Cell cycle arrest by transforming growth factor β1 enhances replication of respiratory syncytial virus in lung epithelial cells

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12424-12431

  Gibbs, John D ^a   Ornoff, Douglas M ^a   Igo, Heather A ^a   Zeng, Jennifer Y ^a   Imani, Farhad ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; ASTHMA; AUTOCRINE EFFECT; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOREGULATION; LUNG ALVEOLUS EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS REPLICATION;

CELL CYCLE; CELL LINE; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; EPITHELIAL CELLS; HUMANS; RESPIRATORY MUCOSA; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; TRANSFORMING GROWTH FACTOR BETA1;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 70450170069     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00806-09     Document Type: Article

References (49)

1. Advani, S. J., R. R. Weichselbaum, and B. Roizman. 2000. The role of cdc2 in the expression of herpes simplex virus genes. Proc. Natl. Acad. Sci. USA 97:10996-11001.
2. Boland, S., E. Boisvieux-Ulrich, O. Houcine, A. Baeza-Squiban, M. Pouchelet, D. Schoevaert, and F. Marano. 1996. TGF beta 1 promotes actin cytoskeleton reorganization and migratory phenotype in epithelial tracheal cells in primary culture. J. Cell Sci. 109:2207-2219. (Pubitemid 26325484)
3. Busse, W. W., and J. E. Gern. 1997. Viruses in asthma. J. Allergy Clin. Immunol. 100:147-150.
4. Chen, C. J., and S. Makino. 2004. Murine coronavirus replication induces cell cycle arrest in G0/G1 phase. J. Virol. 78:5658-5669.
5. Chu, H. W., S. Balzar, G. J. Seedorf, J. Y. Westcott, J. B. Trudeau, P. Silkoff, and S. E. Wenzel. 2004. Transforming growth factor-beta2 induces bronchial epithelial mucin expression in asthma. Am. J. Pathol. 165:1097-1106.
6. Cohn, L., J. A. Elias, and G. L. Chupp. 2004. Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 22:789-815.
7. Davy, C., and J. Doorbar. 2007. G2/M cell cycle arrest in the life cycle of viruses. Virology 368:219-226. (Pubitemid 350016216)
8. Desai, T. R., N. J. Leeper, K. L. Hynes, and B. L. Gewertz. 2002. Interleukin- 6 causes endothelial barrier dysfunction via the protein kinase C pathway. J. Surg. Res. 104:118-123.
9. Doherty, T., and D. Broide. 2007. Cytokines and growth factors in airway remodeling in asthma. Curr. Opin. Immunol. 19:676-680.
10. Estripeaut, D., J. P. Torres, C. S. Somers, C. Tagliabue, S. Khokhar, V. G. Bhoj, S. M. Grube, A. Wozniakowski, A. M. Gomez, O. Ramilo, H. S. Jafri, and A. Mejias. 2008. Respiratory syncytial virus persistence in the lungs correlates with airway hyperreactivity in the mouse model. J. Infect. Dis. 198:1435-1443.
11. Fodha, I., A. Vabret, L. Ghedira, H. Seboui, S. Chouchane, J. Dewar, N. Gueddiche, A. Trabelsi, N. Boujaafar, and F. Freymuth. 2007. Respiratory syncytial virus infections in hospitalized infants: association between viral load, virus subgroup, and disease severity. J. Med. Virol. 79:1951-1958.
12. Gern, J. E., and W. W. Busse. 2002. Relationship of viral infections to wheezing illnesses and asthma. Nat. Rev. Immunol. 2:132-138.
13. Graham, B. S., L. A. Bunton, P. F. Wright, and D. T. Karzon. 1991. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Investig. 88:1026-1033.
14. Graham, B. S., T. R. Johnson, and R. S. Peebles. 2000. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology 48:237-247. (Pubitemid 30674110)
15. Graham, B. S., M. D. Perkins, P. F. Wright, and D. T. Karzon. 1988. Primary respiratory syncytial virus infection in mice. J. Med. Virol. 26:153-162.
16. Groskreutz, D. J., M. M. Monick, T. O. Yarovinsky, L. S. Powers, D. E. Quelle, S. M. Varga, D. C. Look, and G. W. Hunninghake. 2007. Respiratory syncytial virus decreases p53 protein to prolong survival of airway epithelial cells. J. Immunol. 179:2741-2747.
17. Hashimoto, K., B. S. Graham, S. B. Ho, K. B. Adler, R. D. Collins, S. J. Olson, W. Zhou, T. Suzutani, P. W. Jones, K. Goleniewska, J. F. O'Neal, and R. S. Peebles, Jr. 2004. Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and gob-5. Am. J. Respir. Crit. Care Med. 170:306-312.
18. Hegele, R. G., P. J. Robinson, S. Gonzalez, and J. C. Hogg. 1993. Production of acute bronchiolitis in guinea-pigs by human respiratory syncytial virus. Eur. Respir. J. 6:1324-1331.
19. Hoffjan, S., I. Ostrovnaja, D. Nicolae, D. L. Newman, R. Nicolae, R. Gangnon, L. Steiner, K. Walker, R. Reynolds, D. Greene, D. Mirel, J. E. Gern, R. F. Lemanske, Jr., and C. Ober. 2004. Genetic variation in immunoregulatory pathways and atopic phenotypes in infancy. J. Allergy Clin. Immunol. 113:511-518.
20. Howat, W. J., S. T. Holgate, and P. M. Lackie. 2002. TGF-beta isoform release and activation during in vitro bronchial epithelial wound repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L115-L123.
21. Izcue, A., J. L. Coombes, and F. Powrie. 2006. Regulatory T cells suppress Immunol. Rev. 212:256-271.
22. Kallewaard, N. L., A. L. Bowen, and J. E. Crowe, Jr. 2005. Cooperativity of actin and microtubule elements during replication of respiratory syncytial virus. Virology 331:73-81.
23. Kelly, M., M. Kolb, P. Bonniaud, and J. Gauldie. 2003. Re-evaluation of fibrogenic cytokines in lung fibrosis. Curr. Pharm. Des. 9:39-49.
24. Klein, M. I., S. Coviello, G. Bauer, A. Benitez, M. E. Serra, M. P. Schiatti, M. F. Delgado, G. A. Melendi, L. Novalli, H. G. Pena, R. A. Karron, S. R. Kleeberger, and F. P. Polack. 2006. The impact of infection with human metapneumovirus and other respiratory viruses in young infants and children at high risk for severe pulmonary disease. J. Infect. Dis. 193:1544-1551.
25. Laiho, M., J. A. DeCaprio, J. W. Ludlow, D. M. Livingston, and J. Massague. 1990. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 62:175-185. (Pubitemid 20216297)
26. Li, H., I. Romieu, H. Wu, J. J. Sienra-Monge, M. Ramirez-Aguilar, B. E. Del Rio-Navarro, I. C. Del Lara-Sanchez, E. O. Kistner, H. K. Gjessing, and S. J. London. 2007. Genetic polymorphisms in transforming growth factor beta-1 (TGFB1) and childhood asthma and atopy. Hum. Genet. 121:529-538.
27. Li, M. O., and R. A. Flavell. 2008. TGF-beta: a master of all T cell trades. Cell 134:392-404.
28. Lukacs, N. W., M. L. Moore, B. D. Rudd, A. A. Berlin, R. D. Collins, S. J. Olson, S. B. Ho, and R. S. Peebles, Jr. 2006. Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am. J. Pathol. 169:977-986.
29. Matsumoto, M., S. Kikkawa, M. Kohase, K. Miyake, and T. Seya. 2002. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem. Biophys. Res. Commun. 293:1364-1369.
30. McCann, K. L., and F. Imani. 2007. Transforming growth factor beta enhances respiratory syncytial virus replication and tumor necrosis factor alpha induction in human epithelial cells. J. Virol. 81:2880-2886.
31. McChesney, M. B., A. Altman, and M. B. Oldstone. 1988. Suppression of T lymphocyte function by measles virus is due to cell cycle arrest in G1. J. Immunol. 140:1269-1273.
32. Minshall, E. M., D. Y. Leung, R. J. Martin, Y. L. Song, L. Cameron, P. Ernst, and Q. Hamid. 1997. Eosinophil-associated TGF-beta1 mRNA expression and airways fibrosis in bronchial asthma. Am. J. Respir. Cell Mol. Biol. 17:326-333.
33. Moore, B., R. F. Murphy, and D. K. Agrawal. 2008. Interaction of TGF-beta with immune cells in airway disease. Curr. Mol. Med. 8:427-436.
34. Moses, H. L., E. Y. Yang, and J. A. Pietenpol. 1990. TGF-beta stimulation and inhibition of cell proliferation: new mechanistic insights. Cell 63:245-247. (Pubitemid 20355445)
35. Naniche, D., S. I. Reed, and M. B. Oldstone. 1999. Cell cycle arrest during measles virus infection: a G0-like block leads to suppression of retinoblastoma protein expression. J. Virol. 73:1894-1901. (Pubitemid 29098090)
36. Peebles, R. S., Jr., J. R. Sheller, J. E. Johnson, D. B. Mitchell, and B. S. Graham. 1999. Respiratory syncytial virus infection prolongs methacholine-induced airway hyperresponsiveness in ovalbumin-sensitized mice. J. Med. Virol. 57:186-192.
37. 2/M cell cycle arrest requires σ1s and occurs in the absence of apoptosis. J. Virol. 74:9562-9570.
38. Pulleyn, L. J., R. Newton, I. M. Adcock, and P. J. Barnes. 2001. TGFbeta1 allele association with asthma severity. Hum Genet. 109:623-627.
39. Roberts, A. B., M. B. Sporn, R. K. Assoian, J. M. Smith, N. S. Roche, L. M. Wakefield, U. I. Heine, L. A. Liotta, V. Falanga, J. H. Kehrl, et al. 1986. Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA 83:4167-4171.
40. Saltis, J. 1996. TGF-beta: receptors and cell cycle arrest. Mol. Cell Endocrinol. 116:227-232.
41. Schwarze, J., E. Hamelmann, K. L. Bradley, K. Takeda, and E. W. Gelfand. 1997. Respiratory syncytial virus infection results in airway hyperresponsiveness and enhanced airway sensitization to allergen. J. Clin. Investig. 100:226-233.
42. Seoane, J., C. Pouponnot, P. Staller, M. Schader, M. Eilers, and J. Massague. 2001. TGFbeta influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nat. Cell Biol. 3:400-408.
43. Silverman, E. S., L. J. Palmer, V. Subramaniam, A. Hallock, S. Mathew, J. Vallone, D. S. Faffe, T. Shikanai, B. A. Raby, S. T. Weiss, and S. A. Shore. 2004. Transforming growth factor-beta1 promoter polymorphism C-509T is associated with asthma. Am. J. Respir. Crit. Care Med. 169:214-219.
44. Simon, K. E., H. H. Cha, and G. L. Firestone. 1995. Transforming growth factor beta down-regulation of CKShs1 transcripts in growth-inhibited epithelial cells. Cell Growth Differ. 6:1261-1269.
45. Taylor, A., J. Verhagen, K. Blaser, M. Akdis, and C. A. Akdis. 2006. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 117:433-442.
46. Ten Dijke, P., M. J. Goumans, F. Itoh, and S. Itoh. 2002. Regulation of cell proliferation by Smad proteins. J. Cell Physiol. 191:1-16. (Pubitemid 34195213)
47. Thomas, B. J., M. Lindsay, H. Dagher, N. J. Freezer, D. Li, R. Ghildyal, and P. G. Bardin. 2009. Transforming growth factor-β enhances rhinovirus infection by diminishing early innate responses. Am. J. Respir. Cell Mol. Biol.
48. Vignola, A. M., P. Chanez, G. Chiappara, A. Merendino, E. Pace, A. Rizzo, A. M. la Rocca, V. Bellia, G. Bonsignore, and J. Bousquet. 1997. Transforming growth factor-beta expression in mucosal biopsies in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 156:591-599.
49. Welliver, R. C., Sr. 2008. The immune response to respiratory syncytial virus infection: friend or foe? Clin. Rev. Allergy Immunol. 34:163-173.