'Multi-epitope-targeted' immune-specific therapy for a multiple sclerosis-like disease via engineered multi-epitope protein is superior to peptides

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Kaushansky, Nathali ^a   de Rosbo, Nicole Kerlero ^a   Zilkha Falb, Rina ^a   Yosef Hemo, Reut ^a   Cohen, Lydia ^a   Ben Nun, Avraham ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 11; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOMODULATING AGENT; MULTI EPITOPE PROTEIN; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEOLIPID PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; EPITOPE; PEPTIDE; PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLONAL ANERGY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; DRUG SCREENING; DRUG TARGETING; FEMALE; IMMUNOMODULATION; IMMUNOTHERAPY; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PROTEIN ENGINEERING; REGULATORY T LYMPHOCYTE; SYSTEMIC THERAPY; T LYMPHOCYTE ACTIVATION; TREATMENT DURATION; ANIMAL; AUTOIMMUNITY; C57BL MOUSE; CELL LINE; HUMAN; IMMUNOLOGY; METHODOLOGY; MYELIN SHEATH; PATHOLOGY;

ANIMALS; AUTOIMMUNITY; CELL LINE; DOWN-REGULATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPITOPES; FEMALE; HUMANS; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; MYELIN SHEATH; PEPTIDES; PROTEIN ENGINEERING; PROTEINS;

EID: 82255173851     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027860     Document Type: Article

References (62)

1. Sospedra M, Martin R, (2005) Immunology of multiple sclerosis. Annu Rev Immunol 23: 683-747.
2. Hohlfeld R, Wekerle H, (2004) Autoimmune concepts of multiple sclerosis as a basis for selective immunotherapy: from pipe dreams to (therapeutic) pipelines. Proc Natl Acad Sci U S A 101 (Suppl 2): 14599-14606.
3. Ben-Nun A, Wekerle H, Cohen IR, (1981) The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur J Immunol 11: 195-199.
4. Ben-Nun A, Lando Z, (1983) Detection of autoimmune cells proliferating to myelin basic protein and selection of T cell lines that mediate experimental autoimmune encephalomyelitis (EAE) in mice. J Immunol 130: 1205-1209.
5. Zamvil S, Nelson P, Trotter J, Mitchell D, Knobler R, et al. (1985) T-cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination. Nature 317: 355-358.
6. Adorini L, (2004) Immunotherapeutic approaches in multiple sclerosis. J Neurol Sci 223: 13-24.
7. Critchfield JM, Racke MK, Zuniga-Pflucker JC, Cannella B, Raine CS, et al. (1994) T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science 263: 1139-1143.
8. Racke MK, Critchfield JM, Quigley L, Cannella B, Raine CS, et al. (1996) Intravenous antigen administration as a therapy for autoimmune demyelinating disease. Ann Neurol 39: 46-56.
9. Devaux B, Enderlin F, Wallner B, Smilek DE, (1997) Induction of EAE in mice with recombinant human MOG, and treatment of EAE with a MOG peptide. J Neuroimmunol 75: 169-173.
10. Ruiz PJ, Garren H, Ruiz IU, Hirschberg DL, Nguyen LV, et al. (1999) Suppressive immunization with DNA encoding a self-peptide prevents autoimmune disease: modulation of T cell costimulation. J Immunol 162: 3336-3341.
11. Chen C, Rivera A, Ron N, Dougherty JP, Ron Y, (2001) A gene therapy approach for treating T-cell-mediated autoimmune diseases. Blood 97: 886-894.
12. Lider O, Reshef T, Beraud E, Ben-Nun A, Cohen IR, (1988) Anti-idiotypic network induced by T cell vaccination against experimental autoimmune encephalomyelitis. Science 239: 181-183.
13. Owhashi M, Heber-Katz E, (1988) Protection from experimental allergic encephalomyelitis conferred by a monoclonal antibody directed against a shared idiotype on rat T cell receptors specific for myelin basic protein. J Exp Med 168: 2153-2164.
14. Urban JL, Kumar V, Kono DH, Gomez C, Horvath SJ, et al. (1988) Restricted use of T cell receptor V genes in murine autoimmune encephalomyelitis raises possibilities for antibody therapy. Cell 54: 577-592.
15. Vandenbark AA, Hashim G, Offner H, (1989) Immunization with a synthetic T-cell receptor V-region peptide protects against experimental autoimmune encephalomyelitis. Nature 341: 541-544.
16. Howell MD, Winters ST, Olee T, Powell HC, Carlo DJ, et al. (1989) Vaccination against experimental allergic encephalomyelitis with T cell receptor peptides. Science 246: 668-670.
17. Sharma SD, Nag B, Su XM, Green D, Spack E, et al. (1991) Antigen-specific therapy of experimental allergic encephalomyelitis by soluble class II major histocompatibility complex-peptide complexes. Proc Natl Acad Sci U S A 88: 11465-11469.
18. Huan J, Subramanian S, Jones R, Rich C, Link J, et al. (2004) Monomeric recombinant TCR ligand reduces relapse rate and severity of experimental autoimmune encephalomyelitis in SJL/J mice through cytokine switch. J Immunol 172: 4556-4566.
19. Wraith DC, Smilek DE, Mitchell DJ, Steinman L, McDevitt HO, (1989) Antigen recognition in autoimmune encephalomyelitis and the potential for peptide-mediated immunotherapy. Cell 59: 247-255.
20. Leadbetter EA, Bourque CR, Devaux B, Olson CD, Sunshine GH, et al. (1998) Experimental autoimmune encephalomyelitis induced with a combination of myelin basic protein and myelin oligodendrocyte glycoprotein is ameliorated by administration of a single myelin basic protein peptide. J Immunol 161: 504-512.
21. Gonsette RE, Delmotte P, Demonty L, (1977) Failure of basic protein therapy for multiple sclerosis. J Neurol 216: 27-31.
22. Campbell B, Vogel PJ, Fisher E, Lorenz R, (1973) Myelin basic protein administration in multiple sclerosis. Arch Neurol 29: 10-15.
23. Warren KG, Catz I, Ferenczi LZ, Krantz MJ, (2006) Intravenous synthetic peptide MBP8298 delayed disease progression in an HLA Class II-defined cohort of patients with progressive multiple sclerosis: results of a 24-month double-blind placebo-controlled clinical trial and 5 years of follow-up treatment. Eur J Neurol 13: 887-895.
24. Kappos L, Comi G, Panitch H, Oger J, Antel J, et al. (2000) Induction of a non-encephalitogenic type 2 T helper-cell autoimmune response in multiple sclerosis after administration of an altered peptide ligand in a placebo-controlled, randomized phase II trial. The Altered Peptide Ligand in Relapsing MS Study Group. Nat Med 6: 1176-1182.
25. Bielekova B, Goodwin B, Richert N, Cortese I, Kondo T, et al. (2000) Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand. Nat Med 6: 1167-1175.
26. Lehmann PV, Forsthuber T, Miller A, Sercarz EE, (1992) Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature 358: 155-157.
27. de Rosbo NK, Ben-Nun A, (1998) T-cell responses to myelin antigens in multiple sclerosis; relevance of the predominant autoimmune reactivity to myelin oligodendrocyte glycoprotein. J Autoimmun 11: 287-299.
28. Tuohy VK, Yu M, Yin L, Kawczak JA, Johnson JM, et al. (1998) The epitope spreading cascade during progression of experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol Rev 164: 93-100.
29. McRae BL, Vanderlugt CL, Dal Canto MC, Miller SD, (1995) Functional evidence for epitope spreading in the relapsing pathology of experimental autoimmune encephalomyelitis. J Exp Med 182: 75-85.
30. Ellmerich S, Takacs K, Mycko M, Waldner H, Wahid F, et al. (2004) Disease-related epitope spread in a humanized T cell receptor transgenic model of multiple sclerosis. Eur J Immunol 34: 1839-1848.
31. Tuohy VK, Yu M, Weinstock-Guttman B, Kinkel RP, (1997) Diversity and plasticity of self recognition during the development of multiple sclerosis. J Clin Invest 99: 1682-1690.
32. Yu M, Kinkel RP, Weinstock-Guttman B, Cook DJ, Tuohy VK, (1998) HLA-DP: a class II restriction molecule involved in epitope spreading during the development of multiple sclerosis. Hum Immunol 59: 15-24.
33. Zhong MC, Kerlero de Rosbo N, Ben-Nun A, (2002) Multiantigen/multiepitope-directed immune-specific suppression of "complex autoimmune encephalomyelitis" by a novel protein product of a synthetic gene. J Clin Invest 110: 81-90.
34. Korn T, Reddy J, Gao W, Bettelli E, Awasthi A, et al. (2007) Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 13: 423-431.
35. Mendel Kerlero de Rosbo N, Ben-Nun A, (1996) 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: 2470-2479.
36. Mendel I, Kerlero de Rosbo N, Ben-Nun A, (1995) 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: 1951-1959.
37. Zhong MC, Cohen L, Meshorer A, Kerlero de Rosbo N, Ben-Nun A, (2000) T-cells specific for soluble recombinant oligodendrocyte-specific protein induce severe clinical experimental autoimmune encephalomyelitis in H-2(b) and H-2(s) mice. J Neuroimmunol 105: 39-45.
38. Ben-Nun A, Kerlero de Rosbo N, Kaushansky N, Eisenstein M, Cohen L, et al. (2006) Anatomy of T cell autoimmunity to myelin oligodendrocyte glycoprotein (MOG): prime role of MOG44F in selection and control of MOG-reactive T cells in H-2b mice. Eur J Immunol 36: 478-493.
39. Kaushansky N, Hemo R, Eisenstein M, Ben-Nun A, (2007) OSP/claudin-11-induced EAE in mice is mediated by pathogenic T cells primarily governed by OSP192Y residue of major encephalitogenic region OSP179-207. Eur J Immunol 37: 2018-2031.
40. Vanderlugt CL, Miller SD, (2002) Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat Rev Immunol 2: 85-95.
41. Pathak SS, Blum JS, (2000) Endocytic recycling is required for the presentation of an exogenous peptide via MHC class II molecules. Traffic 1: 561-569.
42. Watts C, (2004) The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat Immunol 5: 685-692.
43. Steinman RM, Hawiger D, Nussenzweig MC, (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21: 685-711.
44. Jin Y, Fuller L, Ciancio G, Burke GW 3rd, Tzakis AG, et al. (2004) Antigen presentation and immune regulatory capacity of immature and mature-enriched antigen presenting (dendritic) cells derived from human bone marrow. Hum Immunol 65: 93-103.
45. Smith CE, Miller SD, (2006) Multi-peptide coupled-cell tolerance ameliorates ongoing relapsing EAE associated with multiple pathogenic autoreactivities. J Autoimmun 27: 218-231.
46. Clayton JP, Gammon GM, Ando DG, Kono DH, Hood L, et al. (1989) Peptide-specific prevention of experimental allergic encephalomyelitis. Neonatal tolerance induced to the dominant T cell determinant of myelin basic protein. J Exp Med 169: 1681-1691.
47. Gaur A, Wiers B, Liu A, Rothbard J, Fathman CG, (1992) Amelioration of autoimmune encephalomyelitis by myelin basic protein synthetic peptide-induced anergy. Science 258: 1491-1494.
48. Elliott EA, McFarland HI, Nye SH, Cofiell R, Wilson TM, et al. (1996) Treatment of experimental encephalomyelitis with a novel chimeric fusion protein of myelin basic protein and proteolipid protein. J Clin Invest 98: 1602-1612.
49. Jurynczyk M, Walczak A, Jurewicz A, Jesionek-Kupnicka D, Szczepanik M, et al. (2010) Immune regulation of multiple sclerosis by transdermally applied myelin peptides. Ann Neurol 68: 593-601.
50. Pedotti R, Sanna M, Tsai M, DeVoss J, Steinman L, et al. (2003) Severe anaphylactic reactions to glutamic acid decarboxylase (GAD) self peptides in NOD mice that spontaneously develop autoimmune type 1 diabetes mellitus. BMC Immunol 4: 2.
51. Liu E, Moriyama H, Abiru N, Miao D, Yu L, et al. (2002) Anti-peptide autoantibodies and fatal anaphylaxis in NOD mice in response to insulin self-peptides B:9-23 and B:13-23. J Clin Invest 110: 1021-1027.
52. Pedotti R, Mitchell D, Wedemeyer J, Karpuj M, Chabas D, et al. (2001) An unexpected version of horror autotoxicus: anaphylactic shock to a self-peptide. Nat Immunol 2: 216-222.
53. Simpson D, Noble S, Perry C, (2002) Glatiramer acetate: a review of its use in relapsing-remitting multiple sclerosis. CNS Drugs 16: 825-850.
54. Smith CE, Eagar TN, Strominger JL, Miller SD, (2005) Differential induction of IgE-mediated anaphylaxis after soluble vs. cell-bound tolerogenic peptide therapy of autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 102: 9595-9600.
55. Kaye JF, Kerlero de Rosbo N, Mendel I, Flechter S, Hoffman M, et al. (2000) The central nervous system-specific myelin oligodendrocytic basic protein (MOBP) is encephalitogenic and a potential target antigen in multiple sclerosis (MS). J Neuroimmunol 102: 189-198.
56. Fritz RB, Zhao ML, (1996) Active and passive experimental autoimmune encephalomyelitis in strain 129/J (H-2b) mice. J Neurosci Res 45: 471-474.
57. Amor S, Groome N, Linington C, Morris MM, Dornmair K, et al. (1994) Identification of epitopes of myelin oligodendrocyte glycoprotein for the induction of experimental allergic encephalomyelitis in SJL and Biozzi AB/H mice. J Immunol 153: 4349-4356.
58. de Rosbo NK, Kaye JF, Eisenstein M, Mendel I, Hoeftberger R, et al. (2004) The myelin-associated oligodendrocytic basic protein region MOBP15-36 encompasses the immunodominant major encephalitogenic epitope(s) for SJL/J mice and predicted epitope(s) for multiple sclerosis-associated HLA-DRB1*1501. J Immunol 173: 1426-1435.
59. Tuohy VK, (1994) Peptide determinants of myelin proteolipid protein (PLP) in autoimmune demyelinating disease: a review. Neurochem Res 19: 935-944.
60. Kaushansky N, Zhong MC, Kerlero de Rosbo N, Hoeftberger R, Lassmann H, et al. (2006) Epitope specificity of autoreactive T and B cells associated with experimental autoimmune encephalomyelitis and optic neuritis induced by oligodendrocyte-specific protein in SJL/J mice. J Immunol 177: 7364-7376.
61. Sakai K, Zamvil SS, Mitchell DJ, Lim M, Rothbard JB, et al. (1988) Characterization of a major encephalitogenic T cell epitope in SJL/J mice with synthetic oligopeptides of myelin basic protein. J Neuroimmunol 19: 21-32.
62. Stevens DB, Chen K, Seitz RS, Sercarz EE, Bronstein JM, (1999) Oligodendrocyte-specific protein peptides induce experimental autoimmune encephalomyelitis in SJL/J mice. J Immunol 162: 7501-7509.