Genetics of susceptibility to chronic experimental encephalomyelitis and arthritis

Current Opinion in Immunology

Volumn 10, Issue 6, 1998, Pages 710-717

  Holmdahl, Rikard ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIC ENCEPHALOMYELITIS; ANIMAL MODEL; ARTHRITIS; CHROMOSOME 3; CHROMOSOME 4; GENETIC SUSCEPTIBILITY; MOUSE; MULTIFACTORIAL INHERITANCE; MULTIPLE SCLEROSIS; NONHUMAN; RAT; REVIEW;

EID: 0032401766     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(98)80093-9     Document Type: Article

References (62)

1. Ebers GC, Sadovnick AD, Risch NJ, Group CCS. A genetic basis for familial aggregation in multiple sclerosis. Nature. 377:1995;150-151.
2. Sawcer S, Jones HB, Feakes R, Gray J, Smaldon N, Chataway J, Robertson N, Clayton D, Goodfellow PN, Compston A. A genome screen in multiple sclerosis reveals susceptibility loci on chromosome 6p21 and 17q22. Nat Genet. 13:1996;464-468.
3. Ebers GC, Kukay K, Bulman DE, Sadovnick AD, Rice G, Anderson C, Armstrong H, Cousin K, Bell RB, Hader W, et al. A full genome search in multiple sclerosis. Nat Genet. 13:1996;472-476.
4. Holmdahl R, Jirholt J, Jansson L, Sundvall M. Genetic analysis of murine models for multiple sclerosis. Dragani TA. human polygenic diseases: animal models. 1998;131-146 Harwood Academic Publishers, Amsterdam.
5. Holmdahl R, Carlsen S, Mikulowska A, Vestberg M, Brunsberg U, Hansson A-S, Sundvall M, Jansson L, Pettersson U. Genetic analysis of murine models for rheumatoid arthritis. Adolpho KW. human genome methods. 1998;215-238 CRC press, New York.
6. Monteyne P, Bureau JF, Brahic M. The infection of mouse by Theiler's virus: from genetics to immunology. Immunol Rev. 159:1997;163-176.
7. Fritz RB, Skeen MJ, Chou CHJ, Garcia M, Egorov IK. Major histocompatibility complex-linked control of the murine immune response to myelin basic protein. J Immunol. 134:1985;2328-2332.
8. Lorentzen JC, Andersson M, Issazadeh S, Dahlman I, Luthman H, Weissert R, Olsson T. Genetic analysis of inflammation, cytokine mRNA expression and disease course of relapsing experimental autoimmune encephalomyelitis in DA rats. of special interest J Neuroimmunol. 80:1997;31-37 The authors provide a comparison of the susceptibility to the EAE that is induced by spinal-chord homogenate in different rat strains (DA, BN, PVG and LEW as well as DA MHC-congenic strains). High disease incidence, and lack of cells secreting transforming growth factor β and IL-10 in the CNS, were found to be associated with the RT1av1 MHC haplotype.
9. Kjellén P, Issazadeh S, Olsson T, Holmdahl R. Genetic influence on disease course and cytokine response in relapsing experimental allergic encephalomyelitis. of special interest Int Immunol. 10:1998;333-340 This reports a comparison of DA MHC-congenic strains and shows that the MHC region is associated with susceptibility to the relapsing EAE that is induced by homologous spinal cord homogenate. In addition, analysis of DA × E3 recombinant inbred strains show a strong influence by genes outside the MHC not only in controlling disease susceptibility but also in the secretion of transforming growth factor β, IFN-γ and IL-10.
10. Fritz RB, Zhao ML. Thymic expression of myelin basic protein (MBP). Activation of MBP-specific T cells by thymic cells in the absence of exogenous MBP. J Immunol. 157:1996;5249-5253.
11. Mustafa M, Vingsbo C, Olsson T, Issazadeh S, Ljungdahl Å, Holmdahl R. Protective influences on experimental autoimmune encephalomyelitis by MHC class I and class II alleles. J Immunol. 153:1994;3337-3344.
12. Mustafa M, Vingsbo C, Olsson T, Ljungdahl A, Höjeberg B, Holmdahl R. The major histocompatibility complex influences myelin basic protein 63-88-induced T cell cytokine profile and experimental autoimmune encephalomyelitis. Eur J Immunol. 23:1993;3089-3095.
13. Issazadeh S, Kjellén P, Olsson T, Mustafa M, Holmdahl R. Major histocompatibility complex-controlled protective influences on experimental autoimmune encephalomyelitis are peptide specific. of special interest Eur J Immunol. 27:1997;1584-1587 Here is shown that the previously described protective effects of the MHC haplotypes RT1u and RT1n are specific for peptides derived from myelin basic protein and correlate with cytokine (IL-4, IL-10 and transforming growth factor β) responses.
14. Sundvall M, Jirholt J, Yang H-T, Jansson L, Engström Å, Pettersson U, Holmdahl R. Identification of murine loci associated with susceptibility to chronic experimental autoimmune encephalomyelitis. Nat Genet. 10:1995;313-317.
15. Encinas JA, Lees MB, Sobel RA, Symonowicz C, Greer JM, Shovlin CL, Weiner HL, Seidman CE, Seidman JG, Kuchroo VK. Genetic analysis of susceptibility to experimental autoimmune encephalomyelitis in a cross between SJL/J and B10.S mice. J Immunol. 157:1996;2186-2192.
16. Baker D, Rosenwasser OA, O'Neill JK, Turk JL. Genetic analysis of experimental allergic encephalomyelitis in mice. J Immunol. 155:1995;4046-4051.
17. Croxford JL, O'Neill JK, Baker D. Polygenic control of experimental allergic encephalomyelitis in Biozzi ABH and BALB/c mice. of special interest J Neuroimmunol. 74:1997;205-211 This is a genome screen of the EAE susceptibility of an F2 intercross between the susceptible ABH and the resistant Balb/c strains. No loci reached significance but a suggestive linkage was found if loci on chromosomes 4, 8 and 17 were combined - indicating complex genetics with gene interactions.
18. Teuscher C, Hickey WF, Grafer CM, Tung KS. A common immunoregulatory locus controls susceptibility to actively induced experimental allergic encephalomyelitis and experimental allergic orchitis in BALB/c mice. of special interest J Immunol. 160:1998;2751-2756 In this paper, the number of loci controlling the EAE susceptibility difference between Balb/cJ and Balb/cByJ strains is analysed. In order to do this, the susceptibility to disease of litters derived from back-cross mice was compared. It is concluded that only one recessive locus accounts for the difference in disease susceptibility between the strains; most probably, one of the substrains has acquired a mutation in an essential gene.
19. Lander ES, Kruglyak L. Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet. 11:1996;241-247.
20. Beebe AM, Mauze S, Schork NJ, Coffman RL. Serial backcross mapping of multiple loci associated with resistance to Leishmania major in mice. Immunity. 6:1997;551-557.
21. Teuscher C, Rhein DM, Livingstone KD, Paynter RA, Doerge RW, Nicholson SM, Melvold RW. Evidence that Tmevd2 and eae3 may represent either a common locus or members of a gene complex controlling susceptibility to immunologically mediated demyelination in mice. of outstanding interest J Immunol. 159:1997;4930-4934 This paper describes a back-cross analysis of TMEVD susceptibility in DBA/2J (susceptible) and Balb/cByJ (resistant) strains. The back-cross was made to the resistant Balb/cByJ strain. A previously reported linkage to chromosome 17 (that contains the MHC) was reproduced. The strongest locus association was found on chromosome 6 (Tmevd2, logarithmic odds ratio [LOD] 3.6 with a dominant inheritance pattern). This was suggested to be located in a 6 cM fragment that correlates with the Eae3 and Mcia2 loci.
22. Podolin PL, Denny P, Lord CJ, Hill NJ, Todd JA, Peterson LB, Wicker LS, Lyons PA. Congenic mapping of the insulin-dependent diabetes (Idd) gene, Idd10, localizes two genes mediating the Idd10 effect and eliminates the candidate Fcgr1. J Immunol. 159:1997;1835-1843.
23. Jirholt J, Cook A, Sundvall M, Emazion T, Jansson L, Pettersson U, Holmdahl R. Evidence for a susceptibility locus to collagen induced arthritis on mouse chromosome 3: a common susceptibility locus in multiple autoimmune disorders. of outstanding interest Eur J Immunol. 1998; This provides the first near-complete genome screen of CIA in the mouse, using an F2 intercross between the susceptible B10RIII and the resistant RIIIS/J strains. The only significant locus identified (Mcia2) was located to chromosome 3, in close proximity to the previously identified Eae3 locus that controls CREAE. Serial back-cross analysis identified a congenic fragment containing the gene. Within this fragment lie other autoimmune disease loci that control TMEVD (Tmevd2) and diabetes (Idd17 and Idd10).
24. Dahlman I, Lorentzen JC, de Graaf KL, Stefferl A, Linington C, Olsson T. Quantitative trait loci disposing for both experimental arthritis and encephalomyelitis in the DA rat; impact on severity of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis and antibody isotype pattern. of outstanding interest Eur J Immunol. 28:1998;2188-2196 The authors provide selected analysis of the previously defined Cia2, Cia3 and Oia2 loci for linkage to MOG-induced EAE in an F2 intercross between DA and PVG.RT1A rats. Markers within the Cia3 locus at chromosome 4 were found to control survival time, suggesting that the presence of a gene that could control both arthritis and EAE. In addition, a closely located marker was significantly associated with an IgG2c anti-MOG response. Interestingly, no effect was seen on the IgG2b response, which is often connected to an IgG2c response, indicating a gene which more specifically controls IgG2c regulation. No disease associations were found to markers within Cia2 or Oia2; however, Oia2 was found to be associated with an IgG1 and IgE anti-MOG response, suggesting that there is a gene within the Oia2 locus on chromosome 4 which is important for the Th1/Th2 cell balance.
25. Kuokkanen S, Sundvall M, Terwilliger JD, Tienari PJ, Wikström J, Holmdahl R, Pettersson U, Peltonen L. A putative vulnerability locus to multiple sclerosis maps to 5p14-p12 in a region syntenic to the murine locus Eae2. Nat Genet. 13:1996;477-480.
26. Rodriguez M, Patick AK, Pease LR, David CS. Role of T cell receptor V beta genes in Theiler's virus-induced demyelination of mice. J Immunol. 148:1992;921-927.
27. Rodriguez M, Leibowitz J, David CS. Susceptibility to Theiler's virus-induced demyelination. Mapping of the gene within the H-2D region. J Exp Med. 163:1986;620-631.
28. Bureau JF, Montagutelli X, Bihl F, Lefebvre S, Guenet JL, Brahic M. Mapping loci influencing the persistence of Theiler's virus in the murine central nervous system. Nat Genet. 5:1993;87-91.
29. Bureau JF, Drescher KM, Pease LR, Vikoren T, Delcroix M, Zoecklein L, Brahic M, Rodriguez M. Chromosome 14 contains determinants that regulate susceptibility to Theiler's virus-induced demyelination in the mouse. of special interest Genetics. 148:1998;1941-1949 This reports on a partial genome scan of an F2 intercross between DBA/2 (susceptible) and B10.D2 (resistant) strains for susceptibility to TMEVD. A suggestive locus on chromosome 14 is identified.
30. Tienari PJ, Kuokkanen S, Pastinen T, Wikström J, Sajantila A, Sandberg-Wollheim M, Palo J, Peltonen L. Golli-MBP gene in multiple sclerosis susceptibility. J Neuroimmunol. 81:1998;158-167.
31. Wooley PH, Luthra HS, Stuart JM, David CS. Type II collagen induced arthritis in mice. I. Major histocompatibility complex (I-region) linkage and antibody correlates. J Exp Med. 154:1981;688-700.
32. Brunsberg U, Gustafsson K, Jansson L, Michaëlsson E, Ährlund-Richter L, Pettersson S, Mattsson R, Holmdahl R. Expression of a transgenic class II Ab gene confers susceptibility to collagen-induced arthritis. Eur J Immunol. 24:1994;1698-1702.
33. Rosloniec EF, Brand DD, Myers LK, Whittington KB, Gumanovskaya M, Zaller DM, Woods A, Altmann DM, Stuart JM, Kang AH. An HLA-DR1 transgene confers susceptibility to collagen-induced arthritis elicited with human type II collagen. J Exp Med. 185:1997;1113-1122.
34. Andersson EC, Hansen BE, Jacobsen H, Madsen LS, Andersen CB, Engberg J, Rothbard JB, Sönderstrup-McDevitt G, Malmström V, Holmdahl R, et al. Definition of MHC and T cell receptor contacts in the HLA-DR4 restricted immunodominant epitope in type II collagen and characterization of collagen-induced arthritis in HLA-DR4 and human CD4 transgenic mice. Proc Natl Acad Sci USA. 95:1998;7574-7579.
35. Zanelli E, Krco CJ, David CS. Critical residues on HLA-DRB1*0402 HV3 peptide for HLA-DQ8-restricted immunogenicity: implications for rheumatoid arthritis predisposition. J Immunol. 158:1997;3545-3551.
36. Nabozny GH, Bull MJ, Hanson J, Griffiths MM, Luthra HS, David CS. Collagen-induced arthritis in T cell receptor Vβ congenic B10.Q mice. J Exp Med. 180:1994;517-524.
37. Nabozny GH, Hanson J, Griffiths MM, Luthra HS, David CS. Altered development of collagen induced arthritis in T cell receptor V beta congenic B10.RIII mice. Autoimmunity. 20:1995;51-58.
38. Andersson M, Goldschmidt TJ, Michaëlsson E, Larsson A, Holmdahl R. T cell receptor Vβ haplotype and complement C5 play no significant role for the resistance to collagen induced arthritis in the SWR mouse. Immunology. 73:1991;191-196.
39. Spinella DG, Jeffers JR, Reife RA, Stuart JM. The role of C5 and T-cell receptor Vb genes in susceptibility to collagen induced arthritis. Immunogenetics. 34:1991;23-27.
40. Banerjee S, Anderson GD, Luthra HS, David CS. Influence of complement C5 and Vβ T cell receptor mutations on susceptibility to collagen-induced arthritis in mice. J Immunol. 142:1989;2237-2243.
41. Mori L, de Libero G. Genetic control of susceptibility to collagen-induced arthritis in T cell receptor β-chain transgenic mice. of special interest Arthritis Rheum. 41:1998;256-262 This investigation aimed to confirm the hypothesis that the lack of complement component C5 in the SWR mouse strain protects against development of CIA. A highly significant linkage was found to a region on chromosome 2 - containing the gene for C5 - in a cross between SWR and DBA/1 strains.
42. Jansson L, Holmdahl R. Genes on the X chromosome affect development of collagen-induced arthritis in mice. Clin Exp Immunol. 94:1993;459-465.
43. Jansson L, Holmdahl R. The Y chromosome-linked "autoimmune accelerating" yaa gene suppresses collagen-induced arthritis. Eur J Immunol. 24:1994;1213-1217.
44. Vidal S, Kono DH, Theofilopoulos AN. Loci predisposing to autoimmunity in MRL-Fas lpr and C57BL/6-Faslpr mice. of special interest J Clin Invest. 101:1998;696-702 In this paper, an F2 cross between B6-lpr and MRL-lpr strains is analysed for genetic control of glomerulonephritis, lymphomegali and arthritis. No significant loci controlling arthritis were found but a weakly suggestive locus was found on chromosome 10.
45. Remmers EF, Longman RE, Du Y, O'Hare A, Cannon GW, Griffiths MM, Wilder RL. A genome scan localizes five non-MHC loci controlling collagen-induced arthritis in rats. Nat Genet. 14:1996;82-85.
46. Jacob HJ, Pettersson A, Wilson D, Mao Y, Lernmark A, Lander ES. Genetic dissection of autoimmune type I diabetes in the BB rat. Nat Genet. 2:1992;56-60.
47. Holmdahl R, Goldschmidt TJ, Kleinau S, Kvick C, Jonsson R. Arthritis induced in rats with adjuvant oil is a genetically restricted, alpha beta T-cell dependent autoimmune disease. Immunology. 76:1992;197-202.
48. Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol. 149:1996;1675-1683.
49. Lorentzen JC, Glaser A, Jacobsson L, Galli J, Fakhrai-Rad H, Klareskog L, Luthman H. Identification of rat susceptibility loci for adjuvant-oil induced arthritis. of outstanding interest Proc Natl Acad Sci USA. 95:1998;6383-6387 This describes the identification of two highly significant QTLs associated with the OIA induced in an F2 intercross between DA (susceptible) and LEW.1AV1 (resistant) strains. The strains have identical MHC regions. It was thus not possible to analyse the earlier suggestion that MHC is associated with OIA. The strongest locus that is associated (Oia2) is located on chromosome 4 but in a different region than the previously identified Cia3. The NK region (i.e. a region containing genes for several NK cell receptors) is suggested to contain the candidate gene since the DA strain is known to have defective alloreactive NK cell function. Another locus on chromosome 10 (Oia3) correlated closely to the Cia5 locus that was shown to control CIA in a cross between DA and F344 strains.
50. Vingsbo-Lundberg C, Nordquist N, Olofsson P, Sundvall M, Saxne T, Pettersson U, Holmdahl R. Genetic control of arthritis onset, severity and chronicity in a model for rheumatoid arthritis. Nat Genet. 1998;. in press.
51. Morel L, Mohan C, Yu Y, Croker BP, Tian N, Deng A, Wakeland EK. Functional dissection of systemic lupus erythematosus using congenic mouse strains. J Immunol. 158:1997;6019-6028.
52. Haines JL, Pericak-Vance MA, Seboun E, Hauser SL, Ter-Minassian M, Bazyk A, Gusella JF, Kim DJ, Terwedow H, Rimmler JB, et al. A complete genomic screen for multiple sclerosis underscores a role for the major histocompatibility complex. Nat Genet. 13:1996;469-471.
53. Sabelko KA, Kelly KA, Nahm MH, Cross AH, Russell JH. Fas and Fas ligand enhance the pathogenesis of experimental allergic encephalomyelitis, but are not essential for immune privilege in the central nervous system. of special interest J Immunol. 159:1997;3096-3099 In this study defective genes for Fas and Fas ligand, back-crossed into B10 mice, decrease rather than enhance the susceptibility to EAE. The interpretation of this is not straightforward but it could be due to interacting genes or it could be that Fas interactions are not of crucial importance for immune tolerance to central nervous system antigens.
54. Watanabe-Fukunaga R, Brannan C, Copeland N, Jenkins N, Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 356:1992;314-317.
55. Nicholson SM, Jokinen DM, Dal Canto MC, Kim BS, Melvold RW. Genetic analysis of susceptibility to Theiler's murine encephalomyelitis virus-induced demyelinating disease in the SWR strain. J Neuroimmunol. 59:1995;19-28.
56. Melvold RW, Jokinen DM, Miller SD, Dal Canto MC, Lipton HL. Identification of a locus on mouse chromosome 3 involved in differential susceptibility to Theiler's murine encephalomyelitis virus-induced demyelinating disease. J Virol. 64:1990;686-690.
57. Melvold RW, Jokinen DM, Knobler RL, Lipton HL. Variations in genetic control of susceptibility to Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. I. Differences between susceptible SJL/J and resistant BALB/c strains map near the T cell beta-chain constant gene on chromosome 6. J Immunol. 138:1987;1429-1433.
58. Bahk YY, Kappel CA, Rasmussen G, Kim BS. Association between susceptibility to Theiler's virus-induced demyelination and T-cell receptor Jbeta1-Cbeta1 polymorphism rather than Vbeta deletion. of outstanding interest J Virol. 71:1997;4181-4185 Here a genetic influence by TCRV genes on the susceptibility to TMEVD is excluded by comparisons between the SJL and C57L strains. These are polymorphic at the TCR-JCB locus but not the TCRVB locus. Gene segregation experiments indicate a susceptible gene close to the TCRB region excluding a genetic influence by TCRV genes. No linkage was seen to the TCRA locus.
59. Holmdahl R, Vingsbo C, Hedrich H, Karlsson M, Kvick C, Goldschmidt TJ, Gustafsson K. Homologous collagen-induced arthritis in rats and mice are associated with structurally different major histocompatibility complex DQ-like molecules. Eur J Immunol. 22:1992;419-424.
60. Murphy ED, Roths JD. A Y chromosome associated factor in strain BXSB producing accelerated autoimmunity and lymphoproliferation. Arthritis Rheum. 22:1979;1188-1194.
61. Pettersson A, Wilson D, Daniels T, Tobin S, Jacob HJ, Lander ES, Lernmark A. Thyroiditis in the BB rat is associated with lymphopenia but occurs independently of diabetes. J Autoimmun. 8:1995;493-505.
62. Butterfield RJ, Sudweeks JD, Blankenhorn EP, Korngold R, Marini JC, Todd JA, Roper RJ, Teuscher C. New genetic loci that control susceptibility and symptoms of experimental allergic encephalomyelitis in inbred mice. J Immunol. 161:1998;1860-1867.