Myelin proteolipid protein: An effective autoantigen and target of autoimmunity in multiple sclerosis

Journal of Autoimmunity

Volumn 31, Issue 3, 2008, Pages 281-287

  Greer, Judith M ^a   Pender, Michael P ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Antibody; Autoimmunity; Central nervous system; Demyelination; Inflammation; Multiple sclerosis; Myelin proteolipid protein; Post translational modification; T cell

Indexed keywords

AUTOANTIGEN; ENCEPHALITOGENIC PROTEIN; MYELIN; PROTEOLIPID PROTEIN;

ARTICLE; AUTOIMMUNITY; DEMYELINATING DISEASE; ENCEPHALOMYELITIS; MULTIPLE SCLEROSIS; PRIORITY JOURNAL;

ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MULTIPLE SCLEROSIS; MYELIN PROTEOLIPID PROTEIN;

EID: 56349140640     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2008.04.018     Document Type: Article

References (67)

1. Greer J.M., and Lees M.B. Myelin proteolipid protein-the first 50 years. Int J Biochem Cell Biol 34 (2002) 211-215
2. Tal C., and Olitsky P.K. Quantitative studies on proteolipide as incitant of disseminated encephalomyelitis in mice. Science 116 (1952) 420-421
3. Waksman B.H., Porter H., Lees M.D., Adams R.D., and Folch J. A study of the chemical nature of components of bovine white matter effective in producing allergic encephalomyelitis in the rabbit. J. Exp. Med. 100 (1954) 451-471
4. Tuohy V.K., Lu Z.J., Sobel R.A., Laursen R.A., and Lees M.B. A synthetic peptide from myelin proteolipid protein induces experimental allergic encephalomyelitis. J Immunol 141 (1988) 1126-1130
5. Tuohy V.K., Sobel R.A., and Lees M.B. Myelin proteolipid protein-induced experimental allergic encephalomyelitis. Variations of disease expression in different strains of mice. J Immunol 140 (1988) 1868-1873
6. Tuohy V.K., Lu Z., Sobel R.A., Laursen R.A., and Lees M.B. Identification of an encephalitogenic determinant of myelin proteolipid protein for SJL mice. J Immunol 142 (1989) 1523-1527
7. Whitham R.H., Jones R.E., Hashim G.A., Hoy C.M., Wang R.Y., Vandenbark A.A., et al. Location of a new encephalitogenic epitope (residues 43 to 64) in proteolipid protein that induces relapsing experimental autoimmune encephalomyelitis in PL/J and (SJL x PL)F1 mice. J Immunol 147 (1991) 3803-3808
8. Greer J.M., Kuchroo V.K., Sobel R.A., and Lees M.B. Identification and characterization of a second encephalitogenic determinant of myelin proteolipid protein (residues 178-191) for SJL mice. J Immunol 149 (1992) 783-788
9. Amor S., Baker D., Groome N., and Turk J.L. Identification of a major encephalitogenic epitope of proteolipid protein (residues 56-70) for the induction of experimental allergic encephalomyelitis in Biozzi AB/H and nonobese diabetic mice. J Immunol 150 (1993) 5666-5672
10. Greer J.M., Sobel R.A., Sette A., Southwood S., Lees M.B., and Kuchroo V.K. Immunogenic and encephalitogenic epitope clusters of myelin proteolipid protein. J Immunol 156 (1996) 371-379
11. Fritz R.B., and Zhao M.L. Active and passive experimental autoimmune encephalomyelitis in strain 129/J (H-2b) mice. J Neurosci Res 45 (1996) 471-474
12. Muller D.M., Pender M.P., and Greer J.M. A neuropathological analysis of experimental autoimmune encephalomyelitis with predominant brain stem and cerebellar involvement and differences between active and passive induction. Acta Neuropathol 100 (2000) 174-182
13. Lyons J.A., Ramsbottom M.J., Trotter J.L., and Cross A.H. Identification of the encephalitogenic epitopes of CNS proteolipid protein in BALB/c mice. J Autoimmun 19 (2002) 195-201
14. Anderson T.J., Montague P., Nadon N., Nave K.A., and Griffiths I.R. Modification of Schwann cell phenotype with Plp transgenes: evidence that the PLP and DM20 isoproteins are targeted to different cellular domains. J Neurosci Res 50 (1997) 13-22
15. Cambi F., Lees M.B., Williams R.M., and Macklin W.B. Chronic experimental allergic encephalomyelitis produced by bovine proteolipid apoprotein: immunological studies in rabbits. Ann Neurol 13 (1983) 303-308
16. Chalk J.B., McCombe P.A., Smith R., and Pender M.P. Clinical and histological findings in proteolipid protein-induced experimental autoimmune encephalomyelitis (EAE) in the Lewis rat. Distribution of demyelination differs from that in EAE induced by other antigens. J Neurol Sci 123 (1994) 154-161
17. Chalk J.B., McCombe P.A., and Pender M.P. Conduction abnormalities are restricted to the central nervous system in experimental autoimmune encephalomyelitis induced by inoculation with proteolipid protein but not with myelin basic protein. Brain 117 (1994) 975-986
18. Fabriek B.O., Zwemmer J.N., Teunissen C.E., Dijkstra C.D., Polman C.H., Laman J.D., et al. In vivo detection of myelin proteins in cervical lymph nodes of MS patients using ultrasound-guided fine-needle aspiration cytology. J Neuroimmunol 161 (2005) 190-194
19. Klein L., Klugmann M., Nave K.A., Tuohy V.K., and 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
20. 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
21. Novotny G.E., Sommerfeld H., and Zirbes T. Thymic innervation in the rat: A light and electron microscopical study. J Comp Neurol 302 (1990) 552-561
22. Feng J.M., Fernandes A.O., Bongarzone E.R., Campagnoni C.W., Kampf K., and Campagnoni A.T. Expression of soma-restricted proteolipid/DM20 proteins in lymphoid cells. J Neuroimmunol 144 (2003) 9-15
23. Greer J.M., Klinguer C., Trifilieff E., Sobel R.A., and Lees M.B. Encephalitogenicity of murine, but not bovine, DM20 in SJL mice is due to a single amino acid difference in the immunodominant encephalitogenic epitope. Neurochem Res 22 (1997) 541-547
24. Olsson T., Zhi W.W., Hojeberg B., Kostulas V., Jiang Y.P., Anderson G., et al. Autoreactive T lymphocytes in multiple sclerosis determined by antigen-induced secretion of interferon-gamma. J Clin Invest 86 (1990) 981-985
25. Sun J.B., Olsson T., Wang W.Z., Xiao B.G., Kostulas V., Fredrikson S., et al. Autoreactive T and B cells responding to myelin proteolipid protein in multiple sclerosis and controls. Eur J Immunol 21 (1991) 1461-1468
26. Trotter J.L., Hickey W.F., van der Veen R.C., and Sulze L. Peripheral blood mononuclear cells from multiple sclerosis patients recognize myelin proteolipid protein and selected peptides. J Neuroimmunol 33 (1991) 55-62
27. Pelfrey C.M., Trotter J.L., Tranquill L.R., and McFarland H.F. Identification of a novel T cell epitope of human proteolipid protein (residues 40-60) recognized by proliferative and cytolytic CD4+T cells from multiple sclerosis patients. J Neuroimmunol 46 (1993) 33-42
28. Pelfrey C.M., Trotter J.L., Tranquill L.R., and McFarland H.F. Identification of a second T cell epitope of human proteolipid protein (residues 89-106) recognized by proliferative and cytolytic CD4+T cells from multiple sclerosis patients. J Neuroimmunol 53 (1994) 153-161
29. Soderstrom M., Link H., Sun J.B., Fredrikson S., Wang Z.Y., and Huang W.X. Autoimmune T cell repertoire in optic neuritis and multiple sclerosis: T cells recognising multiple myelin proteins are accumulated in cerebrospinal fluid. J Neurol Neurosurg Psychiatry 57 (1994) 544-551
30. Correale J., McMillan M., McCarthy K., Le T., and Weiner L.P. Isolation and characterization of autoreactive proteolipid protein-peptide specific T-cell clones from multiple sclerosis patients. Neurology 45 (1995) 1370-1378
31. Greer J.M., Csurhes P.A., Cameron K.D., McCombe P.A., Good M.F., and Pender M.P. Increased immunoreactivity to two overlapping peptides of myelin proteolipid protein in multiple sclerosis. Brain 120 (1997) 1447-1460
32. Trotter J.L., Pelfrey C.M., Trotter A.L., Selvidge J.A., Gushleff K.C., Mohanakumar T., et al. T cell recognition of myelin proteolipid protein and myelin proteolipid protein peptides in the peripheral blood of multiple sclerosis and control subjects. J Neuroimmunol 84 (1998) 172-178
33. Crawford M.P., Yan S.X., Ortega S.B., Mehta R.S., Hewitt R.E., Price D.A., et al. High prevalence of autoreactive, neuroantigen-specific CD8+T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood 103 (2004) 4222-4231
34. Messier A.M., and Bizzozero O.A. Conserved fatty acid composition of proteolipid protein during brain development and in myelin subfractions. Neurochem Res 25 (2000) 449-455
35. Barrese N., Mak B., Fisher L., and Moscarello M.A. Mechanism of demyelination in DM20 transgenic mice involves increased fatty acylation. J Neurosci Res 53 (1998) 143-152
36. Greer J.M., Denis B., Sobel R.A., and Trifilieff E. Thiopalmitoylation of myelin proteolipid protein epitopes enhances immunogenicity and encephalitogenicity. J Immunol 166 (2001) 6907-6913
37. Pfender N.A., Grosch S., Roussel G., Koch M., Trifilieff E., and Greer J.M. Route of uptake of palmitoylated encephalitogenic peptides of myelin proteolipid protein by antigen-presenting cells: importance of the type of bond between lipid chain and peptide and relevance to autoimmunity. J Immunol 180 (2008) 1398-1404
38. Pender M.P., and Greer J.M. Immunology of multiple sclerosis. Curr Allergy Asthma Rep 7 (2007) 285-292
39. Johnson D., Hafler D.A., Fallis R.J., Lees M.B., Brady R.O., Quarles R.H., et al. Cell-mediated immunity to myelin-associated glycoprotein, proteolipid protein, and myelin basic protein in multiple sclerosis. J Neuroimmunol 13 (1986) 99-108
40. Hafler D.A., Benjamin D.S., Burks J., and Weiner H.L. Myelin basic protein and proteolipid protein reactivity of brain- and cerebrospinal fluid-derived T cell clones in multiple sclerosis and postinfectious encephalomyelitis. J Immunol 139 (1987) 68-72
41. Ohashi T., Yamamura T., Inobe J., Kondo T., Kunishita T., and Tabira T. Analysis of proteolipid protein (PLP)-specific T cells in multiple sclerosis: identification of PLP 95-116 as an HLA-DR2,w15-associated determinant. Int Immunol 7 (1995) 1771-1778
42. Tuohy V.K., Yu M., Weinstock-Guttman B., and Kinkel R.P. Diversity and plasticity of self recognition during the development of multiple sclerosis. J Clin Invest 99 (1997) 1682-1690
43. Sellebjerg F., Christiansen M., and Garred P. MBP, anti-MBP and anti-PLP antibodies, and intrathecal complement activation in multiple sclerosis. Mult Scler 4 (1998) 127-131
44. Pender M.P., Csurhes P.A., Greer J.M., Mowat P.D., Henderson R.D., Cameron K.D., et al. Surges of increased T cell reactivity to an encephalitogenic region of myelin proteolipid protein occur more often in patients with multiple sclerosis than in healthy subjects. J Immunol 165 (2000) 5322-5331
45. Tejada-Simon M.V., Zang Y.C., Yang D., Hong J., Li S., Singh R.A., et al. Aberrant T cell responses to myelin antigens during clinical exacerbation in patients with multiple sclerosis. Int Immunol 12 (2000) 1641-1650
46. Pelfrey C.M., Rudick R.A., Cotleur A.C., Lee J.C., Tary-Lehmann M., and Lehmann P.V. Quantification of self-recognition in multiple sclerosis by single-cell analysis of cytokine production. J Immunol 165 (2000) 1641-1651
47. Minohara M., Ochi H., Matsushita S., Irie A., Nishimura Y., and Kira J. Differences between T-cell reactivities to major myelin protein-derived peptides in opticospinal and conventional forms of multiple sclerosis and healthy controls. Tissue Antigens 57 (2001) 447-456
48. Hellings N., Gelin G., Medaer R., Bruckers L., Palmers Y., Raus J., and Stinissen P. Longitudinal study of antimyelin T-cell reactivity in relapsing-remitting multiple sclerosis: association with clinical and MRI activity. J Neuroimmunol 126 (2002) 143-160
49. Yentur S.P., Akman-Demir G., Eraksoy M., and Saruhan-Direskeneli G. Autoreactivity to myelin antigens related to HLA associations with multiple sclerosis. Mult Scler 8 (2002) 278-283
50. Greer J.M., Csurhes P.A., Pender M.P., and McCombe P.A. Effect of gender on T-cell proliferative responses to myelin proteolipid protein antigens in patients with multiple sclerosis and controls. J Autoimmun 22 (2004) 345-352
51. Moldovan I.R., Rudick R.A., Cotleur A.C., Born S.E., Lee J.C., Karafa M.T., et al. Longitudinal single-cell cytokine responses reveal recurrent autoimmune myelin reactivity in relapsing-remitting multiple sclerosis patients. Mult Scler 11 (2005) 251-260
52. Markovic-Plese S., Fukaura H., Zhang J., al-Sabbagh A., Southwood S., Sette A., et al. T cell recognition of immunodominant and cryptic proteolipid protein epitopes in humans. J Immunol 155 (1995) 982-992
53. Warren K.G., and Catz I. Relative frequency of autoantibodies to myelin basic protein and proteolipid protein in optic neuritis and multiple sclerosis cerebrospinal fluid. J Neurol Sci 121 (1994) 66-73
54. Biddison W.E., Taub D.D., Cruikshank W.W., Center D.M., Connor E.W., and Honma K. Chemokine and matrix metalloproteinase secretion by myelin proteolipid protein-specific CD8+T cells: potential roles in inflammation. J Immunol 158 (1997) 3046-3053
55. Takashima H., Smith D.R., Fukaura H., Khoury S.J., Hafler D.A., and Weiner H.L. Pulse cyclophosphamide plus methylprednisolone induces myelin-antigen-specific IL-4-secreting T cells in multiple sclerosis patients. Clin Immunol Immunopathol 88 (1998) 28-34
56. Greer J.M., Csurhes P.A., Muller D.M., and Pender M.P. Correlation of blood T-cell and antibody reactivity to myelin proteins with HLA type and lesion localization in multiple sclerosis. J Immunol 180 (2008) 6402-6410
57. Greer J.M., and Pender M.P. The presence of glutamic acid at positions 71 or 74 in pocket 4 of the HLA-DRβ1 chain is associated with the clinical course of multiple sclerosis. J Neurol Neurosurg Psychiatry 76 (2005) 656-662
58. Sobel R.A., and Kuchroo V.K. The immunopathology of acute experimental allergic encephalomyelitis induced with myelin proteolipid protein. T cell receptors in inflammatory lesions. J Immunol 149 (1992) 1444-1451
59. Muller D.M., Pender M.P., and Greer J.M. Blood-brain barrier disruption and lesion localisation in experimental autoimmune encephalomyelitis with predominant cerebellar and brainstem involvement. J Neuroimmunol 160 (2005) 162-169
60. Lou Y.H., and Borillo J. Migration of T cells from nearby inflammatory foci into antibody bound tissue: a relay of T cell and antibody actions in targeting native autoantigen. J Autoimmun 21 (2003) 27-35
61. Lees M.B., and Paxman S.A. Myelin proteins from different regions of the central nervous system. J Neurochem 23 (1974) 825-831
62. Butt A.M., Ibrahim M., Ruge F.M., and Berry M. Biochemical subtypes of oligodendrocyte in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip. Glia 14 (1995) 185-197
63. Hajihosseini M., Tham T.N., and Dubois-Dalcq M. Origin of oligodendrocytes within the human spinal cord. J Neurosci 16 (1996) 7981-7994
64. Yan Y., Lagenaur C., and Narayanan V. Molecular cloning of M6: identification of a PLP/DM20 gene family. Neuron 11 (1993) 423-431
65. Greenfield E.A., Reddy J., Lees A., Dyer C.A., Koul O., Nguyen K., et al. Monoclonal antibodies to distinct regions of human myelin proteolipid protein simultaneously recognize central nervous system myelin and neurons of many vertebrate species. J Neurosci Res 83 (2006) 415-431
66. Tompkins S.M., Padilla J., Dal Canto M.C., Ting J.P., Van Kaer L., and Miller S.D. De novo central nervous system processing of myelin antigen is required for the initiation of experimental autoimmune encephalomyelitis. J Immunol 168 (2002) 4173-4183
67. Tuohy V.K., and Thomas D.M. Sequence 104-117 of myelin proteolipid protein is a cryptic encephalitogenic T cell determinant for SJL/J mice. J Neuroimmunol 56 (1995) 161-170