Genetic basis of systemic lupus erythematosus

Current Opinion in Immunology

Volumn 8, Issue 6, 1996, Pages 843-851

  Vyse, Timothy J ^a   Kotzin, Brian L ^b,c  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c National Jewish Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; GENE; GENE LOCUS; GENETIC LINKAGE; GENETIC SUSCEPTIBILITY; HISTOCOMPATIBILITY GENE; HUMAN; MOUSE; NONHUMAN; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 0030444204     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(96)80014-8     Document Type: Article

References (79)

1. O'Dell JR, Kotzin BL: Systemic Lupus Erythematosus. In Ssmter's Immunologic Diseases, edn 5. Edited by Frank MM, Austen KF, daman HN, Unanue ER. Boston: Little, Brown and Company; 1995:667-697.
2. Kotzin BL: Systemic lupus erythematosus. Cell 1996, 85:303-306.
3. Vyse TJ, Todd JA: Genetic analysis of autoimmune disease. Cell 1996, 85:311-318.
4. Deapen D, Escalante A, Weinrib L, Horwitz D, Bachman B, RoyBurman R Walker A, Mack TM: A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis Rheum 1992, 35:311-318.
5. Reveille JD: The molecular genetics of systemic lupus erythematosus and Sjogren's syndrome. Curr Opin Rheumatol 1992, 4:544-856.
6. Arnett FC, Olser ML, Andersen KL, Reveille JD: Molecular analysis of major histocompatibility complex atleles associated with the lupus anticoagulant J Clin Invest 1991, 87:1490-1495.
7. Kuwana M, Okano Y, Kaburaki J, Inoko H: Clinical correlations with HLA type in Japanese patients with connective tissue disease and anti-U1 small nuclear RNP antibodies. Arthritis Rheum 1996, 39:938-942.
8. Theofilopoulos AN: The basis of autoimmunity: part II genetic predisposition. Immunol Today 1995, 16:150-159.
9. Drake CG, Rozzo SJ, Vyse TJ, Palmer E. Kotzin BL: Genetic contributions to lupus-like disease in (NZB x NZW)F1 mice. Immunol Rev 1995, 144:51-74.
10. Theofilopoulos AN: Murine models of systemic lupus erythematosus. In Systeme Lupus Erythematosus, edn 2. Edited by Lahita RG. New York: Churchill Livingstone; 1992:121-194.
11. Cohen PL, Eisenberg RA: Lpr and ghj: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 1991, 9:243-269.
12. Van Houten N, Budd RC: Lessons from the Ipr mouse. Semin Immunol 1994, 6:1-69.
13. Izut S. Iwamoto M, Fossati L, Merino R, Takahasrii S. Ibnou-Zekri N: The Yaa gene model of systemic lupus erythematosus. Immunol Rev 1995, 144:137-156.
14. Dietrich WF, Miller J, Steen R, Merchant MA, Damron-Boles D, Husain Z, Dredge R, Daly MJ, In galls KA, O'Connor TJ et al.: A comprehensive map of the mouse genome. Nature 1996, 380:149-151
15. Dib C, Fauré S, Fizames C, Samson D, Drouot N, Vignal A. Millassaeu P, Marc S, Hazan J, Seboun E et al.: A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 1996, 380:152-154.
16. Lander E, Kruglyak L: Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 1995, 11:241-247. Genome-wide scans involve multiple hypothesis testing and therefore the potential for false-positive results. Statistical thresholds for suggestive, probable and confirmed linkage are proposed in this paper, to be used in linkage analyses involving experimental animal crosses and multiplex human families.
17. Drake CG, Babcock SK, Palmer E, Kotzin BL: Genetic analysis of the NZB contribution to lupus-like autoimmune disease in (NZB x NZW)F1 mice. Proc Natl Acad Sci USA 1994, 91:4002-4066.
18. Morel L, Rudofsky UH, Longmate JA, Schiffenbauer J, Wakeland EK: Polygenic control of susceptibility to murine systemic lupus erytnematosus. Immunity 1994, 1:219-229.
19. Kono DH, Burlingame RW, Owens DG, Kuramochi A, Balderas RS, Balomenos D. Theofilopoulos AN: Lupus susceptibility loci in New Zealand mice. Proc Nat! Acad Sci USA 1994, 91:10168-10172.
20. Drake CG, Rozzo SJ, Hirschfeld HF, Smarnworawong NP, Palmer E, Kotzin BL: Analysis of the New Zealand Black contribution to lupus-like renal disease. Multiple genes that operate in a threshold manner. J Immunol 1995, 154:2441-2447.
21. Vyse TJ, Morel L, Tanner FJ, Wakeland EK, Kotzin BL: Backcross analysis of genes linked to autoantibody production in New Zealand white mice. J Immunol 1996, 157:2719-2727 NZW mice contribute to IgG autoantibody production and nephritis in (NZB x NZW)F1 mice. The phenotype of the NZW strain is predominantly increased production of IgG autoantibodies to single-stranded DNA. This study mapped loci linked to this trait in (NZW x BALB/c)F1 x NZW backcross mice.
22. Vyse TJ, Drake CG, Rozzo SJ, Roper E, Izui S, Katzin BL: Genetic linkage of IgG autoantibody production in relation to lupus nephritis in New Zealand hybrid mice. J Clin Invest 1996, 98:1762-1772. A linkage analysis of (NZB x NZW)F1 x NZW backcross mice was used to provide insight into whether different autoantibodies are subject to separate genetic influences and to infer which autoantibodies are most important in the development of lupus-like nephritis in this model. Loci linked with antibodies to gp70, compared to antinuclear antibodies, demonstrated the strongest linakge with renal disease, Interestingly, a locus on distal chromosome 4 (Nba1, see Fig, 1) was linked with nephritis but not with any of the autoantibodies measured, suggesting that it contributes to renal disease at a checkpoint distal to autoantibody production.
23. Todd JA: Genetic analysis of type I diabetes using whole genome approaches. Proc Natl Acad Sci USA 1995, 92:8560-9565.
24. Rozzo SJ, Vyse TJ, Drake CG, Kotzin BL: Effect of genetic background on the contribution of New Zealand black loci to autoimmune lupus nephritis. Proc Natl Acad Sci USA 1996, in press A linkage analysis of NZB genes that contribute to lupus-like nephritis in two different backcrosses that involve two different nonautoimmune strains. This study confirmed the linkage of a distal chromosome 1 locus (Nba2), and this was the only NZB locus that spanned both crosses and showed linkage when all mice were considered. Other disease linked loci were apparent, but only in one or the other backcross. These results indicate that disease-susceptibility loci, including MHC, may vary markedly depending on the nonautoimmune background genes present These studies provide insight into variables that affect genetic heterogeneity and add an important dimension of complexity for linkage analyses of human SLE.
25. Knight JG, Adams DD: Three genes for lupus nephritis in NZB x NZW mice. J Exp Med 197B, 147:1653-1660.
26. Morel L, Yu Y. Blenman KR, Caldwetl RA, Wakeland EK: Production of congenic mouse strains carrying genomic intervals containing SLE-susceptibility genes derived from the SLE-prone NZM/Aeg2410 strain. Mamm Genome 1996, 7:335-339 This is the first report of mice congenic for NZM (NZB or NZW) intervals, on a C57BL/6 background, that contain disease-susceptibility genes in the New Zealand hybrid model of SLE. Loci on chromosomes 1 (S/e1) and chromosome 7 (S/e3), depicted in Figure 1, appeared to be contained in NZW intervals.
27. Koch-Nolte F. Klein J, Hollmann C, Kuhl M, Haag F, Gaskins HR, Leiter E, Thiele HG: Defects in the structure and expression of the genes for the T cell marker Rt6 in NZW and (NZB x NZW)F1 mice. Int Immunot 1995, 7:883-890
28. Watson ML, Rao JK, Gilkeson GS, Ruiz P. Eicher EM, Pisetsky DS, Maisuzawa A, Rochelle JM, Seldin MF: Genetic analysis of MRL-fcr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. J Exp Med 1992, 176:1645-1656,
29. Wu J-M, Longmate JA, Adamus G, Margrave PA, ' Jakeland EK: Interval mapping of quantitative trait loci controlling humoral immunity to exogenous antigens: evidence that non-MHC Ir genes may influence susceptibility to autoimmunity. J Immunol 1996, 157:2498-2505.
30. Kotzin BL, Palmer E: The contribution of NZW genes to lupus-like disease in (NZB x NZW)F1 mice. J Exp Med 1987, 165:1237-1251.
31. Maruyama N, Furukawa F, Nakai Y, Sasaki Y, Ohla K, Ozaki S, Hirose S, Shirai T: Genetic studies of autoimmunity in New Zealand mice. IV. Contribution of NZB and NZW genes to the spontaneous occurrence of retroviral gp70 immune complexes in (NZB x NZW)F1 hybrid and the correlation to renal disease. J Immunol 1983, 130:740-746.
32. Hirose S, Ueda G. Noguchi K, Okada T, Sekigawa I, Sato H, Shirai T: Requirement of H-2 heterozygoslty for autoimmunity in (NZB x NZW)F1 hybrid mice. Eur J Immunol 1986, 16:1631-1633.
33. Chiang BL, Bearer E, Ansari A, Dorshkind K, Gershwin ME: The BM12 mutation and autoantibodies to dsDNA in NZB. H-2bm12 mice. J Immunol 1990, 145:94-101.
34. 1 mice detected by T cell clones. J Immunol 1993, 150:4777-4737.
35. Todd JA, Farrall M: Panning for gold: genome-wide scanning in type 1 diabetes. Hum Mol Genet 1996, 5:1443-1448. A review of the Icci that have been mapped in linkage analyses, transmission testing and association studies of human type I diabetes mellitus, The non-MHC loci mapped thus far are the VNTR at the 5 end of the insulin (INS) gene (IDDM2), and a polymorphism within the first exon ol the CTLA4 gene (IDDMT2). No genome-wide linkage studies have yet been published in human SLE.
36. Bell JI, Lathrop M: Multiple loci for multiple sclerosis. Nat Genet 1996, 13:377-378. This is a news and views that calls attention to four linkage analyses in multiple sclerosis, in the same issue. It is of interest that a locus mapped in human multiple sclerosis colocalized with the syntenic region of a locus mapped in the murine model of multiple sclerosis, experimental autoimmune encephalomyelitis.
37. Tsao BP, Cantor RM, Kalunian KC, Chen S-L, Shen N, Song YW, Isenberg DA, Yu C-L, Hahn BH, Rotter Jl: Evidence for linkage of a candidate chromosome 1 region to human systemic lupus erythematosus (SLE). J Clin Invest 1997, in press. This is the First report of a linkage analysis in human SLE using affected sibling pairs. Genetic mapping was directed to a region on human chromosome 1 that was believed to correspond to the syntenic interval on murine chromosome 1 that contained a NZB/NZW susceptibility locus (Sle1/Nba2/Lbw7). Despite a relatively small number of affected sibling pairs and considerable racial diversity in the population analyzed, results showed suggestive linkage for markers at 1q41-1q42. Confirmation fo these findings in a separate data set will be required.
38. Walpart MJ, Lachmann PJ: Complement deficiencies and abnormalities of the complement system in systemic lupus erythematosus and related disorders. Curr Opin Rheumatol 1990, 2:661-663
39. Bowness P, Davies KA, Norsworthy PJ, Athanassiou P, Taylor-Wiedeman J, Borysiewicz LK, Meyer PAR. Walport MJ: Hereditary C1q deficiency and systemic lupus erythematosus. Quart J Med 1994, 87:455-464.
40. Kölble K, Reid KBM: Genetic deficiencies of the complement system and association with disease - early components. Int Rev Immunol 1993, 10:1-17.
41. Hauptmann G, Tappeiner G, Schifferli JA: Inherited deficiency of the fourth component of human complement Immurtodet Rev 1988, 1:3-22.
42. Hulelt MD, Hogarth PM: Molecular basis of Fc receptor function. Adv Immunol 1994, 57:1-127.
43. Salmon JE, Millard S, Schachter LA, Arnett FC. Gmzler EM, Gourley MF, Ramsey-Goldman R, Peterson MGE, Kimberley RP: FcγRIIA alleles are heritable risk factors for lupus nephritis in African Americans. J Clin Invest 1996, 97:1348-1354. An association analysis of a particular FCGR2A allele in patients with SLE. The allele, H131, has important functional properties in terms of efficient clearance of immune complexes containing human IgG2. African-American patients with SLE (especially those with lu'jus nephritis) were found to have a significantly skewed distribution of FCCR2A alleles compared to controls. This finding has been confirmed in a separate data set [42].
44. Duits AJ, Bootsma H, Derksen RHWM, Sprcnk PE, Kater L, Kallanberg CGM, Capel PJA, Westerdall NAG, Spierenberg GTh, Gmelig-Meyling FHJ, Van der Winkel JGJ: Skewed distribution of Fc receptor Ma (CD32) polymorphism is associated with renal disease in systemic lupus erythematosus patients. Arthritis Rheum 1996, 39:1832-1836. A skewed distribution of the same FCGR2A alleles (as tested in [41]) in a separate group of patients with lupus nephritis.
45. Botta M, Theodoridis E, Thompson EM, Beynon HL, Briggs D, Isenberg DA, Walport MJ, Davies KA: FcERIIα polymorphism in systemic lupus erythematosus (SLE): no association with disease. Clin Exp Immunol 1996, 104:264-268.
46. Nagata S, Golstein P: The Fas death factor. Science 1995, 267:1449-1456.
47. Goodnow CC, Cyster JC, Hartley SB, Bell SE, Cooke MR Healy JL, Akkaraju S, Rathmell JC. Pogue SL, Shokat KP: Self-tolerance checkpoints in B lymphocyte development Adv Immunol 1995, 59:279-368.
48. + T cells. Nature 1995, 376:181-184.
49. Rothstein TL, Julia JMW, Panka DJ, Foote LC, Wang Z, Stanger B, Cui H, Ju S-T, Marshak-Rothstein A: Protection against Fasdependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature 1995, 374:163-165.
50. Fisher GH, Rosenberg FJ, Straus SE, Dale JK, Middleton LA, Lin AY, Strober W, Lenardo MJ. Puck JM: Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell 1995, 81:935-946.
51. Rieux-Laucat F, Le Deist F, Hivroz C, Roberts IAG, Debatin KM, Fischer A, De Villarty JP: Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995, 268:1347-1349.
52. Cheng J, Zhou T, Liu C, Shapiro JP, Brauer MJ, Kiefer MC, Barr PJ, Mountz JD: Protection from Fas-mediated apoptosis by a soluble farm of the Fas molecule. Science 1 994, 263:1759-1762.
53. Knipping E, Krammer PH, Onel KB, Lehman TJA, Myster E, Elkon KB: Levels of soluble Fas/APO-1/CD95 in systemic lupus erythematosus and juvenile rheumatoid arthritis. Arthritis Rheum 1998, 38:1735-1737.
54. Goel N, Ulrich DT, St. Clair W, Fleming JA, Lynch DH, Seldin MF: Lack of correlation between serum soluble Fas/APO-1 levels and autoimmune disease. Arthritis Rheum 1995, 38:1738-1742.
55. Cory S: Regulation of lymphocyte survival by the bel-2 gene family. Annu Rev Immunol 1995, 13:513-543.
56. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S. Harris AW: Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 1991, 88:8651-8665.
57. Lee M-S, Mueller R, Wicker LS, Peterson LB, Sarvetnick N; IL-10 is necessary and sufficient for autoimmune diabetes in conjunction with NOD MHC homozygosity. J Exp Med 1996, 163:2663-2668.
58. Levy Y, Brouet J-C: Interleukin-10 prevents the spontaneous death of germinal center B cells by induction of the bcl-2 protein. J Clin Invest 1 994, 93:424-428.
59. Smith CA, Farrah T, Goodwin RG: The TNF receptor superfamity of cellular and viral proteins: activation, costimulation, and death. Cell 1994, 76:959-962.
60. Tartaglia LA, Ayres TM, Wong GHW, Goeddel DV: A novel domain within the 55 kd TNF receptor signals cell death. Cell 1993,74:845-853.
61. Zheng L, Fisher G, Miller RE, Peschon J, Lynch DH, Lenardo MJ: Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 1995, 377:348-351.
62. Sytwu H-K, Liblau RS, McDevitt HO: The roles of Fas/APO-1 (CD95) and TNF in antigen-induced programmed cell death in T cell receptor transgenic mice. Immunity 1996, 5:17-30.
63. Zhou T, Edwards III CK, Yang P, Wang T, Bleuthmann H, Mourttz JD: Greatly accelerated lymphadenopathy and autoimmune disease in Ipr mice lacking tumor necrosis factor receptor I. J Immunol 1996, 156:2661-2665.
64. Zhang L, Eddy A, Teng Y-T, Fritzler M, Kluppel M, Melet F, Bernstein A: An immunolgical renal disease in transgenic mice that overexpress FUI, a member of the efs family of transcription factors. Mol Cell Biol 1995, 15:6961-6970.
65. Hibbs ML, Tarlinton DM, Armes J, Grail D, Hodgson G, Maglitto R, Stacker SA, Dunn AR: Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995, 83:301-311. See annotation [66].
66. 166*], are of lupus-like autoimmunity in lyn knockout mice. The mechanism almost certainly involves alterations in B cell receptor signaling.
67. Tsui HW, Siminowtch KA, De Souza L, Tsui FWl: Motheaten and viable motheaten mice have a mutation in the haematopoietic cell phosphatase gene. War Genet 1993, 4:124-129.
68. Scrtultz LD, Schweitzer PA, Rajan TV, Yi T, Ihle JN, Matthews RJ, Thomas ML, Beir DR: Mutations at the murine motheaten locus are within the hematopoietic cell protein tyrosine phosphatase (Hcph) gene, Cell 1993, 73:1445-1454.
69. Kozlowski M, Mlinaric-Rascan I, Feng G-S, Shen R, Pawson T, Siminovitch KA: Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely inpaired in motheaten and viable motheaten mice. J Exp Med 1993, 178:2157-2163.
70. Lankester AC, Van Schijndel GM, Van Lier RA: Haematopoietic cell phosphatease is recruited to CD22 following B cell antigen receptor ligation. J Biol Chem 1995, 270:20305-20308
71. D'Ambrosio D, Hippen KL, Minskoff SA, Mellman I, Pani G, Siminovitch KA, Cambier JC: Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by FcγHIIβ1. Science 1995, 268:293-297.
72. Cyster JG, Goodnow CC: Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 1995, 2:13-24.
73. Yu CCK, Tsui H-W, Ngar BY, Shulman MJ, Wu GE, Tsui FWL: B and T cells are not required for the viable motheaten phenotype. J Exp Med 1996, 163:371-330.
74. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold R, Yin M, Allen R, Sidman C, Proetzel G, Calvin N et al.: Targeted disruption of the mouse TGF-β1 gene results in multifocal inflammatory bowel disease. Nature 1992, 359:393-699.
75. Kulkarni AB, Huh C-G, Decker D, Geiser A, Lyght M, Flander KC, Roberts AB, Sporn MB, Ward JM, Karlsson S: Transforming growth factor-β1 null mutation in mice causes excessive inflammatory response and early death. Pros Natl Acad Sci USA 1993, 90:770-774.
76. Dang H, Geiser AG, Lelterio JJ, Nakabayashi T, Kong L, Fernandes G, Talal N: SLE-like autoantibodies and Sjögren's syndrome-like lymphoproliferation in TGF-β knockout mice. J Immunol 1995, 155:3205-3212.
77. Sanderson N, Factor V, Nagy P, Kopp J, Kondaiah P, Wakefield L, Roberts AB, Sporn MB, Thorgeirsson SS: Hepatic expression of mature transforming growth factor β1 in transgenic mice results in multiple tissue lesions. Proc Natl Acad Sci USA 1995, 92:2572-2576.
78. Horak I, Lohler J, Ma A, Smith KA: lnterleukin-2 deficient mice: a new model to study autoimmunity and self-tolerance. Immunol Rev 1995, 146:35-44,
79. Suzuki H, Kündig TM, Furlonger C, Wakeriam A, Timms E, Matsuyama T, Schmits R, Simard JJL, Ohashi PS, Griesser H et al.: Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor β. Science 1995, 268:1472-1476.