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Potential Role of Bacterial Infection in Autoimmune Diseases: A New Aspect of Molecular Mimicry

  • Alam, Jehan (Department of Immunology and Molecular Microbiology, Dental research Institute, Seoul National University School of Dentistry) ;
  • Kim, Yong Chul (Department of Immunology and Molecular Microbiology, Dental research Institute, Seoul National University School of Dentistry) ;
  • Choi, Youngnim (Department of Immunology and Molecular Microbiology, Dental research Institute, Seoul National University School of Dentistry)
  • Received : 2013.11.28
  • Accepted : 2014.01.13
  • Published : 2014.02.28

Abstract

Molecular mimicry is an attractive mechanism for triggering autoimmunity. In this review, we explore the potential role of evolutionary conserved bacterial proteins in the production of autoantibodies with focus on granulomatosis with polyangiitis (GPA) and rheumatoid arthritis (RA). Seven autoantigens characterized in GPA and RA were BLASTed against a bacterial protein database. Of the seven autoantigens, proteinase 3, type II collagen, binding immunoglobulin protein, glucose-6-phosphate isomerase, ${\alpha}$-enolase, and heterogeneous nuclear ribonuclear protein have well-conserved bacterial orthologs. Importantly, those bacterial orthologs are also found in human-associated bacteria. The wide distribution of the highly conserved stress proteins or enzymes among the members of the normal flora and common infectious microorganisms raises a new question on how cross-reactive autoantibodies are not produced during the immune response to these bacteria in most healthy people. Understanding the mechanisms that deselect auto-reactive B cell clones during the germinal center reaction to homologous foreign antigens may provide a novel strategy to treat autoimmune diseases.

Keywords

References

  1. Albert, L. J. and R. D. Inman. 1999. Molecular mimicry and autoimmunity. N. Engl. J. Med. 341: 2068-2074. https://doi.org/10.1056/NEJM199912303412707
  2. Libbey, J. E., L. L. McCoy, and R. S. Fujinami. 2007. Molecular mimicry in multiple sclerosis. Int. Rev. Neurobiol. 79: 127-147. https://doi.org/10.1016/S0074-7742(07)79006-2
  3. Ang, C. W., B. C. Jacobs, and J. D. Laman. 2004. The Guillain-Barré syndrome: a true case of molecular mimicry. Trends Immunol. 25: 61-66. https://doi.org/10.1016/j.it.2003.12.004
  4. Guilherme, L., J. Kalil, and M. Cunningham. 2006. Molecular mimicry in the autoimmune pathogenesis of rheumatic heart disease. Autoimmunity 39: 31-39. https://doi.org/10.1080/08916930500484674
  5. Hu, N., J. Westra, and C. G. Kallenberg. 2009. Membranebound proteinase 3 and its receptors: relevance for the pathogenesis of Wegener's Granulomatosis. Autoimmun. Rev. 8: 510-514. https://doi.org/10.1016/j.autrev.2008.01.003
  6. Chen, M. and C. G. Kallenberg. 2010. The environment, geoepidemiology and ANCA-associated vasculitides. Autoimmun. Rev. 9: A293-A298. https://doi.org/10.1016/j.autrev.2009.10.008
  7. Watts, R. A. and D. G. I. Scott. 2012. ANCA vasculitis: to lump or split? Rheumatology (Oxford) 51: 2115-2117. https://doi.org/10.1093/rheumatology/kes230
  8. Pinching, A. J., A. J. Rees, B. A. Pussell, C. M. Lockwood, R. S. Mitchison, and D. K. Peters. 1980. Relapses in Wegener's granulomatosis: the role of infection. Br. Med. J. 281: 836-838. https://doi.org/10.1136/bmj.281.6244.836
  9. Stegeman, C. A., J. W. Tervaert, W. J. Sluiter, W. L. Manson, P. E. de Jong, and C. G. Kallenberg. 1994. Association of chronic nasal carriage of Staphylococcus aureus and higher relapse rates in Wegener granulomatosis. Ann. Intern. Med. 120: 12-17. https://doi.org/10.7326/0003-4819-120-1-199401010-00003
  10. Stegeman, C. A., J. W. Tervaert, P. E. de Jong, and C. G. Kallenberg. 1996. Trimethoprim-sulfamethoxazole (co-trimoxazole) for the prevention of relapses of Wegener's granulomatosis. Dutch Co-Trimoxazole Wegener Study Group. N. Engl. J. Med. 335: 16-20. https://doi.org/10.1056/NEJM199607043350103
  11. Kain, R., M. Exner, R. Brandes, R. Ziebermayr, D. Cunningham, C. A. Alderson, A. Davidovits, I. Raab, R. Jahn, O. Ashour, S. Spitzauer, G. Sunder-Plassmann, M. Fukuda, P. Klemm, A. J. Rees, and D. Kerjaschki. 2008. Molecular mimicry in pauci-immune focal necrotizing glomerulonephritis. Nat. Med. 14: 1088-1096. https://doi.org/10.1038/nm.1874
  12. Kim, Y. C., J. E. Shin, S. H. Lee, W. J. Chung, Y. S. Lee, B. K. Choi, and Y. Choi. 2011. Membrane-bound proteinase 3 and PAR2 mediate phagocytosis of non-opsonized bacteria in human neutrophils. Mol. Immunol. 48: 1966-1974. https://doi.org/10.1016/j.molimm.2011.05.026
  13. Pati, A., J. Sikorski, M. Nolan, A. Lapidus, A. Copeland, T. Glavina Del Rio, S. Lucas, F. Chen, H. Tice, S. Pitluck, J. F. Cheng, O. Chertkov, T. Brettin, C. Han, J. C. Detter, C. Kuske, D. Bruce, L. Goodwin, P. Chain, P. D'haeseleer, A. Chen, K. Palaniappan, N. Ivanova, K. Mavromatis, N. Mikhailova, M. Rohde, B. J. Tindall, M. Göker, J. Bristow, J. A. Eisen, V. Markowitz, P. Hugenholtz, N. C. Kyrpides, and H. P. Klenk. 2009. Complete genome sequence of Saccharomonospora viridis type strain (P101). Stand. Genomic Sci. 1: 141-149. https://doi.org/10.4056/sigs.20263
  14. Wegner, N., R. Wait, and P. J. Venables. 2009. Evolutionarily conserved antigens in autoimmune disease: implications for an infective aetiology. Int. J. Biochem. Cell Biol. 41: 390-397. https://doi.org/10.1016/j.biocel.2008.09.012
  15. Artandi, S. E., K. L. Calame, S. L. Morrison, and V. R. Bonagura. 1992. Monoclonal IgM rheumatoid factors bind IgG at a discontinuous epitope comprised of amino acid loops from heavy-chain constant-region domains 2 and 3. Proc. Natl. Acad. Sci. USA 89: 94-98. https://doi.org/10.1073/pnas.89.1.94
  16. Schellekens, G. A., B. A. de Jong, F. H. van den Hoogen, L. B. van de Putte, and W. J. van Venrooij. 1998. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 101: 273-281. https://doi.org/10.1172/JCI1316
  17. Song, Y. W. and E. H. Kang. 2010. Autoantibodies in rheumatoid arthritis: rheumatoid factors and anticitrullinated protein antibodies. QJM. 103: 139-146. https://doi.org/10.1093/qjmed/hcp165
  18. Bateman, A., S. R. Eddy, and C. Chothia. 1996. Members of the immunoglobulin superfamily in bacteria. Protein Sci. 5: 1939-1941. https://doi.org/10.1002/pro.5560050923
  19. Cho, Y. G., M. L. Cho, S. Y. Min, and H. Y. Kim. 2007. Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun. Rev. 7: 65-70. https://doi.org/10.1016/j.autrev.2007.08.001
  20. Sammons, J. S., R. Localio, R. Xiao, S. E. Coffin, and T. Zaoutis. 2013. Clostridium difficile infection is associated with increased risk of death and prolonged hospitalization in children. Clin. Infect. Dis. 57: 1-8. https://doi.org/10.1093/cid/cit155
  21. Bottone, E. J. 2010. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 23: 382-398. https://doi.org/10.1128/CMR.00073-09
  22. Nakajima, N. and Y. Matsuura. 1997. Purification and characterization of konjac glucomannan degrading enzyme from anaerobic human intestinal bacterium, Clostridium butyricum- Clostridium beijerinckii group. Biosci. Biotechnol. Biochem. 61: 1739-1742. https://doi.org/10.1271/bbb.61.1739
  23. Lindquist, S. and E. A. Craig. 1988. The heat-shock proteins. Annu. Rev. Genet. 22: 631-677. https://doi.org/10.1146/annurev.ge.22.120188.003215
  24. Rajaiah, R. and K. D. Moudgil. 2009. Heat-shock proteins can promote as well as regulate autoimmunity. Autoimmun. Rev. 8: 388-393. https://doi.org/10.1016/j.autrev.2008.12.004
  25. Schubert, D., B. Maier, L. Morawietz, V. Krenn, and T. Kamradt. 2004. Immunization with glucose-6-phosphate isomerase induces T cell-dependent peripheral polyarthritis in genetically unaltered mice. J. Immunol. 172: 4503-4509. https://doi.org/10.4049/jimmunol.172.7.4503
  26. Fan, L. Y., M. Zong, Q. Wang, L. Yang, L. S. Sun, Q. Ye, Y. Y. Ding, and J. W. Ma. 2010. Diagnostic value of glucose- 6-phosphate isomerase in rheumatoid arthritis. Clin. Chim. Acta 411: 2049-2053. https://doi.org/10.1016/j.cca.2010.08.043
  27. Wygrecka, M., L. M. Marsh, R. E. Morty, I. Henneke, A.Guenther, J. Lohmeyer, P. Markart, and K. T. Preissner. 2009. Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 113: 5588- 5598. https://doi.org/10.1182/blood-2008-08-170837
  28. Pancholi, V., P. Fontan, and H. Jin. 2003. Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells. Microb. Pathog. 35: 293-303. https://doi.org/10.1016/j.micpath.2003.08.004
  29. Hoffmann, M. H., K. Skriner, S. Herman, C. Baumann, C. W. Steiner, C. Ospelt, B. Meyer, A. Gleiss, J. Pfatschbache, B. Niederreiter, J. Tuncel, G. Zanoni, and G. Steiner. 2011. Nucleic acid-stimulated antigen-presenting cells trigger T cells to induce disease in a rat transfer model of inflammatory arthritis. J. Autoimmun. 36: 288-300. https://doi.org/10.1016/j.jaut.2011.02.007
  30. Prati, C., E. Bertolini, E. Toussirot, and D. Wendling. 2010. Reactive arthritis due to Clostridium difficile. Joint Bone Spine. 77: 190-192. https://doi.org/10.1016/j.jbspin.2010.01.007
  31. Cuchacovich, R., S. Japa, W. Q. Huang, A. Calvo, L. Vega, R. B. Vargas, R. Singh, D. Flores, I. Castro, and L. R. Espinoza. 2002. Detection of bacterial DNA in Latin American patients with reactive arthritis by polymerase chain reaction and sequencing analysis. J. Rheumatol. 29: 1426-1429.
  32. Maggi, R. G., B. R. Mozayeni, E. L. Pultorak, B. C. Hegarty, J. M. Bradley, M. Correa, and E. B. Breitschwerdt. 2012. Bartonella spp. bacteremia and rheumatic symptoms in patients from Lyme disease-endemic region. Emerg. Infect. Dis. 18: 783-791.
  33. Hasanoglu, I., T. Guven, Y. Maras, R. Guner, M. A. Tasyaran, and Z. C. Acikgoz. 2013. Brucellosis as an aetiology of septic arthritis. Trop. Doct. in press: doi: 10.1177/0049475513512645.
  34. Steere, A. C., E. E. Drouin, and L. J. Glickstein. 2011. Relationship between immunity to Borrelia burgdorferi outer- surface protein A (OspA) and Lyme arthritis. Clin. Infect. Dis. 52 Suppl 3: s259-s265. https://doi.org/10.1093/cid/ciq117
  35. Chaudhry, M. A. and R. H. Scofield. 2013. Atypical rocky mountain spotted Fever with polyarticular arthritis. Am. J. Med. Sci. 346: 427-429. https://doi.org/10.1097/MAJ.0b013e318295c788
  36. Leo, J. C. and M. Skurnik. 2011. Adhesins of human pathogens from the genus Yersinia. Adv. Exp. Med. Biol. 715: 1-15. https://doi.org/10.1007/978-94-007-0940-9_1
  37. Bonet Llorach, M., D. Arnam Fernandez, J. Valles Daunis, J. Maymo Guarch, and H. Carbonell Abello. 1989. Haemophilus influenza septic arthritis in the adult. Clin. Rheumatol. 8: 292-293. https://doi.org/10.1007/BF02030090
  38. Acar, J. F. 1986. Serratia marcescens infections. Infect. Control 7: 273-278. https://doi.org/10.1017/S0195941700064201
  39. Yeoh, N., J. P. Burton, P. Suppiah, G. Reid, and S. Stebbings. 2013. The role of the microbiome in rheumatic diseases. Curr. Rheumatol. Rep. 15: 314. https://doi.org/10.1007/s11926-012-0314-y

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