Respiratory syncytial virus proteins modulate suppressors of cytokine signaling 1 and 3 and the type I interferon response to infection by a toll-like receptor pathway

Viral Immunology

Volumn 22, Issue 3, 2009, Pages 147-161

  Oshansky, Christine M ^a   Krunkosky, Thomas M ^a   Barber, Jamie ^a   Jones, Les P ^a   Tripp, Ralph A ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON STIMULATED GENE FACTOR 15; MEMBRANE PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; ALPHA INTERFERON; BETA INTERFERON; F PROTEIN, HUMAN RESPIRATORY SYNCYTIAL VIRUS; G GLYCOPROTEIN, RESPIRATORY SYNCYTIAL VIRUS; ISG15 PROTEIN, HUMAN; SOCS1 PROTEIN, HUMAN; SOCS3 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING; UBIQUITIN; VIRUS FUSION PROTEIN;

ARTICLE; BRONCHUS MUCOSA; GENE; HUMAN; HUMAN CELL; MUTANT; PROTEIN EXPRESSION; REGULATORY MECHANISM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION; VIRUS INFECTION; VIRUS REPLICATION; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSCRIPTION INITIATION; VIROLOGY;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

CELL LINE; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-ALPHA; INTERFERON-BETA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTORS; TRANSCRIPTIONAL ACTIVATION; UBIQUITINS; VIRAL FUSION PROTEINS; VIRUS REPLICATION;

EID: 67049119148     PISSN: 08828245     EISSN: None     Source Type: Journal    
DOI: 10.1089/vim.2008.0098     Document Type: Article

References (77)

1. Alexander WS: Suppressors of cytokine signalling (SOCS) in the immune system. Nat Rev Immunol 2002;2:410-416. (Pubitemid 37328748)
2. Backhed F, and Hornef M: Toll-like receptor 4-mediated signaling by epithelial surfaces: necessity or threat? Microbes Infect 2003;5:951-959.
3. Baetz A, Frey M, Heeg K, and Dalpke AH: Suppressor of cytokine signaling (SOCS) proteins indirectly regulate toll-like receptor signaling in innate immune cells. J Biol Chem 2004;279:54708-54715. (Pubitemid 40053215)
4. Baetz A, Koelsche C, Strebovsky J, Heeg K, and Dalpke AH: Identification of a nuclear localization signal in suppressor of cytokine signaling 1. FASEB J 2008;22:4296-4305.
5. Bartz H, Avalos NM, Baetz A, Heeg K, and Dalpke AH: Involvement of suppressors of cytokine signaling in toll-like receptor-mediated block of dendritic cell differentiation. Blood 2006;108:4102-4108. (Pubitemid 44913281)
6. Becker Y: Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy - a review. Virus Genes 2006;33:235-252.
7. Bitko V, Shulyayeva O, Mazumder B, Musiyenko A, Ramaswamy M, Look DC, and Barik S: Nonstructural proteins of respiratory syncytial virus suppress premature apoptosis by an NF-kappaB-dependent, interferon-independent mechanism and facilitate virus growth. J Virol 2007;81:1786-1795. (Pubitemid 46214452)
8. Bode JG, Ludwig S, Ehrhardt C, Albrecht U, Erhardt A, Schaper F, Heinrich PC, and Haussinger D: IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J 2003;17:488-490.
9. Bossert B, Marozin S, and Conzelmann KK: Nonstructural proteins NS1 and NS2 of bovine respiratory syncytial virus block activation of interferon regulatory factor 3. J Virol 2003;77:8661-8668. (Pubitemid 36936076)
10. Chen XP, Losman JA, Cowan S, et al.: Pim serine/threonine kinases regulate the stability of Socs-1 protein. Proc Natl Acad Sci USA 2002;99:2175-2180. (Pubitemid 34169034)
11. Collins PL, Hill MG, Camargo E, Grosfeld H, Chanock RM, and Murphy BR: Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5′ proximal open reading frame of the M2 mRNA in gene expression and provides a capability for vaccine development. Proc Natl Acad Sci USA 1995;92:11563-11567. (Pubitemid 26014154)
12. Collins PL, and Wertz GW: cDNA cloning and transcriptional mapping of nine polyadenylylated RNAs encoded by the genome of human respiratory syncytial virus. Proc Natl Acad Sci USA 1983;80:3208-3212.
13. Culley FJ, Pennycook AM, Tregoning JS, Hussell T, and Openshaw PJ: Differential chemokine expression following respiratory virus infection reflects Th1- or Th2-biased immunopathology. J Virol 2006;80:4521-4527.
14. Dalpke A, and Heeg K: Suppressors of cytokine signaling proteins in innate and adaptive immune responses. Arch Immunol Ther Exp (Warsz) 2003;51:91-103. (Pubitemid 36522988)
15. Dalpke A, Heeg K, Bartz H, and Baetz A: Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 2008;213:225-235.
16. Dalpke AH, Opper S, Zimmermann S, and Heeg K: Suppressors of cytokine signaling (SOCS)-1 and SOCS-3 are induced by CpG-DNA and modulate cytokine responses in APCs. J Immunol 2001;166:7082-7089. (Pubitemid 32525577)
17. Der SD, Zhou A, Williams BR, and Silverman RH: Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 1998;95:15623-15628.
18. Falsey AR. Hennessey PA, Formica MA, Cox C, and Walsh EE: Respiratory syncytial virus infection in elderly and highrisk adults. N Engl J Med 2005;352:1749-1759. (Pubitemid 40570923)
19. Farrell PJ, Broeze RJ, and Lengyel P: Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 1979;279:523-525. (Pubitemid 9195259)
20. Fields BN. Knipe DM, Howley PM, and Griffin DE: Fields' Virology, 4th ed. Lippincott Williams & Wilkins, Baltimore, 2001 [Online.]
21. Gruber C, and Levine S: Respiratory syncytial virus polypeptides. V. The kinetics of glycoprotein synthesis. J Gen Virol 1985;66(Pt 6):1241-1247.
22. Haan S, Ferguson P, Sommer U, et al.: Tyrosine phosphorylation disrupts elongin interaction and accelerates SOCS3 degradation. J Biol Chem 2003;278:31972-31979. (Pubitemid 37048385)
23. Haeberle HA, Takizawa R, Casola A, et al.: 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. (Pubitemid 35192997)
24. Harcourt J, Alvarez R, Jones LP, Henderson C, Anderson LJ, and Tripp RA: Respiratory syncytial virus G protein and G protein CX3C motif adversely affect CX3CR1+ T cell responses. J Immunol 2006;176:1600-1608. (Pubitemid 43134304)
25. Haynes LM, Moore DD, Kurt-Jones EA, Finberg RW, Anderson LJ, and Tripp RA: Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 2001;75:10730-10737.
26. Kagan JC, Su T, Horng T, Chow A, Akira S, and Medzhitov R: TRAM couples endocytosis of toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 2008;9:361-368.
27. Kawai T, Takeuchi O, Fujita T, et al.: Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 2001;167:5887-5894. (Pubitemid 33062783)
28. Kim T, Kim TY, Lee WG, Yim J, and Kim TK: Signaling pathways to the assembly of an interferon-beta enhanceosome. Chemical genetic studies with a small molecule. J Biol Chem 2000;275:16910-16917. (Pubitemid 30398929)
29. Kim T, Kim TY, Song YH, Min IM, Yim J, and Kim TK: Activation of interferon regulatory factor 3 in response to DNAdamaging agents. J Biol Chem 1999;274:30686-30689. (Pubitemid 129576811)
30. Kinjyo I, Hanada T, Inagaki-Ohara K, et al.: SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 2002;17:583-591. (Pubitemid 35351504)
31. Kolokoltsov AA, Deniger D, Fleming EH, Roberts NJ Jr, Karpilow JM, and Davey RA: Small interfering RNA pro- filing reveals key role of clathrin-mediated endocytosis and early endosome formation for infection by respiratory syncytial virus. J Virol 2007;81:7786-7800. (Pubitemid 47047865)
32. Korant BD, Blomstrom DC, Jonak GJ, and Knight E Jr: Interferon-induced proteins. Purification and characterization of a 15,000-dalton protein from human and bovine cells induced by interferon. J Biol Chem 1984;259:14835-14839.
33. Krebs DL, and Hilton DJ: SOCS proteins: negative regulators of cytokine signaling. Stem Cells 2001;19:378-387.
34. Krunkosky TM, Fischer BM, Martin LD, Jones N, Akley NJ, and Adler KB: Effects of TNF-alpha on expression of ICAM- 1 in human airway epithelial cells in vitro. Signaling pathways controlling surface and gene expression. Am J Respir Cell Mol Biol 2000;22:685-692. (Pubitemid 30400247)
35. Kurt-Jones EA, Popova L, Kwinn L, et al.: Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 2000;1:398-401.
36. Lambert DM, Hambor J, Diebold M, and Galinski B: Kinetics of synthesis and phosphorylation of respiratory syncytial virus polypeptides. J Gen Virol 1988;69(Pt 2):313-323. (Pubitemid 18064163)
37. Lo AK, Lo KW, Tsao SW, et al.: Epstein-Barr virus infection alters cellular signal cascades in human nasopharyngeal epithelial cells. Neoplasia 2006;8:173-180.
38. Lo MS, Brazas RM, and Holtzman MJ: Respiratory syncytial virus nonstructural proteins NS1 and NS2 mediate inhibition of Stat2 expression and alpha/beta interferon responsiveness. J Virol 2005;79:9315-9319. (Pubitemid 40934843)
39. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, and Boucher RC: Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 1998;95:1005-1015. (Pubitemid 29019052)
40. Miyoshi H, Fujie H, Shintani Y, et al.: Hepatitis C virus core protein exerts an inhibitory effect on suppressor of cytokine signaling (SOCS)-1 gene expression. J Hepatol 2005;43:757-763. (Pubitemid 41414500)
41. Monick MM, Yarovinsky TO, Powers LS, Butler NS, Carter AB, Gudmundsson G, and Hunninghake GW: Respiratory syncytial virus up-regulates TLR4 and sensitizes airway epithelial cells to endotoxin. J Biol Chem 2003;278:53035-53044. (Pubitemid 38035906)
42. Moore EC, Barber J, and Tripp RA: Respiratory syncytial virus (RSV) attachment and nonstructural proteins modify the type I interferon response associated with suppressor of cytokine signaling (SOCS) proteins and IFN-stimulated gene-15 (ISG15). J Virol 2008;5:116.
43. Moore ML, and Peebles RS Jr: Respiratory syncytial virus disease mechanisms implicated by human, animal model, and in vitro data facilitate vaccine strategies and new therapeutics. Pharmacol Ther 2006;112:405-424.
44. Murphy BR, Sotnikov AV, Lawrence LA, Banks SM, and Prince GA: Enhanced pulmonary histopathology is observed in cotton rats immunized with formalin-inactivated respiratory syncytial virus (RSV) or purified F glycoprotein and challenged with RSV 3-6 months after immunization. Vaccine 1990;8:497-502. (Pubitemid 20332861)
45. Nakagawa R, Naka T, Tsutsui H, et al.: SOCS-1 participates in negative regulation of LPS responses. Immunity 2002;17: 677-687. (Pubitemid 35351512)
46. Navarro L, and David M: p38-dependent activation of interferon regulatory factor 3 by lipopolysaccharide. J Biol Chem 1999;274:35535-35538. (Pubitemid 129512848)
47. Nicola NA, and Greenhalgh CJ: The suppressors of cytokine signaling (SOCS) proteins: important feedback inhibitors of cytokine action. Exp Hematol 2000;28:1105-1112.
48. Oshiumi H, Matsumoto M, Funami K, Akazawa T, and Seya T: TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003;4:161-167. (Pubitemid 36193018)
49. Pickles RJ, McCarty D, Matsui H, Hart PJ, Randell SH, and Boucher RC: Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J Virol 1998;72:6014-6023. (Pubitemid 28283390)
50. Poltorak A, He X, Smirnova I, et al.: Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998;282:2085-2088. (Pubitemid 29001265)
51. Pothlichet J, Chignard M, and Si-Tahar M: Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/ IFNAR1-dependent pathway. J Immunol 2008;180:2034-2038.
52. Puthothu B, Forster J, Heinzmann A, and Krueger M: TLR-4 and CD14 polymorphisms in respiratory syncytial virus associated disease. Dis Markers 2006;22:303-308. (Pubitemid 46333629)
53. Qiao X, He B, Chiu A, Knowles DM, Chadburn A, and Cerutti A: Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 2006;7:302-310.
54. Ramaswamy M, Shi L, Monick MM, Hunninghake GW, and Look DC: Specific inhibition of type I interferon signal transduction by respiratory syncytial virus. Am J Respir Cell Mol Biol 2004;30:893-900. (Pubitemid 38736915)
55. Ramaswamy M, Shi L, Varga SM, Barik S, Behlke MA, and Look DC: Respiratory syncytial virus nonstructural protein 2 specifically inhibits type I interferon signal transduction. Virology 2006;344:328-339. (Pubitemid 43049621)
56. Ritchie KJ, and Zhang DE: ISG15: the immunological kin of ubiquitin. Semin Cell Dev Biol 2004;15:237-246.
57. Ryo A, Tsurutani N, Ohba K, et al.: SOCS1 is an inducible host factor during HIV-1 infection and regulates the intracellular trafficking and stability of HIV-1 Gag. Proc Natl Acad Sci USA 2008;105:294-299.
58. Schlender J, Bossert B, Buchholz U, and Conzelmann K: Bovine respiratory syncytial virus nonstructural proteins NS1 and NS2 cooperatively antagonize alpha/beta interferon- induced antiviral response. J Virol 2000;74:8234-8242. (Pubitemid 30666671)
59. Shay DK, Holman RC, Newman RD, Liu LL, Stout JW, and Anderson LJ: Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 1999;282:1440-1446.
60. Spann KM, Tran KC, Chi B, Rabin RL, and Collins PL: Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J Virol 2004;78:4363-4369. (Pubitemid 38437240)
61. Spann KM, Tran KC, and Collins PL: Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on interferon regulatory factor 3, NF-kappaB, and proinflammatory cytokines. J Virol 2005;79:5353-5362.
62. Starr R, Willson TA, Viney EM, et al.: A family of cytokineinducible inhibitors of signalling. Nature 1997;387:917-921.
63. Stoiber D, Kovarik P, Cohney S, Johnston JA, Steinlein P, and Decker T: Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 1999;163:2640-2647. (Pubitemid 29399188)
64. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, and Fukuda K: Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003;289:179-186. (Pubitemid 36068705)
65. Tripp RA: Pathogenesis of respiratory syncytial virus infection. Viral Immunol 2004;17:165-181. (Pubitemid 38880419)
66. Tripp RA, Dakhama A,. Jones LP, Barskey A, Gelfand EW, and Anderson LJ: The G glycoprotein of respiratory syncytial virus depresses respiratory rates through the CX3C motif and substance P. J Virol 2003;77:6580-6584. (Pubitemid 36588431)
67. Tripp RA, Jones L, and Anderson LJ: Respiratory syncytial virus G and/or SH glycoproteins modify CC and CXC chemokine mRNA expression in the BALB/c mouse. J Virol 2000;74:6227-6229. (Pubitemid 30413000)
68. Tripp RA, Jones LP, Haynes LM, Zheng H, Murphy PM, and Anderson LJ: CX3C chemokine mimicry by respiratory syncytial virus G glycoprotein. Nat Immunol 2001;2:732-738. (Pubitemid 32747163)
69. Tripp RA, Moore D, and Anderson LJ: TH(1)- and TH(2)- TYPE cytokine expression by activated T lymphocytes from the lung and spleen during the inflammatory response to respiratory syncytial virus. Cytokine 2000;12:801-807.
70. Tripp RA, Moore D, Jones L, Sullender W, Winter J, and Anderson LJ: Respiratory syncytial virus G and/or SH protein alters Th1 cytokines, natural killer cells, and neutrophils responding to pulmonary infection in BALB/c mice. J Virol 1999;73:7099-7107. (Pubitemid 29383189)
71. Tripp RA, Oshansky C, and Alvarez R: Cytokines and respiratory syncytial virus infection. Proc Am Thorac Soc 2005;2:147-149. (Pubitemid 41233382)
72. van Boxel-Dezaire AH, Rani MR, and Stark GR: Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 2006;25:361-372.
73. Welliver RC: Respiratory syncytial virus and other respiratory viruses. Pediatr Infect Dis J 2003;22:S6-10; discussion S10-12.
74. Yamamoto M, Sato S, Mori K, Hoshino K, Takeuchi O, Takeda K, and Akira S: Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 2002;169:6668-6672. (Pubitemid 36899248)
75. Yoneyama M, Kikuchi M, Natsukawa T, et al.: The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5:730-737. (Pubitemid 39023305)
76. Zhao DC, Yan T, Li L, You S, and Zhang C: Respiratory syncytial virus inhibits interferon-alpha-inducible signaling in macrophage-like U937 cells. J Infect 2007;54:393-398. (Pubitemid 46395017)
77. Zhao ZX, Cai QX, Peng XM, Chong YT, and Gao ZL: Expression of SOCS-1 in the liver tissues of chronic hepatitis B and its clinical significance. World J Gastroenterol 2008;14: 607-611. (Pubitemid 351320829)