The magnitude and encephalogenic potential of autoimmune response to MOG is enhanced in MOG deficient mice

Journal of Autoimmunity

Volumn 21, Issue 4, 2003, Pages 339-351

  Liñares, David ^a,b   Mañá, Paula ^a,b   Goodyear, Melinda ^a   Chow, Anne M ^a   Clavarino, Chelsea ^a   Huntington, Nicholas D ^a,c   Barnett, Louise ^c   Koentgen, Frank ^d   Tomioka, Ryo ^e   Bernard, Claude C A ^a   Freire Garabal, Manuel ^b   Reid, Hugh H ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d Ozgene Pty Ltd   (Australia)

^e SAITAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

EAE; MOG; MS; Myelin; Tolerance

Indexed keywords

EPITOPE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EFFECTOR CELL; FEMALE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; SPECIES COMPARISON; TH1 CELL; WILD TYPE;

EID: 0242659140     PISSN: 08968411     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaut.2003.09.001     Document Type: Article

References (69)

1. Mondino A., Khoruts A., Jenkins M.K. The anatomy of T-cell activation and tolerance. Proc Natl Acad Sci U S A. 93:1996;2245-2252.
2. Sebzda E., Mariathasan S., Ohteki T., Jones R., Bachmann M.F., Ohashi P.S. Selection of the T cell repertoire. Annu Rev Immunol. 17:1999;829-874.
3. Miller J.F., Basten A. Mechanisms of tolerance to self. Curr Opin Immunol. 8:1996;815-821.
4. Schluesener H.J., Wekerle H. Autoaggressive T lymphocyte lines recognizing the encephalitogenic region of myelin basic protein: in vitro selection from unprimed rat T lymphocyte populations. J Immunol. 135:1985;3128-3133.
5. Van Parijs L., Abbas A.K. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science. 280:1998;243-248.
6. Seddon B., Mason D. The third function of the thymus. Immunol Today. 21:2000;95-99.
7. Campagnoni A.T., Pribyl T.M., Campagnoni C.W., Kampf K., Amur-Umarjee S., Landry C.F., et al. Structure and developmental regulation of Golli-mbp, a 105-kilobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain. J Biol Chem. 268:1993;4930-4938.
8. Fritz R.B., Kalvakolanu I. Thymic expression of the golli-myelin basic protein gene in the SJL/J mouse. J Neuroimmunol. 57:1995;93-99.
9. MacKenzie-Graham A.J., Pribyl T.M., Kim S., Porter V.R., Campagnoni A.T., Voskuhl R.R. Myelin protein expression is increased in lymph nodes of mice with relapsing experimental autoimmune encephalomyelitis. J Immunol. 159:1997;4602-4610.
10. Kalwy S., Marty M.C., Bausero P., Pessac B. Myelin basic protein-related proteins in mouse brain and immune tissues. J Neurochem. 70:1998;435-438.
11. Pribyl T.M., Campagnoni C.W., Kampf K., Kashima T., Handley V.W., McMahon J., et al. The human myelin basic protein gene is included within a 179-kilobase transcription unit: expression in the immune and central nervous systems. Proc Natl Acad SciUSA. 90:1993;10695-10699.
12. Pribyl T.M., Campagnoni C., Kampf K., Handley V.W., Campagnoni A.T. The major myelin protein genes are expressed in the human thymus. J Neurosci Res. 45:1996;812-819.
13. Mor F., Boccaccio G.L., Unger T. Expression of autoimmune disease-related antigens by cells of the immune system. J Neurosci Res. 54:1998;254-262.
14. Liu H., MacKenzie-Graham A.J., Palaszynski K., Liva S., Voskuhl R.R. "Classic" myelin basic proteins are expressed in lymphoid tissue macrophages. J Neuroimmunol. 116:2001;83-93.
15. Klein L., Klugmann M., Nave K.A., Tuohy V.K., Kyewski B. Shaping of the autoreactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat Med. 6:2000;56-61.
16. Pribyl T.M., Campagnoni C.W., Kampf K., Kashima T., Handley V.W., McMahon J., et al. Expression of the myelin proteolipid protein gene in the human fetal thymus. J Neuroimmunol. 67:1996;125-130.
17. Bruno R., Sabater L., Sospedra M., Ferrer-Francesch X., Escudero D., Martinez-Caceres E., et al. Multiple sclerosis candidate autoantigens except myelin oligodendrocyte glycoprotein are transcribed in human thymus. Eur J Immunol. 32:2002;2737-2747.
18. Derbinski J., Schulte A., Kyewski B., Klein L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat Immunol. 2:2001;1032-1039.
19. Gold R., Hartung H.P., Toyka K.V. Animal models for autoimmune demyelinating disorders of the nervous system. Mol Med Today. 6:2000;88-91.
20. Fritz R.B., Chou C.H., McFarlin D.E. Relapsing murine experimental allergic encephalomyelitis induced by myelin basic protein. J Immunol. 130:1983;1024-1026.
21. Tuohy V.K., Lu Z.J., Sobel R.A., Laursen R.A., Lees M.B. A synthetic peptide from myelin proteolipid protein induces experimental allergic encephalomyelitis. J Immunol. 141:1988;1126-1130.
22. Amor S., Groome N., Linington C., Morris M.M., Dornmair K., Gardinier M.V., et al. Identification of epitopes of myelin oligodendrocyte glycoprotein for the induction of experimental allergic encephalomyelitis in SJL and Biozzi AB/H mice. J Immunol. 153:1994;4349-4356.
23. Linington C., Bradl M., Lassmann H., Brunner C., Vass K. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am J Pathol. 130:1988;443-454.
24. Kerlero de Rosbo N., Mendel I., Ben-Nun A. Chronic relapsing experimental autoimmune encephalomyelitis with a delayed onset and an atypical clinical course, induced in PL/J mice by myelin oligodendrocyte glycoprotein (MOG)-derived peptide: preliminary analysis of MOG T cell epitopes. Eur J Immunol. 25:1995;985-993.
25. Mokhtarian F., Zhang Z., Shi Y., Gonzales E., Sobel R.A. Molecular mimicry between a viral peptide and a myelin oligodendrocyte glycoprotein peptide induces autoimmune demyelinating disease in mice. J Neuroimmunol. 95:1999;43-54.
26. Stefferl A., Schubart A., Storch M., Amini A., Mather I., Lassmann H., et al. Butyrophilin, a milk protein, modulates the encephalitogenic T cell response to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis. J Immunol. 165:2000;2859-2865.
27. Linnington C., Webb M., Woodhams P.L. A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J Neuroimmunol. 6:1984;387-396.
28. Barnett L.D., Kontgen F. Gene targeting in a centralized facility. Methods Mol Biol. 158:2001;65-82.
29. Norton W.T., Poduslo S.E. Myelination in rat brain: method of myelin isolation. J Neurochem. 21:1973;749-757.
30. Mendel I., Kerlero de Rosbo N., Ben-Nun A. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: fine specificity and T cell receptor V beta expression of encephalitogenic T cells. Eur J Immunol. 25:1995;1951-1959.
31. Harrington C.J., Paez A., Hunkapiller T., Mannikko V., Brabb T., Ahearn M., et al. Differential tolerance is induced in T cells recognizing distinct epitopes of myelin basic protein. Immunity. 8:1998;571-580.
32. Espejo C., Carrasco J., Hidalgo J., Penkowa M., Garcia A., Saez-Torres I., et al. Differential expression of metallothioneins in the CNS of mice with experimental autoimmune encephalomyelitis. Neuroscience. 105:2001;1055-1065.
33. Gately M.K., Renzetti L.M., Magram J., Stern A.S., Adorini L., Gubler U., et al. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol. 16:1998;495-521.
34. Kuchroo V.K., Anderson A.C., Waldner H., Munder M., Bettelli E., Nicholson L.B. T cell response in experimental autoimmune encephalomyelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu Rev Immunol. 20:2002;101-123.
35. Sun D., Whitaker J.N., Huang Z., Liu D., Coleclough C., Wekerle H., et al. Myelin antigen-specific CD8+ T cells are encephalitogenic and produce severe disease in C57BL/6 mice. J Immunol. 166:2001;7579-7587.
36. Huseby E.S., Liggitt D., Brabb T., Schnabel B., Ohlen C., Goverman J. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J Exp Med. 194:2001;669-676.
37. Huseby E.S., Ohlen C., Goverman J. Cutting edge: myelin basic protein-specific cytotoxic T cell tolerance is maintained in vivo by a single dominant epitope in H-2k mice. J Immunol. 163:1999;1115-1118.
38. Baker D., O'Neill J.K., Gschmeissner S.E., Wilcox C.E., Butter C., Turk J.L. Induction of chronic relapsing experimental allergic encephalomyelitis in Biozzi mice. J Neuroimmunol. 28:1990;261-270.
39. Mattner F., Smiroldo S., Galbiati F., Muller M., Di Lucia P., Poliani P.L., et al. Inhibition of Th1 development and treatment of chronic-relapsing experimental allergic encephalomyelitis by a non-hypercalcemic analogue of 1,25-dihydroxyvitamin D(3). Eur J Immunol. 30:2000;498-508.
40. Morris-Downes M.M., Smith P.A., Rundle J.L., Piddlesden S.J., Baker D., Pham-Dinh D., et al. Pathological and regulatory effects of anti-myelin antibodies in experimental allergic encephalomyelitis in mice. J Neuroimmunol. 125:2002;114-124.
41. Iglesias A., Bauer J., Litzenburger T., Schubart A., Linington C. T- and B-cell responses to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis and multiple sclerosis. Glia. 36:2001;220-234.
42. Amiguet P., Gardinier M.V., Zanetta J.P., Matthieu J.M. Purification and partial structural and functional characterization of mouse myelin/ oligodendrocyte glycoprotein. J Neurochem. 58:1992;1676-1682.
43. Scolding N.J., Frith S., Linington C., Morgan B.P., Campbell A.K., Compston D.A. Myelin-oligodendrocyte glycoprotein (MOG) is a surface marker of oligodendrocyte maturation. J Neuroimmunol. 22:1989;169-176.
44. Brunner C., Lassmann H., Waehneldt T.V., Matthieu J.M., Linington C. Differential ultrastructural localization of myelin basic protein, myelin/oligodendroglial glycoprotein, and 2′,3′-cyclic nucleotide 3′-phosphodiesterase in the CNS of adult rats. J Neurochem. 52:1989;296-304.
45. Matthieu J.M., Amiguet P. Myelin/oligodendrocyte glycoprotein expression during development in normal and myelin-deficient mice. Dev Neurosci. 12:1990;293-302.
46. Stoffel W., Boison D., Bussow H. Functional analysis in vivo of the double mutant mouse deficient in both proteolipid protein (PLP) and myelin basic protein (MBP) in the central nervous system. Cell Tissue Res. 289:1997;195-206.
47. de Rosbo N.K., Ben-Nun A. T-cell responses to myelin antigens in multiple sclerosis; relevance of the predominant autoimmune reactivity to myelin oligodendrocyte glycoprotein. J Autoimmun. 11:1998;287-299.
48. von Budingen H.C., Tanuma N., Villoslada P., Ouallet J.C., Hauser S.L., Genain C.P. Immune responses against the myelin/oligodendrocyte glycoprotein in experimental autoimmune demyelination. J Clin Immunol. 21:2001;155-170.
49. Lyons J.A., San M., Happ M.P., Cross A.H. B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. Eur J Immunol. 29:1999;3432-3439.
50. Mendel Kerlero de Rosbo N., Ben-Nun A. Delineation of the minimal encephalitogenic epitope within the immunodominant region of myelin oligodendrocyte glycoprotein: diverse V beta gene usage by T cells recognizing the core epitope encephalitogenic for T cell receptor V beta b and T cell receptor V beta a H-2b mice. Eur J Immunol. 26:1996;2470-2479.
51. Yoshizawa I., Bronson R., Dorf M.E., Abromson-Leeman S. T-cell responses to myelin basic protein in normal and MBP-deficient mice. J Neuroimmunol. 84:1998;131-138.
52. Targoni O.S., Lehmann P.V. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J Exp Med. 187:1998;2055-2063.
53. Anderson A.C., Nicholson L.B., Legge K.L., Turchin V., Zaghouani H., Kuchroo V.K. High frequency of autoreactive myelin proteolipid protein-specific T cells in the periphery of naive mice: mechanisms of selection of the self-reactive repertoire. J Exp Med. 191:2000;761-770.
54. Ignatowicz L., Rees W., Pacholczyk R., Ignatowicz H., Kushnir E., Kappler J., et al. T cells can be activated by peptides that are unrelated in sequence to their selecting peptide. Immunity. 7:1997;179-186.
55. Klein L., Kyewski B. Self-antigen presentation by thymic stromal cells: a subtle division of labor. Curr Opin Immunol. 12:2000;179-186.
56. Anderson G., Moore N.C., Owen J.J., Jenkinson E.J. Cellular interactions in thymocyte development. Annu Rev Immunol. 14:1996;73-99.
57. Hanahan D. Peripheral-antigen-expressing cells in thymic medulla: factors in self-tolerance and autoimmunity. Curr Opin Immunol. 10:1998;656-662.
58. Kishimoto H., Sprent J. Negative selection in the thymus includes semimature T cells. J Exp Med. 185:1997;263-271.
59. Klein L., Klein T., Ruther U., Kyewski B. CD4 T cell tolerance to human C-reactive protein, an inducible serum protein, is mediated by medullary thymic epithelium. J Exp Med. 188:1998;5-16.
60. Klein L., Roettinger B., Kyewski B. Sampling of complementing self-antigen pools by thymic stromal cells maximizes the scope of central T cell tolerance. Eur J Immunol. 31:2001;2476-2486.
61. Maloy K.J., Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol. 2:2001;816-822.
62. Jordan M.S., Boesteanu A., Reed A.J., Petrone A.L., Holenbeck A.E., Lerman M.A., et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol. 2:2001;301-306.
63. Thornton A.M., Shevach E.M. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med. 188:1998;287-296.
64. Seddon B., Mason D. Peripheral autoantigen induces regulatory T cells that prevent autoimmunity. J Exp Med. 189:1999;877-882.
65. Pugliese A., Brown D., Garza D., Murchison D., Zeller M., Redondo M., et al. Self-antigen-presenting cells expressing diabetes-associated autoantigens exist in both thymus and peripheral lymphoid organs. J Clin Invest. 107:2001;555-564.
66. Weller R.O. Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol. 57:1998;885-894.
67. Yamada S., DePasquale M., Patlak C.S., Cserr H.F. Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am J Physiol. 261:1991;H1197-H1204.
68. de Vos A.F., van Meurs M., Brok H.P., Boven L.A., Hintzen R.Q., van der Valk P., et al. Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J Immunol. 169:2002;5415-5423.
69. Lindert R.B., Haase C.G., Brehm U., Linington C., Wekerle H., Hohlfeld R. Multiple sclerosis: B- and T-cell responses to the extracellular domain of the myelin oligodendrocyte glycoprotein. Brain. 122:(Pt 11):1999;2089-2100.