Mapping Lupus Susceptibility Genes in the NZM2410 Mouse Model

Advances in Immunology

Volumn 115, Issue , 2012, Pages 113-139

  Morel, Laurence ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Human immune system; Lupus; Mouse; NZM2410

Indexed keywords

ARTICLE; AUTOIMMUNITY; CONGENIC STRAIN; DISEASE MODEL; GENE; GENE CONSTRUCT; GENE MAPPING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CROSS; GENETIC RISK; GENETIC SUSCEPTIBILITY; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE STRAIN; NONHUMAN; NZM2410 MOUSE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SLE1 GENE; SLE2 GENE; SLE3 GENE; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 84861146526     PISSN: 00652776     EISSN: 15578445     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394299-9.00004-7     Document Type: Chapter

References (135)

1. Babcock S.K., Appel V.B., Schiff M., Palmer E., Kotzin B.L. Genetic analysis of the imperfect association of H-2 haplotype with lupus-like autoimmune disease. Proc. Natl. Acad. Sci. USA 1989, 86:7552-7555.
2. Blenman K.R.M., Bahjat F.R., Moldawer L.L., Morel L. Aberrant signaling in the TNF[alpha]/TNF receptor 1 pathway of the NZM2410 lupus-prone mouse. Clin. Immunol. 2004, 110:124-133.
3. Boackle S.A., Holers V.M., Chen X.J., Szakonyi G., Karp D.R., Wakeland E.K., Morel L. Cr2, a candidate gene in the murine Sle1c lupus susceptibility locus, encodes a dysfunctional protein. Immunity 2001, 15:775-785.
4. Brown D.R., Calpe S., Keszei M., Wang N., McArdel S., Terhorst C., Sharpe A.H. Cutting edge: An NK cell-independent role for Slamf4 in controlling humoral autoimmunity. J. Immunol. 2011, 187:21-25.
5. Bygrave A.E., Rose K.L., Cortes-Hernandez J., Warren J., Rigby R.J., Cook H.T., Walport M.J., Vyse T.J., Botto M. Spontaneous autoimmunity in 129 and C57BL/6 mice-Implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2004, 2:1081-1090.
6. Carlucci F., Cortes-Hernandez J., Fossati-Jimack L., Bygrave A.E., Walport M.J., Vyse T.J., Cook H.T., Botto M. Genetic dissection of spontaneous autoimmunity driven by 129-derived chromosome 1 loci when expressed on C57BL/6 mice. J. Immunol. 2007, 178:2352-2360.
7. Cha S., Nagashima H., Brown V.B., Peck A.B., Humphreys-Beher M.G. Two NOD Idd-associated intervals contribute synergistically to the development of autoimmune exocrinopathy (Sjogren's syndrome) on a healthy murine background. Arthritis Rheum. 2002, 46:1390-1398.
8. Chen Y., Cuda C., Morel L. Genetic determination of T cell help in loss of tolerance to nuclear antigens. J. Immunol. 2005, 174:7692-7702.
9. Chen Y., Perry D., Boackle S.A., Sobel E.S., Molina H., Croker B.P., Morel L. Several genes contribute to the production of autoreactive B and T cells in the murine lupus susceptibility locus Sle1c. J. Immunol. 2005, 175:1080-1089.
10. Cuda C.M., Wan S., Sobel E.S., Croker B.P., Morel L. Murine lupus susceptibility locus Sle1a controls regulatory T cell number and function through multiple mechanisms. J. Immunol. 2007, 179:7439-7447.
11. Cuda C.M., Zeumer L., Sobel E.S., Croker B.P., Morel L. Murine lupus susceptibility locus Sle1a requires the expression of two sub-loci to induce inflammatory T cells. Genes Immun. 2010, 11:542-553.
12. Cuda C.M., Li S., Chen Y., Potula H.S.K., Xu Z., Butfiloski E.J., Chang L.J., Baker H.V., Dozmorov I., Sobel E.S., Morel L. Pre-B cell leukemia homeobox protein is associated with lupus susceptibility in mice and humans. J. Immunol. 2012, 188:604-614.
13. Detre C., Keszei M., Romero X., Tsokos G.C., Terhorst C. SLAM family receptors and the SLAM-associated protein (SAP) modulate T cell functions. Semin. Immunopathol. 2010, 32:157-171.
14. Douglas K.B., Windels D.C., Zhao J., Gadeliya A.V., Wu H., Kaufman K.M., Harley J.B., Merrill J., Kimberly R.P., Alarcon G.S., et al. Complement receptor 2 polymorphisms associated with systemic lupus erythematosus modulate alternative splicing. Genes Immun. 2009, 10:457-469.
15. Drake C.G., Babcock S.K., Palmer E., Kotzin B.L. Genetic analysis of the Nzb contribution to lupus-like autoimmune-disease in (Nzb X Nzw)F-1 mice. Proc. Natl. Acad. Sci. USA 1994, 91:4062-4066.
16. Drake C.G., Rozzo S.J., Hirschfeld H.F., Smarnworawong N.P., Palmer E., Kotzin B.L. 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.
17. Duan B., Morel L. Role of B-1a cells in autoimmunity. Autoimmun. Rev. 2006, 5:403-408.
18. Duan B., Croker B.P., Morel L. Lupus resistance is associated with marginal zone abnormalities in an NZM murine model. Lab. Invest. 2007, 87:14-28.
19. hi B cells is associated with autoimmune pathology in a mouse model of lupus. Lab. Invest. 2008, 88:1008-1019.
20. Elkon K.B., Stone V.V. Type I interferon and systemic lupus erythematosus. J. Interferon Cytokine Res. 2011, 31:803-812.
21. Enghard P., Humrich J.Y., Chu V.T., Grussie E., Hiepe F., Burmester G.R., Radbruch A., Berek C., Riemekasten G. Class switching and consecutive loss of dsDNA reactive B1a B cells from the peritoneal cavity during murine lupus development. Eur. J. Immunol. 2010, 40:1809-1818.
22. Erickson L.D., Lin L.L., Duan B., Morel L., Noelle R.J. A genetic lesion that arrests plasma cell homing to the bone marrow. Proc. Natl. Acad. Sci. USA 2003, 100:12905-12910.
23. Fraser H.I., Dendrou C.A., Healy B., Rainbow D.B., Howlett S., Smink L.J., Gregory S., Steward C.A., Todd J.A., Peterson L.B., et al. Nonobese diabetic congenic strain analysis of autoimmune diabetes reveals genetic complexity of the Idd18 locus and identifies Vav3 as a candidate gene. J. Immunol. 2010, 184:5075-5084.
24. Fujimura T., Hirose S., Jiang Y., Kodera S., Ohmuro H., Zhang D., Hamano Y., Ishida H., Furukawa S., Shirai T. Dissection of the effects of tumor necrosis factor-alpha and class II gene polymorphisms within the MHC on murine systemic lupus erythematosus (SLE). Int. Immunol. 1998, 10:1467-1472.
25. Garcia-Romo G.S., Caielli S., Vega B., Connolly J., Allantaz F., Xu Z., Punaro M., Baisch J., Guiducci C., Coffman R.L., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 2011, 3:73ra20.
26. Giguere V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev. 2008, 29:677-696.
27. Giles B.M., Tchepeleva S.N., Kachinski J.J., Ruff K., Croker B.P., Morel L., Boackle S.A. Augmentation of NZB autoimmune phenotypes by the Sle1c murine lupus susceptibility interval. J. Immunol. 2007, 178:4667-4675.
28. Graham D.S.C., Vyse T.J., Fortin P.R., Montpetit A., Cai Y., Lim S., McKenzie T., Farwell L., Rhodes B., Chad L., et al. Association of LY9 in UK and Canadian SLE families. Genes Immun. 2008, 9:93-102.
29. Haraldsson M.K., Louis-Dit-Sully C.A., Lawson B.R., Sternik G., Santiago-Raber M.L., Gascoigne N.R., Theofilopoulos A.N., Kono D.H. The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity 2008, 28:40-51.
30. Harley I.T., Kaufman K.M., Langefeld C.D., Harley J.B., Kelly J.A. Genetic susceptibility to SLE: New insights from fine mapping and genome-wide association studies. Nat. Rev. Genet. 2009, 10:285-290.
31. Haywood M.E.K., Rogers N.J., Rose S.J., Boyle J., McDermott A., Rankin J.M., Thiruudaian V., Lewis M.R., Fossati-Jimack L., Izui S., et al. Dissection of BXSB lupus phenotype using mice congenic for chromosome 1 demonstrates that separate intervals direct different aspects of disease. J. Immunol. 2004, 173:4277-4285.
32. Hudson C.A., Cao L., Kasten-Jolly J., Kirkwood J.N., Lawrence D.A. Susceptibility of lupus-prone NZM mouse strains to lead exacerbation of systemic lupus erythematosus symptoms. J. Toxicol. Environ. Health A 2003, 66:895-918.
33. Hudson C.A., Mondal T.K., Cao L., Kasten-Jolly J., Huber V.C., Lawrence D.A. The dietary supplement ephedrine induces beta-adrenergic mediated exacerbation of systemic lupus erythematosus in NZM391 mice. Lupus 2005, 14:293-307.
34. Ichii O., Konno A., Sasaki N., Endoh D., Hashimoto Y., Kon Y. Autoimmune glomerulonephritis induced in congenic mouse strain carrying telomeric region of chromosome 1 derived from MRL/MpJ. Histol. Histopathol. 2008, 23:411-422.
35. Jacob C.O., Mcdevitt H.O. Tumor necrosis factor-alpha in murine autoimmune lupus nephritis. Nature 1988, 331:356-358.
36. Jacob C.O., Fronek Z., Lewis G.D., Koo M., Hansen J.A., Mcdevitt H.O. Heritable major histocompatibility complex class-II-associated differences in production of tumor necrosis factor-alpha-Relevance to genetic predisposition to systemic lupus-erythematosus. Proc. Natl. Acad. Sci. USA 1990, 87:1233-1237.
37. Jacob C.O., Hwang F., Lewis G.D., Stall A.M. Tumor-necrosis-factor-alpha in murine systemic lupus-erythematosus disease-models-Implications for genetic predisposition and immune regulation. Cytokine 1991, 3:551-561.
38. Jacob C.O., Zang S., Li L., Ciobanu V., Quismorio F., Mizutani A., Satoh M., Koss M. Pivotal role of Stat4 and Stat6 in the pathogenesis of the lupus-like disease in the New Zealand mixed 2328 mice. J. Immunol. 2003, 171:1564-1571.
39. Jacob C.O., Pricop L., Putterman C., Koss M.N., Liu Y., Kollaros M., Bixler S.A., Ambrose C.M., Scott M.L., Stohl W. Paucity of clinical disease despite serological autoimmunity and kidney pathology in lupus-prone New Zealand mixed 2328 mice deficient in BAFF. J. Immunol. 2006, 177:2671-2680.
40. Jacob N., Guo S., Mathian A., Koss M.N., Gindea S., Putterman C., Jacob C.O., Stohl W. B Cell and BAFF dependence of IFN-alpha-exaggerated disease in systemic lupus erythematosus-prone NZM 2328 mice. J. Immunol. 2011, 186:4984-4993.
41. Jongeneel C.V., Acha-Orbea H., Blankenstein T. A polymorphic microsatellite in the tumor necrosis factor alpha promoter identifies an allele unique to the NZW mouse strain. J. Exp. Med. 1990, 171:2141-2146.
42. Kanta H., Mohan C. Three checkpoints in lupus development: Central tolerance in adaptive immunity, peripheral amplification by innate immunity and end-organ inflammation. Genes Immun. 2009, 10:390-396.
43. Keszei M., Detre C., Rietdijk S.T., Munoz P., Romero X., Berger S.B., Calpe S., Liao G., Castro W., Julien A., et al. A novel isoform of the Ly108 gene ameliorates murine lupus. J. Exp. Med. 2011, 208:811-822.
44. Keszei M., Latchman Y.E., Vanguri V.K., Brown D.R., Detre C., Morra M., Arancibia C.V., Paul E., Calpe S., Castro W., et al. Auto-antibody production and glomerulonephritis in congenic Slamf1-/- and Slamf2-/- [B6.129] but not in Slamf1-/- and Slamf2-/- [BALB/c.129] mice. Int. Immunol. 2011, 23:149-158.
45. Kong P.L., Morel L., Croker B.P., Craft J. The centromeric region of chromosome 7 from MRL mice (Lmb3) is an epistatic modifier of Fas for autoimmune disease expression. J. Immunol. 2004, 172:2785-2794.
46. Kono D.H., Burlingame R.W., Owens D.G., Kuramochi A., Balderas R.S., Balomenos D., Theofilopoulos A.N. Lupus susceptibility loci in New Zealand mice. Proc. Natl. Acad. Sci. USA 1994, 91:10168-10172.
47. Kotzin B.L., Palmer E. The contribution of NZW genes to lupus-like disease in (NZB X NZW)F1 mice. J. Exp. Med. 1987, 165:1237-1251.
48. Kumar K.R., Li L.N., Yan M., Bhaskarabhatla M., Mobley A.B., Nguyen C., Mooney J.M., Schatzle J.D., Wakeland E.K., Mohan C. Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science 2006, 312:1665-1669.
49. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., Meller S., Chamilos G., Sebasigari R., Riccieri V., et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 2011, 3:73ra19.
50. Li J., Liu Y., Xie C., Zhu J., Kreska D., Morel L., Mohan C. Deficiency of type I interferon contributes to Sle2-associated component lupus phenotypes. Arthritis Rheum. 2005, 52:3063-3072.
51. Li Q.Z., Zhou J., Yang R., Yan M., Ye Q., Liu K., Liu S., Shao X., Li L., Zhou X.J., et al. The lupus-susceptibility gene kallikrein downmodulates antibody-mediated glomerulonephritis. Genes Immun. 2009, 10:503-508.
52. Liu K., Li Q.Z., Yu Y., Liang C., Subramanian S., Zeng Z., Wang H.W., Xie C., Zhou X.J., Mohan C., et al. Sle3 and Sle5 can independently couple with Sle1 to mediate severe lupus nephritis. Genes Immun. 2007, 8:634-645.
53. Liu Y., Li L., Kumar K.R., Xie C., Lightfoot S., Zhou X.J., Kearney J.F., Weigert M., Mohan C. Lupus susceptibility genes may breach tolerance to DNA by impairing receptor editing of nuclear antigen-reactive B cells. J. Immunol. 2007, 179:1340-1352.
54. Liu K., Li Q.Z., Delgado-Vega A.M., Abelson A.K., Sanchez E., Kelly J.A., Li L., Liu Y., Zhou J., Yan M., 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.
55. Manolio T.A., Collins F.S., Cox N.J., Goldstein D.B., Hindorff L.A., Hunter D.J., McCarthy M.I., Ramos E.M., Cardon L.R., Chakravarti A., et al. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753.
56. Mehrad B., Park S.J., Akangire G., Standiford T.J., Wu T., Zhu J., Mohan C. The lupus-susceptibility locus, Sle3, mediates enhanced resistance to bacterial infections. J. Immunol. 2006, 176:3233-3239.
57. Michalek R.D., Gerriets V.A., Jacobs S.R., Macintyre A.N., MacIver N.J., Mason E.F., Sullivan S.A., Nichols A.G., Rathmell J.C. Cutting edge: Distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 2011, 186:3299-3303.
58. Mohan, C., Morel L., Yang P., Wakeland E.K. Genetic dissection of systemic lupus erythematosus -Sle2 on murine chromosome 2 leads to B cell hyperactivity. J. Immunol. 1997, 159:454-465.
59. Mohan C., Alas E., Morel L., Yang P., Wakeland E.K. Genetic dissection of SLE pathogenesis-Sle1 on murine chromosome 1 leads to a selective loss of tolerance to H2A/H2B/DNA subnucleosomes. J. Clin. Invest. 1998, 101:1362-1372.
60. Mohan C., Morel L., Yang P., Wakeland E.K. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum. 1998, 41:1652-1662.
61. Mohan C., Morel L., Yang P., Watanabe H., Croker B., Gilkeson G., Wakeland E.K. Genetic dissection of lupus pathogenesis: A recipe for nephrophilic autoantibodies. J. Clin. Invest. 1999, 103:1685-1695.
62. Mohan C., Yu Y., Morel L., Yang P., Wakeland E.K. Genetic dissection of Sle pathogenesis: Sle3 on murine chromosome 7 impacts T cell activation, differentiation, and cell death. J. Immunol. 1999, 162:6492-6502.
63. Morahan G., Morel L. Genetics of autoimmune diseases in humans and in animal models. Curr. Opin. Immunol. 2002, 14:803-811.
64. Morel L. Genetics of SLE: Evidence from mouse models. Nat. Rev. Rheumatol. 2010, 6:348-357.
65. Morel L., Wakeland E.K. Susceptibility to lupus nephritis in the NZB/W model system. Curr. Opin. Immunol. 1998, 10:718-725.
66. Morel L., Rudofsky U.H., Longmate J.A., Schiffenbauer J., Wakeland E.K. Polygenic control of susceptibility to murine systemic lupus erythematosus. Immunity 1994, 1:219-229.
67. Morel L., Yu Y., Blenman K.R., Caldwell R.A., Wakeland E.K. Production of congenic mouse strains carrying genomic intervals containing SLE-susceptibility genes derived from the SLE-prone NZM2410 strain. Mamm. Genome 1996, 7:335-339.
68. Morel L., Mohan C., Yu Y., Croker B.P., Tian N., Deng A., Wakeland E.K. Functional dissection of systemic lupus erythematosus using congenic mouse strains. J. Immunol. 1997, 158:6019-6028.
69. Morel L., Mohan C., Yu Y., Schiffenbauer J., Rudofsky U.H., Tian N., Longmate J.A., Wakeland E.K. Multiplex inheritance of component phenotypes in a murine model of lupus. Mamm. Genome 1999, 10:176-181.
70. Morel L., Tian X.H., Croker B.P., Wakeland E.K. Epistatic modifiers of autoimmunity in a murine model of lupus nephritis. Immunity 1999, 11:131-139.
71. Morel L., Croker B.P., Blenman K.R., Mohan C., Huang G., Gilkeson G., Wakeland E.K. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc. Natl. Acad. Sci. USA 2000, 97:6670-6675.
72. Morel L., Blenman K.R., Croker B.P., Wakeland E.K. The major murine systemic lupus erythematosus susceptibility locus, Sle1, is a cluster of functionally related genes. Proc. Natl. Acad. Sci. USA 2001, 98:1787-1792.
73. Morris S.C., Cheek R.L., Cohen P.L., Eisenberg R.A. Autoantibodies in chronic graft versus host result from cognate T-B interactions. J. Exp. Med. 1990, 171:503-517.
74. Morris E.S., MacDonald K.P.A., Kuns R.D., Morris H.M., Banovic T., Don A.L.J., Rowe V., Wilson Y.A., Raffelt N.C., Engwerda C.R., et al. Induction of natural killer T cell-dependent alloreactivity by administration of granulocyte colony-stimulating factor after bone marrow transplantation. Nat. Med. 2009, 15:436-441.
75. Niu H., Sobel E.S., Morel L. Defective B-cell response to T-dependent immunization in lupus-prone mice. Eur. J. Immunol. 2008, 38:3028-3040.
76. Paisansinsup T., Vallejo A.N., Luthra H., David C.S. HLA-DR modulates autoantibody repertoire, but not mortality, in a humanized mouse model of systemic lupus erythematosus. J. Immunol. 2001, 167:4083-4090.
77. Pan L., Delmonte J.J., Jalonen C.K., Ferrara J.L. Pretreatment of donor mice with granulocyte colony-stimulating factor polarizes donor T lymphocytes toward type-2 cytokine production and reduces severity of experimental graft-versus-host disease. Blood 1995, 86:4422-4429.
78. Peeva E., Gonzalez J., Hicks R., Diamond B. Cutting edge: Lupus susceptibility interval Sle3/5 confers responsiveness to prolactin in C57BL/6 mice. J. Immunol. 2006, 177:1401-1405.
79. Perl A., Gergely P., Banki K. Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int. Rev. Immunol. 2004, 23:293-313.
80. Perry D.J., Yin Y., Telarico T., Baker H.V., Dozmorov I., Wakeland B., Wakeland E.K., Perl A., Morel L. Murine lupus susceptibility locus Sle1c2 mediates CD4+ T cell hyperactivation and maps to estrogen-related receptor gamma Esrrg. J. Immunol. 2012, (submitted).
81. Peters A.L., Stunz L.L., Meyerholz D.K., Mohan C., Bishop G.A. Latent membrane protein 1, the EBV-encoded oncogenic mimic of CD40, accelerates autoimmunity in B6.Sle1 mice. J. Immunol. 2010, 185:4053-4062.
82. Piatelli M.J., Tanguay D., Rothstein T.L., Chiles T.C. Cell cycle control mechanisms in B-1 and B-2 lymphoid subsets. Immunol. Res. 2003, 27:31-51.
83. Prodeus A.P., Goerg S., Shen L.M., Pozdnyakova O.O., Chu L., Alicot E.M., Goodnow C.C., Carroll M.C. A critical role for complement in maintenance of self-tolerance. Immunity 1998, 9:721-731.
84. Rahman Z.S.M., Niu H., Perry D., Wakeland E., Manser T., Morel L. Expression of the autoimmune Fcgr2b NZW allele fails to be upregulated in germinal center B cells and is associated with increased IgG production. Genes Immun. 2007, 8:604-612.
85. Ramanujam M., Wang X., Huang W., Liu Z., Schiffer L., Tao H., Frank D., Rice J., Diamond B., Yu K.O.A., et al. Similarities and differences between selective and nonselective BAFF blockade in murine SLE. J. Clin. Invest. 2006, 116:724-734.
86. Ramanujam M., Bethunaickan R., Huang W., Tao H., Madaio M.P., Davidson A. Selective blockade of BAFF for the prevention and treatment of systemic lupus erythematosus nephritis in NZM2410 mice. Arthritis Rheum. 2010, 62:1457-1468.
87. Rozzo S.J., Vyse T.J., David C.S., Palmer E., Izui S., Kotzin B.L. Analysis of MHC class II genes in the susceptibility to lupus in New Zealand mice. J. Immunol. 1999, 162:2623-2630.
88. Rudofsky U.H., Evans B.D., Balaban S.L., Mottironi V.D., Gabrielsen A.E. Differences in expression of lupus nephritis in New Zealand mixed H-2z homozygous inbred strains of mice derived from New Zealand black and New Zealand white mice. Origins and initial characterization. Lab. Invest. 1993, 68:419-426.
89. Rutella S., Zavala F., Danese S., Kared H., Leone G. Granulocyte colony-stimulating factor: A novel mediator of T cell tolerance. J. Immunol. 2005, 175:7085-7091.
90. Shi X.Y., Xie C., Kreska D., Richardson J.A., Mohan C. Genetic dissection of SLE: SLE1 and FAS impact alternate pathways leading to lymphoproliferative autoimmunity. J. Exp. Med. 2002, 196:281-292.
91. Shi L.Z., Wang R., Huang G., Vogel P., Neale G., Green D.R., Chi H. HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 2011, 208:1367-1376.
92. Singh R.R., Saxena V., Zang S., Li L., Finkelman F.D., Witte D.P., Jacob C.O. Differential contribution of IL-4 and STAT6 vs STAT4 to the development of lupus nephritis. J. Immunol. 2003, 170:4818-4825.
93. Sobel E.S., Mohan C., Morel L., Schiffenbauer J., Wakeland E.K. Genetic dissection of SLE pathogenesis: Adoptive transfer of Sle1 mediates the loss of tolerance by bone marrow-derived B cells. J. Immunol. 1999, 162:2415-2421.
94. Sobel E.S., Morel L., Baert R., Mohan C., Schiffenbauer J., Wakeland E.K. Genetic dissection of systemic lupus erythematosus pathogenesis: Evidence for functional expression of Sle3/5 by non-T cells. J. Immunol. 2002, 169:4025-4032.
95. Sobel E.S., Satoh M., Chen W.F., Wakeland E.K., Morel L. The major murine systemic lupus erythematosus susceptibility locus Sle1 results in abnormal functions of both B and T cells. J. Immunol. 2002, 169:2694-2700.
96. Sobel E.S., Brusko T.M., Butfiloski E.J., Hou W., Li S., Cuda C.M., Abid A.N., Reeves W.H., Morel L. Defective response of CD4+ T cells to retinoic acid and TGFbeta in systemic lupus erythematosus. Arthritis Res. Ther. 2011, 13:R106.
97. Stohl W., Xu D., Metzger T.E., Kim K.S., Morel L., Kotzin B.L. Dichotomous effects of complete versus partial class II major histocompatibility complex deficiency on circulating autoantibody levels in autoimmune-prone mice. Arthritis Rheum. 2004, 50:2227-2239.
98. Subramanian S., Yim Y.S., Liu K., Tus K., Zhou X.J., Wakeland E.K. Epistatic suppression of systemic lupus erythematosus: Fine mapping of Sles1 to less than 1 Mb. J. Immunol. 2005, 175:1062-1072.
99. Subramanian S., Tus K., Li Q.Z., Wang A., Tian X.H., Zhou J., Liang C., Bartov G., McDaniel L.D., Zhou X.J. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc. Natl. Acad. Sci. USA 2006, 103:9970-9975.
100. Suzuki A., Yamada R., Kochi Y., Sawada T., Okada Y., Matsuda K., Kamatani Y., Mori M., Shimane K., Hirabayashi Y., et al. Functional SNPs in CD244 increase the risk of rheumatoid arthritis in a Japanese population. Nat. Genet. 2008, 40:1224-1229.
101. Taylor K.E., Chung S.A., Graham R.R., Ortmann W.A., Lee A.T., Langefeld C.D., Jacob C.O., Kamboh M.I., Alarcón-Riquelme M.E., Tsao B.P., et al. Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet. 2011, 7:e1001311.
102. The Complex Trait Consortium The nature and identification of quantitative trait loci: A community's view. Nat. Rev. Genet. 2003, 4:911-916.
103. Theofilopoulos A.N., Dixon F.J. Murine models of systemic lupus erythematosus. Adv. Immunol. 1985, 37:269-379.
104. Tourigny M.R., Ursini-Siegel J., Lee H., Toellner K.M., Cunningham A.F., Franklin D.S., Ely S., Chen M.H., Qin X.F., Xiong Y., et al. CDK inhibitor p18(INK4c) is required for the generation of functional plasma cells. Immunity 2002, 17:179-189.
105. Tsao B.P. Update on human systemic lupus erythematosus genetics. Curr. Opin. Rheumatol. 2004, 16:513-521.
106. Vidal S., Kono D.H., Theofilopoulos A.N. Loci predisposing to autoimmunity in MRL-Fas(lpr) and C57BL/6-Fas(lpr) mice. J. Clin. Invest. 1998, 101:696-702.
107. Vuyyuru R., Mohan C., Manser T., Rahman Z.S.M. The lupus susceptibility locus Sle1 breaches peripheral B cell tolerance at the antibody-forming cell and germinal center checkpoints. J. Immunol. 2009, 183:5716-5727.
108. Vyse T.J., Morel L., Tanner F.J., Wakeland E.K., Kotzin B.L. Backcross analysis of genes linked to autoantibody production in New Zealand white mice. J. Immunol. 1996, 157:2719-2727.
109. Vyse T.J., Rozzo S.J., Drake C.G., Appel V.B., Lemeur M., Izui S., Palmer E., Kotzin B.L. Contributions of Ea(z) and Eb(z) MHC genes to lupus susceptibility in New Zealand mice. J. Immunol. 1998, 160:2757-2766.
110. Wade N.S., Stevenson B.G., Dunlap D.S., Major A.S. The lupus susceptibility locus Sle3 is not sufficient to accelerate atherosclerosis in lupus-susceptible low density lipoprotein receptor-deficient mice. Lupus 2010, 19:34-42.
111. Wakeland E.K., Morel L., Mohan C., Yui M. Genetic dissection of lupus nephritis in murine models of SLE. J. Clin. Immunol. 1997, 17:272-281.
112. Wakeland E.K., Wandstrat A.E., Liu K., Morel L. Genetic dissection of systemic lupus erythematosus. Curr. Opin. Immunol. 1999, 11:701-707.
113. Wakeland E.K., Liu K., Graham R.R., Behrens T.W. Delineating the genetic basis of systemic lupus erythematosus. Immunity 2001, 15:397-408.
114. Wakui M., Kim J., Butfiloski E.J., Morel L., Sobel E.S. Genetic dissection of lupus pathogenesis: Sle3/5 impacts IgH CDR3 sequences, somatic mutations, and receptor editing. J. Immunol. 2004, 173:7368-7376.
115. Wakui M., Morel L., Butfiloski E.J., Kim C., Sobel E.S. Genetic dissection of systemic lupus erythematosus pathogenesis: Partial functional complementation between Sle1 and Sle3/5 demonstrates requirement for intracellular coexpression for full phenotypic expression of lupus. J. Immunol. 2005, 175:1337-1345.
116. Wan S., Xia C., Morel L. IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4+CD25+ T cell regulatory functions. J. Immunol. 2007, 178:271-279.
117. Wan S., Zhou Z., Duan B., Morel L. Dendritic cells from lupus prone mice directly interact with B cells to increase their effector functions. Arthritis Rheum. 2008, 58:1741-1750.
118. Wandstrat A.E., Nguyen C., Limaye N., Chan A.Y., Subramanian S., Tian X.H., Yim Y.S., Pertsemlidis A., Garner H.R., Morel L., et al. Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus. Immunity 2004, 21:769-780.
119. Waters S.T., Fu S.M., Gaskin F., Deshmukh U.S., Sung S.S.J., Kannapell C.C., Tung K.S.K., Mcewen S.B., McDuffie M. NZM2328: A new mouse model of systemic lupus erythematosus with unique genetic susceptibility loci. Clin. Immunol. 2001, 100:372-383.
120. Waters S.T., McDuffie M., Bagavant H., Deshmukh U.S., Gaskin F., Jiang C., Tung K.S.K., Fu S.M. Breaking tolerance to double stranded DNA, nucleosome, and other nuclear antigens is not required for the pathogenesis of lupus glomerulonephritis. J. Exp. Med. 2004, 199:255-264.
121. Watson M.L., Rao J.K., Gilkeson G.S., Ruiz P., Eicher E.M., Pisetsky D.S., Matsuzawa A., Rochelle J.M., Seldin M.F. Genetic analysis of Mrl-Lpr mice-Relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. J. Exp. Med. 1992, 176:1645-1656.
122. Wither J.E., Paterson A.D., Vukusic B. Genetic dissection of B cell traits in New Zealand black mice. The expanded population of B cells expressing up-regulated costimulatory molecules shows linkage to Nba2. Eur. J. Immunol. 2000, 30:356-365.
123. Wu H., Boackle S.A., Hanvivadhanakul P., Ulgiati D., Grossman J.M., Lee Y., Shen N., Abraham L.J., Mercer T.R., Park E., et al. Association of a common complement receptor 2 haplotype with increased risk of systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 2007, 104:3961-3966.
124. Xu Z., Butfiloski E.J., Sobel E.S., Morel L. Mechanisms of peritoneal B-1a cells accumulation induced by murine lupus susceptibility locus Sle2. J. Immunol. 2004, 173:6050-6058.
125. Xu Z., Duan B., Croker B.P., Wakeland E.K., Morel L. Genetic dissection of the murine lupus susceptibility locus Sle2: Contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J. Immunol. 2005, 175:936-943.
126. Xu Z., Duan B., Croker B.P., Morel L. STAT4 deficiency reduces autoantibody production and glomerulonephritis in a mouse model of lupus. Clin. Immunol. 2006, 120:189-198.
127. Xu Z., Potula H.H., Vallurupalli A., Perry D., Baker H., Croker B.P., Dozmorov I., Morel L. Cyclin-dependent kinase inhibitor Cdkn2c regulates B cell homeostasis and function in the NZM2410-derived murine lupus susceptibility locus Sle2c1. J. Immunol. 2011, 186:6673-6682.
128. Xu Z., Vallurupalli A., Fuhrman C., Ostrov D., Morel L. An NZB-derived locus suppresses chronic graft versus host disease and autoantibody production through non-lymphoid bone-marrow derived cells. J. Immunol. 2011, 186:4130-4139.
129. Xu Z., Cuda C.M., Croker B.P., Morel L. The NZM2410-derived lupus susceptibility locus Sle2c1 increases TH17 polarization and induces nephritis in Fas-deficient mice. Arthritis Rheum. 2011, 63:764-774.
130. Zavala F., Masson A., Hadaya K., Ezine S., Schneider E., Babin O., Bach J.F. Granulocyte-colony stimulating factor treatment of lupus autoimmune disease in MRL-lpr/lpr mice. J. Immunol. 1999, 163:5125-5132.
131. Zeumer L., Sang A., Niu H., Morel L. Murine lupus susceptibility locus Sle2 activates DNA-reactive B cells through two sub-loci with distinct phenotypes. Genes Immun. 2011, 12:199-207.
132. Zhong X., Gao W., Degauque N., Bai C., Lu Y., Kenny J., Oukka M., Strom T.B., Rothstein T.L. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur. J. Immunol. 2007, 9:2400-2404.
133. Zhou Z., Niu H., Zheng Y.Y., Morel L. Autoreactive marginal zone B cells enter the follicles and interact with CD4+ T cells in lupus-prone mice. BMC Immunol. 2011, 12:7.
134. Zhou X.J., Lu X.L., Nath S.K., Lv J.C., Zhu S.N., Yang H.Z., Qin L.X., Zhao M.H., Su Y., Shen N., Li Z.G., Zhang H., et al. Gene-gene interaction of BLK, TNFSF4, TRAF1, TNFAIP3, REL in systemic lupus erythematosus. Arthritis Rheum. 2012, 64:222-231. 10.1002/art.33318.
135. Zhu J.K., Liu X.B., Xie C., Yan M., Yu Y., Sobel E.S., Wakeland E.K., Mohan C. T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J. Clin. Invest. 2005, 115:1869-1878.