The respiratory syncytial virus (RSV) nonstructural proteins mediate RSV suppression of glucocorticoid receptor transactivation

Virology

Volumn 449, Issue , 2014, Pages 62-69

  Webster Marketon, Jeanette I ^a   Corry, Jacqueline ^a   Teng, Michael N ^b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Gene regulation; Glucocorticoid; Nonstructural proteins; Respiratory syncytial virus

Indexed keywords

GLUCOCORTICOID RECEPTOR; LEUCINE ZIPPER PROTEIN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE DELETION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MYELOID DIFFERENTIATION PRIMARY RESPONSE GENE 88; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RETINOIC ACID INDUCIBLE GENE 1; VIRUS GENE;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

GENE REGULATION; GLUCOCORTICOID; NONSTRUCTURAL PROTEINS; RESPIRATORY SYNCYTIAL VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; DEAD-BOX RNA HELICASES; DOWN-REGULATION; GLUCOCORTICOIDS; HUMANS; RECEPTORS, GLUCOCORTICOID; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; TRANSCRIPTIONAL ACTIVATION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84888216992     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.11.014     Document Type: Article

References (70)

1. Adcock I.M., Lane S.J. Corticosteroid-insensitive asthma: molecular mechanisms. J. Endocrinol. 2003, 178:347-355.
2. Aguirre S., Maestre A.M., Pagni S., Patel J.R., Savage T., Gutman D., Maringer K., Bernal-Rubio D., Shabman R.S., Simon V., Rodriguez-Madoz J.R., Mulder L.C., Barber G.N., Fernandez-Sesma A. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 2012, 8:e1002934.
3. Ayroldi E., Cannarile L., Migliorati G., Nocentini G., Delfino D.V., Riccardi C. Mechanisms of the anti-inflammatory effects of glucocorticoids: genomic and nongenomic interference with MAPK signaling pathways. FASEB J. 2012, 26:4805-4820.
4. Bonville C.A., Mehta P.A., Krilov L.R., Rosenberg H.F., Domachowske J.B. Epithelial cells infected with respiratory syncytial virus are resistant to the anti-inflammatory effects of hydrocortisone. Cell Immunol. 2001, 213:134-140.
5. Boyapalle S., Wong T., Garay J., Teng M., San Juan-Vergara H., Mohapatra S., Mohapatra S. Respiratory syncytial virus NS1 protein colocalizes with mitochondrial antiviral signaling protein MAVS following infection. PLoS One 2012, 7:e29386.
6. Buchholz U.J., Ward J.M., Lamirande E.W., Heinze B., Krempl C.D., Collins P.L. Deletion of nonstructural proteins NS1 and NS2 from pneumonia virus of mice attenuates viral replication and reduces pulmonary cytokine expression and disease. J. Virol. 2009, 83:1969-1980.
7. Buckingham S.C., Jafri H.S., Bush A.J., Carubelli C.M., Sheeran P., Hardy R.D., Ottolini M.G., Ramilo O., DeVincenzo J.P. A randomized, double-blind, placebo-controlled trial of dexamethasone in severe respiratory syncytial virus (RSV) infection: effects on RSV quantity and clinical outcome. J. Infect. Dis. 2002, 185:1222-1228.
8. Bulow S.M., Nir M., Levin E., Friis B., Thomsen L.L., Nielsen J.E., Holm J.C., Moller T., Bonde-Hansen M.E., Nielsen H.E. Prednisolone treatment of respiratory syncytial virus infection: a randomized controlled trial of 147 infants. Pediatrics 1999, 104:e77.
9. Cade A., Brownlee K.G., Conway S.P., Haigh D., Short A., Brown J., Dassu D., Mason S.A., Phillips A., Eglin R., Graham M., Chetcuti A., Chatrath M., Hudson N., Thomas A., Chetcuti P.A. Randomised placebo controlled trial of nebulised corticosteroids in acute respiratory syncytial viral bronchiolitis. Arch. Dis. Child. 2000, 82:126-130.
10. Carpenter L.R., Moy J.N., Roebuck K.A. Respiratory syncytial virus and TNF alpha induction of chemokine gene expression involves differential activation of Rel A and NF-kappa B1. BMC Infect. Dis. 2002, 2:5.
11. Chen N., Baudino T., MacDonald P.N., Green M., Kelley W.L., Burnett J.W., Buller R.M. Selective inhibition of nuclear steroid receptor function by a protein from a human tumorigenic poxvirus. Virology 2000, 274:17-25.
12. Diez D., Goto S., Fahy J.V., Erle D.J., Woodruff P.G., Wheelock A.M., Wheelock C.E. Network analysis identifies a putative role for the PPAR and type 1 interferon pathways in glucocorticoid actions in asthmatics. BMC Med. Genomics 2012, 5:27.
13. Ermers M.J., Rovers M.M., van Woensel J.B., Kimpen J.L., Bont L.J. The effect of high dose inhaled corticosteroids on wheeze in infants after respiratory syncytial virus infection: randomised double blind placebo controlled trial. BMJ 2009, 338:b897.
14. Falsey A.R., Walsh E.E. Respiratory syncytial virus infection in elderly adults. Drugs Aging 2005, 22:577-587.
15. Flammer J.R., Dobrovolna J., Kennedy M.A., Chinenov Y., Glass C.K., Ivashkiv L.B., Rogatsky I. The type I interferon signaling pathway is a target for glucocorticoid inhibition. Mol. Cell Biol. 2010, 30:4564-4574.
16. Garofalo R., Sabry M., Jamaluddin M., Yu R.K., Casola A., Ogra P.L., Brasier A.R. Transcriptional activation of the interleukin-8 gene by respiratory syncytial virus infection in alveolar epithelial cells: nuclear translocation of the RelA transcription factor as a mechanism producing airway mucosal inflammation. J. Virol. 1996, 70:8773-8781.
17. Gavrilin M.A., Bouakl I.J., Knatz N.L., Duncan M.D., Hall M.W., Gunn J.S., Wewers M.D. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:141-146.
18. Haeberle H.A., Takizawa R., Casola A., Brasier A.R., Dieterich H.J., Van Rooijen N., Gatalica Z., Garofalo R.P. Respiratory syncytial virus-induced activation of nuclear factor-kappaB in the lung involves alveolar macrophages and toll-like receptor 4-dependent pathways. J. Infect. Dis. 2002, 186:1199-1206.
19. Hallak L.K., Spillmann D., Collins P.L., Peeples M.E. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J. Virol. 2000, 74:10508-10513.
20. Heinze B., Frey S., Mordstein M., Schmitt-Graff A., Ehl S., Buchholz U.J., Collins P.L., Staeheli P., Krempl C.D. Both nonstructural proteins NS1 and NS2 of pneumonia virus of mice are inhibitors of the interferon type I and type III responses in vivo. J. Virol. 2011, 85:4071-4084.
21. Hinzey A., Alexander J., Corry J., Adams K.M., Claggett A.M., Traylor Z.P., Davis I.C., Webster Marketon J.I. Respiratory syncytial virus represses glucocorticoid receptor-mediated gene activation. Endocrinology 2011, 152:483-494.
22. Hu F., Pace T.W., Miller A.H. Interferon-alpha inhibits glucocorticoid receptor-mediated gene transcription via STAT5 activation in mouse HT22 cells. Brain Behav. Immun. 2009, 23:455-463.
23. Huang Y.C., Li Z., Hyseni X., Schmitt M., Devlin R.B., Karoly E.D., Soukup J.M. Identification of gene biomarkers for respiratory syncytial virus infection in a bronchial epithelial cell line. Genomic Med. 2008, 2:113-125.
24. Irusen E., Matthews J.G., Takahashi A., Barnes P.J., Chung K.F., Adcock I.M. p38 Mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma. J. Allergy Clin. Immunol. 2002, 109:649-657.
25. Ishiguro Y. Mucosal proinflammatory cytokine production correlates with endoscopic activity of ulcerative colitis. J. Gastroenterol. 1999, 34:66-74.
26. Jiang Z., Kunimoto M., Patel J.A. Autocrine regulation and experimental modulation of interleukin-6 expression by human pulmonary epithelial cells infected with respiratory syncytial virus. J. Virol. 1998, 72:2496-2499.
27. Kino T., Gragerov A., Kopp J.B., Stauber R.H., Pavlakis G.N., Chrousos G.P. The HIV-1 virion-associated protein vpr is a coactivator of the human glucocorticoid receptor. J. Exp. Med. 1999, 189:51-62.
28. Kino T., Gragerov A., Slobodskaya O., Tsopanomichalou M., Chrousos G.P., Pavlakis G.N. Human immunodeficiency virus type 1 (HIV-1) accessory protein Vpr induces transcription of the HIV-1 and glucocorticoid-responsive promoters by binding directly to p300/CBP coactivators. J. Virol. 2002, 76:9724-9734.
29. Kino T., Hurt D.E., Ichijo T., Nader N., Chrousos G.P. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci. Signaling 2010, 3:ra8.
30. Kurt-Jones E.A., Popova L., Kwinn L., Haynes L.M., Jones L.P., Tripp R.A., Walsh E.E., Freeman M.W., Golenbock D.T., Anderson L.J., Finberg R.W. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 2000, 1:398-401.
31. Leung D.Y., Martin R.J., Szefler S.J., Sher E.R., Ying S., Kay A.B., Hamid Q. Dysregulation of interleukin 4, interleukin 5, and interferon gamma gene expression in steroid-resistant asthma. J. Exp. Med. 1995, 181:33-40.
32. Lindemans C.A., Coffer P.J., Schellens I.M., de Graaff P.M., Kimpen J.L., Koenderman L. Respiratory syncytial virus inhibits granulocyte apoptosis through a phosphatidylinositol 3-kinase and NF-kappaB-dependent mechanism. J. Immunol. 2006, 176:5529-5537.
33. Ling Z., Tran K.C., Arnold J.J., Teng M.N. Purification and characterization of recombinant human respiratory syncytial virus nonstructural protein NS1. Protein Expression Purif. 2008, 57:261-270.
34. Ling Z., Tran K.C., Teng M.N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J. Virol. 2009, 83:3734-3742.
35. Liu P., Jamaluddin M., Li K., Garofalo R.P., Casola A., Brasier A.R. Retinoic acid-inducible gene I mediates early antiviral response and Toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J. Virol. 2007, 81:1401-1411.
36. Liu P., Li K., Garofalo R.P., Brasier A.R. Respiratory syncytial virus induces RelA release from cytoplasmic 100-kDa NF-kappa B2 complexes via a novel retinoic acid-inducible gene-INF- kappa B-inducing kinase signaling pathway. J. Biol. Chem. 2008, 283:23169-23178.
37. Loebbermann J., Schnoeller C., Thornton H., Durant L., Sweeney N.P., Schuijs M., O'Garra A., Johansson C., Openshaw P.J. IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice. PLoS One 2012, 7:e32371.
38. Loppow D., Schleiss M.B., Kanniess F., Taube C., Jorres R.A., Magnussen H. In patients with chronic bronchitis a four week trial with inhaled steroids does not attenuate airway inflammation. Respir. Med. 2001, 95:115-121.
39. Lukacs N.W., Smit J.J., Mukherjee S., Morris S.B., Nunez G., Lindell D.M. Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation. J. Immunol. 2010, 185:2231-2239.
40. Marwick J.A., Caramori G., Stevenson C.S., Casolari P., Jazrawi E., Barnes P.J., Ito K., Adcock I.M., Kirkham P.A., Papi A. Inhibition of PI3Kdelta restores glucocorticoid function in smoking-induced airway inflammation in mice. Am. J. Respir. Crit. Care Med. 2009, 179:542-548.
41. Mastronarde J.G., He B., Monick M.M., Mukaida N., Matsushima K., Hunninghake G.W. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-kappa B and NF-IL-6. J. Infect. Dis. 1996, 174:262-267.
42. Matthews J.G., Ito K., Barnes P.J., Adcock I.M. Defective glucocorticoid receptor nuclear translocation and altered histone acetylation patterns in glucocorticoid-resistant patients. J. Allergy Clin. Immunol. 2004, 113:1100-1108.
43. McCoy C.E., Carpenter S., Palsson-McDermott E.M., Gearing L.J., O'Neill L.A. Glucocorticoids inhibit IRF3 phosphorylation in response to Toll-like receptor-3 and -4 by targeting TBK1 activation. J. Biol. Chem. 2008, 283:14277-14285.
44. Mibayashi M., Martinez-Sobrido L., Loo Y.M., Cardenas W.B., Gale M., Garcia-Sastre A. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 2007, 81:514-524.
45. Murawski M.R., Bowen G.N., Cerny A.M., Anderson L.J., Haynes L.M., Tripp R.A., Kurt-Jones E.A., Finberg R.W. Respiratory syncytial virus activates innate immunity through Toll-like receptor 2. J. Virol. 2009, 83:1492-1500.
46. Pace T.W., Hu F., Miller A.H. Activation of cAMP-protein kinase A abrogates STAT5-mediated inhibition of glucocorticoid receptor signaling by interferon-alpha. Brain Behav. Immun. 2011, 25:1716-1724.
47. Panickar J., Lakhanpaul M., Lambert P.C., Kenia P., Stephenson T., Smyth A., Grigg J. Oral prednisolone for preschool children with acute virus-induced wheezing. N. Engl. J. Med. 2009, 360:329-338.
48. Paramore L.C., Ciuryla V., Ciesla G., Liu L. Economic impact of respiratory syncytial virus-related illness in the US: an analysis of national databases. Pharmacoeconomics 2004, 22:275-284.
49. Patel J.A., Jiang Z., Nakajima N., Kunimoto M. Autocrine regulation of interleukin-8 by interleukin-1alpha in respiratory syncytial virus-infected pulmonary epithelial cells in vitro. Immunology 1998, 95:501-506.
50. Patel J.A., Kunimoto M., Sim T.C., Garofalo R., Eliott T., Baron S., Ruuskanen O., Chonmaitree T., Ogra P.L., Schmalstieg F. Interleukin-1 alpha mediates the enhanced expression of intercellular adhesion molecule-1 in pulmonary epithelial cells infected with respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 1995, 13:602-609.
51. Prins K.C., Cardenas W.B., Basler C.F. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J. Virol. 2009, 83:3069-3077.
52. Raboni S.M., Nogueira M.B., Tsuchiya L.R., Takahashi G.A., Pereira L.A., Pasquini R., Siqueira M.M. Respiratory tract viral infections in bone marrow transplant patients. Transplantation 2003, 76:142-146.
53. Ray A., Prefontaine K.E. Physical association and functional antagonism between the p65 subunit of transcription factor NF-kappa B and the glucocorticoid receptor. Proc. Nat. Acad. Sci. U.S.A. 1994, 91:752-756.
54. Richter H., Seddon P. Early nebulized budesonide in the treatment of bronchiolitis and the prevention of postbronchiolitic wheezing. J. Pediatr. 1998, 132:849-853.
55. Roosevelt G., Sheehan K., Grupp-Phelan J., Tanz R.R., Listernick R. Dexamethasone in bronchiolitis: a randomised controlled trial. Lancet 1996, 348:292-295.
56. Rudd B.D., Burstein E., Duckett C.S., Li X., Lukacs N.W. Differential role for TLR3 in respiratory syncytial virus-induced chemokine expression. J. Virol. 2005, 79:3350-3357.
57. Segovia J., Sabbah A., Mgbemena V., Tsai S.Y., Chang T.H., Berton M.T., Morris I.R., Allen I.C., Ting J.P., Bose S. TLR2/MyD88/NF-kappaB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 2012, 7:e29695.
58. Sher E.R., Leung D.Y., Surs W., Kam J.C., Zieg G., Kamada A.K., Szefler S.J. Steroid-resistant asthma. Cellular mechanisms contributing to inadequate response to glucocorticoid therapy. J. Clin. Invest. 1994, 93:33-39.
59. Sherman M.P., de Noronha C.M., Pearce D., Greene W.C. Human immunodeficiency virus type 1 Vpr contains two leucine-rich helices that mediate glucocorticoid receptor coactivation independently of its effects on G(2) cell cycle arrest. J. Virol. 2000, 74:8159-8165.
60. Singh D., McCann K.L., Imani F. MAPK and heat shock protein 27 activation are associated with respiratory syncytial virus induction of human bronchial epithelial monolayer disruption. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 293:L436-445.
61. Somers C.C., Ahmad N., Mejias A., Buckingham S.C., Carubelli C., Katz K., Leos N., Gomez A.M., DeVincenzo J.P., Ramilo O., Jafri H.S. Effect of dexamethasone on respiratory syncytial virus-induced lung inflammation in children: results of a randomized, placebo controlled clinical trial. Pediatr. Allergy Immunol. 2009, 20:477-485.
62. Stockman L.J., Curns A.T., Anderson L.J., Fischer-Langley G. Respiratory syncytial virus-associated hospitalizations among infants and young children in the United States, 1997-2006. Pediatr. Infect. Dis. J. 2012, 31:5-9.
63. Strahle L., Marq J.B., Brini A., Hausmann S., Kolakofsky D., Garcin D. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J. Virol. 2007, 81:12227-12237.
64. Sun J., Cardani A., Sharma A.K., Laubach V.E., Jack R.S., Muller W., Braciale T.J. Autocrine regulation of pulmonary inflammation by effector T-cell derived IL-10 during infection with respiratory syncytial virus. PLoS Pathog. 2011, 7:e1002173.
65. Swedan S., Andrews J., Majumdar T., Musiyenko A., Barik S. Multiple functional domains and complexes of the two nonstructural proteins of human respiratory syncytial virus contribute to interferon suppression and cellular location. J. Virol. 2011, 85:10090-10100.
66. Tan Y.R., Peng D., Chen C.M., Qin X.Q. Nonstructural protein-1 of respiratory syncytial virus regulates HOX gene expression through interacting with histone. Mol. Biol. Rep. 2013, 40:675-679.
67. Thomas K.W., Monick M.M., Staber J.M., Yarovinsky T., Carter A.B., Hunninghake G.W. Respiratory syncytial virus inhibits apoptosis and induces NF-kappa B activity through a phosphatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 2002, 277:492-501.
68. Tliba O., Damera G., Banerjee A., Gu S., Baidouri H., Keslacy S., Amrani Y. Cytokines induce an early steroid resistance in airway smooth muscle cells: novel role of interferon regulatory factor-1. Am. J. Respir. Cell Mol. Biol. 2008, 38:463-472.
69. Tran K.C., He B., Teng M.N. Replacement of the respiratory syncytial virus nonstructural proteins NS1 and NS2 by the V protein of parainfluenza virus 5. Virology 2007, 368:73-82.
70. Wright P.F., Karron R.A., Madhi S.A., Treanor J.J., King J.C., O'Shea A., Ikizler M.R., Zhu Y., Collins P.L., Cutland C., Randolph V.B., Deatly A.M., Hackell J.G., Gruber W.C., Murphy B.R. The interferon antagonist NS2 protein of respiratory syncytial virus is an important virulence determinant for humans. J. Infect. Dis. 2006, 193:573-581.