Barr RG, Seliger S., Appel GB, et al. Prognosis in proliferative lupus nephritis: the role of socio-economic status and race/ethnicity. Nephrol Dial Transplant 2003 ; 18: 2039-2046. (Pubitemid 37220309)
82. Austin HA III, Boumpas DT, Vaughan EM, et al. High-risk features of lupus nephritis: importance of race and clinical and histological factors in 166 patients. Nephrol Dial Transplant 1995 ; 10: 1620-1628.
83. Berden JHM. Lupus nephritis: Nephrology forum. Kidney Int 1997 ; 52: 538-558.
84. Moroni G., Ventura D., Riva P., et al. Antiphospholipid antibodies are associated with an increased risk for chronic renal insufficiency in patients with lupus nephritis. Am J Kidney Dis 2004 ; 43: 28-36. (Pubitemid 38049432)
85. Korbet SM, Lewis EJ, Schwartz M., et al. Factors predictive of outcome in severe lupus nephritis. Lupus Nephritis Collaborative Study Group. Am J Kidney Dis 2000 ; 35: 904-914.
86. Ioannidis JP, Boki KA, Katsorida ME, et al. Remission, relapse and re-remission of proliferative lupus nephritis treated with cyclophosphamide. Kidney Int 2000 ; 57: 258-264. (Pubitemid 30227773)
87. Illei GG, Takada K., Parkin D., et al. Renal flares are common in patients with severe proliferative lupus nephritis treated with pulse immunosuppressive therapy: long-term follow-up of a cohort of 145 patients participating in randomized controlled studies. Arthritis Rheum 2002 ; 46: 995-1002. (Pubitemid 34303812)
88. Mok CC, Ying KY, Tang S., et al. Predictors and outcome of renal flares after successful cyclophosphamide treatment for diffuse proliferative lupus glomerulonephritis. Arthritis Rheum 2004 ; 50: 2559-2568. (Pubitemid 39062717)
89. Hill GS, Delahousse M., Nochy D., et al. Outcome of relapse in lupus nephritis: roles of reversal of renal fibrosis and response of inflammation to therapy. Kidney Int 2002 ; 61: 2176-2186. (Pubitemid 34539335)
90. Austin HA, Balow JE Natural history and treatment of lupus nephritis. Semin Nephrol 1999 ; 19: 2-11. (Pubitemid 29048841)
91. Euler HH, Schroeder JO, Zeuner RA, et al. A randomized trial of plasmapheresis and subsequent pulse cyclophosphamide in severe lupus: design of the LPSG trial. Int J Artif Organs 1991 ; 14: 639-646.
92. Lewis EJ, Hunsicker LG, Lan S-P., et al. For the Lupus Nephritis Collaborative Study Group: A controlled trial of plasmapheresis therapy in severe lupus nephritis. New Engl J Med 1992 ; 326: 1373-1379.
93. Austin HA III, Klippel JH, Balow JE, et al. Therapy of lupus nephritis. Controlled trial of prednisone and cytotoxic drugs. N Engl J Med 1986 ; 314: 614-619. (Pubitemid 16132725)
94. Steinberg AD, Steinberg SC Long-term preservation of renal function in patients with lupus nephritis receiving treatment that includes cyclophosphamide versus those treated with prednisone only. Arthritis Rheum 1991 ; 34: 945-950.
95. Gourley MF, Austin HA III, Scott D., et al. Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis. A randomized, controlled trial. Ann Intern Med 1996 ; 125: 549-557. (Pubitemid 126450087)
96. Illei GG, Austin HA, Crane M., et al. Combination therapy with pulse cyclophosphamide plus pulse methylprednisolone improves long-term renal outcome without adding toxicity in patients with lupus nephritis. Ann Intern Med 2001 ; 135: 248-257. (Pubitemid 32799338)
97. Bansal VK, Beto JA Treatment of lupus nephritis: a meta-analysis of clinical trials. Am J Kidney Dis 1997 ; 29: 193-199. (Pubitemid 27130728)
98. Flanc RT, Roberts MA, Strippoli GFM, et al. Treatment of diffuse proliferative lupus nephritis: a meta-analysis of randomized controlled clinical trials. Am J Kidney Dis 2004 ; 43: 197-208.
99. Boumpas DT, Austin HA III, Vaughn EM, et al. Controlled trial of pulse methylprednisolone versus two regimens of pulse cyclophosphamide in severe lupus nephritis. Lancet 1992 ; 340: 741-745.
100. Chan TM, Li FK, Wong RW, et al. Sequential therapy for diffuse proliferative and membranous lupus nephritis: cyclophosphamide and prednisolone followed by azathioprine and prednisolone. Nephron 1995 ; 71: 321 327.
101. Contreras G., Pardo V., Leclercq B., et al. Sequential therapies for proliferative lupus nephritis. N Engl J Med 2004 ; 350: 971-980. (Pubitemid 38269274)
102. Aspreva Pharmaceuticals. Aspreva Lupus Management Study (ALMS) (NCT00121082), http://www.clinicaltrials.gov (accessed March 2006 ).
103. Houssiau FA, Jadoul M. Cytotoxic therapy of lupus nephritis: recent developments. Nephrol Dial Transplant 2002 ; 17: 955-957. (Pubitemid 34746192)
104. Houssiau FA, Vasconcelos C., DCruz D., et al. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002 ; 46: 2121-2131.
105. Mok CC, Ho CT, Siu YP, et al. Treatment of diffuse proliferative lupus glomerulonephritis: a comparison of two cyclophosphamide-containing regimens. Am J Kidney Dis 2001 ; 38: 256-264.
106. Grootscholten C., Ligtenberg G., Hagen EC, et al. Azathioprine/ methylprednisolone versus cyclophosphamide in proliferative lupus nephritis. A randomized controlled trial. Kidney Int 2006 ; 70: 732-742. (Pubitemid 44215349)
107. Allison AC, Hovi T., Watts RW, et al. Immunological observations on patients with Lesch-Nyhan syndrome and on the role of de-novo purine synthesis in lymphocyte transformation. Lancet 1975 ; 2 (7946). 1179-1183.
108. Eugui EM, Almquist SJ, Muller CD, et al. Lymphocyte-selective cytostatic and immunosuppressive effects of mycophenolic acid in vitro: role of deoxyguanosine nucleotide depletion. Scand J Immunol 1991 ; 33: 161-173.
109. Allison AC, Eugui EM Mycophenolate mofetil and its mechanisms of action. Immunopharmacology 2000 ; 47: 85-118.
110. Corna D., Morigi M., Facchinetti D., et al. Mycophenolate mofetil limits renal damage and prolongs life in murine lupus autoimmune disease. Kidney Int 1997 ; 51: 1583-1589. (Pubitemid 27239915)
111. Van Bruggen MC, Walgreen B., Rijke TP, et al. Attenuation of murine lupus nephritis by mycophenolate mofetil. J Am Soc Nephrol 1998 ; 9: 1407-1415. (Pubitemid 28354550)
112. Chan TM, Li FK, Tang CS, et al. Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. Hong Kong-Guangzhou Nephrology Study Group. N Engl J Med 2000 ; 343: 1156-1162.
113. Hu W., Liu Z., Chen H., et al. Mycophenolate mofetil vs cyclophosphamide therapy for patients with diffuse proliferative lupus nephritis. Chin Med J (Engl) 2002 ; 115: 705-709. (Pubitemid 34594285)
114. Ong LM, Hooi LS, Lim TO, et al. Randomized controlled trial of pulse intravenous cyclophosphamide versus mycophenolate mofetil in the induction therapy of proliferative lupus nephritis. Nephrology (Carlton) 2005 ; 10: 504-510.
115. Ginzler EM, Dooley MA, Aranow C., et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med 2005 ; 353: 2219-2228. (Pubitemid 41697285)
116. Chan TM, Tse KC, Tang CS, et al. Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis. J Am Soc Nephrol 2005 ; 16: 1076-1084.
117. Dooley MA, Hogan S., Jennette C., et al. For the Glomerular Disease Collaborative Network: Cyclophosphamide therapy for lupus nephritis: poor renal survival in black Americans. Kidney Int 1997 ; 51: 1188-1195.
118. Appel GB, Contreras G., Dooley MA, et al. for the Aspreva Lupus Management Study (ALMS). Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J Am Soc Nephrol 2009 ; 20: 1103-1112.
119. Tam LS, Li EK, Leung CB, et al. Long-term treatment of lupus nephritis with cyclosporin A. Q J Med 1998 ; 91: 573-580. (Pubitemid 28383236)
120. Dostal C., Tesar V., Rychlik I., et al. Effect of 1 year cyclosporine A treatment on the activity and renal involvement of systemic lupus erythematosus: a pilot study. Lupus 1998 ; 7: 29-36. (Pubitemid 28052659)
121. Moroni G., Doria A., Mosca M., et al. A randomized pilot trial comparing cyclosporine and azathioprine for maintenance therapy in diffuse lupus nephritis over four years. Clin J Am Soc Nephrol 2006 ; 1: 925-932.
122. Austin HA III, Illei GG, Braun MJ, et al. Randomized, controlled clinical trial of prednisone, cyclophosphamide and cyclosporine in lupus membranous nephropathy. J Am Soc Nephrol 2009 ; 20: 901-911.
123. Entani C., Izumino K., Iida H., et al. Effect of a novel immunosuppressant, FK506, on spontaneous lupus nephritis in MRL/MpJ-lpr/lpr mice. Nephron 1993 ; 64: 471-475. (Pubitemid 23202862)
124. Bao H., Liu Z-H., Xie H-L., et al. Successful treatment of class V + IV lupus nephritis with multitarget therapy. J Am Soc Nephrol 2008 ; 19: 2001-2010.
125. Bertsias G., Ioannidis JPA, Boletis J., et al. EULAR recommendations for the management of systemic lupus erythematosis. Report of a task force of the EULAR standing committee for international clinical studies including therapeutics. Ann Rheum Dis 2008 ; 67: 195-205. (Pubitemid 351183308)
126. Boumpas DT, Tassiulas IO, Fleisher TA, et al. A pilot study of low-dose fludarabine in membranous nephropathy refractory to therapy. Clin Nephrol 1999 ; 52: 67-75.
127. Davis JC Jr, Austin H. III, Boumpas D., et al. A pilot study of 2-chloro-2ĝ€2-deoxyadenosine in the treatment of systemic lupus erythematosus-associated glomerulonephritis. Arthritis Rheum 1998 ; 41: 335-343. (Pubitemid 28087702)
128. Llorente L., Richaud-Patin Y., Garcia-Padilla C., et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 2000 ; 43: 1790-1800.
129. National Institute of Diabetes and Digestive and Kidney Diseases. Sirolimus therapy in idiopathic and lupus membranous nephropathy (NCT00050713), http://clinicaltrials.gov.
130. Schiffer LE, Hussain N., Wang X., et al. Lowering anti-dsDNA antibodies - whats new? Lupus 2002 ; 11: 885-894. (Pubitemid 36069985)
131. Furie RA, Cash JM, Cronin ME, et al. Treatment of systemic lupus erythematosus with LJP 394. J Rheumatol 2001 ; 28: 257-265. (Pubitemid 32165130)
132. Strand V., Aranow C., Cardiel MH, et al. Improvement in health-related quality of life in systemic lupus erythematosus patients enrolled in a randomized clinical trial comparing LJP 394 treatment with placebo. Lupus 2003 ; 12: 677-686. (Pubitemid 37173664)
133. Alarcon-Segovia D., Tumlin JA, Furie RA, et al. LJP 394 for the prevention of renal flare in patients with systemic lupus erythematosus: results from a randomized, double-blind, placebo-controlled study. Arthritis Rheum 2003 ; 48: 442-454. (Pubitemid 36278013)
134. Early GS, Zhao W., Burns CM Anti-CD40 ligand antibody treatment prevents the development of lupus-like nephritis in a subset of New Zealand black × New Zealand white mice. Response correlates with the absence of an anti-antibody response. J Immunol 1996 ; 157: 3159-3164. (Pubitemid 126450078)
135. Davis JC Jr, Totoritis MC, Rosenberg J., et al. Phase I clinical trial of a monoclonal antibody against CD40-ligand (IDEC-131) in patients with systemic lupus erythematosus. J Rheumatol 2001 ; 28: 95-101. (Pubitemid 32062030)
136. Dharnidharka VR Costimulation blockade with belatacept in renal transplantation. N Engl J Med 2005 ; 353: 2085-2086.
137. Niaid / tTN: Abatacept and Cyclophosphamide Combination Therapy for Lupus Nephritis (ACCESS) (NCT00774852), http:/www.clinicaltrials.gov.
138. Brisol-Myers Squibb. A phase II/III multi-center, randomized, double-blind, placebo-controlled study to evaluate the efficacy and safety of abatacept versus placebo on a background of mycophenolate mofetil and glucocorticosteroids in subjects with active proliferative glomerulonephritis due to systemic lupus erythematosus (NCT00430677), http://www.clinicaltrials.gov (accessed on March 2009 ).
139. Daikh DI, Wofsy D. Cutting edge: reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J Immunol 2001 ; 166: 2913-2916. (Pubitemid 33117284)
140. Burt R. Cyclophosphamide and CAMPATH in patients with systemic lupus erythematosus (NCT00278538), http://www.clinicaltrials.gov.
141. Genentech. A study to evaluate the efficacy and safety of rituximab in subjects with isn/rps class iii or iv lupus nephritis (NCT00282347), http://www.clinicaltrials.gov.
142. Phase II study of rituxan in lupus nephritis did not meet end point; Genentech press release.
143. Genentech: a study to evaluate ocrelizumab in patients with nephritis due to systemic lupus erythematosus (BELONG) (NCT00626197), http:/www. clinicaltrials.gov.
144. Results of the first interim analysis for Riquent Phase III ASPEN trail: continuation of the trial is futile; Bomarin press release.
145. Remuzzi G., Ruggenenti P., Perico N. Chronic renal diseases: renoprotective benefits of renin-angiotensin system inhibition. Ann Intern Med 2002 ; 136: 604-615. (Pubitemid 34407045)
146. Fried LF, Orchard TJ, Kasiske BL Effect of lipid reduction on the progression of renal disease: a meta-analysis. Kidney Int 2001 ; 59: 260-269.
147. Orth SR Effects of smoking on systemic and intrarenal hemodynamics: influence on renal function. J Am Soc Nephrol 2004 ; 15: S63.
148. Khamashta MA, Cuadrado MJ, Mujic F., et al. The management of thrombosis in the antiphospholipid-antibody syndrome. N Engl J Med 1995 ; 332: 993-997.
149. de Deus RB, Ferreira AC, Kirsztajn GM, et al. Osteopenia in patients with glomerular diseases requiring long-term corticosteroid therapy. Nephron Clin Practice 2003 ; 94: c69 - c74.
150. Joseph RE, Radhakrishnan J., Appel GB Antiphospholipid antibody syndrome and renal disease. Curr Opin Nephrol Hypertens 2001 ; 10: 175-181. (Pubitemid 32221758)
151. Nissenson AR, Port FK Outcome of end-stage renal disease in patients with rare causes of renal failure. III. Systemic/vascular disorders. Q J Med 1990 ; 273: 63-74.
152. Ward MM Cardiovascular and cerebrovascular morbidity and mortality among women with end-stage renal disease attributable to lupus nephritis. Am J Kidney Dis 2000 ; 36: 516-525.
153. Tang H., Chelamcharla M., Baird BC, et al. Factors affecting kidney-transplant outcome in recipients with lupus nephritis. Clin Transplant 2008 ; 22: 263-272. (Pubitemid 351689656)
154. Mojcik CF, Klippel JH End-stage renal disease and systemic lupus erythematosus. Am J Med 1996 ; 101: 100-107. (Pubitemid 26285947)
155. Goral S., Ynares G., Shapelli S., et al. Recurrent lupus nephritis in renal transplant recipients revisited: it is not rare. Transplantion 2003 ; 75: 651-656. (Pubitemid 36337363)
156. Nyberg G., Blohme I., Persson H., et al. Recurrence of SLE in transplanted kidneys: a follow-up transplant biopsy study. Nephrol Dial Transplant 1992 ; 7: 1116-1123.
157. Burgos PI, Perkins EL, Pons-Estel GJ, et al. Risk factors and impact of recurrent lupus nephritis in patients with systemic lupus erythematosus undergoing renal transplantation. Arthritis Rheum 2009 ; 60: 2757-2766.