Influenza A (H1N1) virus infection triggers severe pulmonary inflammation in lupus-prone mice following viral clearance

Journal of Autoimmunity

Volumn 57, Issue , 2015, Pages 66-76

  Slight Webb, Samantha R ^a   Bagavant, Harini ^a   Crowe, Sherry R ^a   James, Judith A ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Influenza; Lupus; MRL Faslpr; Pulmonary inflammation; SLE

Indexed keywords

ANTINUCLEAR ANTIBODY; AUTOANTIBODY; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA; VIRUS RNA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; M1 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE PREDISPOSITION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLOMERULONEPHRITIS; HEMAGGLUTINATION INHIBITION TEST; HISTOLOGY; IMMUNE RESPONSE; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LUNG INFECTION; LUNG INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SCORING SYSTEM; SPLEEN CELL; SPLENOMEGALY; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; VIRAL CLEARANCE; VIRAL RESPIRATORY TRACT INFECTION; VIRUS DETECTION; VIRUS PNEUMONIA; ANIMAL; APOPTOSIS; C57BL MOUSE; COMPLICATION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); KIDNEY DISEASE; LUNG; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; PNEUMONIA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

ANIMALS; ANTIBODIES, VIRAL; APOPTOSIS; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLUENZA A VIRUS, H1N1 SUBTYPE; KIDNEY DISEASES; LUNG; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE, INBRED C57BL; MICE, INBRED MRL LPR; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLENOMEGALY; T-LYMPHOCYTES; VIRAL MATRIX PROTEINS;

EID: 84922764379     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2014.12.003     Document Type: Article

References (53)

1. Dasaraju P.V., Liu C. Infections of the respiratory system. Medical microbiology, Galveston (TX) 1996, S. Baron (Ed.).
2. Zambon M.C. The pathogenesis of influenza in humans. Rev Med Virol 2001, 11:227-241.
3. Roman E., Miller E., Harmsen A., Wiley J., Von Andrian U.H., Huston G., et al. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. JExp Med 2002, 196:957-968.
4. Powell T.J., Brown D.M., Hollenbaugh J.A., Charbonneau T., Kemp R.A., Swain S.L., et al. CD8+ T cells responding to influenza infection reach and persist at higher numbers than CD4+ T cells independently of precursor frequency. Clin Immunol 2004, 113:89-100.
5. Hamada H., Bassity E., Flies A., Strutt T.M., Garcia-Hernandez Mde L., McKinstry K.K., et al. Multiple redundant effector mechanisms of CD8+ T cells protect against influenza infection. JImmunol 2013, 190:296-306.
6. Brincks E.L., Gurung P., Langlois R.A., Hemann E.A., Legge K.L., Griffith T.S. The magnitude of the T cell response to a clinically significant dose of influenza virus is regulated by TRAIL. JImmunol 2011, 187:4581-4588.
7. Durbin J.E., Fernandez-Sesma A., Lee C.K., Rao T.D., Frey A.B., Moran T.M., et al. Type I IFN modulates innate and specific antiviral immunity. JImmunol 2000, 164:4220-4228.
8. Liu B., Mori I., Hossain M.J., Dong L., Chen Z., Kimura Y. Local immune responses to influenza virus infection in mice with a targeted disruption of perforin gene. Microb Pathog 2003, 34:161-167.
9. McKinstry K.K., Strutt T.M., Swain S.L. Regulation of CD4+ T-cell contraction during pathogen challenge. Immunol Rev 2010, 236:110-124.
10. Cervera R., Khamashta M.A., Font J., Sebastiani G.D., Gil A., Lavilla P., et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine 2003, 82:299-308.
11. Edwards C.J., Lian T.Y., Badsha H., Teh C.L., Arden N., Chng H.H. Hospitalization of individuals with systemic lupus erythematosus: characteristics and predictors of outcome. Lupus 2003, 12:672-676.
12. Nelson P., Rylance P., Roden D., Trela M., Tugnet N. Viruses as potential pathogenic agents in systemic lupus erythematosus. Lupus 2014, 23:596-605.
13. Barzilai O., Ram M., Shoenfeld Y. Viral infection can induce the production of autoantibodies. Curr Opin Rheumatol 2007, 19:636-643.
14. Anders H.J., Vielhauer V., Eis V., Linde Y., Kretzler M., Perez de Lema G., et al. Activation of toll-like receptor-9 induces progression of renal disease in MRL-Fas(lpr) mice. FASEB J 2004, 18:534-536.
15. Granholm N.A., Cavallo T. Enhancement of renal disease in BXSB lupus prone mice after prior exposure to bacterial lipopolysaccharide. Lupus 1995, 4:339-347.
16. Granholm N.A., Cavallo T. Defective disposal of immune complexes and polyclonal B cell activation persist long after exposure to bacterial lipopolysaccharide in mice. Lab Investig 1989, 61:504-508.
17. Fujiwara M., Makino M., Watanabe H. Schistosoma mansoni: induction of severe glomerulonephritis in female BXSB mice following chronic infection. Exp Parasitol 1988, 65:214-221.
18. Larson J.D., Thurman J.M., Rubtsov A.V., Claypool D., Marrack P., van Dyk L.F., et al. Murine gammaherpesvirus 68 infection protects lupus-prone mice from the development of autoimmunity. Proc Natl Acad Sci U S A 2012, 109:E1092-E1100.
19. Castro A.P., Esaguy N., Aguas A.P. Effect of mycobacterial infection in the lupus-prone MRL/lpr mice: enhancement of life span of autoimmune mice, amelioration of kidney disease and transient decrease in host resistance. Autoimmunity 1993, 16:159-166.
20. 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.
21. Daly K., Nguyen P., Woodland D.L., Blackman M.A. Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. JVirol 1995, 69:7416-7422.
22. Slight S.R., Rangel-Moreno J., Gopal R., Lin Y., Fallert Junecko B.A., Mehra S., et al. CXCR5(+) T helper cells mediate protective immunity against tuberculosis. JClin Invest 2013, 123:712-726.
23. Kudva A., Scheller E.V., Robinson K.M., Crowe C.R., Choi S.M., Slight S.R., et al. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. JImmunol 2011, 186:1666-1674.
24. Crowe C.R., Chen K., Pociask D.A., Alcorn J.F., Krivich C., Enelow R.I., et al. Critical role of IL-17RA in immunopathology of influenza infection. JImmunol 2009, 183:5301-5310.
25. Slight S.R., Monin L., Gopal R., Avery L., Davis M., Cleveland H., et al. IL-10 restrains IL-17 to limit lung pathology characteristics following pulmonary infection with Francisella tularensis live vaccine strain. Am J Pathol 2013, 183:1397-1404.
26. Bagavant H., Tung K.S. Failure of CD25+ T cells from lupus-prone mice to suppress lupus glomerulonephritis and sialoadenitis. JImmunol 2005, 175:944-950.
27. Jonges M., Liu W.M., van der Vries E., Jacobi R., Pronk I., Boog C., et al. Influenza virus inactivation for studies of antigenicity and phenotypic neuraminidase inhibitor resistance profiling. JClin Microbiol 2010, 48:928-940.
28. Andrews B.S., Eisenberg R.A., Theofilopoulos A.N., Izui S., Wilson C.B., McConahey P.J., et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. JExp Med 1978, 148:1198-1215.
29. Tam V.C., Quehenberger O., Oshansky C.M., Suen R., Armando A.M., Treuting P.M., et al. Lipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation. Cell 2013, 154:213-227.
30. Deberge M.P., Ely K.H., Enelow R.I. Soluble, but not transmembrane, TNF-alpha is required during influenza infection to limit the magnitude of immune responses and the extent of immunopathology. JImmunol 2014, 195:5839-5851.
31. Boyden A.W., Frickman A.M., Legge K.L., Waldschmidt T.J. Primary and long-term B-cell responses in the upper airway and lung after influenza A virus infection. Immunol Res 2014, 59:73-80.
32. Delogu L.G., Deidda S., Delitala G., Manetti R. Infectious diseases and autoimmunity. JInfect Dev Ctries 2011, 5:679-687.
33. Watanabe-Fukunaga R., Brannan C.I., Copeland N.G., Jenkins N.A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 1992, 356:314-317.
34. Kil L.P., Hendriks R.W. Aberrant B cell selection and activation in systemic lupus erythematosus. Int Rev Immunol 2013, 32:445-470.
35. Munoz L.E., Lauber K., Schiller M., Manfredi A.A., Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol 2010, 6:280-289.
36. Moudi B., Salimi S., Farajian Mashhadi F., Sandoughi M., Zakeri Z. Association of FAS and FAS ligand genes polymorphism and risk of systemic lupus erythematosus. ScientificWorldJournal 2013, 2013:176741.
37. Komatsuda A., Wakui H., Iwamoto K., Togashi M., Maki N., Masai R., et al. Up-regulation of TRAIL mRNA expression in peripheral blood mononuclear cells from patients with active systemic lupus erythematosus. Clin Immunol 2007, 125:26-29.
38. Colamussi M.L., White M.R., Crouch E., Hartshorn K.L. Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 1999, 93:2395-2403.
39. StudnickaBenke A., Steiner G., Petera P., Smolen J.S. Tumour necrosis factor alpha and its soluble receptors parallel clinical disease and autoimmune activity in systemic lupus erythematosus. Br J Rheumatol 1996, 35:1067-1074.
40. Mangale D., Kariuki S.N., Chrabot B.S., Kumabe M., Kelly J.A., Harley J.B., et al. Familial aggregation of high tumor necrosis factor alpha levels in systemic lupus erythematosus. Clin Dev Immunol 2013, 2013:267430.
41. Kontoyiannis D., Kollias G. Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor. Eur J Immunol 2000, 30:2038-2047.
42. Debandt M., Vittecoq O., Descamps V., Le Loet X., Meyer O. Anti-TNF-alpha-induced systemic lupus syndrome. Clin Rheumatol 2003, 22:56-61.
43. Deng G.M., Liu L., Tsokos G.C. Targeted tumor necrosis factor receptor I preligand assembly domain improves skin lesions in MRL/lpr mice. Arthritis Rheum 2010, 62:2424-2431.
44. Chan P.K.S. Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 2002, 34:S58-S64.
45. Hinshaw V.S., Olsen C.W., Dybdahl-Sissoko N., Evans D. Apoptosis: a mechanism of cell killing by influenza A and B viruses. JVirol 1994, 68:3667-3673.
46. Su Y.J., Cheng T.T., Chen C.J., Chiu W.C., Hsu C.Y., Chang W.N., et al. The association among leukocyte apoptosis, autoantibodies and disease severity in systemic lupus erythematosus. JTransl Med 2013, 11:261.
47. Lorenz H.M., Grunke M., Hieronymus T., Herrmann M., Kuhnel A., Manger B., et al. Invitro apoptosis and expression of apoptosis-related molecules in lymphocytes from patients with systemic lupus erythematosus and other autoimmune diseases. Arthritis Rheum 1997, 40:306-317.
48. Rastin M., Mahmoudi M., Hatef M., Sahebari M., Tabasi N., Haghmorad D., et al. Tlymphocyte apoptosis in systemic lupus erythematosus patients. Iran J Basic Med Sci 2013, 16:936-941.
49. El-Karaksy S.M., Kholoussi N.M., Shahin R.M., El-Ghar M.M., Gheith Rel S. TRAIL mRNA expression in peripheral blood mononuclear cells of Egyptian SLE patients. Gene 2013, 527:211-214.
50. Hutcheson J., Scatizzi J.C., Siddiqui A.M., Haines G.K., Wu T., Li Q.Z., et al. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity 2008, 28:206-217.
51. Jiao Q., Liu C., Yang Z., Ding Q., Wang M., Li M., et al. Upregulated PD-1 expression is associated with the development of systemic lupus erythematosus, but not the PD-1.1 allele of the PDCD1 gene. Int J Genomics 2014, 2014:950903.
52. Damjanovic D., Divangahi M., Kugathasan K., Small C.L., Zganiacz A., Brown E.G., et al. Negative regulation of lung inflammation and immunopathology by TNF-alpha during acute influenza infection. Am J Pathol 2011, 179:2963-2976.
53. Mozdzanowska K., Maiese K., Furchner M., Gerhard W. Treatment of influenza virus-infected SCID mice with nonneutralizing antibodies specific for the transmembrane proteins matrix 2 and neuraminidase reduces the pulmonary virus titer but fails to clear the infection. Virology 1999, 254:138-146.