Animal models used to examine the role of the environment in the development of autoimmune disease: Findings from an NIEHS Expert Panel Workshop

Journal of Autoimmunity

Volumn 39, Issue 4, 2012, Pages 285-293

  Germolec, Dori ^a   Kono, Dwight H ^b   Pfau, Jean C ^c   Pollard, K Michael ^b  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Nucl Eng Idaho State University   (United States)

Author keywords

Animal model; Autoimmunity; Biological; Chemicals; Environmental factors

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; GLUTEN; GOLD; IODINE; MERCURY; MINERAL OIL; ORGANOCHLORINE PESTICIDE; PRISTANE; RAPESEED OIL; SILICON DIOXIDE; SILVER; TRICHLOROETHYLENE; TRYPTOPHAN;

ANIMAL MODEL; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BACTERIAL INFECTION; COXSACKIE VIRUS INFECTION; DIETARY INTAKE; DISEASE SEVERITY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EOSINOPHILIA MYALGIA SYNDROME; GENOTYPE ENVIRONMENT INTERACTION; IMMUNE RESPONSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; REVIEW; STREPTOCOCCUS INFECTION; ULTRAVIOLET RADIATION; VIRUS INFECTION;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; BIOLOGICAL AGENTS; CONGRESSES AS TOPIC; DISEASE MODELS, ANIMAL; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; HUMANS; MICE; MODELS, IMMUNOLOGICAL; RATS; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY; ULTRAVIOLET RAYS;

EID: 84869874107     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2012.05.020     Document Type: Review

References (119)

1. Dedeoglu F. Drug-induced autoimmunity. Curr Opin Rheumatol 2009, 21:547-551.
2. Vedove C.D., Del Giglio M., Schena D., Girolomoni G. Drug-induced lupus erythematosus. Arch Dermatol Res 2009, 301:99-105.
3. Rubin R.L., Kretz-Rommel A. A nondeletional mechanism for central T-cell tolerance. Crit Rev Immunol 2001, 21:29-40.
4. Pollard K.M., Hultman P., Kono D.H. Toxicology of autoimmune diseases. Chem Res Toxicol 2010, 23:455-466.
5. Richardson B. DNA methylation and autoimmune disease. Clin Immunol 2003, 109:72-79.
6. Roep B.O., Atkinson M., von Herrath M. Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes. Nat Rev Immunol 2004, 4:989-997.
7. Kono D.H., Theofilopoulos A.N. Genetics of SLE in mice. Springer Semin Immunopathol 2006, 28:83-96.
8. Andersson A., Karlsson J. Genetics of experimental autoimmune encephalomyelitis in the mouse. Arch Immunol Ther Exp (Warsz) 2004, 52:316-325.
9. Cohen P.L., Caricchio R., Abraham V., Camenisch T.D., Jennette J.C., Roubey R.A., et al. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 2002, 196:135-140.
10. Seery J.P. IFN-gamma transgenic mice: clues to the pathogenesis of systemic lupus erythematosus?. Arthritis Res 2000, 2:437-440.
11. Rubin R.L. Drug-induced lupus. Toxicology 2005, 209:135-147.
12. Vas J., Monestier M. Immunology of mercury. Ann N Y Acad Sci 2008, 1143:240-267.
13. Hultman P., Lindh U., Horsted-Bindslev P. Activation of the immune system and systemic immune-complex deposits in Brown Norway rats with dental amalgam restorations. J Dent Res 1998, 77:1415-1425.
14. Abedi-Valugerdi M., Hansson M., Moller G. Genetic control of resistance to mercury-induced immune/autoimmune activation. Scand J Immunol 2001, 54:190-197.
15. Kono D.H., Balomenos D., Pearson D.L., Park M.S., Hildebrandt B., Hultman P., et al. The prototypic Th2 autoimmunity induced by mercury is dependent on IFN- gamma and not Th1/Th2 imbalance. J Immunol 1998, 161:234-240.
16. Warfvinge K., Hansson H., Hultman P. Systemic autoimmunity due to mercury vapor exposure in genetically susceptible mice: dose-response studies. Toxicol Appl Pharmacol 1995, 132:299-309.
17. Hultman P., Johansson U., Turley S.J., Lindh U., Enestrom S., Pollard K.M. Adverse immunological effects and autoimmunity induced by dental amalgam and alloy in mice. Faseb J 1994, 8:1183-1190.
18. Hultman P., Turley S.J., Enestrom S., Lindh U., Pollard K.M. Murine genotype influences the specificity, magnitude and persistence of murine mercury-induced autoimmunity. J Autoimmun 1996, 9:139-149.
19. Lockie L.M., Smith D.M. Forty-seven years experience with gold therapy in 1,019 rheumatoid arthritis patients. Semin Arthritis Rheum 1985, 14:238-246.
20. Tournade H., Guery J.C., Pasquier R., Nochy D., Hinglais N., Guilbert B., et al. Experimental gold-induced autoimmunity. Nephrol Dial Transplant 1991, 6:621-630.
21. Qasim F.J., Thiru S., Gillespie K. Gold and D-penicillamine induce vasculitis and up-regulate mRNA for IL-4 in the Brown Norway rat: support for a role for Th2 cell activity. Clin Exp Immunol 1997, 108:438-445.
22. Savignac M., Badou A., Delmas C., Subra J.F., De Cramer S., Paulet P., et al. Gold is a T cell polyclonal activator in BN and LEW rats but favors IL-4 expression only in autoimmune prone BN rats. Eur J Immunol 2001, 31:2266-2276.
23. Tournade H., Guery J.C., Pasquier R., Vial M.C., Mandet C., Druet E., et al. Effect of the thiol group on experimental gold-induced autoimmunity. Arthritis Rheum 1991, 34:1594-1599.
24. 2 and gold sodium thiomalate enhance serum IgE and IgG concentrations in susceptible mouse strains. Int Arch Allergy Appl Immunol 1989, 90:47-53.
25. Havarinasab S., Johansson U., Pollard K.M., Hultman P. Gold causes genetically determined autoimmune and immunostimulatory responses in mice. Clin Exp Immunol 2007, 150:179-188.
26. Hansson M., Abedi-Valugerdi M. Xenobiotic metal-induced autoimmunity: mercury and silver differentially induce antinucleolar autoantibody production in susceptible H-2s, H-2q and H-2f mice. Clin Exp Immunol 2003, 131:405-414.
27. Hultman P., Ganowiak K., Turley S.J., Pollard K.M. Genetic susceptibility to silver-induced anti-fibrillarin autoantibodies in mice. Clin Immunol Immunopathol 1995, 77:291-297.
28. Abedi-Valugerdi M. Mercury and silver induce B cell activation and anti-nucleolar autoantibody production in outbred mouse stocks: are environmental factors more important than the susceptibility genes in connection with autoimmunity?. Clin Exp Immunol 2009, 155:117-124.
29. Reeves W.H., Lee P.Y., Weinstein J.S., Satoh M., Lu L. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol 2009, 30:455-464.
30. Holmdahl R., Lorentzen J.C., Lu S., Olofsson P., Wester L., Holmberg J., et al. Arthritis induced in rats with nonimmunogenic adjuvants as models for rheumatoid arthritis. Immunol Rev 2001, 184:184-202.
31. Kleinau S., Erlandsson H., Holmdahl R., Klareskog L. Adjuvant oils induce arthritis in the DA rat. I. Characterization of the disease and evidence for an immunological involvement. J Autoimmun 1991, 4:871-880.
32. Olofsson P., Holmdahl R. Pristane-induced arthritis in the rat. Methods Mol Med 2007, 136:255-268.
33. Wooley P.H., Seibold J.R., Whalen J.D., Chapdelaine J.M. Pristane-induced arthritis. The immunologic and genetic features of an experimental murine model of autoimmune disease. Arthritis Rheum 1989, 32:1022-1030.
34. Clynes R., Calvani N., Croker B.P., Richards H.B. Modulation of the immune response in pristane-induced lupus by expression of activation and inhibitory Fc receptors. Clin Exp Immunol 2005, 141:230-237.
35. Satoh M., Richards H.B., Shaheen V.M., Yoshida H., Shaw M., Naim J.O., et al. Widespread susceptibility among inbred mouse strains to the induction of lupus autoantibodies by pristane. Clin Exp Immunol 2000, 121:399-405.
36. Yoshida H., Satoh M., Behney K.M., Lee C.G., Richards H.B., Shaheen V.M., et al. Effect of an exogenous trigger on the pathogenesis of lupus in (NZB x NZW)F1 mice. Arthritis Rheum 2002, 46:2235-2244.
37. Satoh M., Weintraub J.P., Yoshida H., Shaheen V.M., Richards H.B., Shaw M., et al. Fas and Fas ligand mutations inhibit autoantibody production in pristane-induced lupus. J Immunol 2000, 165:1036-1043.
38. Pestana A., Munoz E. Anilides and the Spanish toxic oil syndrome. Nature 1982, 298:608.
39. Berking C., Hobbs M.V., Chatelain R., Meurer M., Bell S.A. Strain-dependent cytokine profile and susceptibility to oleic acid anilide in a murine model of the toxic oil syndrome. Toxicol Appl Pharmacol 1998, 148:222-228.
40. Bell S.A., Hobbs M.V., Rubin R.L. Isotype-restricted hyperimmunity in a murine model of the toxic oil syndrome. J Immunol 1992, 148:3369-3376.
41. Clauw D.J. Animal models of the eosinophilia-myalgia syndrome. J Rheumatol Suppl 1996, 46:93-97. discussion 92, 97-8.
42. Okada S., Kamb M.L., Pandey J.P., Philen R.M., Love L.A., Miller F.W. Immunogenetic risk and protective factors for the development of L-tryptophan-associated eosinophilia-myalgia syndrome and associated symptoms. Arthritis Rheum 2009, 61:1305-1311.
43. Gross B., Ronen N., Honigman S., Livne E. Tryptophan toxicity-time and dose response in rats. Adv Exp Med Biol 1999, 467:507-516.
44. Crofford L.J., Rader J.I., Dalakas M.C., Hill R.H., Page S.W., Needham L.L., et al. L-tryptophan implicated in human eosinophilia-myalgia syndrome causes fasciitis and perimyositis in the Lewis rat. J Clin Invest 1990, 86:1757-1763.
45. Love L.A., Rader J.I., Crofford L.J., Raybourne R.B., Principato M.A., Page S.W., et al. Pathological and immunological effects of ingesting L-tryptophan and 1,1'-ethylidenebis (L-tryptophan) in Lewis rats. J Clin Invest 1993, 91:804-811.
46. Silver R.M., Ludwicka A., Hampton M., Ohba T., Bingel S.A., Smith T., et al. A murine model of the eosinophilia-myalgia syndrome induced by 1,1'-ethylidenebis (L-tryptophan). J Clin Invest 1994, 93:1473-1480.
47. Stahl J.L., Cook E.B., Pariza M.A., Cook M.E., Graziano F.M. Effect of L-tryptophan supplementation on eosinophils and eotaxin in guinea pigs. Exp Biol Med (Maywood) 2001, 226:177-184.
48. Teng X., Shan Z., Teng W., Fan C., Wang H., Guo R. Experimental study on the effects of chronic iodine excess on thyroid function, structure, and autoimmunity in autoimmune-prone NOD.H-2h4 mice. Clin Exp Med 2009, 9:51-59.
49. McLachlan S.M., Braley-Mullen H., Chen C.R., Aliesky H., Pichurin P.N., Rapoport B. Dissociation between iodide-induced thyroiditis and antibody-mediated hyperthyroidism in NOD.H-2h4 mice. Endocrinology 2005, 146:294-300.
50. Braley-Mullen H., Sharp G.C., Medling B., Tang H. Spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J Autoimmun 1999, 12:157-165.
51. Hutchings P.R., Verma S., Phillips J.M., Harach S.Z., Howlett S., Cooke A. Both CD4(+) T cells and CD8(+) T cells are required for iodine accelerated thyroiditis in NOD mice. Cell Immunol 1999, 192:113-121.
52. Rasooly L., Burek C.L., Rose N.R. Iodine-induced autoimmune thyroiditis in NOD-H-2h4 mice. Clin Immunol Immunopathol 1996, 81:287-292.
53. Mooij P., de Wit H.J., Drexhage H.A. An excess of dietary iodine accelerates the development of a thyroid-associated lymphoid tissue in autoimmune prone BB rats. Clin Immunol Immunopathol 1993, 69:189-198.
54. Ebner S.A., Lueprasitsakul W., Alex S., Fang S.L., Appel M.C., Braverman L.E. Iodine content of rat thyroglobulin affects its antigenicity in inducing lymphocytic thyroiditis in the BB/Wor rat. Autoimmunity 1992, 13:209-214.
55. Murphy G.E., Swift H.F. Induction of cardiac lesions, closely resembling those of rheumatic fever, in rabbits following repeated skin infections with group A streptococci. J Exp Med 1949, 89:687-698.
56. Murphy G.E., Swift H.F. The induction of rheumatic-like cardiac lesions in rabbits by repeated focal infections with group A streptococci; comparison with the cardiac lesions of serum disease. J Exp Med 1950, 91:485-498.
57. Cunningham M.W. Streptococcus-induced myocarditis in mice. Autoimmunity 2001, 34:193-197.
58. Liao L., Sindhwani R., Rojkind M., Factor S., Leinwand L., Diamond B. Antibody-mediated autoimmune myocarditis depends on genetically determined target organ sensitivity. J Exp Med 1995, 181:1123-1131.
59. Malkiel S., Liao L., Cunningham M.W., Diamond B. T-Cell-dependent antibody response to the dominant epitope of streptococcal polysaccharide, N-acetyl-glucosamine, is cross-reactive with cardiac myosin. Infect Immun 2000, 68:5803-5808.
60. Quinn A., Kosanke S., Fischetti V.A., Factor S.M., Cunningham M.W. Induction of autoimmune valvular heart disease by recombinant streptococcal m protein. Infect Immun 2001, 69:4072-4078.
61. Li Y., Heuser J.S., Cunningham L.C., Kosanke S.D., Cunningham M.W. Mimicry and antibody-mediated cell signaling in autoimmune myocarditis. J Immunol 2006, 177:8234-8240.
62. Gorton D., Govan B., Olive C., Ketheesan N. B- and T-cell responses in group a streptococcus M-protein- or Peptide-induced experimental carditis. Infect Immun 2009, 77:2177-2183.
63. Yoshitomi H., Sakaguchi N., Kobayashi K., Brown G.D., Tagami T., Sakihama T., et al. A role for fungal {beta}-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005, 201:949-960.
64. Pordeus V., Szyper-Kravitz M., Levy R.A., Vaz N.M., Shoenfeld Y. Infections and autoimmunity: a panorama. Clin Rev Allergy Immunol 2008, 34:283-299.
65. Mohindru M., Kang B., Kim B.S. Initial capsid-specific CD4(+) T cell responses protect against Theiler's murine encephalomyelitisvirus-induced demyelinating disease. Eur J Immunol 2006, 36:2106-2115.
66. Denic A., Johnson A.J., Bieber A.J., Warrington A.E., Rodriguez M., Pirko I. The relevance of animal models in multiple sclerosis research. Pathophysiology 2010.
67. Pope J.G., Karpus W.J., VanderLugt C., Miller S.D. Flow cytometric and functional analyses of central nervous system-infiltrating cells in SJL/J mice with Theiler's virus-induced demyelinating disease. Evidence for a CD4+ T cell-mediated pathology. J Immunol 1996, 156:4050-4058.
68. Rose N.R. Myocarditis: infection versus autoimmunity. J Clin Immunol 2009, 29:730-737.
69. Esfandiarei M., McManus B.M. Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol 2008, 3:127-155.
70. Wolfgram L.J., Beisel K.W., Herskowitz A., Rose N.R. Variations in the susceptibility to Coxsackievirus B3-induced myocarditis among different strains of mice. J Immunol 1986, 136:1846-1852.
71. McManus B.M., Chow L.H., Wilson J.E., Anderson D.R., Gulizia J.M., Gauntt C.J., et al. Direct myocardial injury by enterovirus: a central role in the evolution of murine myocarditis. Clin Immunol Immunopathol 1993, 68:159-169.
72. Shi Y., Chen C., Lisewski U., Wrackmeyer U., Radke M., Westermann D., et al. Cardiac deletion of the Coxsackievirus-adenovirus receptor abolishes Coxsackievirus B3 infection and prevents myocarditis in vivo. J Am Coll Cardiol 2009, 53:1219-1226.
73. Jun H.S., Yoon J.W. A new look at viruses in type 1 diabetes. Diabetes Metab Res Rev 2003, 19:8-31.
74. Yoon J.W., Jun H.S. Viruses cause type 1 diabetes in animals. Ann N Y Acad Sci 2006, 1079:138-146.
75. Atkinson M.A., Bowman M.A., Campbell L., Darrow B.L., Kaufman D.L., Maclaren N.K. Cellular immunity to a determinant common to glutamate decarboxylase and coxsackie virus in insulin-dependent diabetes. J Clin Invest 1994, 94:2125-2129.
76. Tarleton R.L., Reithinger R., Urbina J.A., Kitron U., Gurtler R.E. The challenges of Chagas disease- grim outlook or glimmer of hope. PLoS Med 2007, 4:e332.
77. Kierszenbaum F. Where do we stand on the autoimmunity hypothesis of Chagas disease?. Trends Parasitol 2005, 21:513-516.
78. Cunha-Neto E., Bilate A.M., Hyland K.V., Fonseca S.G., Kalil J., Engman D.M. Induction of cardiac autoimmunity in Chagas heart disease: a case for molecular mimicry. Autoimmunity 2006, 39:41-54.
79. Andersson J., Orn A., Sunnemark D. Chronic murine Chagas' disease: the impact of host and parasite genotypes. Immunol Lett 2003, 86:207-212.
80. Leon J.S., Godsel L.M., Wang K., Engman D.M. Cardiac myosin autoimmunity in acute Chagas' heart disease. Infect Immun 2001, 69:5643-5649.
81. Traystman M.D., Beisel K.W. Genetic control of Coxsackievirus B3-induced heart-specific autoantibodies associated with chronic myocarditis. Clin Exp Immunol 1991, 86:291-298.
82. Brown J.M., Pfau J.C., Holian A. Immunoglobulin and lymphocyte responses following silica exposure in New Zealand mixed mice. Inhal Toxicol 2004, 16:133-139.
83. Brown J.M., Archer A.J., Pfau J.C., Holian A. Silica accelerated systemic autoimmune disease in lupus-prone New Zealand mixed mice. Clin Exp Immunol 2003, 131:415-421.
84. Al-Mogairen S.M. Role of sodium silicate in induction of scleroderma-related autoantibodies in brown Norway rats through oral and subcutaneous administration. Rheumatol Int 2011, 31:611-615.
85. al-Balaghi S., Moller E., Moller G., Abedi-Valugerdi M. Mercury induces polyclonal B cell activation, autoantibody production and renal immune complex deposits in young (NZB x NZW)F1 hybrids. Eur J Immunol 1996, 26:1519-1526.
86. Pollard K.M., Pearson D.L., Hultman P., Hildebrandt B., Kono D.H. Lupus-prone mice as models to study xenobiotic-induced acceleration of systemic autoimmunity. Environ Health Perspect 1999, 107(Suppl. 5):729-735.
87. Pollard K.M., Pearson D.L., Hultman P., Deane T.N., Lindh U., Kono D.H. Xenobiotic acceleration of idiopathic systemic autoimmunity in lupus- prone bxsb mice. Environ Health Perspect 2001, 109:27-33.
88. Hansson M., Djerbi M., Rabbani H., Mellstedt H., Gharibdoost F., Hassan M., et al. Exposure to mercuric chloride during the induction phase and after the onset of collagen-induced arthritis enhances immune/autoimmune responses and exacerbates the disease in DBA/1 mice. Immunology 2005, 114:428-437.
89. Brenden N., Rabbani H., Abedi-Valugerdi M. Analysis of mercury-induced immune activation in nonobese diabetic (NOD) mice. Clin Exp Immunol 2001, 125:202-210.
90. Hansson M., Abedi-Valugerdi M. Mercuric chloride induces a strong immune activation, but does not accelerate the development of dermal fibrosis in tight skin 1 mice. Scand J Immunol 2004, 59:469-477.
91. Schecter A., Birnbaum L., Ryan J.J., Constable J.D. Dioxins: an overview. Environ Res 2006, 101:419-428.
92. Signorini S., Gerthoux P.M., Dassi C., Cazzaniga M., Brambilla P., Vincoli N., et al. Environmental exposure to dioxin: the Seveso experience. Andrologia 2000, 32:263-270.
93. Baccarelli A., Mocarelli P., Patterson D.G., Bonzini M., Pesatori A.C., Caporaso N., et al. Immunologic effects of dioxin: new results from Seveso and comparison with other studies. Environ Health Perspect 2002, 110:1169-1173.
94. Tonn T., Esser C., Schneider E.M., Steinmann-Steiner-Haldenstatt W., Gleichmann E. Persistence of decreased T-helper cell function in industrial workers 20 years after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Environ Health Perspect 1996, 104:422-426.
95. Kim H.A., Kim E.M., Park Y.C., Yu J.Y., Hong S.K., Jeon S.H., et al. Immunotoxicological effects of agent Orange exposure to the Vietnam War Korean veterans. Ind Health 2003, 41:158-166.
96. Jennings A.M., Wild G., Ward J.D., Ward A.M. Immunological abnormalities 17 years after accidental exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Br J Ind Med 1988, 45:701-704.
97. Holladay S.D., Mustafa A., Gogal R.M. Prenatal TCDD in mice increases adult autoimmunity. Reprod Toxicol 2011, 31:312-318.
98. Mustafa A., Holladay S.D., Witonsky S., Sponenberg D.P., Karpuzoglu E., Gogal R.M. A single mid-gestation exposure to TCDD yields a postnatal autoimmune signature, differing by sex, in early geriatric C57BL/6 mice. Toxicology 2011.
99. Ishimaru N., Takagi A., Kohashi M., Yamada A., Arakaki R., Kanno J., et al. Neonatal exposure to low-dose 2,3,7,8-tetrachlorodibenzo-p-dioxin causes autoimmunity due to the disruption of T cell tolerance. J Immunol 2009, 182:6576-6586.
100. Sobel E.S., Wang F., Butfiloski E., Croker B., Roberts S.M. Comparison of chlordecone effects on autoimmunity in (NZBxNZW) F(1) and BALB/c mice. Toxicology 2006, 218:81-89.
101. Sobel E.S., Gianini J., Butfiloski E.J., Croker B.P., Schiffenbauer J., Roberts S.M. Acceleration of autoimmunity by organochlorine pesticides in (NZB x NZW)F1 mice. Environ Health Perspect 2005, 113:323-328.
102. Cooper G.S., Makris S.L., Nietert P.J., Jinot J. Evidence of autoimmune-related effects of trichloroethylene exposure from studies in mice and humans. Environ Health Perspect 2009, 117:696-702.
103. Griffin J.M., Blossom S.J., Jackson S.K., Gilbert K.M., Pumford N.R. Trichloroethylene accelerates an autoimmune response by Th1 T cell activation in MRL +/+ mice. Immunopharmacology 2000, 46:123-137.
104. Khan M.F., Kaphalia B.S., Prabhakar B.S., Kanz M.F., Ansari G.A. Trichloroethene-induced autoimmune response in female MRL +/+ mice. Toxicol Appl Pharmacol 1995, 134:155-160.
105. Griffin J.M., Gilbert K.M., Pumford N.R. Inhibition of CYP2E1 reverses CD4+ T-cell alterations in trichloroethylene-treated MRL+/+ mice. Toxicol Sci 2000, 54:384-389.
106. Griffin J.M., Gilbert K.M., Lamps L.W., Pumford N.R. CD4(+) T-cell activation and induction of autoimmune hepatitis following trichloroethylene treatment in MRL+/+ mice. Toxicol Sci 2000, 57:345-352.
107. Blossom S.J., Pumford N.R., Gilbert K.M. Activation and attenuation of apoptosis of CD4+ T cells following in vivo exposure to two common environmental toxicants, trichloroacetaldehyde hydrate and trichloroacetic acid. J Autoimmun 2004, 23:211-220.
108. Blossom S.J., Doss J.C., Gilbert K.M. Chronic exposure to a trichloroethylene metabolite in autoimmune-prone MRL+/+ mice promotes immune modulation and alopecia. Toxicol Sci 2007, 95:401-411.
109. Blossom S.J., Doss J.C. Trichloroethylene alters central and peripheral immune function in autoimmune-prone MRL(+/+) mice following continuous developmental and early life exposure. J Immunotoxicol 2007, 4:129-141.
110. Blossom S.J., Doss J.C., Hennings L.J., Jernigan S., Melnyk S., James S.J. Developmental exposure to trichloroethylene promotes CD4+ T cell differentiation and hyperactivity in association with oxidative stress and neurobehavioral deficits in MRL+/+ mice. Toxicol Appl Pharmacol 2008, 231:344-353.
111. Werth V.P. Cutaneous lupus: insights into pathogenesis and disease classification. Bull NYU Hosp Jt Dis 2007, 65:200-204.
112. Ansel J.C., Mountz J., Steinberg A.D., DeFabo E., Green I. Effects of UV radiation on autoimmune strains of mice: increased mortality and accelerated autoimmunity in BXSB male mice. J Invest Dermatol 1985, 85:181-186.
113. Menke J., Hsu M.Y., Byrne K.T., Lucas J.A., Rabacal W.A., Croker B.P., et al. Sunlight triggers cutaneous lupus through a CSF-1-dependent mechanism in MRL-Fas(lpr) mice. J Immunol 2008, 181:7367-7379.
114. Foltyn V.N., Golan T.D. In vitro ultraviolet irradiation induces pro-inflammatory responses in cells from premorbid SLE mice. Lupus 2001, 10:272-283.
115. Garden O.A., Pidduck H., Lakhani K.H., Walker D., Wood J.L., Batt R.M. Inheritance of gluten-sensitive enteropathy in Irish Setters. Am J Vet Res 2000, 61:462-468.
116. Bodinier M., Leroy M., Ah-Leung S., Blanc F., Tranquet O., Denery-Papini S., et al. Sensitization and elicitation of an allergic reaction to wheat gliadins in mice. J Agric Food Chem 2009, 57:1219-1225.
117. Maurano F., Mazzarella G., Luongo D., Stefanile R., D'Arienzo R., Rossi M., et al. Small intestinal enteropathy in non-obese diabetic mice fed a diet containing wheat. Diabetologia 2005, 48:931-937.
118. Verdu E.F., Huang X., Natividad J., Lu J., Blennerhassett P.A., David C.S., et al. Gliadin-dependent neuromuscular and epithelial secretory responses in gluten-sensitive HLA-DQ8 transgenic mice. Am J Physiol Gastrointest Liver Physiol 2008, 294:G217-G225.
119. von Herrath M., Nepom G.T. Animal models of human type 1 diabetes. Nat Immunol 2009, 10:129-132.