Hemagglutinin from the H5N1 virus activates Janus kinase 3 to dysregulate innate immunity

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Xu, Wei ^a   Chen, Minhui ^a   Ge, Nanhai ^a   Xu, Jun ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2 RECEPTOR GAMMA; JANUS KINASE 2; JANUS KINASE 3; JANUS KINASE 3 INHIBITOR; STAT1 PROTEIN; VIRUS HEMAGGLUTININ; CYTOKINE; HEMAGGLUTININ; JAK3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNE DYSREGULATION; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROVOCATION TEST; VIRUS GENE; VIRUS VIRULENCE; ANIMAL; DRUG EFFECT; EPITHELIUM CELL; IMMUNOLOGY; LUNG; METABOLISM; MOUSE; MOUSE MUTANT; SIGNAL TRANSDUCTION; VIROLOGY;

ANIMALS; CYTOKINES; EPITHELIAL CELLS; HEMAGGLUTININS; IMMUNITY, INNATE; INFLUENZA A VIRUS, H5N1 SUBTYPE; JANUS KINASE 3; LUNG; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 84863125847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031721     Document Type: Article

References (50)

1. Swayne DE, Suarez DL, (2000) Highly pathogenic avian influenza. Rev Sci Tech 19: 463-482.
2. WHO (2010) Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1) Reported to WHO.
3. Peiris JS, de Jong MD, Guan Y, (2007) Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20: 243-267.
4. Gu J, Xie Z, Gao Z, Liu J, Korteweg C, et al. (2007) H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370: 1137-1145.
5. Zhang Z, Zhang J, Huang K, Li KS, Yuen KY, et al. (2009) Systemic infection of avian influenza A virus H5N1 subtype in humans. Hum Pathol 40: 735-739.
6. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, et al. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12: 1203-1207.
7. Mer M, Richards GA, (1998) Corticosteroids in life-threatening varicella pneumonia. Chest 114: 426-431.
8. Gomersall CD, Joynt GM, Lam P, Li T, Yap F, et al. (2004) Short-term outcome of critically ill patients with severe acute respiratory syndrome. Intensive Care Med 30: 381-387.
9. Jorens PG, Van Damme J, De Backer W, Bossaert L, De Jongh RF, et al. (1992) Interleukin 8 (IL-8) in the bronchoalveolar lavage fluid from patients with the adult respiratory distress syndrome (ARDS) and patients at risk for ARDS. Cytokine 4: 592-597.
10. Beigel JH, Farrar J, Han AM, Hayden FG, Hyer R, et al. (2005) Avian influenza A (H5N1) infection in humans. N Engl J Med 353: 1374-1385.
11. Maines TR, Szretter KJ, Perrone L, Belser JA, Bright RA, et al. (2008) Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol Rev 225: 68-84.
12. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, et al. (2009) Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A 106: 3455-3460.
13. Uiprasertkul M, Kitphati R, Puthavathana P, Kriwong R, Kongchanagul A, et al. (2007) Apoptosis and pathogenesis of avian influenza A (H5N1) virus in humans. Emerg Infect Dis 13: 708-712.
14. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, et al. (2002) Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360: 1831-1837.
15. To KF, Chan PK, Chan KF, Lee WK, Lam WY, et al. (2001) Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 63: 242-246.
16. Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, et al. (2005) Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 6: 135.
17. Opitz B, van Laak V, Eitel J, Suttorp N, (2010) Innate immune recognition in infectious and noninfectious diseases of the lung. Am J Respir Crit Care Med 181: 1294-1309.
18. Beutler BA, (2009) TLRs and innate immunity. Blood 113: 1399-1407.
19. O'Neill LA, (2008) 'Fine tuning' TLR signaling. Nat Immunol 9: 459-461.
20. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, et al. (2006) H5N1 Virus Attachment to Lower Respiratory Tract. Science 312: 399.
21. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, et al. (2007) Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171: 1215-1223.
22. Hiemstra PS, Bals R, (2004) Series introduction: Innate host defense of the respiratory epithelium. J Leukoc Biol 75: 3-4.
23. Knowles MR, Boucher RC, (2002) Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109: 571-577.
24. Kagnoff MF, Eckmann L, (1997) Epithelial cells as sensors for microbial infection. J Clin Invest 100: 6-10.
25. Sandrock C, Kelly T, (2007) Clinical review: update of avian influenza A infections in humans. Crit Care 11: 209.
26. Steinberg KP, Hudson LD, Goodman RB, Hough CL, Lanken PN, et al. (2006) Efficacy and safety of corticosteroids for persistent acute respiratory distress syndrome. N Engl J Med 354: 1671-1684.
27. Annane D, Sebille V, Bellissant E, (2006) Effect of low doses of corticosteroids in septic shock patients with or without early acute respiratory distress syndrome. Crit Care Med 34: 22-30.
28. Gambotto A, Barratt-Boyes SM, de Jong MD, Neumann G, Kawaoka Y, (2008) Human infection with highly pathogenic H5N1 influenza virus. Lancet 371: 1464-1475.
29. Jaruga B, Hong F, Kim WH, Gao B, (2004) IFN-gamma/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1. Am J Physiol Gastrointest Liver Physiol 287: G1044-1052.
30. Schroder K, Hertzog PJ, Ravasi T, Hume DA, (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189.
31. Shi M, Lin TH, Appell KC, Berg LJ, (2008) Janus-kinase-3-dependent signals induce chromatin remodeling at the Ifng locus during T helper 1 cell differentiation. Immunity 28: 763-773.
32. Morens DM, Taubenberger JK, Fauci AS, (2008) Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 198: 962-970.
33. Herold S, von Wulffen W, Steinmueller M, Pleschka S, Kuziel WA, et al. (2006) Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J Immunol 177: 1817-1824.
34. Cetkovic-Cvrlje M, Tibbles HE, (2004) Therapeutic potential of Janus kinase 3 (JAK3) inhibitors. Curr Pharm Des 10: 1767-1784.
35. Kawamura M, McVicar DW, Johnston JA, Blake TB, Chen YQ, et al. (1994) Molecular cloning of L-JAK, a Janus family protein-tyrosine kinase expressed in natural killer cells and activated leukocytes. Proc Natl Acad Sci U S A 91: 6374-6378.
36. Jiang Y, Xu J, Zhou C, Wu Z, Zhong S, et al. (2005) Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am J Respir Crit Care Med 171: 850-857.
37. Hatada EN, Krappmann D, Scheidereit C, (2000) NF-kappaB and the innate immune response. Curr Opin Immunol 12: 52-58.
38. Salomon R, Hoffmann E, Webster RG, (2007) Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc Natl Acad Sci U S A 104: 12479-12481.
39. Zheng BJ, Chan KW, Lin YP, Zhao GY, Chan C, et al. (2008) Delayed antiviral plus immunomodulator treatment still reduces mortality in mice infected by high inoculum of influenza A/H5N1 virus. Proc Natl Acad Sci U S A 105: 8091-8096.
40. Aldridge JR Jr, Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, et al. (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106: 5306-5311.
41. Adams C, Aldous DJ, Amendola S, Bamborough P, Bright C, et al. (2003) Mapping the kinase domain of Janus Kinase 3. Bioorg Med Chem Lett 13: 3105-3110.
42. Changelian PS, Flanagan ME, Ball DJ, Kent CR, Magnuson KS, et al. (2003) Prevention of organ allograft rejection by a specific Janus kinase 3 inhibitor. Science 302: 875-878.
43. West K, (2009) CP-690550, a JAK3 inhibitor as an immunosuppressant for the treatment of rheumatoid arthritis, transplant rejection, psoriasis and other immune-mediated disorders. Curr Opin Investig Drugs 10: 491-504.
44. Lantz O, Grandjean I, Matzinger P, Di Santo JP, (2000) Gamma chain required for naive CD4+ T cell survival but not for antigen proliferation. Nat Immunol 1: 54-58.
45. Hacker G, Bauer A, Villunger A, (2006) Apoptosis in activated T cells: what are the triggers, and what the signal transducers? Cell Cycle 5: 2421-2424.
46. Nwe N, He Q, Damrongwatanapokin S, Du Q, Manopo I, et al. (2006) Expression of hemagglutinin protein from the avian influenza virus H5N1 in a baculovirus/insect cell system significantly enhanced by suspension culture. BMC Microbiol 6: 16.
47. Wan XF, Ren T, Luo KJ, Liao M, Zhang GH, et al. (2005) Genetic characterization of H5N1 avian influenza viruses isolated in southern China during the 2003-04 avian influenza outbreaks. Arch Virol 150: 1257-1266.
48. Lewandowski D, Marquis M, Aumont F, Lussier-Morin AC, Raymond M, et al. (2006) Altered CD4+ T cell phenotype and function determine the susceptibility to mucosal candidiasis in transgenic mice expressing HIV-1. J Immunol 177: 479-491.
49. Hutchinson KL, Villinger F, Miranda ME, Ksiazek TG, Peters CJ, et al. (2001) Multiplex analysis of cytokines in the blood of cynomolgus macaques naturally infected with Ebola virus (Reston serotype). J Med Virol 65: 561-566.
50. Miyamoto T, Min W, Lillehoj HS, (2002) Lymphocyte proliferation response during Eimeria tenella infection assessed by a new, reliable, nonradioactive colorimetric assay. Avian Dis 46: 10-16.