The cryptic interplay between systemic lupus erythematosus and infections

Autoimmunity Reviews

Volumn 13, Issue 2, 2014, Pages 96-102

  Rigante, Donato ^a   Mazzoni, Marta Benedetta ^b   Esposito, Susanna ^b  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CHOLERA TOXIN B SUBUNIT; CORTICOSTEROID; CROSS REACTING ANTIGEN; HLA DR2 ANTIGEN; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 3; MICRORNA; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TOXIN; VIRUS DNA; VIRUS PROTEIN;

ANTIBODY PRODUCTION; ANTIGEN PRESENTING CELL; APOPTOSIS; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CD4+ CD25+ T LYMPHOCYTE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; ENDOGENOUS RETROVIRUS; EPSTEIN BARR VIRUS INFECTION; ERYTHEMA INFECTIOSUM; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENETICS; HEPATITIS C; HEPATITIS C VIRUS; HEREDITY; HUMAN; HUMAN PARVOVIRUS B19; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFECTION; LABORATORY; MOLECULAR MIMICRY; NONHUMAN; PATHOGENESIS; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; TORQUE TENO VIRUS; TORQUE TENO VIRUS INFECTION; TOXOPLASMA GONDII; TOXOPLASMOSIS; VIRUS; VIRUS LOAD; VIRUS TRANSMISSION;

AUTOANTIGENS; AUTOIMMUNITY; BACTERIAL INFECTIONS; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; VIRUS DISEASES;

EID: 84888013695     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2013.09.004     Document Type: Review

References (91)

1. Habibi S., Saleem M.A., Ramanan A.V. Juvenile systemic lupus erythematosus: review of clinical features and management. Indian Pediatr 2011, 48:879-887.
2. O'Neill S., Cervera R. Systemic lupus erythematosus. Best Pract Res Clin Rheumatol 2010, 24:841-855.
3. Hoffman I.E., Lauwerys B.R., De Keyser F., Huizinga T.W., Isenberg D., Cebecauer L., et al. Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis 2009, 68:412-415.
4. Doria A., Iaccarino L., Ghirardello A., Zampieri S., Arienti S., Sarzi-Puttini P., et al. Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 2006, 119:700-706.
5. Petty R.E., Laxer R.M. Systemic lupus erythematosus. Textbook of pediatric rheumatology 2005, 342-391. Elsevier Saunders, Philadelphia, PA. J.T. Cassidy, R.E. Petty, R.M. Laxer, C.B. Lindsley (Eds.).
6. Brunner H.I., Gladman D.D., Ibanez D., Urowitz M.D., Silverman E.D. Difference in disease features between childhood-onset and adult-onset systemic lupus erythematosus. Arthritis Rheum 2008, 58:556-562.
7. Samanta A., Roy S., Feehally J., Symmons D.P. The prevalence of systemic lupus erythematosus in whites and Indian Asian immigrants in Leicester City, UK. Br J Rheumatol 1992, 31:679-682.
8. Serdula M.K., Rhoads G.G. Frequency of systemic lupus erythematosus in different ethnic groups in Hawaii. Arthritis Rheum 1979, 22:328-333.
9. Huang J.L., Yao T.C., See L.C. Prevalence of pediatric systemic lupus erythematosus and juvenile chronic arthritis in a Chinese population: a nation-wide prospective population-based study in Taiwan. Clin Exp Rheumatol 2004, 22:776-780.
10. Kurahara D.K., Grandinetti A., Fujii L.L., Tokuda A.A., Galario J.A., Han M.J., et al. Visiting consultant clinics to study prevalence rates of juvenile rheumatoid arthritis and childhood systemic lupus erythematosus across dispersed geographic areas. J Rheumatol 2007, 34:425-429.
11. Lehman T.J., McCurdy D.K., Bernstein B.H., King K.K., Hanson V. Systemic lupus erythematosus in the first decade of life. Pediatrics 1989, 83:235.
12. Taddio A., Rossetto E., Rosé C.D., Brescia A.M., Bracaglia C., Cortis E., et al. Prognostic impact of atypical presentation in pediatric systemic lupus erythematosus: results from a multicenter study. J Pediatr 2010, 156:972-977.
13. Font J., Cervera R., Espinosa G., Pallarés L., Ramos-Casals M., Jiménez S., et al. Systemic lupus erythematosus (SLE) in childhood: analysis of clinical and immunological findings in 34 patients and comparison with SLE characteristics in adults. Ann Rheum Dis 1998, 57:456-459.
14. Rood M.J., ten Cate R., van Suijlekom-Smit L.W., den Ouden E.J., Ouwerkerk F.E., Breedveld F.C., et al. Childhood-onset systemic lupus erythematosus: clinical presentation and prognosis in 31 patients. Scand J Rheumatol 1999, 28:222-226.
15. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J., Rothfield N.F., et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271.
16. Petri M., Orbai A.M., Alarcòn G.S., Gordon C., Merrill J.T., Fortin P.R., et al. Derivation and validation of the systemic lupus erythematosus. International collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 2012, 64:2677-2686.
17. Zandman-Goddard G., Solomon M., Rosman Z., Peeva E., Shoenfeld Y. Environment and lupus-related diseases. Lupus 2012, 21:241-250.
18. Avçin T., Canova M., Guilpain P., Guillevin L., Kallenberg C.G., Tincani A., et al. Infections, connective tissue diseases and vasculitis. Clin Exp Rheumatol 2008, 26(1 Suppl. 48):S18-S26.
19. Sebastiani G.D., Galeazzi M. Infection-genetics relationship in systemic lupus erythematosus. Lupus 2009, 18:1169-1175.
20. Sciascia S., Ceberio L., Garcia-Fernandez C., Roccatello D., Karim Y., Cuadrado M.J. Systemic lupus erythematosus and infections: clinical importance of conventional and upcoming biomarkers. Autoimmun Rev 2012, 12:157-163.
21. Sciascia S., Bertolaccini M.L., Baldovino S., Roccatello D., Khamashta M.A., Sanna G. Central nervous system involvement in systemic lupus erythematosus: overview on classification criteria. Autoimmun Rev 2013, 12:426-429.
22. Barzilai O., Sherer Y., Ram M., Izhaky D., Anaya J.M., Shoenfeld Y. Epstein-Barr virus and cytomegalovirus in autoimmune diseases: are they truly notorious? A preliminary report. Ann N Y Acad Sci 2007, 1108:567-577.
23. Koutouzov S., Mathian A., Dalloul A. Type-I interferons and systemic lupus erythematosus. Autoimmun Rev 2006, 5:554-562.
24. Santana-de Anda K., Gómez-Martín D., Díaz-Zamudio M., Alcocer-Varela J. Interferon regulatory factors: beyond the antiviral response and their link to the development of autoimmune pathology. Autoimmun Rev 2011, 11:98-103.
25. Sekigawa I., Kawasaki M., Ogasawara H., Kaneda K., Kaneko H., Takasaki Y., et al. DNA methylation: its contribution to systemic lupus erythematosus. Clin Exp Med 2006, 6:69-106.
26. Kivity S., Agmon-Levin N., Blank M., Shoenfeld Y. Infections and autoimmunity-friends or foes?. Trends Immunol 2009, 30:409-414.
27. Arbuckle M.R., McClain M.T., Rubertone M.V., Scofield R.H., Dennis G.J., James J.A., et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003, 349:1526-1533.
28. Edwards C.J., Syddall H., Goswami R., Goswami P., Dennison E.M., Cooper C. Infections in infancy and the presence of antinuclear antibodies in adult life. Lupus 2006, 15:213-217.
29. Zandman-Goddard G., Berkun Y., Barzilai O., Boaz M., Ram M., Anaya J.M., et al. Neuropsychiatric lupus and infectious triggers. Lupus 2008, 17:380-384.
30. Zandman-Goddard G., Berkun Y., Barzilai O., Boaz M., Blank M., Ram M., et al. Exposure to Epstein-Barr virus infection is associated with mild systemic lupus erythematosus disease. Ann N Y Acad Sci 2009 Sep, 1173:658-663.
31. Praprotnik S., Sodin-Semrl S., Tomsic M., Shoenfeld Y. The curiously suspicious: infectious disease may ameliorate an ongoing autoimmune destruction in systemic lupus erythematosus patients. J Autoimmun 2008, 30:37-41.
32. Keynan Y., Card C.M., McLaren P.J., Dawood M.R., Kasper K., Fowke K.R. The role of regulatory T cells in chronic and acute viral infections. Clin Infect Dis 2008, 46:1046-1052.
33. Bopp T., Jonuleit H., Schmitt E. Regulatory T cells. The renaissance of the suppressor T cells. Ann Med 2007, 39:322-334.
34. Doria A., Sarzi-Puttini P., Shoenfeld Y. Infections, rheumatism and autoimmunity: the conflicting relationship between humans and their environment. Autoimmun Rev 2008, 8:1-4.
35. Perl A. Mechanisms of viral pathogenesis in rheumatic disease. Ann Rheum Dis 1999, 58:454-461.
36. Evans A.S. E.B. virus antibody in systemic lupus erythematosus. Lancet 1971, 1(7707):1023-1024.
37. De Carvalho J.F., Pereira R.M., Shoenfeld Y. The mosaic of autoimmunity: the role of environmental factors. Front Biosci 2009, 1:501-509.
38. James J.A., Kaufman K.M., Farris A.D., Taylor-Albert E., Lehman T.J., Harley J.B. An increased prevalence of Epstein Barr virus infection in young patients suggests a possible etiology for systemic lupus erythematosus. J Clin Invest 1997, 100:3019-3026.
39. Gergely P., Pullmann R., Stancato C., Otvos L., Koncz A., Blazsek A., et al. Increased prevalence of transfusion transmitted virus and cross reactivity with immunodominant epitopes of the HRES-1/p28 endogenous retroviral autoantigen in patients with systemic lupus erythematosus. Clin Immunol 2005, 116:124-134.
40. Arbuckle M.R., Gross T., Scofield R.H., Hinshaw L.B., Chang A.C., Taylor F.B., et al. Lupus humoral autoimmunity induced in a primate model by short peptide immunization. J Invest Med 1998, 46:58-65.
41. Yadav P., Tran H., Ebegbe R., Gottlieb P., Wei H., Lewis R.H., et al. Antibodies elicited in response to EBNA-1 may cross-react with dsDNA. PLoS One 2011, 6:e14488.
42. Sundar K., Jacques S., Gottlieb P., Villars R., Benito M.E., Taylor D.K., et al. Expression of the Epstein-Barr virus nuclear antigen-1 (EBNA-1) in the mouse can elicit the production of anti-dsDNA and anti-Sm antibodies. J Autoimmun 2004, 23:127-140.
43. McClain M.T., Heinlen L.D., Dennis G.J., Roebuck J., Harley J.B., James J.A., et al. Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry. Nat Med 2005, 11:85-89.
44. James J., Harley J.B., Scofield R.H. Role of Epstein-Barr Virus in systemic lupus erythematosus. Curr Opin Rheumatol 2006, 18:462-467.
45. Peters A.L., Stunz L.L., Meyerholz D.K., Mohan C., Bishop G.A. Latent membrane protein 1, the EBV-encoded oncogenic mimic of CD40, accelerates autoimmunity in B6.Sle1 mice. J Immunol 2010, 185:4053-4062.
46. Arcipowski K.M., Bishop G.A. Roles of the kinase TAK1 in TRAF6-dependent signaling by CD40 and its oncogenic viral mimic, LMP1. PLoS One 2012, 7:e42478.
47. Poole B.D., Templeton A.K., Guthridge J.M., Brown E.J., Harley J.B., James J.A. Aberrant Epstein-Barr viral infection in systemic lupus erythematosus. Autoimmun Rev 2009, 8:337-342.
48. Niller H.H., Wolf H., Ay E., Minarovits J. Epigenetic dysregulation of Epstein-Barr virus latency and development of autoimmune disease. Adv Exp Med Biol 2011, 711:82-102.
49. Francis L., Perl A. Infection in systemic lupus erythematosus: friend or foe?. Int J Clin Rheumatol 2010, 5:59-74.
50. Moon U.Y., Park S.J., Oh S.T., Kim W.U., Park S.H., Lee S.H., et al. Patients with systemic lupus erythematosus have abnormally elevated Epstein-Barr virus load in blood. Arthritis Res Ther 2004, 6:295-302.
51. Goddard G.Z., Shoenfeld Y. Infections and SLE. Autoimmunity 2005, 38:473-485.
52. Zandman-Goddard G., Shoenfeld Y. Infections and SLE. Autoimmunity 2005, 38:473-485.
53. Kang I., Quan T., Nolasco H., Park S.H., Hong M.S., Crouch J., et al. Defective control of latent Epstein-Barr virus infection in systemic lupus erythematosus. J Immunol 2004, 172:1287-1294.
54. Blank M., Shoenfeld Y., Perl A. Cross-talk of the environment with the host genome and the immune system through endogenous retroviruses in systemic lupus erythematosus. Lupus 2009, 18:1136-1143.
55. Poole B.D., Scofield R.H., Harley J.B., James J.A. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity 2006, 39:63-70.
56. Pavlovic M., Kats A., Cavallo M., Shoenfeld Y. Clinical and molecular evidence for association of SLE with parvovirus B19. Lupus 2010, 19:783-792.
57. Perl A., Fernandez D., Telarico T., Phillips P.E. Endogenous retroviral pathogenesis in lupus. Curr Opin Rheumatol 2010, 22:483-492.
58. Gergely P., Perl A., Poor G. Possible pathogenic nature of the recently discovered TT virus: does it play a role in autoimmune rheumatic diseases?. Autoimmun Rev 2006, 6:5-9.
59. Emlen W., Niebur J.A., Kadera R. Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol 1994, 152:3685-3692.
60. Pullmann R., Bonilla E., Phillips P.E., Middleton F.A., Perl A. Haplotypes of the HRES-1 endogenous retrovirus are associated with development and disease manifestations of systemic lupus erythematosus. Arthritis Rheum 2008, 58:532-540.
61. Yoshiki T., Mellors R.C., Strand M., August J.T. The viral envelope glycoprotein of murine leukemia virus and the pathogenesis of immune complex glomerulonephritis of New Zealand mice. J Exp Med 1974, 140:1011-1027.
62. Perl A., Nagy G., Koncz A., Gergely P., Fernandez D., Doherty E., et al. Molecular mimicry and immunomodulation by the HRES-1 endogenous retrovirus in SLE. Autoimmunity 2008, 41:287-297.
63. Perl A., Colombo E., Dai H., Agarwal R., Mark K.A., Banki K., et al. Antibody reactivity to the HRES-1 endogenous retroviral element identifies a subset of patients with systemic lupus erythematosus and overlap syndromes. Correlation with antinuclear antibodies and HLA class II alleles. Arthritis Rheum 1995, 38:1660-1671.
64. Perl A., Fernandez D.R., Telarico T., Doherty E., Francis L., Phillips P.E. T-cell and B-cell signaling biomarkers and treatment targets in lupus. Curr Opin Rheumatol 2009, 21:454-464.
65. Hayashi T., Lee S., Ogasawara H., Sekigawa I., Iida N., Tomino Y., et al. Exacerbation of systemic lupus erythematosus related to cytomegalovirus infection. Lupus 1998, 7:561-564.
66. Nawata M., Seta N., Yamada M., Sekigawa I., Lida N., Hashimoto H. Possible triggering effect of cytomegalovirus infection on systemic lupus erythematosus. Scand J Rheumatol 2001, 30:360-362.
67. Ramos-Casals M., Font J., García-Carrasco M., Cervera R., Jiménez S., Trejo O., et al. Hepatitis C virus infection mimicking systemic lupus erythematosus: study of hepatitis C virus infection in a series of 134 Spanish patients with systemic lupus erythematosus. Arthritis Rheum 2000, 43:2801-2806.
68. Karakov Y., Dilek K., Güllülü M., Yavuz M., Ersoy A., Akalyn H., et al. Prevalence of hepatitis C virus antibody in patients with systemic lupus erythematosus. Ann Rheum Dis 1997, 56:570-571.
69. Mercado U., Avendaño-Reyes M., Araiza-Casillas R., Díaz-Molina R. Prevalence of antibodies against hepatitis C and B viruses in patients with systemic lupus erythematosus. Rev Gastroenterol Mex 2005, 70:399-401.
70. Pisetsky D.S. The role of innate immunity in the induction of autoimmunity. Autoimmun Rev 2008, 8:69-72.
71. Corthésy B. Role of secretory IgA in infection and maintenance of homeostasis. Autoimmun Rev 2013, 12:661-665.
72. Green N.M., Marshak-Rothstein A. Toll-like receptor driven B cell activation in the induction of systemic autoimmunity. Semin Immunol 2011, 23:106-112.
73. Riethmüller J., Riehle A., Grassmé H., Gulbins E. Membrane rafts in host-pathogen interactions. Biochim Biophys Acta 2006, 1758:2139-2147.
74. Jury E.C., Kabouridis P.S., Flores-Borja F., Mageed R.A., Isenberg D.A. Altered lipid raft-associated signaling and ganglioside expression in T lymphocytes from patients with systemic lupus erythematosus. J Clin Invest 2004, 113:1176-1187.
75. Deng G.M., Tsokos G.C. Cholera toxin B accelerates disease progression in lupus-prone mice by promoting lipid raft aggregation. J Immunol 2008, 181:4019-4026.
76. Fischer S., Agmon-Levin N., Shapira Y., Porat Katz B.S., Graell E., Cervera R., et al. Toxoplasma gondii: bystander or cofactor in rheumatoid arthritis. Immunol Res 2013, 56:287-292.
77. Lakota K., Zigon P., Mrak-Poljsak K., Rozman B., Shoenfeld Y., Sodin-Semrl S. Antibodies against acute phase proteins and their functions in the pathogenesis of disease: a collective profile of 25 different antibodies. Autoimmun Rev 2011, 10:779-789.
78. Strachan D.P. Hay fever, hygiene, and household size. BMJ 1989, 299:1259-1260.
79. Liu G., Zhao Y. Toll-like receptors and immune regulation: their direct and indirect modulation on regulatory CD4+ CD25+ T cells. Immunology 2007, 122:149-156.
80. Bach J.F. Protective role of infections and vaccinations on autoimmune diseases. J Autoimmun 2001, 16:347-353.
81. Zandman-Goddard G., Shoenfeld Y. Parasitic infection and autoimmunity. Lupus 2009, 18:1144-1148.
82. Butcher G.A. Does malaria select for predisposition to autoimmune disease?. J R Soc Med 1991, 84:451-453.
83. Greenwood B., Corrah T. Systemic lupus erythematosus in African immigrants. Lancet 2001, 358(9288):1182.
84. Ram M., Anaya J.M., Barzilai O., Izhaky D., Porat Katz B.S., Blank M., et al. The putative protective role of hepatitis B virus (HBV) infection from autoimmune disorders. Autoimmun Rev 2008, 7:621-625.
85. Chen M., Aosai F., Norose K., Mun H.S., Ishikura H., Hirose S., et al. Toxoplasma gondii infection inhibits the development of lupus-like syndrome in autoimmune (New Zealand black×New Zealand white) F1 mice. Int Immunol 2004, 16:937-946.
86. Graham R.R., Ortmann W., Rodine P., Espe K., Langefeld C., Lange E., et al. Specific combinations of HLA-DR2 and DR3 class II haplotypes contribute graded risk for disease susceptibility and autoantibodies in human SLE. Eur J Hum Genet 2007, 15:823-830.
87. Chakravarty E.F. Viral infection and reactivation in autoimmune disease. Arthritis Rheum 2008, 58:2949-2957.
88. Morris D.L., Taylor K.E., Fernando M.M., Nititham J., Alarcón-Riquelme M.E., Barcellos L.F., et al. Unraveling multiple MHC gene associations with systemic lupus erythematosus: model choice indicates a role for HLA alleles and non-HLA genes in Europeans. Am J Hum Genet 2012, 91:778-793.
89. Shoenfeld Y., Gilburd B., Abu-Shakra M., Amital H., Barzilai O., Berkun Y., et al. The mosaic of autoimmunity: genetic factors involved in autoimmune diseases-2008. Isr Med Assoc J 2008, 10:3-7.
90. Schulze C., Munoz L.E., Franz S., Sarter K., Chaurio R.A., Gaipl U.S., et al. Clearance deficiency-a potential link between infections and autoimmunity. Autoimmun Rev 2008, 8:5-8.
91. Kim W.U., Sreih A., Bucala R. Toll-like receptors in systemic lupus erythematosus; prospects for therapeutic intervention. Autoimmun Rev 2009, 8:204-208.