Malondialdehyde modification of myelin oligodendrocyte glycoprotein leads to increased immunogenicity and encephalitogenicity

European Journal of Immunology

Volumn 37, Issue 7, 2007, Pages 1986-1995

  Wållberg, Maja ^a   Bergquist, Jonas ^b   Achour, Adnane ^a   Breij, Esther ^c   Harris, Robert A ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Autoimmunity; EAE; Immune response; Oxidation; Post translational modification

Indexed keywords

AUTOANTIGEN; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 23; MALONALDEHYDE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; RECOMBINANT PROTEIN; SCAVENGER RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BIOCHEMISTRY; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; MOLECULAR MODEL; MOLECULAR WEIGHT; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FOURIER ANALYSIS; ISOELECTRIC FOCUSING; MALONDIALDEHYDE; MICE; MYELIN-ASSOCIATED GLYCOPROTEIN; POLYMERASE CHAIN REACTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RATS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 34447537998     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636912     Document Type: Article

References (51)

1. Zinkernagel, R. M., Antiinfection immunity and autoimmunity. Ann. N. Y. Acad. Sci. 2002. 958: 3-6.
2. Leib, S. L., Kim, Y. S., Chow, L. L., Sheldon, R. A. and Tauber, M. G., Reactive oxygen intermediates contribute to necrotic and apoptotic neuronal injury in an infant rat model of bacterial meningitis due to group B streptococci. J. Clin. Invest. 1996. 98: 2632-2639.
3. Wuttge, D. M., Bruzelius, M. and Stemme, S., T-cell recognition of lipid peroxidation products breaks tolerance to self proteins. Immunology 1999. 98: 273-279.
4. Abraham, R., Singh, N., Mukhopadhyay, A., Basu, S. K., Bal, V. and Rath, S., Modulation of immunogenicity and antigenicity of proteins by maleylation to target scavenger receptors on macrophages. J. Immunol. 1995. 154: 1-8.
5. Abraham, R., Choudhury, A., Basu, S. K., Bal, V. and Rath, S., Disruption of T cell tolerance by directing a self antigen to macrophage-specific scavenger receptors. J. Immunol. 1997. 158: 4029-4035.
6. Singh, N., Bhatia, S., Abraham, R., Basu, S. K., George, A., Bal, V. and Rath, S., Modulation of T cell cytokine profiles and peptide-MHC complex availability in vivo by delivery to scavenger receptors via antigen maleylation. J. Immunol. 1998. 160: 4869-4880.
7. Goldstein, J. L., Ho, Y. K., Basu, S. K. and Brown, M. S., Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA 1979. 76: 333-337.
8. Podrez, E. A., Febbraio, M., Sheibani, N., Schmitt, D., Silverstein, R. L., Hajjar, D. P., Cohen, P. A. et al., Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J. Clin. Invest. 2000. 105: 1095-1108.
9. Uchida, K., Role of reactive aldehyde in cardiovascular diseases. Free Radic. Biol. Med. 2000. 28: 1685-1696.
10. van der Veen, R. C. and Roberts, L. J., Contrasting roles for nitric oxide and peroxynitrite in the peroxidation of myelin lipids. J. Neuroimmunol. 1999. 95: 1-7.
11. Espejo, C., Penkowa, M., Saez-Torres, I., Hidalgo, J., Garcia, A., Montalban, X. and Martinez-Caceres, E. M., Interferon-gamma regulates oxidative stress during experimental autoimmune encephalomyelitis. Exp. Neurol. 2002. 177: 21-31.
12. Keles, M. S., Taysi, S., Sen, N., Aksoy, H. and Akcay, F., Effect of corticosteroid therapy on serum and CSF malondialdehyde and antioxidant proteins in multiple sclerosis. Can. J. Neurol. Sci. 2001. 28: 141-143.
13. Greer, J. M., Denis, B., Sobel, R. A. and Trifilieff, E., Thiopalmitoylation of myelin proteolipid protein epitopes enhances immunogenicity and encephalitogenicity. J. Immunol. 2001. 166: 6907-6913.
14. Wood, D. D. and Moscarello, M. A., The isolation, characterization, and lipid-aggregating properties of a citrulline containing myelin basic protein. J. Biol. Chem. 1989. 264: 5121-5127.
15. Moscarello, M. A., Wood, D. D., Ackerley, C. and Boulias, C., Myelin in multiple sclerosis is developmentally immature. J. Clin. Invest. 1994. 94: 146-154.
16. Tranquill, L. R., Cao, L., Ling, N. C., Kalbacher, H., Martin, R. M. and Whitaker, J. N., Enhanced T cell responsiveness to citrulline-containing myelin basic protein in multiple sclerosis patients. Mult. Scler. 2000. 6: 220-225.
17. Cao, L., Sun, D. and Whitaker, J. N., Citrullinated myelin basic protein induces experimental autoimmune encephalomyelitis in Lewis rats through a diverse T cell repertoire. J. Neuroimmunol. 1998. 88: 21-29.
18. Tuohy, V. K., Yu, M., Yin, L., Kawczak, J. A., Johnson, J. M., Mathisen, P. M., Weinstock-Guttman, B. and Kinkel, R. P., The epitope spreading cascade during progression of experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Rev. 1998. 164: 93-100.
19. Sollid, L. M., Molecular basis of celiac disease. Annu. Rev. Immunol. 2000. 18: 53-81.
20. Doyle, H. A. and Mamula, M. J., Post-translational protein modifications in antigen recognition and autoimmunity. Trends Immunol. 2001. 22: 443-449.
21. Doyle, H. A. and Mamula, M. J., Posttranslational protein modifications: New flavors in the menu of autoantigens. Curr. Opin. Rheumatol. 2002. 14: 244-249.
22. Cloos, P. A. and Christgau, S., Post-translational modifications of proteins: Implications for aging, antigen recognition, and autoimmunity. Biogerontology 2004. 5: 139-158.
23. Anderton, S. M., Post-translational modifications of self antigens: Implications for autoimmunity. Curr. Opin. Immunol. 2004. 16: 753-758.
24. McLaurin, J., Hashim, G. and Moscarello, M. A., An antibody specific for component 8 of myelin basic protein from normal brain reacts strongly with component 8 from multiple sclerosis brain. J. Neurochem. 1992. 59: 1414-1420.
25. Cao, L., Goodin, R., Wood, D., Moscarello, M. A. and Whitaker, J. N., Rapid release and unusual stability of immunodominant peptide 45-89 from citrullinated myelin basic protein. Biochemistry 1999. 38: 6157-6163.
26. Pritzker, L. B., Joshi, S., Gowan, J. J., Harauz, G. and Moscarello, M. A., Deimination of myelin basic protein. 1. Effect of deimination of arginyl residues of myelin basic protein on its structure and susceptibility to digestion by cathepsin D. Biochemistry 2000. 39: 5374-5381.
27. Mamula, M. J., Gee, R. J., Elliott, J. I., Sette, A., Southwood, S., Jones, P. J. and Blier, P. R., Isoaspartyl post-translational modification triggers autoimmune responses to self-proteins. J. Biol. Chem. 1999. 274: 22321-22327.
28. van Venrooij, W. J. and Pruijn, G. J., Citrullination: A small change for a protein with great consequences for rheumatoid arthritis. Arthritis Res. 2000. 2: 249-251.
29. Allison, M. E. and Fearon, D. T., Enhanced immunogenicity of aldehyde-bearing antigens: A possible link between innate and adaptive immunity. Eur. J. Immunol. 2000. 30: 2881-2887.
30. Shakushiro, K., Yamasaki, Y., Nishikawa, M. and Takakura, Y., Efficient scavenger receptor-mediated uptake and cross-presentation of negatively charged soluble antigens by dendritic cells. Immunology 2004. 112: 211-218.
31. Nicoletti, A., Caligiuri, G., Tornberg, I., Kodama, T., Stemme, S. and Hansson, G. K., The macrophage scavenger receptor type A directs modified proteins to antigen presentation. Eur. J. Immunol. 1999. 29: 512-521.
32. Ricci, R., Sumara, G., Sumara, I., Rozenberg, I., Kurrer, M., Akhmedov, A., Hersberger, M. et al., Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science 2004. 306: 1558-1561.
33. Gordon, S., Pattern recognition receptors: Doubling up for the innate immune response. Cell 2002. 111: 927-930.
34. Horiuchi, S., Sakamoto, Y. and Sakai, M., Scavenger receptors for oxidized and glycated proteins. Amino Acids 2003. 25: 283-292.
35. Krieger, M. and Herz, J., Structures and functions of multiligand lipoprotein receptors: Macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu. Rev. Biochem. 1994. 63: 601-637.
36. Podrez, E. A., Hoppe, G., O'Neil, J. and Hoff, H. F., Phospholipids in oxidized LDL not adducted to apoB are recognized by the CD36 scavenger receptor. Free Radic. Biol. Med. 2003. 34: 356-364.
37. Krieger, M. and Stern, D. M., Series introduction: Multiligand receptors and human disease. J. Clin. Invest. 2001. 108: 645-647.
38. Carrasco-Marin, E., Paz-Miguel, J. E., Lopez-Mato, P., Alvarez-Dominguez, C. and Leyva-Cobian, F., Oxidation of defined antigens allows protein unfolding and increases both proteolytic processing and exposes peptide epitopes which are recognized by specific T cells. Immunology 1998. 95: 314-321.
39. Cua, D. J., Sherlock, J., Chen, Y., Murphy, C. A., Joyce, B., Seymour, B., Lucian, L. et al., Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003. 421: 744-748.
40. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T. et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005. 201: 233-240.
41. Andersson, A., Kokkola, R., Wefer, J., Erlandsson-Harris, H. and Harris, R. A., Differential macrophage expression of IL-12 and IL-23 upon innate immune activation defines rat autoimmune susceptibility. J. Leukoc. Biol. 2004. 76: 1118-1124.
42. Linton, M. F. and Fazio, S., Class A scavenger receptors, macrophages, and atherosclerosis. Curr. Opin. Lipidol. 2001. 12: 489-495.
43. Bastos, K. R., Marinho, C. R., Barboza, R., Russo, M., Alvarez, J. M. and D'Imperio Lima, M. R., What kind of message does IL-12/IL-23 bring to macrophages and dendritic cells? Microbes Infect. 2004. 6: 630-636.
44. 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. 1994. 153: 4349-4356.
45. Palinski, W., Rosenfeld, M. E., Yla-Herttuala, S., Gurtner, G. C., Socher, S. S., Butler, S. W., Parthasarathy, S. et al., Low density lipoprotein undergoes oxidative modification in vivo. Proc. Natl. Acad. Sci. USA 1989. 86: 1372-1376.
46. Nilsson, S., Wetterhall, M., Bergquist, J., Nyholm, L. and Markides, K. E., A simple and robust conductive graphite coating for sheathless electrospray emitters used in capillary electrophoresis/mass spectrometry. Rapid Commun. Mass Spectrom. 2001. 15: 1997-2000.
47. Bergquist, J., Palmblad, M., Wetterhall, M., Hakansson, P. and Markides, K. E., Peptide mapping of proteins in human body fluids using electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Mass Spectrom. Rev. 2002. 21: 2-15.
48. Collaborative Computational Project, N., The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994. 50: 760-763.
49. Abdul-Majid, K. B., Jirholt, J., Stadelmann, C., Stefferl, A., Kjellen, P., Wallstrom, E., Holmdahl, R. et al., Screening of several H-2 congenic mouse strains identified H-2(q) mice as highly susceptible to MOG-induced EAE with minimal adjuvant requirement. J. Neuroimmunol. 2000. 111: 23-33.
50. Wållberg, M., Wefer, J. and Harris, R. A., Vaccination with myelin oligodendrocyte glycoprotein adsorbed to alum effectively protects DBA/1 mice from experimental autoimmune encephalomyelitis. Eur. J. Immunol. 2003. 33: 1539-1547.
51. Wefer, J., Harris, R. A. and Lobell, A., Protective DNA vaccination against experimental autoimmune encephalomyelitis is associated with induction of IFNbeta. J. Neuroimmunol. 2004. 149: 66-76.