Autoimmunity and antibody affinity maturation are modulated by genetic variants on mouse chromosome 12

Journal of Autoimmunity

Volumn 58, Issue , 2015, Pages 90-99

  Collin, Roxanne ^a,b   Dugas, Véronique ^a,b,c   Chabot Roy, Geneviève ^a   Salem, David ^d   Zahn, Astrid ^e   Di Noia, Javier M ^b,e   Rauch, Joyce ^d   Lesage, Sylvie ^a,b  

^a MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c Cent de Recherche Informatique de Montreal   (Canada)

^d RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Affinity maturation; Autoantibodies; Autoimmune diabetes; NOD congenic mice; Systemic lupus erythematosus; Transgenic model

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; AUTOANTIBODY; AUTOANTIGEN; HEN EGG LYSOZYME; INSULIN; LYSOZYME;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY AFFINITY; ANTIBODY RESPONSE; ANTIGENIC MODULATION; ARTICLE; AUTOIMMUNITY; CHROMOSOME 12; CONGENIC STRAIN; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE SEVERITY; EPISTASIS; FEMALE; GENETIC VARIABILITY; GERMINAL CENTER; HUMORAL IMMUNITY; IMMUNIZATION; INCIDENCE; INSULITIS; MATURATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; TRANSGENE; ANIMAL; BIOSYNTHESIS; CHROMOSOME; DISEASE MODEL; GENE LOCUS; GENETICS; HUMAN; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; NONOBESE DIABETIC MOUSE; RAT; TRANSGENIC MOUSE;

ANIMALS; ANTIBODY AFFINITY; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; CHROMOSOMES, MAMMALIAN; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; GENETIC LOCI; GENETIC VARIATION; HUMANS; INSULIN; MICE; MICE, CONGENIC; MICE, INBRED NOD; MICE, TRANSGENIC; MURAMIDASE; RATS;

EID: 84930320445     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2015.01.007     Document Type: Article

References (41)

1. Maier L.M., Wicker L.S. Genetic susceptibility to type 1 diabetes. Curr Opin Immunol 2005, 17:601-608.
2. Wicker L.S., Clark J., Fraser H.I., Garner V.E., Gonzalez-Munoz A., Healy B., et al. Type 1 diabetes genes and pathways shared by humans and NOD mice. JAutoimmun 2005, 25(Suppl.):29-33.
3. Wallis R.H., Wang K., Marandi L., Hsieh E., Ning T., Chao G.Y., et al. Type 1 diabetes in the BB rat: a polygenic disease. Diabetes 2009, 58:1007-1017.
4. Anderson M.S., Bluestone J.A. THE NOD MOUSE: a model of immune dysregulation. Annu Rev Immunol 2005, 23:447-485.
5. Driver J.P., Serreze D.V., Chen Y.G. Mouse models for the study of autoimmune type 1 diabetes: a NOD to similarities and differences to human disease. Semin Immunopathol 2011, 33:67-87.
6. Wicker L.S., Todd J.A., Peterson L.B. Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 1995, 13:179-200.
7. Barrett J.C., Clayton D.G., Concannon P., Akolkar B., Cooper J.D., Erlich H.A., et al. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 2009, 41:703-707.
8. Consortium.WTCC Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007, 447:661-678.
9. Allen P.M., Matsueda G.R., Evans R.J., Dunbar J.B., Marshall G.R., Unanue E.R. Identification of the T-cell and Ia contact residues of a T-cell antigenic epitope. Nature 1987, 327:713-715.
10. Lesage S., Hartley S.B., Akkaraju S., Wilson J., Townsend M., Goodnow C.C. Failure to censor forbidden clones of CD4 T cells in autoimmune diabetes. JExp Med 2002, 196:1175-1188.
11. Liston A., Lesage S., Wilson J., Peltonen L., Goodnow C.C. Aire regulates negative selection of organ-specific T cells. Nat Immunol 2003, 4:350-354.
12. Zhang M., Vacchio M.S., Vistica B.P., Lesage S., Egwuagu C.E., Yu C.R., et al. Tcell tolerance to a neo-self antigen expressed by thymic epithelial cells: the soluble form is more effective than the membrane-bound form. JImmunol 2003, 170:3954-3962.
13. Liston A., Gray D.H., Lesage S., Fletcher A.L., Wilson J., Webster K.E., et al. Gene dosage-limiting role of aire in thymic expression, clonal deletion, and organ-specific autoimmunity. JExp Med 2004, 200:1015-1026.
14. Liston A., Lesage S., Gray D.H., O'Reilly L.A., Strasser A., Fahrer A.M., et al. Generalized resistance to thymic deletion in the NOD mouse; a polygenic trait characterized by defective induction of bim. Immunity 2004, 21:817-830.
15. Guimont-Desrochers F., Beauchamp C., Chabot-Roy G., Dugas V., Hillhouse E.E., Dusseault J., et al. Absence of CD47 invivo influences thymic dendritic cell subset proportions but not negative selection of thymocytes. Int Immunol 2009, 21:167-177.
16. Collin R., Dugas V., Pelletier A.N., Chabot-Roy G., Lesage S. The mouse Idd2 locus is linked to the proportion of immunoregulatory double-negative T Cells, a trait associated with autoimmune diabetes resistance. JImmunol 2014, 193:3503-3512.
17. Dugas V., Liston A., Hillhouse E.E., Collin R., Chabot-Roy G., Pelletier A.N., et al. Idd13 is involved in determining immunoregulatory DN T-cell number in NOD mice. Genes Immun 2014, 15:82-87.
18. Akkaraju S., Ho W.Y., Leong D., Canaan K., Davis M.M., Goodnow C.C. Arange of CD4 T cell tolerance: partial inactivation to organ-specific antigen allows nondestructive thyroiditis or insulitis. Immunity 1997, 7:255-271.
19. Podolin P.L., Pressey A., DeLarato N.H., Fischer P.A., Peterson L.B., Wicker L.S. I-E+ nonobese diabetic mice develop insulitis and diabetes. JExp Med 1993, 178:793-803.
20. Yu L., Robles D.T., Abiru N., Kaur P., Rewers M., Kelemen K., et al. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes. Proc Natl Acad Sci U S A 2000, 97:1701-1706.
21. Wenzlau J.M., Juhl K., Yu L., Moua O., Sarkar S.A., Gottlieb P., et al. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci U S A 2007, 104:17040-17045.
22. Steck A.K., Johnson K., Barriga K.J., Miao D., Yu L., Hutton J.C., et al. Age of islet autoantibody appearance and mean levels of insulin, but not GAD or IA-2 autoantibodies, predict age of diagnosis of type 1 diabetes: diabetes autoimmunity study in the young. Diabetes Care 2011, 34:1397-1399.
23. Achenbach P., Warncke K., Reiter J., Williams A.J., Ziegler A.G., Bingley P.J., et al. Type 1 diabetes risk assessment: improvement by follow-up measurements in young islet autoantibody-positive relatives. Diabetologia 2006, 49:2969-2976.
24. Greeley S.A., Katsumata M., Yu L., Eisenbarth G.S., Moore D.J., Goodarzi H., et al. Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nat Med 2002, 8:399-402.
25. Melanitou E., Devendra D., Liu E., Miao D., Eisenbarth G.S. Early and quantal (by litter) expression of insulin autoantibodies in the nonobese diabetic mice predict early diabetes onset. JImmunol 2004, 173:6603-6610.
26. Silva D.G., Daley S.R., Hogan J., Lee S.K., Teh C.E., Hu D.Y., et al. Anti-islet autoantibodies trigger autoimmune diabetes in the presence of an increased frequency of islet-reactive CD4 T cells. Diabetes 2011, 60:2102-2111.
27. Quintana F.J., Cohen I.R. Autoantibody patterns in diabetes-prone NOD mice and in standard C57BL/6 mice. JAutoimmun 2001, 17:191-197.
28. Rigby R.J., Rozzo S.J., Boyle J.J., Lewis M., Kotzin B.L., Vyse T.J. New loci from New Zealand black and New Zealand white mice on chromosomes 4 and 12 contribute to lupus-like disease in the context of BALB/c. JImmunol 2004, 172:4609-4617.
29. Wandstrat A., Wakeland E. The genetics of complex autoimmune diseases: non-MHC susceptibility genes. Nat Immunol 2001, 2:802-809.
30. Bonifacio E., Atkinson M., Eisenbarth G., Serreze D., Kay T.W., Lee-Chan E., et al. International workshop on lessons from animal models for human type 1 diabetes: identification of insulin but not glutamic acid decarboxylase or IA-2 as specific autoantigens of humoral autoimmunity in nonobese diabetic mice. Diabetes 2001, 50:2451-2458.
31. Burt R.A., Watkins L., Tan I.K.L., Wang N., Quirk F., Mackin L., et al. An NZW-derived interval on chromosome 7 moderates sialadenitis, but not insulitis in congenic nonobese diabetic mice. JImmunol 2009, 184:859-868.
32. Hillhouse E.E., Collin R., Chabot-Roy G., Guyon M.-J., Tessier N., Boulay M., et al. Nearby construction impedes the progression to overt autoimmune diabetes in NOD mice. JDiabetes Res 2013, 2013:1-7.
33. Martin R.M., Brady J.L., Lew A.M. The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. JImmunol Methods 1998, 212:187-192.
34. Zahn A., Daugan M., Safavi S., Godin D., Cheong C., Lamarre A., et al. Separation of function between isotype switching and affinity maturation invivo during acute immune responses and circulating autoantibodies in UNG-deficient mice. JImmunol 2013, 190:5949-5960.
35. Levine J.S., Subang R., Nasr S.H., Fournier S., Lajoie G., Wither J., et al. Immunization with an apoptotic cell-binding protein recapitulates the nephritis and sequential autoantibody emergence of systemic lupus erythematosus. JImmunol 2006, 177:6504-6516.
36. Wang N., Elso C.M., Mackin L., Mannering S.I., Strugnell R.A., Wijburg O.L., et al. Congenic mice reveal genetic epistasis and overlapping disease loci for autoimmune diabetes and listeriosis. Immunogenetics 2014, 66:501-506.
37. Carlborg O., Haley C.S. Epistasis: too often neglected in complex trait studies?. Nat Rev Genet 2004, 5:618-625.
38. Victora G.D., Nussenzweig M.C. Germinal centers. Annu Rev Immunol 2012, 30:429-457.
39. Damotte D., Colomb E., Cailleau C., Brousse N., Charreire J., Carnaud C. Analysis of susceptibility of NOD mice to spontaneous and experimentally induced thyroiditis. Eur J Immunol 1997, 27:2854-2862.
40. Lehuen A., Diana J., Zaccone P., Cooke A. Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol 2010, 10:501-513.
41. Tarasenko T., Kole H.K., Bolland S. Alupus-suppressor BALB/c locus restricts IgG2 autoantibodies without altering intrinsic B cell-tolerance mechanisms. JImmunol 2008, 180:3807-3814.