Suppression of IRG-1 reduces inflammatory cell infiltration and lung injury in respiratory syncytial virus infection by reducing production of reactive oxygen species

Journal of Virology

Volumn 90, Issue 16, 2016, Pages 7313-7322

  Ren, Ke ^a   Lv, Yuanzi ^a   Zhuo, Yujie ^b   Chen, Changmai ^a   Shi, Hengfei ^a   Guo, Lin ^a   Yang, Guang ^b   Hou, Yayi ^a   Tan, Ren Xiang ^a   Li, Erguang ^a  

^a NANJING UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYTOKINE; IRG1 PROTEIN; ITACONIC ACID; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; HYDROLYASE; IRG1 PROTEIN, HUMAN; IRG1 PROTEIN, MOUSE; PROTEIN;

A549 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATORY CELL; LUNG INJURY; LUNG PARENCHYMA; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RESPIRATORY EPITHELIUM; RESPIRATORY SYNCYTIAL VIRUS INFECTION; T LYMPHOCYTE; VIRUS REPLICATION; ANIMAL; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; METABOLISM; PATHOGENICITY; PATHOLOGY;

ANIMALS; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDRO-LYASES; LUNG INJURY; MICE; PROTEINS; REACTIVE OXYGEN SPECIES; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES;

EID: 84982234778     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00563-16     Document Type: Article

References (58)

1. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O'Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simoes EA, Rudan I, Weber MW, Campbell H. 2010. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375:1545-1555. http://dx.doi.org/10.1016/S0140-6736(10)60206-1.
2. Collins PL, Graham BS. 2008. Viral and host factors in human respiratory syncytial virus pathogenesis. J Virol 82:2040-2055. http://dx.doi.org/10 .1128/JVI.01625-07.
3. Matias G, Taylor R, Haguinet F, Schuck-Paim C, Lustig R, Shinde V. 2014. Estimates of mortality attributable to influenza and RSV in the United States during 1997-2009 by influenza type or subtype, age, cause of death, and risk status. Influenza Other Respir Viruses 8:507-515. http://dx .doi.org/10.1111/irv.12258.
4. Fleming DM, Taylor RJ, Lustig RL, Schuck-Paim C, Haguinet F, Webb DJ, Logie J, Matias G, Taylor S. 2015. Modelling estimates of the burden of respiratory syncytial virus infection in adults and the elderly in the United Kingdom. BMC Infect Dis 15:443. http://dx.doi.org/10.1186 /s12879-015-1218-z.
5. Zhang Y, Yuan L, Zhang Y, Zhang X, Zheng M, Kyaw MH. 2015. Burden of respiratory syncytial virus infections in China: systematic review and meta-analysis. J Glob Health 5:020417. http://dx.doi.org/10 .7189/jogh.05.020417.
6. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults.NEngl J Med 352:1749-1759. http://dx.doi.org/10.1056/NEJMoa043951.
7. Chen R, Mias GI, Li-Pook-Than J, Jiang L, Lam HY, Chen R, Miriami E, Karczewski KJ, Hariharan M, Dewey FE, Cheng Y, Clark MJ, Im H, Habegger L, Balasubramanian S, O'Huallachain M, Dudley JT, Hillenmeyer S, Haraksingh R, Sharon D, Euskirchen G, Lacroute P, Bettinger K, Boyle AP, Kasowski M, Grubert F, Seki S, Garcia M, Whirl-Carrillo M, Gallardo M, Blasco MA, Greenberg PL, Snyder P, Klein TE, Altman RB, Butte AJ, Ashley EA, Gerstein M, Nadeau KC, Tang H, Snyder M. 2012. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148:1293-1307. http://dx.doi.org/10.1016/j.cell.2012.02 .009.
8. Collins PL, Crowe JEJ. 2007. Respiratory syncytial virus and metapneumovirus. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
9. Bueno SM, Gonzalez PA, Riedel CA, Carreno LJ, Vasquez AE, Kalergis AM. 2011. Local cytokine response upon respiratory syncytial virus infection. Immunol Lett 136:122-129. http://dx.doi.org/10.1016/j.imlet.2010 .12.003.
10. Goritzka M, Makris S, Kausar F, Durant LR, Pereira C, Kumagai Y, Culley FJ, Mack M, Akira S, Johansson C. 2015. Alveolar macrophagederived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J Exp Med 212:699-714. http://dx.doi .org/10.1084/jem.20140825.
11. Ogra PL. 2004. Respiratory syncytial virus: the virus, the disease and the immune response. Paediatr Respir Rev 5(Suppl A):S119-S126. http://dx .doi.org/10.1016/S1526-0542(04)90023-1.
12. Lambert L, Sagfors AM, Openshaw PJ, Culley FJ. 2014. Immunity to RSV in early-life. Front Immunol 5:466.
13. Gonzalez PA, Bueno SM, Carreno LJ, Riedel CA, Kalergis AM. 2012. Respiratory syncytial virus infection and immunity. Rev Med Virol 22: 230-244. http://dx.doi.org/10.1002/rmv.1704.
14. Villenave R, Thavagnanam S, Sarlang S, Parker J, Douglas I, Skibinski G, Heaney LG, McKaigue JP, Coyle PV, Shields MD, Power UF. 2012. In vitro modeling of respiratory syncytial virus infection of pediatric bronchial epithelium, the primary target of infection in vivo. Proc Natl Acad Sci U S A 109:5040-5045. http://dx.doi.org/10.1073/pnas.1110203109.
15. Fonceca AM, Flanagan BF, Trinick R, Smyth RL, McNamara PS. 2012. Primary airway epithelial cultures from children are highly permissive to respiratory syncytial virus infection. Thorax 67:42-48. http://dx.doi.org /10.1136/thoraxjnl-2011-200131.
16. Barik S. 2013. Respiratory syncytial virus mechanisms to interfere with type 1 interferons. Curr Top Microbiol Immunol 372:173-191.
17. Borchers AT, Chang C, Gershwin ME, Gershwin LJ. 2013. Respiratory syncytial virus-a comprehensive review. Clin Rev Allergy Immunol 45: 331-379. http://dx.doi.org/10.1007/s12016-013-8368-9.
18. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, Tripp RA, Walsh EE, Freeman MW, Golenbock DT, Anderson LJ, Finberg RW. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 1:398-401. http://dx.doi.org/10 .1038/80833.
19. Haynes LM, Moore DD, Kurt-Jones EA, Finberg RW, Anderson LJ, Tripp RA. 2001. Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 75:10730-10737. http://dx.doi.org/10 .1128/JVI.75.22.10730-10737.2001.
20. Monick MM, Yarovinsky TO, Powers LS, Butler NS, Carter AB, Gudmundsson G, Hunninghake GW. 2003. Respiratory syncytial virus upregulates TLR4 and sensitizes airway epithelial cells to endotoxin. J Biol Chem 278:53035-53044. http://dx.doi.org/10.1074/jbc.M308093200.
21. Caballero MT, Serra ME, Acosta PL, Marzec J, Gibbons L, Salim M, Rodriguez A, Reynaldi A, Garcia A, Bado D, Buchholz UJ, Hijano DR, Coviello S, Newcomb D, Bellabarba M, Ferolla FM, Libster R, Berenstein A, Siniawaski S, Blumetti V, Echavarria M, Pinto L, Lawrence A, Ossorio MF, Grosman A, Mateu CG, Bayle C, Dericco A, Pellegrini M, Igarza I, Repetto HA, Grimaldi LA, Gudapati P, Polack NR, Althabe F, Shi M, Ferrero F, Bergel E, Stein RT, Peebles RS, Boothby M, Kleeberger SR, Polack FP. 2015. TLR4 genotype and environmental LPS mediate RSV bronchiolitis through Th2 polarization. J Clin Investig 125: 571-582. http://dx.doi.org/10.1172/JCI75183.
22. Goritzka M, Durant LR, Pereira C, Salek-Ardakani S, Openshaw PJ, Johansson C. 2014. Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J Virol 88:6128-6136. http://dx.doi.org/10.1128 /JVI.00333-14.
23. Garofalo RP, Kolli D, Casola A. 2013. Respiratory syncytial virus infection: mechanisms of redox control and novel therapeutic opportunities. Antioxid Redox Signal 18:186-217. http://dx.doi.org/10.1089/ars.2011 .4307.
24. Hosakote YM, Jantzi PD, Esham DL, Spratt H, Kurosky A, Casola A, Garofalo RP. 2011. Viral-mediated inhibition of antioxidant enzymes contributes to the pathogenesis of severe respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 183:1550-1560. http://dx.doi.org/10 .1164/rccm.201010-1755OC.
25. Jamaluddin M, Tian B, Boldogh I, Garofalo RP, Brasier AR. 2009. Respiratory syncytial virus infection induces a reactive oxygen species- MSK1-phospho-Ser-276 RelA pathway required for cytokine expression. J Virol 83:10605-10615. http://dx.doi.org/10.1128/JVI.01090-09.
26. Liu T, Castro S, Brasier AR, Jamaluddin M, Garofalo RP, Casola A. 2004. Reactive oxygen species mediate virus-induced STAT activation: role of tyrosine phosphatases. J Biol Chem 279:2461-2469. http://dx.doi .org/10.1074/jbc.M307251200.
27. Hosakote YM, Liu T, Castro SM, Garofalo RP, Casola A. 2009. Respiratory syncytial virus induces oxidative stress by modulating antioxidant enzymes. Am J Respir Cell Mol Biol 41:348-357. http://dx.doi.org/10 .1165/rcmb.2008-0330OC.
28. Grandvaux N, Mariani M, Fink K. 2015. Lung epithelial NOX/DUOX and respiratory virus infections. Clin Sci (Lond) 128:337-347. http://dx .doi.org/10.1042/CS20140321.
29. Castro SM, Guerrero-Plata A, Suarez-Real G, Adegboyega PA, Colasurdo GN, Khan AM, Garofalo RP, Casola A. 2006. Antioxidant treatment ameliorates respiratory syncytial virus-induced disease and lung inflammation. AmJ Respir Crit Care Med 174:1361-1369. http://dx.doi.org /10.1164/rccm.200603-319OC.
30. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. 2014. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20:1126-1167. http://dx.doi.org/10.1089/ars.2012.5149.
31. Dickinson BC, Chang CJ. 2011. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7:504-511. http: //dx.doi.org/10.1038/nchembio.607.
32. Whitsett JA, Alenghat T. 2015. Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol 16:27-35.
33. Chow CW, Herrera Abreu MT, Suzuki T, Downey GP. 2003. Oxidative stress and acute lung injury. Am J Respir Cell Mol Biol 29:427-431. http: //dx.doi.org/10.1165/rcmb.F278.
34. Komaravelli N, Tian B, Ivanciuc T, Mautemps N, Brasier AR, Garofalo RP, Casola A. 2015. Respiratory syncytial virus infection down-regulates antioxidant enzyme expression by triggering deacetylation-proteasomal degradation of Nrf2. Free Radic Biol Med 88:391-403. http://dx.doi.org /10.1016/j.freeradbiomed.2015.05.043.
35. Pearce EL, Poffenberger MC, Chang CH, Jones RG. 2013. Fueling immunity: insights into metabolism and lymphocyte function. Science 342:1242454. http://dx.doi.org/10.1126/science.1242454.
36. Odegaard JI, Chawla A. 2013. The immune system as a sensor of the metabolic state. Immunity 38:644-654. http://dx.doi.org/10.1016/j .immuni.2013.04.001.
37. Hall CJ, Boyle RH, Astin JW, Flores MV, Oehlers SH, Sanderson LE, Ellett F, Lieschke GJ, Crosier KE, Crosier PS. 2013. Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating beta-oxidation-dependent mitochondrial ROS production. Cell Metab 18:265-278. http://dx.doi.org/10.1016/j.cmet.2013.06.018.
38. Lee CG, Jenkins NA, Gilbert DJ, Copeland NG, O'Brien WE. 1995. Cloning and analysis of gene regulation of a novel LPS-inducible cDNA. Immunogenetics 41:263-270.
39. Smith J, Sadeyen JR, Paton IR, Hocking PM, Salmon N, Fife M, Nair V, Burt DW, Kaiser P. 2011. Systems analysis of immune responses in Marek's disease virus-infected chickens identifies a gene involved in susceptibility and highlights a possible novel pathogenicity mechanism. J Virol 85:11146-11158. http://dx.doi.org/10.1128/JVI.05499-11.
40. Degrandi D, Hoffmann R, Beuter-Gunia C, Pfeffer K. 2009. The proinflammatory cytokine-induced IRG1 protein associates with mitochondria. J Interferon Cytokine Res 29:55-67. http://dx.doi.org/10.1089/jir .2008.0013.
41. Basler T, Jeckstadt S, Valentin-Weigand P, Goethe R. 2006. Mycobacterium paratuberculosis, Mycobacterium smegmatis, and lipopolysaccharide induce different transcriptional and post-transcriptional regulation of the IRG1 gene in murine macrophages. J Leukoc Biol 79:628-638.
42. Janssen R, Pennings J, Hodemaekers H, Buisman A, van Oosten M, de Rond L, Ozturk K, Dormans J, Kimman T, Hoebee B. 2007. Host transcription profiles upon primary respiratory syncytial virus infection. J Virol 81:5958-5967. http://dx.doi.org/10.1128/JVI.02220-06.
43. Ioannidis I, McNally B, Willette M, Peeples ME, Chaussabel D, Durbin JE, Ramilo O, Mejias A, Flano E. 2012. Plasticity and virus specificity of the airway epithelial cell immune response during respiratory virus infection. J Virol 86:5422-5436. http://dx.doi.org/10.1128/JVI.06757-11.
44. Rodriguez N, Mages J, Dietrich H, Wantia N, Wagner H, Lang R, Miethke T. 2007. MyD88-dependent changes in the pulmonary transcriptome after infection with Chlamydia pneumoniae. Physiol Genomics 30: 134-145. http://dx.doi.org/10.1152/physiolgenomics.00011.2007.
45. Gautam A, Dixit S, Philipp MT, Singh SR, Morici LA, Kaushal D, Dennis VA. 2011. Interleukin-10 alters effector functions of multiple genes induced by Borrelia burgdorferi in macrophages to regulate Lyme disease inflammation. Infect Immun 79:4876-4892. http://dx.doi.org/10 .1128/IAI.05451-11.
46. Strelko CL, Lu W, Dufort FJ, Seyfried TN, Chiles TC, Rabinowitz JD, Roberts MF. 2011. Itaconic acid is a mammalian metabolite induced during macrophage activation. J Am Chem Soc 133:16386-16389. http: //dx.doi.org/10.1021/ja2070889.
47. Michelucci A, Cordes T, Ghelfi J, Pailot A, Reiling N, Goldmann O, Binz T, Wegner A, Tallam A, Rausell A, Buttini M, Linster CL, Medina E, Balling R, Hiller K. 2013. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc Natl Acad Sci U S A 110:7820 -7825. http://dx.doi.org /10.1073/pnas.1218599110.
48. Cho H, Proll SC, Szretter KJ, Katze MG, Gale M, Jr, Diamond MS. 2013. Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positive-stranded RNA viruses. Nat Med 19:458-464. http://dx.doi.org/10.1038 /nm.3108.
49. Preusse M, Tantawy MA, Klawonn F, Schughart K, Pessler F. 2013. Infection- and procedure-dependent effects on pulmonary gene expression in the early phase of influenza A virus infection in mice. BMC Microbiol 13:293. http://dx.doi.org/10.1186/1471-2180-13-293.
50. Alsuwaidi AR, Albawardi A, Almarzooqi S, Benedict S, Othman AR, Hartwig SM, Varga SM, Souid AK. 2014. Respiratory syncytial virus increases lung cellular bioenergetics in neonatal C57BL/6 mice. Virology 454-455:263-269.
51. Guo X, Liu T, Shi H, Wang J, Ji P, Wang H, Hou Y, Tan RX, Li E. 2015. Respiratory syncytial virus infection upregulates NLRC5 and major histocompatibility complex class I expression through RIG-I induction in airway epithelial cells. J Virol 89:7636-7645. http://dx.doi.org/10.1128/JVI .00349-15.
52. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. http://dx.doi.org/10 .1038/nprot.2008.73.
53. Raeisi E, Mir LM. 2012. 2-NBDG, a fluorescent analogue of glucose, as a marker for detecting cell electropermeabilization in vitro. J Membr Biol 245:633-642. http://dx.doi.org/10.1007/s00232-012-9479-6.
54. Stark JM, McDowell SA, Koenigsknecht V, Prows DR, Leikauf JE, Le Vine AM, Leikauf GD. 2002. Genetic susceptibility to respiratory syncytial virus infection in inbred mice. J Med Virol 67:92-100. http://dx.doi .org/10.1002/jmv.2196.
55. Li Y, Zhang P, Wang C, Han C, Meng J, Liu X, Xu S, Li N, Wang Q, Shi X, Cao X. 2013. Immune responsive gene 1 (IRG1) promotes endotoxin tolerance by increasing A20 expression in macrophages through reactive oxygen species. J Biol Chem 288:16225-16234. http://dx.doi.org /10.1074/jbc.M113.454538.
56. Somers CC, Ahmad N, Mejias A, Buckingham SC, Carubelli C, Katz K, Leos N, Gomez AM, DeVincenzo JP, Ramilo O, Jafri HS. 2009. Effect of dexamethasone on respiratory syncytial virus-induced lung inflammation in children: results of a randomized, placebo controlled clinical trial. Pediatr Allergy Immunol 20:477-485. http://dx.doi.org /10.1111/j.1399-3038.2009.00852.x.
57. Lee FE, Walsh EE, Falsey AR. 2011. The effect of steroid use in hospitalized adults with respiratory syncytial virus-related illness. Chest 140:1155-1161. http://dx.doi.org/10.1378/chest.11-0047.
58. Hinzey A, Alexander J, Corry J, Adams KM, Claggett AM, Traylor ZP, Davis IC, Webster Marketon JI. 2011. Respiratory syncytial virus represses glucocorticoid receptor-mediated gene activation. Endocrinology 152:483-494. http://dx.doi.org/10.1210/en.2010-0774.