809
Views
11
CrossRef citations to date
0
Altmetric
Reviews

Contribution of mouse models in our understanding of lupus

, &
Pages 174-187 | Received 27 Dec 2019, Accepted 28 Feb 2020, Published online: 23 Mar 2020

References

  • Kotzin BL. Systemic lupus erythematosus. Cell. 1996;85(3):303–306. doi:10.1016/S0092-8674(00)81108-3.
  • Singh RR. SLE: translating lessons from model systems to human disease. Trends Immunol. 2005;26(11):572–579. doi:10.1016/j.it.2005.08.013.
  • Theofilopoulos A, Dixon F. Murine models of systemic lupus erythematosus. Adv Immunol. 1985;37:269–390. doi:10.1016/s0065-2776(08)60342-9.
  • Morel L. Genetics of SLE: evidence from mouse models. Nat Rev Rheumatol. 2010;6(6):348–357. doi:10.1038/nrrheum.2010.63.
  • Howie JB, Helyer BJ. The immunology and pathology of NZB mice. Adv Immunol. 1968; 9:215–266. doi:10.1016/s0065-2776(08)60444-7.
  • Bielschowsky M, Helyer BJ, Howie JB. Spontaneous haemolytic anemia in mice of the NZB/B1 strain. Proc Univ Otago Med Sch (NZ). 1959;37:9–11.
  • Yoshida S, Castles JJ, Gershwin ME. The pathogenesis of autoimmunity in New Zealand mice. Semin Arthritis Rheum1990. 1990;19(4):224–242. doi:10.1016/0049-0172(90)90002-W.
  • Helyer BJ, Howie JB. Renal disease associated with positive lupus erythematosus tests in an across-bred strain of mice. Nature. 1963;197(4863):197. doi:10.1038/197197a0.
  • Andrews BS, Eisenberg RA, Theofilopoulos AN, et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med. 1978;148(5):1198–1215. doi:10.1084/jem.148.5.1198.
  • Dixon FJ, Andrews BS, Eisenberg RA, et al. Etiology and pathogenesis of a spontaneous lupus-like syndrome in mice. Arthritis Rheum. 1978;21(S1):S64–S67. doi:10.1002/art.1780210909.
  • Virdis A, Tani C, Duranti E, et al. Early treatment with hydroxychloroquine prevents the development of endothelial dysfunction in a murine model of systemic lupus erythematosus. Arthritis Res Ther. 2015;17(1):277. doi:10.1186/s13075-015-0790-3.
  • Crampton SP, Morawski PA, Bolland S. Linking susceptibility genes and pathogenesis mechanisms using mouse models of systemic lupus erythematosus. Dis Model Mech. 2014;7(9):1033–1046. doi:10.1242/dmm.016451.
  • Murphy ED, Roths JB. A single gene for massive lymphoproliferation with immune complex disease in a new mouse strain MRL. In: Proceedings of the 16th International Congress in Hematology. Amsterdam: Excerpta Medica; 1976: 69–80.
  • Murphy ED. Lymphoproliferation (Lpr) and Other Single-Locus Models for Murine Lupus, In: Gershwin, M.E., and Merchant, B., eds. Immunologic Defects in Laboratory Animals. Vol. 1. New York: Plenum Press; 1981: 143–173.
  • Izui S, McConahey PJ, Dixon FJ. Increased spontaneous polyclonal activation of B lymphocytes in mice with spontaneous autoimmune disease. J. Immunol. 1978;121(6):2213–2219.
  • Adachi M, Watanabe-Fukunaga R, Nagata S. Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Proc. Natl. Acad. Sci. USA. 1993;90(5):1756–1760. doi:10.1073/pnas.90.5.1756.
  • Rodriguez-Rodriguez N, Apostolidis SA, Fitzgerald L, et al. Pro-inflammatory self-reactive T cells are found within murine TCR-ab(þ) CD4() CD8() PD-1(þ) cells. Eur J Immunol. 2016; 46:1383–1139. doi:10.1002/eji.201546056.
  • Crispı´N JC, Oukka M, Bayliss G, et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J Immunol. 2008; 181:8761–8766. doi:10.4049/jimmunol.181.12.8761.
  • Sakić B, Szechtman H, Denburg JA. Neurobehavioral alterations in autoimmune mice. Neurosci Biobehav Rev. 1997;21(3):327–340. doi:10.1016/s0149-7634(96)00018-8.
  • Eisenberg RA, Tan EM, Dixon FJ. Presence of anti-Sm reactivity in autoimmune mouse strains. J Exp Med. 1978;147(2):582–587. doi:10.1084/jem.147.2.582.
  • Alexander EL, Murphy ED, Roths JB, et al. Congenic autoimmune murine models of central nervous system disease in connective tissue disorders. Ann Neurol. 1983;14(2):242–248. doi:10.1002/ana.410140211.
  • Alexander EL, Mover C, Travlos GS, et al. Two histopathologic types of inflammatory vascular disease in MRL/Mp autoimmune mice. Model for human vasculitis in connective tissue disease. Arthritis Rheum. 1985;28(10):1146–1155. doi:10.1002/art.1780281011.
  • Kelley VE, Roths JB. Interaction of mutant lpr gene with background strain influences renal disease. Clin Immunol Immunopathol. 1985;37(2):220–229. doi:10.1016/0090-1229(85)90153-9.
  • Wu J, Wilson J, He J, Xiang L, Schur PH, Mountz JD. Fas ligand mutation in a patient with systemic lupus erythematosus and lymphoproliferative disease. J Clin Invest. 1996;98(5):1107–1113. doi:10.1172/JCI118892.
  • Christensen SR, Shupe J, Nickerson K, et al. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity. 2006;25(3):417–428. doi:10.1016/j.immuni.2006.07.013.
  • Teichmann LL, Schenten D, Medzhitov R, et al. Signals via the adaptor MyD88 in B cells and DCs make distinct and synergistic contributions to immune activation and tissue damage in lupus. Immunity. 2013;38(3):528–540. doi:10.1016/j.immuni.2012.11.017.
  • Ols ML, Cullen JL, Turqueti-Neves A, et al. Dendritic cells regulate extrafollicular autoreactive B cells via T cells expressing Fas and Fas ligand. Immunity. 2016;45(5):1052–1065. doi:10.1016/j.immuni.2016.10.005.
  • Roths JB, Murphy ED, Eicher EM. A new mutation, gld that produces lymphoproliferation and autoimmunity in C3H/HeJ mice. J Exp Med. 1984;159(1):1–20. doi:10.1084/jem.159.1.1.
  • Takahashi T, Tanaka M, Brannan C, et al. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell. 1994;76(6):969–976. doi:10.1016/0092-8674(94)90375-1.
  • Lynch D, Watson M, Alderson M, et al. The mouse Fas-ligand gene is mutated in gld mice and is part of a TNF family gene cluster. Immunity. 1994;1(2):131–136. doi:10.1016/1074-7613(94)90106-6.
  • Davidson WF, Giese T, Fredrickson TN. Spontaneous development of plasmacytoid tumors in mice with defective Fas-Fas ligand interactions. J Exp Med. 1998;187(11):1825–1838. doi:10.1084/jem.187.11.1825.
  • Murphy ED, Roths JB. New inbred strains. Mouse News Lett. 1978; 1978(58):51–65.
  • Murphy ED, Roths JB. A Y chromosome associated factor in strain BXSB producing accelerated autoimmunity and lymphoproliferation. Arthritis Rheum. 1979;22(11):1188–1194. doi:10.1002/art.1780221105.
  • Maibaum MA, Haywood MEK, Walport MJ, Morley BJ. Lupus susceptibility loci map within regions of BXSB derived from the SB/Le parental strain. Immunogenetics. 2000;51(4-5):370–372. doi:10.1007/s002510050632.
  • Eisenberg R, Dixon F. Effect of castration on male-determined acceleration of autoimmune disease in BXSB mice. J Immunol. 1980;125(5):1959–1961.
  • Pisitkun P, Deane JA, Di Fi Lippantonio MJ, et al. Autoreactive B cell responses to RNArelated antigens due to TLR7 gene duplication. Science. 2006;312(5780):1669–1672. doi:10.1126/science.1124978.
  • Subramanian S, Tus K, Li QZ, et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci USA. 2006;103(26):9970–9975. doi:10.1073/pnas.0603912103.
  • Walker SE, Gray RH, Fulton M, et al. Palmerston North mice, a new animal model of systemic lupus erythematosus. J Lab Clin Med. 1978;92(6):932–945.
  • Luzina IG, Knitzer RH, Atamas SP, et al. Vasculitis in the Palmerston North mouse model of lupus: phenotype and cytokine production profile of infiltrating cells. Arthritis Rheum. 1999;42(3):561–568. doi:10.1002/1529-0131(199904)42:3<561::AID-ANR22>3.0.CO;2-X.
  • Nakamura K, Kashiwazaki S, Takagishi K, et al. Spontaneous degenerative polyarthritis in male New Zealand Black/KN mice. Arthritis Rheum. 1991;34(2):171–179., doi:10.1002/art.1780340207.
  • Hiroi A, Ito T, Furukawa F. Immunopathological study on alopecia of the NZB/KN mouse. J Wakayama Med Soc. 2001; 52:377–383.
  • Hiroi A, Ito T, Seo N, et al. Male New Zealand Black/KN mice: a novel model for autoimmune-induced permanent alopecia? Br J Dermatol. 2006;155(2):437–445. doi:10.1111/j.1365-2133.2006.07204.x.
  • Rudofsky UH, Evans BD, Balaban SL, et al. 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(4):419–426.
  • Morel L, Rudofsky UH, Longmate JA, et al. Polygenic control of susceptibility to murine systemic lupus erythematosus. Immunity. 1994;1(3):219–229. doi:10.1016/1074-7613(94)90100-7.
  • Bader-Meunier B, Quartier P, Deschênes G, et al.; Group française d’étude du lupus érythémateux disséminé de l’enfant. Childhood-onset systemic lupus erythematosus. Arch. Pediatr. 2003;10:147–157. [ doi:10.1016/S0929-693X(03)00313-0.
  • Morel L, Wakeland EK. Susceptibility to lupus nephritis in the NZB/W model system. Curr. Opin. Immunol. 1998;10(6):718–725. doi:10.1016/S0952-7915(98)80094-0.
  • Mohan C, Alas E, Morel L, Yang P, Wakeland EK. 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(6):1362–1372. doi:10.1172/jci728.
  • Mohan C, Morel L, Yang P, Wakeland EK. Genetic dissection of systemic lupus erythematosus pathogenesis: Sle2 on murine chromosome 4 leads to B cell hyperactivity. J Immunol. 1997;159(1):454–465.
  • Mohan C, Yu Y, Morel L, Yang P, Wakeland EK. Genetic dissection of Sle pathogenesis: Sle3 on murine chromosome 7 impacts T cell activation, differentiation,and cell death. J Immunol. 1999;162(11):6492–6502.
  • Waters ST, McDuffie M, Bagavant H, et al. 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(2):255–264. doi:10.1084/jem.20031519.
  • Zharkova O, Celhar T, Cravens PD, et al. Pathways leading to an immunological diseses: systemic lupus erythematosus. Rheumatology (Oxford.). 2017; 56(suppl_1):i55–i66. doi:10.1093/rheumatology/kew427.
  • Waters ST, Fu SM, Gaskin F, et al. NZM2328: a new mouse model of systemic lupus erythematosus with unique genetic susceptibility loci. Clin Immunol. 2001;100(3):372–383. doi:10.1006/clim.2001.5079.
  • Ge Y, Brown MG, Wang H, et al. Genetic approach to study lupus glomerulonephritis. Methods Mol Biol. 2012;900:271–290. doi:10.1007/978-1-60761-720-4_13.
  • Rudofsky UH, Lawrence DA. New Zealand mixed mice: agenetic systemic lupus erythematosus model for assessing environmental effects. Environ Health Perspect. 1999;107:71321. doi:10.2307/3434332.
  • Morse HC, III, Chused TM, Hartley JW, et al. Expression of xenotropic murine leukemia viruses as cell-surface gp70 in genetic crosses between strains DBA/2 and C57BL/6. J Exp Med. 1979;149(5):1183–1196. doi:10.1084/jem.149.5.1183.
  • Mountz JD, Yang P, Wu Q, et al. Genetic segregation of spontaneous erosive arthritis and generalized autoimmune disease in the BXD2 recombinant inbred strain of mice. Scand J Immunol. 2005;61(2):128–138. doi:10.1111/j.0300-9475.2005.01548.x.
  • Kim YU, Lim H, Jung HE, Wetsel RA, Chung Y. Regulation of autoimmune germinal center reactions in lupus-prone BXD2 mice by follicular helper T cells. PLoS One. 2015;10(3):e0120294–Published 2015 Mar 13. doi:10.1371/journal.pone.0120294.
  • Kaliyaperumal A, Mohan C, Wu W, et al. Nucleosomal peptide epitopes for nephritis-inducing T helper cells of murine lupus. J Exp Med. 1996;183(6):2459–2469. doi:10.1084/jem.183.6.2459.
  • Gavalchin J, Nicklas JA, Eastcott JW, et al. Lupus prone (SWR x NZB)F1 mice produce potentially nephritogenic autoantibodies inherited from the normal SWR parent. J Immunol. 1985;134(2):885–894.
  • Gavalchin J, Datta SK. The NZB X SWR model of lupus nephritis. II. Autoantibodies deposited in renal lesions show a distinctive and restricted idiotypic diversity. J Immunol. 1987;138(1):138–148.
  • Gavalchin J, Seder RA, Datta SK. The NZB X SWR model of lupus nephritis. I. Cross-reactive idiotypes of monoclonal anti-DNA antibodies in relation to antigenic specificity, charge, and allotype. Identification of interconnected idiotype families inherited from the normal SWR and the autoimmune NZB parents. J Immunol. 1987; 138(1):128–137.
  • Dumont F, Monier J. Sex-dependent systemic lupus erythematosus-like syndrome in (NZB × SJL)F1 mice. Clin Immunol Immunopathol. 1983;29(2):306–317. doi:10.1016/0090-1229(83)90032-6.
  • Dumont F, Robert F. Age- and sex-dependent thymic abnormalities in NZB X SJL F1 hybrid mice. Clin Exp Immunol. 1980;41(1):63–72.
  • Dumont F. Effects of ovariectomy and androgen treatment on the thymic pathology of NZB X SJL mice. Thymus. 1985;7(1):37–48.
  • Hashimoto Y, Kawamura M, Ichikawa K, et al. Anticardiolipin antibodies in NZW × BXSB F1 mice. A model of antiphospholipid syndrome. J Immunol. 1992;149(3):1063–1068.
  • Mizutani H, Engelman RW, Kinjoh K, et al. Gastrointestinal vasculitis in autoimmune-prone (NZW × BXSB)F1 mice: association with anticardiolipin autoantibodies. Proc Soc Exp Biol Med. 1995;209(3):279–285. doi:10.3181/00379727-209-43903.
  • Ida A, Hirose S, Hamano Y, et al. Multigenic control of lupus-associated antiphospholipid syndrome in a model of (NZW × BXSB) F1 mice. Eur J Immunol. 1998;28(9):2694–2703. doi:10.1002/(SICI)1521-4141(199809)28:09<2694::AID-IMMU2694>3.0.CO;2-#.
  • Vidal S, Gelpi C, Rodriguez-Sanchez J. (SWR × SJL)F1 mice: a new model of lupus-like disease. J Exp Med. 1994;179(5):1429–1435. doi:10.1084/jem.179.5.1429.
  • Izui S, Masuda K, Yoshida H. Acute SLE in F1 hybrids between SB/Le and NZW mice; prominently enhanced formation of gp70 immune complexes by a Ychromosome-associated factor from SB/Le mice. J Immunol. 1984;132(2):701–704.
  • Kinjoh K, Kyogoku M, Good RA. Genetic selection for crescent formation yields mouse strain with rapidly progressive glomerulonephritis and small vessel vasculitis. Proc. Natl. Acad. Sci. USA. 1993;90(8):3413–3417. doi:10.1073/pnas.90.8.3413.
  • Satoh M, Reeves WH. Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane. J Exp Med. 1994;180(6):2341–2346. doi:10.1084/jem.180.6.2341.
  • Reeves WH, Lee PY, Weinstein JS, et al. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol. 2009;30(9):455–464. doi:10.1016/j.it.2009.06.003.
  • Potter M, Wax J. Genetics of susceptibility to pristane-induced plasmacytomas in BALB/cAn: reduced susceptibility in BALB/cJ with a brief description of pristane-induced arthritis. J Immunol. 1981;127(4):1591–1595.
  • Satoh M, Kumar A, Kanwar YS, et al. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc Natl Acad Sci USA. 1995;92(24):10934–10938. doi:10.1073/pnas.92.24.10934.
  • Zhuang H, Han S, Lee PY, et al. Pathogenesis of Diffuse Alveolar Hemorrhage in Murine Lupus. Arthritis Rheumatol. 2017;69(6):1280–1293. doi:10.1002/art.40077.
  • Smith DL, Dong X, Du S, et al. A female preponderance for chemically induced lupus in SJL/J mice. Clin Immunol. 2007;122(1):101–107. doi:10.1016/j.clim.2006.09.009.
  • Lee P, Li Y, Kumagai Y, et al. Type I interferon modulates monocyte recruitment and maturation in chronic inflammation. Am J Pathol. 2009;175(5):2023–2033. doi:10.2353/ajpath.2009.090328.
  • Nacionales DC, Kelly-Scumpia KM, Lee PY, et al. Deficiency of the type I interferon receptor protects mice from experimental lupus. Arthritis Rheum. 2007;56(11):3770–3783.
  • Van Rappard-Van Der Veen FM, Radaszkiewicz T, Terraneo L, Gleichmann E. Attempts at standardization of lupus-like graft-vs-host disease: inadvertent repopulation by DBA/2 spleen cells of H-2-different nonirradiated F1 mice. J Immunol. 1983; 130(6):2693–2701.
  • Eisenberg RA, Via CS. T cells, murine chronic graft-versus-host disease and autoimmunity. 2012; 39(3):240–247. doi:10.1016/j.jaut.2012.05.017.
  • Grader-Beck T, Casciola-Rosen L, Lang TJ, Puliaev R, Rosen A, Via CS. Apoptotic splenocytes drive the autoimmune response to poly(ADP-ribose) polymerase 1 in a murine model of lupus. J Immunol. 2007;178(1):95–102. doi:10.4049/jimmunol.178.1.95.
  • Lang TJ, Nguyen P, Papadimitriou JC, Via CS. Increased severity of murine lupus in female mice is due to enhanced expansion of pathogenic T cells. J Immunol. 2003;171(11):5795–5801. doi:10.4049/jimmunol.171.11.5795.
  • Via CS. Advances in lupus stemming from the parent-into-F1 model. Trends in Immunology. 2010;31(6):236–245. doi:10.1016/j.it.2010.02.001.
  • Bruijn JA, van Elven EH, Hogendoorn PC, Corver WE, Hoedemaeker PJ, Fleuren GJ. Murine chronic graft-vs-host disease as a model for lupus nephritis. Am J Pathol. 1988;130(3):639–641.
  • Mendlovic S, Brocke S, Shoenfeld Y, et al. Induction of a systemic lupus erythematosus-like disease in mice by a common human anti-DNA idiotype. Proc Natl Acad Sci USA. 1988;85(7):2260–2264. doi:10.1073/pnas.85.7.2260.
  • Waisman A, Mendlovic S, Ruiz PJ, Zinger H, Meshorer A, Mozes E. The role of the 16/6 idiotype network in the induction and manifestation of systemic lupus erythematosus. Int Immunol. 1993;5:1293–1300. doi:10.1093/intimm/5.10.1293.
  • Blank M, Cohen J, Toder V, et al. Induction of anti-phospholipid syndrome in naive mice with mouse lupus monoclonal and human polyclonal anti-cardiolipin antibodies. Proc Natl Acad Sci USA. 1991;88(8):3069–3073. doi:10.1073/pnas.88.8.3069.
  • Blank M, Krause I, Ben-Bassat M, Shoenfeld Y. Induction of experimental anti-phospholipid syndrome associated with SLE following immunization with human monoclonal pathogenic anti-DNA idiotype. J.Autoimmun. 1992;5(4):495–509. doi:10.1016/0896-8411(92)90008-E.
  • Shoenfeld Y, Ziporen L. Lessons from experimental APS models. Lupus. 1998;7(2_suppl):158–S161. doi:10.1177/096120339800700234.
  • Mozes E, Shoenfeld Y, Brocke S, Mendlovic S. Induction of experimental systemic lupus erythematosus in mice. Isr J Med Sci. 1988;24(12):741–744.
  • Krause I, Blank M, Kopolovic J, et al. Abrogation of experimental systemic lupus erythematosus and primary antiphospholipid syndrome with intravenous gamma globulin. J Rheumatol. 1995;22(6):1068–1074.
  • Blank M, Tomer Y, Slavin S, et al. Induction of tolerance to experimental anti-phospholipid syndrome (APS) by syngeneic bone marrow cell transplantation. Scand J Immunol. 1995;42(2):226–234. doi:10.1111/j.1365-3083.1995.tb03649.x.
  • Blank M, Krause I, Buskila D, et al. Bromocriptine immunomodulation of experimental SLE and primary antiphospholipid syndrome via induction of nonspecific T suppressor cells. Cell Immunol. 1995;162(1):114–122. doi:10.1006/cimm.1995.1058.
  • Shoenfeld Y, Blank M. Effect of long-acting thromboxane receptor antagonist (BMS 180,291) on experimental antiphospholipid syndrome. Lupus. 1994;3(5):397–400. doi:10.1177/096120339400300506.
  • Tomer Y, Blank M, Shoenfeld Y. Suppression of experimental antiphospholipid syndrome and systemic lupus erythematosus in mice by anti-CD4 monoclonal antibodies. Arthritis Rheum. 1994;37(8):1236–1244. doi:10.1002/art.1780370819.
  • Levite M, Zinger H, Zisman E, et al. Beneficial effects of bone marrow transplantation on the serological manifestations and kidney pathology of experimental systemic lupus erythematosus. Cell Immunol. 1995;162(1):138–145. doi:10.1006/cimm.1995.1061.
  • Yokogawa M, Takaishi M, Nakajima K, et al. Epicutaneous application of toll-like receptor 7 agonists leads to systemic autoimmunity in wild-type mice: a new model of systemic Lupus erythematosus. Arthritis Rheumatol. 2014;66(3):694–706. doi:10.1002/art.3829.
  • Hasham MG, Baxan N, Stuckey DJ, et al. Systemic autoimmunity induced by the TLR7/8 agonist Resiquimod causes myocarditis and dilated cardiomyopathy in a new mouse model of autoimmune heart disease. Dis Model Mech. 2017;10(3):259–270. doi:10.1242/dmm.027409.
  • Liu Y, Seto NL1, Carmona-Rivera C, Kaplan M. Accelerated model of lupus autoimmunity and vasculopathy driven by toll-like receptor 7/9 imbalance. Lupus Sci Med. 2018;5(1):e000259. doi:10.1136/lupus-2018-000259.
  • Ruff WE, Kriegel MA. Autoimmune host-microbiota interactions at barrier sites and beyond. Trends Mol. Med. 2015;21(4):233–244. doi:10.1016/j.molmed.2015.02.006.
  • Zhang H, Liao X, Sparks JB, Luo XM. Dynamics of gut microbiota in autoimmune lupus. Appl Environ Microbiol. 2014;80(24):7551–7560. doi:10.1128/AEM.02676-14.
  • Luo XM, Edwards MR, Mu Q, et al. Gut microbiota in human systemic lupus erythematosus and a mouse model of lupus. Appl Environ Microbiol. 2018;84:e02288–e02317.
  • Johnson BM, Gaudreau MC, Al-Gadban MM, Gudi R, Vasu C. Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. Clin Exp Immunol. 2015;181(2):323–337. doi:10.1111/cei.12609.
  • Avni O, Koren O. Molecular (Me)micry?. Cell Host Microbe. 2018;23(5):576–578. doi:10.1016/j.chom.2018.04.012.
  • M, Vieira, et al. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science. 2018;359(6380):1156–1161. doi:10.1126/science.aar7201.
  • Rahman A, DA. Isenberg Systemic lupus erythematosus. N Engl J Med. 2008;358(9):929–939. doi:10.1056/NEJMra071297.
  • D’Cruz DP, MA, Khamashta GR. Hughes Systemic lupuserythematosus. Lancet. 2007;369:587–596. doi:10.1016/S0140-6736(07)60279-7.
  • Duhlin A, Chen Y, Wermeling F, et al. Selective memory to apoptotic cell-derived self-antigens with implications for systemic lupus erythematosus development. JI. 2016;197(7):2618–2626. doi:10.4049/jimmunol.1401129.
  • Tabata N, Miyazawa M, Fujisawa R, Takei YA, Abe H, Hashimoto K. Establishment of monoclonal anti-retroviral gp70 autoantibodies from MRL/lpr lupus mice and induction of glomerular gp70 deposition and pathology by transfer into non-autoimmune mice. J Virol. 2000;74(9):4116–4126. doi:10.1128/JVI.74.9.4116-4126.2000.
  • Sado Y, Naito I, Okigaki T. Transfer of anti-glomerular basement membrane antibody-induced glomerulonephritis in inbred rats with isologous antibodies from the urine of nephritic rats. J Pathol. 1989;158(4):325–332. doi:10.1002/path.1711580410.
  • Lefkowith JB, Gilkeson GS. Nephritogenic autoantibodies in lupus: current concepts and continuing controversies. Arthritis Rheum. 1996;39(6):894–903. doi:10.1002/art.1780390605.
  • Du Y, Fu Y, Mohan C. Experimental anti-GBM nephritis as an analytical tool for studying spontaneous lupus nephritis. Arch Immunol Ther Exp. 2008;56(1):31–40. doi:10.1007/s00005-008-0007-4.
  • Molina V, Shoenfeld Y. Yehuda Shoenfeld Infection, vaccines and other environmental triggers of autoimmunity. Autoimmunity. 2005;38(3):235–245. doi:10.1080/08916930500050277.
  • M, Molokhia P. McKeigue Systemic lupus erythematosus: genes versus environment in high-risk populations. Lupus. 2006;15(11):827–832. doi:10.1177/0961203306070007.
  • P, Sarzi-Puttini F, Atzeni L, Iaccarino A. Doria Environment, and systemic lupus erythematosus: an overview. Autoimmunity. 2005;38(7):465–472. doi:10.1080/08916930500285394.
  • JF, Simard KH. Costenbader What can epidemiology tell us about systemic lupus erythematosus? Int J Clin Pract. 2007; 61(7):1170–1180. doi:10.1111/j.1742-1241.2007.01434.x.
  • Brown JM, Archer AJ, Pfau JC, Holian A. Silica accelerated systemic autoimmune disease in lupus-prone New Zealand mixed mice. Clin Exp Immunol. 2003;131(3):415–421. [PubMed: 12605693] doi:10.1046/j.1365-2249.2003.02094.x.
  • Finckh A, Cooper GS, Chibnik LB, et al. Occupational Silica and Solvent Exposures and Risk of Systemic Lupus Erythematosus in Urban Women. Arthritis Rheum. 2006;54(11):3648–3654. doi:10.1002/art.22210.
  • Via CS, Nguyen P, Niculescu F, Papadimitriou J, Hoover D, Silbergeld EK. Low-dose exposure to inorganic mercury accelerates disease and mortality in acquired murine lupus. Environ Health Perspect. 2003;111(10):1273–1277. doi:10.1289/ehp.6064.
  • Kaneko T, Saegusa M, Tasaka K, Sato A. Immunotoxicity of trichloroethylene: a study with MRL-lpr/lpr mice. J Appl Toxicol. 2000;20(6):471–475. doi:10.1002/1099-1263(200011/12)20:6<471::aid-jat716>3.0.co;2-e.
  • Khan MF, Kaphalia BS, Prabhakar BS, Kanz MF, Ansari GAS. Trichloroethene-induced autoimmune response in female MRL +/+ mice. Toxicol. Appl. Pharmacol. 1995;134(1):155–160. doi:10.1006/taap.1995.1179.
  • Wallace S, Gilkeson G, Peden-Adams MM, EuDaly J, Keil DE. A comparative study evaluating the immunological effects of trichloroethylene in NZB/NZW and B6C3F1 mice. Toxicologist. 2001;60(S-1):141.
  • Keil DE, Peden-Adams MM, Wallace S, Ruiz P, Gilkeson GS. Assessment of trichloroethylene (TCE) exposure in murine strains genetically-prone and non-prone to develop autoimmune disease. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2009;44(5):443–453. doi:10.1080/10934520902719738.
  • Brehm MA, Shultz LD, Greiner DL. Humanized mouse models to study human diseases. Curr Opin Endocrinol Diabetes Obes. 2010;17(2):120–125. doi:10.1097/MED.0b013e328337282f.
  • Walsh NC, Kenney LL, Jangalwe S, et al. Humanized mouse models of clinical disease. Annu Rev Pathol Mech Dis. 2017;12(1):187–215. doi:10.1146/annurev-pathol-052016-100332.
  • Sthoeger Z, Zinger H, Dekel B, Arditi F, Reisner Y, Mozes E. Lupus manifestations in severe combined immunodeficient (SCID) mice and in human/mouse radiation chimera. J Clin Immunol. 2003;23(2):91–99.
  • Lubin I, Segall H, Marcus H, et al. Engraftment of human peripheral blood lymphocytes in normal strains of mice. Blood. 1994;83(8):2368–2381. doi:10.1182/blood.V83.8.2368.2368.
  • Duchosal MA, McConahey PJ, Robinson CA, Dixon FJ. Transfer of human systemic lupus erythematosus in severe combined immunodeficient (SCID) mice. J Exp Med. 1990;172(3):985–988. doi:10.1084/jem.172.3.985.
  • Vladutiu AO. The severe combined immunodeficient (SCID) mouse as a model for the study of autoimmune diseases. Clin Exp Immunol. 2008;93(1):1–8. doi:10.1111/j.1365-2249.1993.tb06488.x.
  • Kerekov N, Mihaylova N, Prechl J, Tchorbanov A. Humanized SCID mice models of SLE. CPD. 2011;17(13):1261–1266. doi:10.2174/138161211795703780.
  • Andrad e D, Redecha PB, Vukelic M. Engraftment of peripheral blood mononuclear cells from systemic lupus erythematosus and antiphospholipid syndrome patient donors into BALB-RAG-2-/- IL-2Rγ-/- mice: a promising model for studying human disease. Arthritis Rheum. 2011;63:2764–2773. doi:10.1002/art.30424.
  • Gunawan M, Her ZS, Liu M, et al. A novel human systemic lupus erythematosus model in humanised mice. Sci Rep. 2017;7(1):16642. doi:10.1038/s41598-017-16999-7.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.