Exceptional Hyperthyroidism and a role for both major histocompatibility class I and class II genes in a murine model of graves' disease

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  McLachlan, Sandra M ^a   Aliesky, Holly A ^a   Chen, Chun Rong ^a   Williams, Robert W ^b   Rapoport, Basil ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; THYROID STIMULATING IMMUNOGLOBULIN; THYROTROPIN RECEPTOR; THYROTROPIN RECEPTOR ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENE MAPPING; GENETIC LINKAGE; GENETIC VARIABILITY; GRAVES DISEASE; HAPLOTYPE; HYPERTHYROIDISM; IMMUNIZATION; LINKAGE ANALYSIS; MOUSE; NONHUMAN; PROTEIN BINDING; QUANTITATIVE TRAIT LOCUS; THYROID HYPERPLASIA; ANIMAL; GENETICS; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; METABOLISM; PHYSIOLOGY;

ADENOVIRIDAE; MURINAE; MUS;

ANIMALS; FEMALE; GENETIC LINKAGE; GRAVES DISEASE; HYPERTHYROIDISM; IMMUNOGLOBULINS, THYROID-STIMULATING; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; QUANTITATIVE TRAIT LOCI; RECEPTORS, THYROTROPIN;

EID: 79959597818     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021378     Document Type: Article

References (42)

1. Jacobson EM, Tomer Y, (2007) The Genetic Basis of Thyroid Autoimmunity. Thyroid 17: 949-961.
2. Rapoport B, McLachlan SM, (2007) The thyrotropin receptor in Graves' disease. Thyroid 17: 911-922.
3. Todd JA, Acha-Orbea H, Bell JI, Chao N, Fronek Z, et al. (1988) A molecular basis for MHC Class II- associated autoimmunity. Science 240: 1003-1009.
4. Jacobson EM, Yang H, Menconi F, Wang R, Osman R, et al. (2009) Employing a recombinant HLA-DR3 expression system to dissect major histocompatibility complex II-thyroglobulin peptide dynamism: a genetic, biochemical, and reverse immunological perspective. J Biol Chem 284: 34231-34243.
5. Burton PR, Clayton DG, Cardon LR, Craddock N, Deloukas P, et al. (2007) Nat Genet 39: 1329-1337.
6. Stenszky V, Kozma L, Balazs C, Rochlitz S, Bear JC, et al. (1985) The genetics of Graves' disease: HLA and disease susceptibility. J Clin Endocrinol Metab 61: 735.
7. Simmonds MJ, Howson JM, Heward JM, Carr-Smith J, Franklyn JA, et al. (2007) A novel and major association of HLA-C in Graves' disease that eclipses the classical HLA-DRB1 effect. Hum Mol Genet 16: 2149-2153.
8. Nagayama Y, (2007) Graves' animal models of Graves' hyperthyroidism. Thyroid 17: 981-988.
9. Nagayama Y, McLachlan SM, Rapoport B, Niwa M, (2003) A major role for non-MHC genes, but not for micro-organisms, in a novel model of Graves' hyperthyroidism. Thyroid 13: 233-238.
10. McLachlan SM, Nagayama Y, Rapoport B, (2005) Insight into Graves' hyperthyroidism from animal models. Endocr Rev 26: 800-832.
11. Aliesky HA, Pichurin PN, Chen CR, Williams RW, Rapoport B, et al. (2006) Probing the genetic basis for thyrotropin receptor antibodies and hyperthyroidism in immunized CXB recombinant inbred mice. Endocrinol 147: 2789-2800.
12. McLachlan SM, Aliesky HA, Pichurin PN, Chen C-R, Williams RW, et al. (2008) Shared and unique susceptibility genes in a mouse model of Graves' disease determined in BXH and CXB recombinant inbred mice. Endocrinol 149: 2001-2009.
13. Williams RW, Gu L, Qi S, Lu L, (2001) The genetic structure of recombinant inbred mice: high-resolution consensus maps for complex trait analysis. Genome Biol 2: Research pp. 0046.1-0046.18.
14. Nagayama Y, Kita-Furuyama M, Ando T, Nakao K, Mizuguchi H, et al. (2002) A novel murine model of Graves' hyperthyroidism with intramuscular injection of adenovirus expressing the thyrotropin receptor. J Immunol 168: 2789-2794.
15. Chen CR, Aliesky H, Pichurin PN, Nagayama Y, McLachlan SM, et al. (2004) Susceptibility rather than resistance to hyperthyroidism is dominant in a thyrotropin receptor adenovirus-induced animal model of Graves' disease as revealed by BALB/c-C57BL/6 hybrid mice. Endocrinol 145: 4927-4933.
16. Rudikoff S, Claflin JL, (1976) Expression of equivalent clonotypes in BALB/c and A/J mice after immunization with phosphorylcholine. J Exp Med 144: 1294-1304.
17. Pisetsky DS, Sachs DH, (1977) The genetic control of the immune response to staphylococcal nuclease VI. Recombination between genes determining the A/J anti-nuclease idiotypes and the heavy chain allotype locus. J Exp Med 146: 1603-1612.
18. Semma M, Sakato N, Fujio H, Amano T, (1981) Idiotypic analysis of antibodies to hen egg-white lysozyme (HEL). II. Distribution and frequency of occurrence of idiotypes shared by A/J anti-HEL antibody. Immunol 42: 45-51.
19. Joshi MB, Gam AA, Boykins RA, Kumar S, Sacci J, et al. (2001) Immunogenicity of well-characterized synthetic Plasmodium falciparum multiple antigen peptide conjugates. Infect Immunol 69: 4884-4890.
20. Lozier JN, Tayebi N, Zhang P, (2005) Mapping of genes that control the antibody response to human factor IX in mice. Blood 105: 1029-1035.
21. Chen C-R, Pichurin P, Nagayama Y, Latrofa F, Rapoport B, et al. (2003) The thyrotropin receptor autoantigen in Graves' disease is the culprit as well as the victim. J Clin Invest 111: 1897-1904.
22. Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, et al. (2006) A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 4: e395.
23. Rapoport B, Williams RW, Chen C-R, McLachlan SM, (2010) Immunoglobulin heavy chain variable region genes contribute to the induction of thyroid stimulating antibodies in recombinant inbred mice. Genes Immun 3: 254-263.
24. Mayfield JA, Rine J, (2007) The genetic basis of variation in susceptibility to infection with Histoplasma capsulatum in the mouse. Genes Immun 8: 468-474.
25. Sanders J, Allen F, Jeffreys J, Bolton J, Richards T, et al. (2005) Characteristics of a monoclonal antibody to the thyrotropin receptor that acts as a powerful thyroid-stimulating autoantibody antagonist. Thyroid 15: 672-682.
26. Metcalfe R, Jordan N, Watson P, Gullu S, Wiltshire M, et al. (2002) Demonstration of immunoglobulin G, A, and E autoantibodies to the human thyrotropin receptor using flow cytometry. J Clin Endocrinol Metab 87: 1754-1761.
27. Morshed SA, Ando T, Latif R, Davies TF, (2010) Neutral antibodies to the TSH receptor are present in Graves' disease and regulate selective signaling cascades. Endocrinol 151: 5537-5549.
28. Schwarz-Lauer L, Pichurin PN, Chen C-R, Nagayama Y, Paras C, et al. (2003) The cysteine-rich amino terminus of the thyrotropin receptor is the immunodominant linear antibody epitope in mice immunized using naked DNA or adenovirus vectors. Endocrinol 144: 1718-1725.
29. Misharin A, Nagayama Y, Aliesky H, Mizutori Y, Rapoport B, et al. (2009) Attenuation of induced hyperthyroidism in mice by pre-treatment with thyrotropin receptor protein: diversion of thyroid stimulating antibody to non-functional antibody induction. Endocrinol 150: 3944-3952.
30. McLachlan SM, Lu L, Aliesky HA, Williams RW, Rapoport B, (2011) Distinct genetic signatures for variability in total and free serum thyroxine levels in four sets of recombinant inbred mice. Endocrinol 152: 1172-1179.
31. Traystman MD, Beisel KW, (1991) Genetic control of Coxsackievirus B3-induced heart-specific autoantibodies associated with chronic myocarditis. Clin Exp Immunol 86: 291-298.
32. Spindler KR, Welton AR, Lim ES, Duvvuru S, Althaus IW, et al. (2010) The major locus for mouse adenovirus susceptibility maps to genes of the hematopoietic cell surface-expressed LY6 family. J Immunol 184: 3055-3062.
33. Mallya M, Campbell RD, Aguado B, (2006) Characterization of the five novel Ly-6 superfamily members encoded in the MHC, and detection of cells expressing their potential ligands. Protein Sci 15: 2244-2256.
34. Ratanachaiyavong S, Demaine AG, Campbell RD, McGregor AM, (1991) Heat shock protein 70 (HSP70) and complement C4 genotypes in patients with hyperthyroid Graves' disease. Clin Exp Immunol 84: 48-52.
35. Heufelder AE, Goellner JR, Wenzel BE, Bahn RS, (1992) Immunohistochemical detection and localization of a 72-kilodalton heat shock protein in autoimmune thyroid disease. J Clin Endocrinol Metab 74: 724-731.
36. McGregor AM, (1992) Heat shock proteins and autoimmune thyroid disease; too hot to handle? J Clin Endocrinol Metab 74: 720-723.
37. Chen CR, Aliesky HA, Guo J, Rapoport B, McLachlan SM, (2006) Blockade of costimulation between T cells and antigen-presenting cells: an approach to suppress murine Graves' disease induced using thyrotropin receptor-expressing adenovirus. Thyroid 16: 427-434.
38. Mittereder N, March KL, Trapnell BC, (1996) Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J Virol 70: 7498-7509.
39. Chazenbalk GD, Jaume JC, McLachlan SM, Rapoport B, (1997) Engineering the human thyrotropin receptor ectodomain from a non-secreted form to a secreted, highly immunoreactive glycoprotein that neutralizes autoantibodies in Graves' patients' sera. J Biol Chem 272: 18959-18965.
40. Chazenbalk GD, Wang Y, Guo J, Hutchison JS, Segal D, et al. (1999) A mouse monoclonal antibody to a thyrotropin receptor ectodomain variant provides insight into the exquisite antigenic conformational requirement, epitopes and in vivo concentration of human autoantibodies. J Clin Endocrinol Metab 84: 702-710.
41. Churchill GA, Doerge RW, (1994) Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
42. Williams RW, Strom RC, Goldowitz D, (1998) Natural variation in neuron number in mice is linked to a major quantitative trait locus on Chr 11. J Neurosci 18: 138-146.