Targeting myelin proteolipid protein to the MHC class I pathway by ubiquitination modulates the course of experimental autoimmune encephalomyelitis

Journal of Neuroimmunology

Volumn 204, Issue 1-2, 2008, Pages 92-100

  Theil, Diethilde J ^a   Libbey, Jane E ^a   Rodriguez, Fernando ^b   Whitton, J Lindsay ^b   Tsunoda, Ikuo ^a   Derfuss, Tobias J ^a   Fujinami, Robert S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CNS demyelinating disease; DNA vaccines; Experimental autoimmune encephalomyelitis; Multiple sclerosis; Ubiquitin degradation pathway

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEOLIPID PROTEIN; UBIQUITIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DNA IMMUNIZATION; DRUG EFFECT; FEMALE; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN TARGETING; UBIQUITINATION;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CELL PROLIFERATION; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HISTOCOMPATIBILITY ANTIGENS CLASS I; LYMPHOCYTE ACTIVATION; MICE; MOLECULAR SEQUENCE DATA; MYELIN PROTEOLIPID PROTEIN; PEPTIDE FRAGMENTS; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; SPINAL CORD; T-LYMPHOCYTES; TIME FACTORS; UBIQUITINATION;

EID: 54849415440     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.07.005     Document Type: Article

References (85)

1. Álvarez-Lafuente R., Garcia-Montojo M., de Las Hervas V., Bartolome M., and Arroyo R. Clinical parameters and HHV-6 active replication in relapsing-remitting multiple sclerosis patients. J. Clin. Virol. 37 Suppl 1 (2006) S24-S26
2. Amor S., Groome N., Linington C., Morris M.M., Dornmair K., Gardinier M.V., Matthieu J.-M., and Baker D. 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
3. Andersen O., Lygner P.E., Bergstrom T., Andersson M., and Vahlne A. Viral infections trigger multiple sclerosis relapses: a prospective seroepidemiological study. J. Neurol. 240 (1993) 417-422
4. Andersson H.A., and Barry M.A. Maximizing antigen targeting to the proteasome for gene-based vaccines. Mol. Ther. 10 (2004) 432-446
5. Barnett L.A., Whitton J.L., Wada Y., and Fujinami R.S. Enhancement of autoimmune disease using recombinant vaccinia virus encoding myelin proteolipid protein. J. Neuroimmunol. 44 (1993) 15-25 [published erratum appears in J. Neuroimmunol. 48:120, 1993]
6. Barnett L.A., Whitton J.L., Wang L.Y., and Fujinami R.S. Virus encoding an encephalitogenic peptide protects mice from experimental allergic encephalomyelitis. J. Neuroimmunol. 64 (1996) 163-173
7. Bauer R., Scheiblhofer S., Kern K., Gruber C., Stepanoska T., Thalhamer T., Hauser-Kronberger C., Alinger B., Zoegg T., Gabler M., Ferreira F., Hartl A., Thalhamer J., and Weiss R. Generation of hypoallergenic DNA vaccines by forced ubiquitination: preventive and therapeutic effects in a mouse model of allergy. J. Allergy. Clin. Immunol. 118 (2006) 269-276
8. Begolka W.S., Vanderlugt C.L., Rahbe S.M., and Miller S.D. Differential expression of inflammatory cytokines parallels progression of central nervous system pathology in two clinically distinct models of multiple sclerosis. J. Immunol. 161 (1998) 4437-4446
9. Berti R., Brennan M.B., Soldan S.S., Ohayon J.M., Casareto L., McFarland H.F., and Jacobson S. Increased detection of serum HHV-6 DNA sequences during multiple sclerosis (MS) exacerbations and correlation with parameters of MS disease progression. J. NeuroVirol. 8 (2002) 250-256
10. Brandsma J.L., Shlyankevich M., Zelterman D., and Su Y. Therapeutic vaccination of rabbits with a ubiquitin-fused papillomavirus E1, E2, E6 and E7 DNA vaccine. Vaccine 25 (2007) 6158-6163
11. Brulet J.-M., Maudoux F., Thomas S., Thielemans K., Burny A., Leo O., Bex F., and Hallez S. DNA vaccine encoding endosome-targeted human papillomavirus type 16 E7 protein generates CD4+ T cell-dependent protection. Eur. J. Immunol. 37 (2007) 376-384
12. Buch T., and Waisman A. Protection from autoimmunity by DNA vaccination against T-cell receptor. Methods. Mol. Med. 127 (2006) 269-280
13. Buljevac D., Flach H.Z., Hop W.C.J., Hijdra D., Laman J.D., Savelkoul H.F.J., van der Meché F.G.A., Van Doorn P.A., and Hintzen R.Q. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 125 (2002) 952-960
14. Christensen T. Human herpesviruses in MS. Int. MS. J. 14 (2007) 41-47
15. Correale J., Fiol M., and Gilmore W. The risk of relapses in multiple sclerosis during systemic infections. Neurology 67 (2006) 652-659
16. De Keyser J., Zwanikken C., and Boon M. Effects of influenza vaccination and influenza illness on exacerbations in multiple sclerosis. J. Neurol. Sci. 159 (1998) 51-53
17. Delogu G., Howard A., Collins F.M., and Morris S.L. DNA vaccination against tuberculosis: expression of a ubiquitin-conjugated tuberculosis protein enhances antimycobacterial immunity. Infect. Immun. 68 (2000) 3097-3102
18. Delogu G., Li A., Repique C., Collins F., and Morris S.L. DNA vaccine combinations expressing either tissue plasminogen activator signal sequence fusion proteins or ubiquitin-conjugated antigens induce sustained protective immunity in a mouse model of pulmonary tuberculosis. Infect. Immun. 70 (2002) 292-302
19. Duan X., Hisaeda H., Shen J., Tu L., Imai T., Chou B., Murata S., Chiba T., Tanaka K., Fehling H.J., Koga T., Sueishi K., and Himeno K. The ubiquitin-proteasome system plays essential roles in presenting an 8-mer CTL epitope expressed in APC to corresponding CD8+ T cells. Int. Immunol. 18 (2006) 679-687
20. Edwards S., Zvartau M., Clarke H., Irving W., and Blumhardt L.D. Clinical relapses and disease activity on magnetic resonance imaging associated with viral upper respiratory tract infections in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 64 (1998) 736-741
21. Falcone M., and Bloom B.R. A T helper cell 2 (Th2) immune response against non-self antigens modifies the cytokine profile of autoimmune T cells and protects against experimental allergic encephalomyelitis. J. Exp. Med. 185 (1997) 901-907
22. Fontoura P., Garren H., and Steinman L. Antigen-specific therapies in multiple sclerosis: going beyond proteins and peptides. Int. Rev. Immunol. 24 (2005) 415-446
23. Fu T.-M., Guan L., Friedman A., Ulmer J.B., Liu M.A., and Donnelly J.J. Induction of MHC class I-restricted CTL response by DNA immunization with ubiquitin-influenza virus nucleoprotein fusion antigens. Vaccine 16 (1998) 1711-1717
24. Garren H., Ruiz P.J., Watkins T.A., Fontoura P., Nguyen L.-V.T., Estline E.R., Hirschberg D.L., and Steinman L. Combination of gene delivery and DNA vaccination to protect from and reverse Th1 autoimmune disease via deviation to the Th2 pathway. Immunity 15 (2001) 15-22
25. Gavioli R., Vertuani S., and Masucci M.G. Proteasome inhibitors reconstitute the presentation of cytotoxic T-cell epitopes in Epstein-Barr virus-associated tumors. Int. J. Cancer 101 (2002) 532-538
26. Gilden D.H. Multiple sclerosis exacerbations and infection. Lancet. Neurol. 1 (2002) 145
27. Granieri E., and Casetta I. Part III: selected reviews common childhood and adolescent infections and multiple sclerosis. Neurology 49 (1997) S42-S54
28. Granieri E., Casetta I., Tola M.R., and Ferrante P. Multiple sclerosis: infectious hypothesis. Neurol. Sci. 22 (2001) 179-185
29. Gravier R., Dory D., Rodriguez F., Bougeard S., Beven V., Cariolet R., and Jestin A. Immune and protective abilities of ubiquitinated and non-ubiquitinated pseudorabies virus glycoproteins. Acta. Virol. 51 (2007) 35-45
30. Ho P.P., Fontoura P., Platten M., Sobel R.A., DeVoss J.J., Lee L.Y., Kidd B.A., Tomooka B.H., Capers J., Agrawal A., Gupta R., Zernik J., Yee M.K., Lee B.J., Garren H., Robinson W.H., and Steinman L. A suppressive oligodeoxynucleotide enhances the efficacy of myelin cocktail/IL-4-tolerizing DNA vaccination and treats autoimmune disease. J. Immunol. 175 (2005) 6226-6234
31. Hung C.-F., Yang M., and Wu T.C. Modifying professional antigen-presenting cells to enhance DNA vaccine potency. Methods. Mol. Med. 127 (2006) 199-220
32. Johnson A.J., Suidan G.L., McDole J., and Pirko I. The CD8 T cell in multiple sclerosis: suppressor cell or mediator of neuropathology?. Int. Rev. Neurobiol. 79 (2007) 73-97
33. Karpus W.J., Gould K.E., and Swanborg R.H. CD4+ suppressor cells of autoimmune encephalomyelitis respond to T cell receptor-associated determinants on effector cells by interleukin-4 secretion. Eur. J. Immunol. 22 (1992) 1757-1763
34. Kriesel J.D., and Sibley W.A. Editorial: the case for rhinoviruses in the pathogenesis of multiple sclerosis. Mult. Scler. 11 (2005) 1-4
35. Kriesel J.D., White A., Hayden F.G., Spruance S.L., and Petajan J. Multiple sclerosis attacks are associated with picornavirus infections. Mult. Scler. 10 (2004) 145-148
36. Kumar V., and Sercarz E. Dysregulation of potentially pathogenic self reactivity is crucial for the manifestation of clinical autoimmunity. J. Neurosci. Res. 45 (1996) 334-339
37. Kumar V., Maglione J., Thatte J., Pederson B., Sercarz E., and Ward E.S. Induction of a type 1 regulatory CD4 T cell response following Vb8.2 DNA vaccination results in immune deviation and protection from experimental autoimmune encephalomyelitis. Int. Immunol. 13 (2001) 835-841
38. Kurtzke J.F. Epidemiologic evidence for multiple sclerosis as an infection. Clin. Microbiol. Rev. 6 (1993) 382-427
39. Leachman S.A., Shylankevich M., Slade M.D., Levine D., Sundaram R.K., Xiao W., Bryan M., Zelterman D., Tiegelaar R.E., and Brandsma J.L. Ubiquitin-fused and/or multiple early genes from cottontail rabbit papillomavirus as DNA vaccines. J. Virol. 76 (2002) 7616-7624
40. Leifert J.A., Rodriguez-Carreno M.P., Rodriguez F., and Whitton J.L. Targeting plasmid-encoded proteins to the antigen presentation pathways. Immunol. Rev. 199 (2004) 40-53
41. Libbey J.E., and Fujinami R.S. Are virus infections triggers for autoimmune disease?. Clin. Microbiol. Newslett. 24 (2002) 73-76
42. Libbey J.E., and Fujinami R.S. Viral demyelinating disease in experimental animals. In: Herndon R.M. (Ed). Multiple Sclerosis: Immunology, Pathology and Pathophysiology (2003), Demos, New York 125-133
43. Liu W.J., Zhao K.-N., Gao F.G., Leggatt G.R., Fernando G.J.P., and Frazer I.H. Polynucleotide viral vaccines: codon optimisation and ubiquitin conjugation enhances prophylactic and therapeutic efficacy. Vaccine 20 (2002) 862-869
44. Marrie R.A., Wolfson C., Sturkenboom M.C., Gout O., Heinzlef O., Roullet E., and Abenhaim L. Multiple sclerosis and antecedent infections: a case-control study. Neurology 54 (2000) 2307-2310
45. Matsumoto Y. New approach to immunotherapy against organ-specific autoimmune diseases with T cell receptor and chemokine receptor DNA vaccines. Curr. Drug. Targets. Immune. Endocr. Metabol. Disord. 5 (2005) 73-77
46. McClain M.A., Gatson N.N., Powell N.D., Papenfuss T.L., Gienapp I.E., Song F., Shawler T.M., Kithcart A., and Whitacre C.C. Pregnancy suppresses experimental autoimmune encephalomyelitis through immunoregulatory cytokine production. J. Immunol. 179 (2007) 8146-8152
47. McRae B.L., Vanderlugt C.L., Dal Canto M.C., and Miller S.D. Functional evidence for epitope spreading in the relapsing pathology of experimental autoimmune encephalomyelitis. J. Exp. Med. 182 (1995) 75-85
48. Metz L.M., McGuinness S.D., and Harris C. Urinary tract infections may trigger relapse in multiple sclerosis. Axone 19 (1998) 67-70
49. Miller A., Lider O., Roberts A.B., Sporn M.B., and Weiner H.L. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor b after antigen-specific triggering. Proc. Natl. Acad. Sci. USA 89 (1992) 421-425
50. Miyakoshi A., Yoon W.K., Jee Y., and Matsumoto Y. Characterization of the antigen specificity and TCR repertoire, and TCR-based DNA vaccine therapy in myelin basic protein-induced autoimmune encephalomyelitis in DA rats. J. Immunol. 170 (2003) 6371-6378
51. Nicholson S.M., Dal Canto M.C., Miller S.D., and Melvold R.W. Adoptively transferred CD8+ T lymphocytes provide protection against TMEV-induced demyelinating disease in BALB/c mice. J. Immunol. 156 (1996) 1276-1283
52. Panitch H.S. Influence of infection on exacerbations of multiple sclerosis. Ann. Neurol. 36 Suppl (1994) S25-S28
53. Pender M.P. Experimental autoimmune encephalomyelitis. In: Pender M.P., and McCombe P.A. (Eds). Autoimmune Neurological Disease (1995), Cambridge University Press, Cambridge, UK 26-88
54. Pickart C.M. Back to the future with ubiquitin. Cell 116 (2004) 181-190
55. Racke M.K., Bonomo A., Scott D.E., Cannella B., Levine A., Raine C.S., Shevach E.M., and Röcken M. Cytokine-induced immune deviation as a therapy for inflammatory autoimmune disease. J. Exp. Med. 180 (1994) 1961-1966
56. Rapp N.S., Gilroy J., and Lerner A.M. Role of bacterial infection in exacerbation of multiple sclerosis. Am. J. Phys. Med. Rehabil. 74 (1995) 415-418
57. Riedl P., Reimann J., and Schirmbeck R. Complexes of DNA vaccines with cationic, antigenic peptides are potent, polyvalent CD8(+) T-cell-stimulating immunogens. Methods Mol. Med. 127 (2006) 159-169
58. Robinson W.H., Fontoura P., Lee B.J., de Vegvar H.E.N., Tom J., Pedotti R., DiGennaro C.D., Mitchell D.J., Fong D., Ho P.P.K., Ruiz P.J., Maverakis E., Stevens D.B., Bernard C.C.A., Martin R., Kuchroo V.K., van Noort J.M., Genain C.P., Amor S., Olsson T., Utz P.J., Garren H., and Steinman L. Protein microarrays guide tolerizing DNA vaccine treatment of autoimmune encephalomyelitis. Nat. Biotechnol. 21 (2003) 1033-1039
59. Rodriguez M., Lindsley M.D., and Pierce M.L. Role of T cells in resistance to Theiler's virus infection. Microb. Pathog. 11 (1991) 269-281
60. Rodriguez F., Zhang J., and Whitton J.L. DNA immunization: ubiquitination of a viral protein enhances cytotoxic T-lymphocyte induction and antiviral protection but abrogates antibody induction. J. Virol. 71 (1997) 8497-8503
61. Rodriguez F., An L.-L., Harkins S., Zhang J., Yokoyama M., Widera G., Fuller J.T., Kincaid C., Campbell I.L., and Whitton J.L. DNA immunization with minigenes: low frequency of memory cytotoxic T lymphocytes and inefficient antiviral protection are rectified by ubiquitination. J. Virol. 72 (1998) 5174-5181
62. Ruiz P.J., Garren H., Ruiz I.U., Hirschberg D.L., Nguyen L.-V.T., Karpuj M.V., Cooper M.T., Mitchell D.J., Fathman C.G., and Steinman L. Suppressive immunization with DNA encoding a self-peptide prevents autoimmune disease: modulation of T cell costimulation. J. Immunol. 162 (1999) 3336-3341
63. Sands W.A., Bulut V., Severn A., Xu D., and Liew F.Y. Inhibition of nitric oxide synthesis by interleukin-4 may involve inhibiting the activation of protein kinase C epsilon. Eur. J. Immunol. 24 (1994) 2345-2350
64. Selmaj K., Kowal C., Walczak A., Nowicka J., and Raine C.S. Naked DNA vaccination differentially modulates autoimmune responses in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 111 (2000) 34-44
65. Sibley W.A., Bamford C.R., and Clark K. Clinical viral infections and multiple sclerosis. Lancet 1 (1985) 1313-1315
66. Sospedra M., and Martin R. Molecular mimicry in multiple sclerosis. Autoimmunity 39 (2006) 3-8
67. Sun D., and Klinkert W.E.F. Functional heterogeneity among CD4+ encephalitogenic T cells in recruitment of CD8+ T cells in experimental autoimmune encephalomyelitis. J. Immunol. 143 (1989) 2867-2872
68. Sun D., Qin Y., Chluba J., Epplen J.T., and Wekerle H. Suppression of experimentally induced autoimmune encephalomyelitis by cytolytic T-T cell interactions. Nature 332 (1988) 843-845
69. Theil D.J., Tsunoda I., Rodriguez F., Whitton J.L., and Fujinami R.S. Viruses can silently prime for and trigger central nervous system autoimmune disease. J. NeuroVirol. 7 (2001) 220-227
70. Thilenius A.R.B., Sabelko-Downes K.A., and Russell J.H. The role of the antigen-presenting cell in Fas-mediated direct and bystander killing: potential in vivo function of Fas in experimental allergic encephalomyelitis. J. Immunol. 162 (1999) 643-650
71. Tobery T.W., and Siliciano R.F. Targeting of HIV-1 antigens for rapid intracellular degradation enhances cytotoxic T lymphocyte (CTL) recognition and the induction of de novo CTL responses in vivo after immunization. J. Exp. Med. 185 (1997) 909-920
72. Tsunoda I., and Fujinami R.S. Two models for multiple sclerosis: experimental allergic encephalomyelitis and Theiler's murine encephalomyelitis virus. J. Neuropathol. Exp. Neurol. 55 (1996) 673-686
73. Tsunoda I., Kuang L.-Q., Tolley N.D., Whitton J.L., and Fujinami R.S. Enhancement of experimental allergic encephalomyelitis (EAE) by DNA immunization with myelin proteolipid protein (PLP) plasmid DNA. J. Neuropathol. Exp. Neurol. 57 (1998) 758-767
74. Tsunoda I., Tolley N.D., Theil D.J., Whitton J.L., Kobayashi H., and Fujinami R.S. Exacerbation of viral and autoimmune animal models for multiple sclerosis by bacterial DNA. Brain. Pathol. 9 (1999) 481-493
75. Tsunoda I., Kuang L.-Q., and Fujinami R.S. Induction of autoreactive CD8+ cytotoxic cells during Theiler's murine encephalomyelitis virus infection: implications for autoimmunity. J. Virol. 76 (2002) 12834-12844
76. Tsunoda I., Terry E.J., Marble B.J., Lazarides E., Woods C.M., and Fujinami R.S. Modulation of experimental autoimmune encephalomyelitis by VLA-2 blockade. Brain. Pathol. 17 (2007) 45-55
77. Vanderlugt C.L., Neville K.L., Nikcevich K.M., Eagar T.N., Bluestone J.A., and Miller S.D. Pathologic role and temporal appearance of newly emerging autoepitopes in relapsing experimental autoimmune encephalomyelitis. J. Immunol. 164 (2000) 670-678
78. Vidalin O., Tanaka E., Spengler U., Trépo C., and Inchauspé G. Targeting of hepatitis C virus core protein for MHC I or MHC II presentation does not enhance induction of immune responses to DNA vaccination. DNA. Cell. Biol. 18 (1999) 611-621
79. Waisman A., Ruiz P.J., Hirschberg D.L., Gelman A., Oksenberg J.R., Brocke S., Mor F., Cohen I.R., and Steinman L. Suppressive vaccination with DNA encoding a variable region gene of the T-cell receptor prevents autoimmune encephalomyelitis and activates Th2 immunity. Nat. Med. 2 (1996) 899-905
80. Wandinger K., Jabs W., Siekhaus A., Bubel S., Trillenberg P., Wagner H., Wessel K., Kirchner H., and Hennig H. Association between clinical disease activity and Epstein-Barr virus reactivation in MS. Neurology 55 (2000) 178-184
81. Wang L.-Y., and Fujinami R.S. Enhancement of EAE and induction of autoantibodies to T-cell epitopes in mice infected with a recombinant vaccinia virus encoding myelin proteolipid protein. J. Neuroimmunol. 75 (1997) 75-83
82. Wang L.-Y., Theil D.J., Whitton J.L., and Fujinami R.S. Infection with a recombinant vaccinia virus encoding myelin proteolipid protein causes suppression of chronic relapsing-remitting experimental allergic encephalomyelitis. J. Neuroimmunol. 96 (1999) 148-157
83. Wang Q.-M., Sun S.-H., Hu Z.-L., Zhou F.-J., Yin M., Xiao C.-J., and Zhang J.-C. Epitope DNA vaccines against tuberculosis: spacers and ubiquitin modulates cellular immune responses elicited by epitope DNA vaccine. Scand. J. Immunol. 60 (2004) 219-225
84. Whitham R.H., Bourdette D.N., Hashim G.A., Herndon R.M., Ilg R.C., Vandenbark A.A., and Offner H. Lymphocytes from SJL/J mice immunized with spinal cord respond selectively to a peptide of proteolipid protein and transfer relapsing demyelinating experimental autoimmune encephalomyelitis. J. Immunol. 146 (1991) 101-107
85. Zhang M., Obata C., Hisaeda H., Ishii K., Murata S., Chiba T., Tanaka K., Li Y., Furue M., Chou B., Imai T., Duan X., and Himeno K. A novel DNA vaccine based on ubiquitin-proteasome pathway targeting 'self'-antigens expressed in melanoma/melanocyte. Gene. Ther. 12 (2005) 1049-1057