About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 505864, 17 pages
http://dx.doi.org/10.1155/2013/505864
Research Article

Systems Approaches to Modeling Chronic Mucosal Inflammation

1Sealy Center for Molecular Medicine, The University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, USA
2Department of Internal Medicine, The University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, USA
3Hamon Center for Therapeutic Oncology Research, Department of Internal Medicine Pharmacology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
4Institute for Translational Sciences, The University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, USA
5Departments of Biochemistry and Molecular Biology, The University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, USA
6Microbiology and Immunology, The University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, USA

Received 12 June 2013; Revised 8 August 2013; Accepted 9 August 2013

Academic Editor: Tao Huang

Copyright © 2013 Mridul Kalita et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. J. Polito and D. Proud, “Epithelial cells as regulators of airway inflammation,” Journal of Allergy and Clinical Immunology, vol. 102, no. 5, pp. 714–718, 1998. View at Scopus
  2. B. N. Lambrecht and H. Hammad, “The airway epithelium in asthma,” Nature Medicine, vol. 18, pp. 684–692, 2012. View at Publisher · View at Google Scholar
  3. B. C. Willis, J. M. Liebler, K. Luby-Phelps et al., “Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-β1: potential role in idiopathic pulmonary fibrosis,” The American Journal of Pathology, vol. 166, no. 5, pp. 1321–1332, 2005. View at Scopus
  4. C. Ward, I. A. Forrest, D. M. Murphy et al., “Phenotype of airway epithelial cells suggests epithelial to mesenchymal cell transition in clinically stable lung transplant recipients,” Thorax, vol. 60, no. 10, pp. 865–871, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. S. G. Royce, L. Tan, A. A. Koek, and M. L. K. Tang, “Effect of extracellular matrix composition on airway epithelial cell and fibroblast structure: implications for airway remodeling in asthma,” Annals of Allergy, Asthma and Immunology, vol. 102, no. 3, pp. 238–246, 2009. View at Scopus
  6. D. E. Davies and S. T. Holgate, “Asthma: the importance of epithelial mesenchymal communication in pathogenesis: inflammation and the airway epithelium in asthma,” International Journal of Biochemistry and Cell Biology, vol. 34, no. 12, pp. 1520–1526, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. S. T. Holgate, J. Holloway, S. Wilson, F. Bucchieri, S. Puddicombe, and D. E. Davies, “Epithelial-mesenchymal communication in the pathogenesis of chronic asthma,” Proceedings of the American Thoracic Society, vol. 1, no. 2, pp. 93–98, 2004. View at Scopus
  8. R. Y. Huang, P. Guilford, and J. P. Thiery, “Early events in cell adhesion and polarity during epithelial-mesenchymal transition,” Journal of Cell Science, vol. 125, pp. 4417–4422, 2012. View at Publisher · View at Google Scholar
  9. J. Lim and J. P. Thiery, “Epithelial-mesenchymal transitions: insights from development,” Development, vol. 139, pp. 3471–3486, 2012. View at Publisher · View at Google Scholar
  10. B. C. Willis and Z. Borok, “TGF-β-induced EMT: mechanisms and implications for fibrotic lung disease,” American Journal of Physiology, vol. 293, no. 3, pp. L525–L534, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Jain, P. W. Shaul, Z. Borok, and B. C. Willis, “Endothelin-1 induces alveolar epithelial-mesenchymal transition through endothelin type A receptor-mediated production of TGF-β1,” American Journal of Respiratory Cell and Molecular Biology, vol. 37, no. 1, pp. 38–47, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. B. C. Willis, R. M. DuBois, and Z. Borok, “Epithelial origin of myofibroblasts during fibrosis in the lung,” Proceedings of the American Thoracic Society, vol. 3, no. 4, pp. 377–382, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. T.-L. Hackett, S. M. Warner, D. Stefanowicz et al., “Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-β1,” American Journal of Respiratory and Critical Care Medicine, vol. 180, no. 2, pp. 122–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. S. S. Sohal, D. Reid, A. Soltani et al., “Evaluation of epithelial mesenchymal transition in patients with chronic obstructive pulmonary disease,” Respiratory Research, vol. 12, p. 130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Y. Adamson, L. Young, and D. H. Bowden, “Relationship of alveolar epithelial injury and repair to the induction of pulmonary fibrosis,” The American Journal of Pathology, vol. 130, no. 2, pp. 377–383, 1988. View at Scopus
  16. S. Cannito, E. Novo, A. Compagnone et al., “Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells,” Carcinogenesis, vol. 29, no. 12, pp. 2267–2278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Vincent, E. P. Neve, J. R. Johnson et al., “A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-β mediated epithelial-mesenchymal transition,” Nature Cell Biology, vol. 11, no. 8, pp. 943–950, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. E. M. Minshall, D. Y. M. Leung, R. J. Martin et al., “Eosinophil-associated TGF-β1 mRNA Expression and airways fibrosis in bronchial asthma,” American Journal of Respiratory Cell and Molecular Biology, vol. 17, no. 3, pp. 326–333, 1997. View at Scopus
  19. J. Yang and R. A. Weinberg, “Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis,” Developmental Cell, vol. 14, no. 6, pp. 818–829, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. O. G. McDonald, H. Wu, W. Timp, A. Doi, and A. P. Feinberg, “Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition,” Nature Structural and Molecular Biology, vol. 18, no. 8, pp. 867–874, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. R. P. Garofalo and H. Haeberle, “Epithelial regulation of innate immunity to respiratory syncytial virus,” American Journal of Respiratory Cell and Molecular Biology, vol. 23, no. 5, pp. 581–585, 2000. View at Scopus
  22. S. Akira, S. Uematsu, and O. Takeuchi, “Pathogen recognition and innate immunity,” Cell, vol. 124, no. 4, pp. 783–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. R. Brasier, “The NF-k B signaling network: insights from systems approaches,” in Cellular Signaling and Innate Immune Responses to RNA Virus Infections, A. R. Brasier, S. M. Lemon, and A. Garcia-Sastre, Eds., pp. 119–135, American Society for Microbiology, 2008.
  24. S. Choudhary, M. Kalita, L. Fang et al., “Inducible TNF receptor associated factor 1 expression couples the canonical to the non-canonical NF-kB pathway in TNF stimulation,” The Journal of Biological Chemistry, vol. 288, pp. 14612–14623, 2013. View at Publisher · View at Google Scholar
  25. A. R. Brasier, “The NF-kappaB regulatory network,” Cardiovascular Toxicology, vol. 6, no. 2, pp. 111–130, 2006. View at Publisher · View at Google Scholar
  26. B. Tian, D. E. Nowak, M. Jamaluddin, S. Wang, and A. R. Brasier, “Identification of direct genomic targets downstream of the nuclear factor-κB transcription factor mediating tumor necrosis factor signaling,” The Journal of Biological Chemistry, vol. 280, no. 17, pp. 17435–17448, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Tian, D. E. Nowak, and A. R. Brasier, “A TNF-induced gene expression program under oscillatory NF-κB control,” BMC Genomics, vol. 6, article 137, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Tian and A. R. Brasier, “Identification of a nuclear factor KappaB-dependent gene network,” Recent Progress in Hormone Research, vol. 58, pp. 95–130, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Thomson, F. Petti, I. Sujka-Kwok et al., “A systems view of epithelial-mesenchymal transition signaling states,” Clinical and Experimental Metastasis, vol. 28, no. 2, pp. 137–155, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Schroeder, O. Mueller, S. Stocker et al., “The RIN: an RNA integrity number for assigning integrity values to RNA measurements,” BMC Molecular Biology, vol. 7, article 3, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. W. J. Kent, “BLAT—the BLAST-like alignment tool,” Genome Research, vol. 12, no. 4, pp. 656–664, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. R. D. Ramirez, S. Sheridan, L. Girard et al., “Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins,” Cancer Research, vol. 64, no. 24, pp. 9027–9034, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Tian, J. Yang, and A. R. Brasier, “Two-step cross-linking for analysis of protein-chromatin interactions,” Methods in Molecular Biology, vol. 809, pp. 105–120, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. D. E. Nowak, B. Tian, and A. R. Brasier, “Two-step cross-linking method for identification of NF-κB gene network by chromatin immunoprecipitation,” BioTechniques, vol. 39, no. 5, pp. 715–724, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Basak, H. Kim, J. D. Kearns et al., “A fourth IκB protein within the NF-κB signaling module,” Cell, vol. 128, no. 2, pp. 369–381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Cheadle, M. P. Vawter, W. J. Freed, and K. G. Becker, “Analysis of microarray data using Z score transformation,” Journal of Molecular Diagnostics, vol. 5, no. 2, pp. 73–81, 2003. View at Scopus
  38. D. E. Nowak, B. Tian, M. Jamaluddin et al., “RelA Ser276 phosphorylation is required for activation of a subset of NF-κB-dependent genes by recruiting cyclin-dependent kinase 9/cyclin t1 complexes,” Molecular and Cellular Biology, vol. 28, no. 11, pp. 3623–3638, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. D. E. Nelson, A. E. C. Ihekwaba, M. Elliott et al., “Oscillations in NF-κB signaling control the dynamics of gene expression,” Science, vol. 306, no. 5696, pp. 704–708, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Chiba, J. Yamamoto, Y. Yamaguchi, and H. Handa, “Promoter-proximal pausing and its release: molecular mechanisms and physiological functions,” Experimental Cell Research, vol. 316, no. 17, pp. 2723–2730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. A. R. Brasier, B. Tian, M. Jamaluddin, M. K. Kalita, R. P. Garofalo, and M. Lu, “RelA Ser276 phosphorylation-coupled Lys310 acetylation controls transcriptional elongation of inflammatory cytokines in respiratory syncytial virus infection,” Journal of Virology, vol. 85, no. 22, pp. 11752–11769, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Tian, Y. Zhao, M. Kalita et al., “CDK9-dependent transcriptional elongation in the innate ISG response to RSV infection in airway epithelial cells,” Journal of Virology, vol. 87, no. 12, pp. 7075–7092, 2013.
  43. J. Yang, A. Mitra, N. Dojer, S. Fu, M. Rowicka, and A. R. Brasier, “A probabilistic approach to learn chromatin architecture and accurate inference of the NF-kappaB/RelA regulatory network using ChIP-Seq,” Nucleic Acids Research, vol. 41, no. 15, pp. 7240–7259, 2013.
  44. L. Yang, L. Gu, Z. Li, and M. Zhou, “Translation of TRAF1 is regulated by IRES-dependent mechanism and stimulated by vincristine,” Nucleic Acids Research, vol. 38, no. 13, pp. 4503–4513, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Choudhary, S. Boldogh, R. Garofalo, M. Jamaluddin, and A. R. Brasier, “Respiratory syncytial virus influences NF-κB-dependent gene expression through a novel pathway involving MAP3K14/NIK expression and nuclear complex formation with NF-κB2,” Journal of Virology, vol. 79, no. 14, pp. 8948–8959, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. Y.-J. Chen, S.-J. Zeng, J. T. Hsu et al., “Amantadine as a regulator of internal ribosome entry site,” Acta Pharmacologica Sinica, vol. 29, no. 11, pp. 1327–1333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. K. K. Kim, M. C. Kugler, P. J. Wolters et al., “Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 35, pp. 13180–13185, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. C. Yang, N. Zhang, K. van Crombruggen, G. H. Hu, S. L. Hong, and C. Bachert, “Transforming growth factor-beta1 in inflammatory airway disease: a key for understanding inflammation and remodeling,” Allergy, vol. 67, no. 10, pp. 1193–1202, 2012. View at Publisher · View at Google Scholar
  49. H. Kasai, J. T. Allen, R. M. Mason, T. Kamimura, and Z. Zhang, “TGF-β1 induces human alveolar epithelial to mesenchymal cell transition (EMT),” Respiratory Research, vol. 6, article 56, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. C. G. Lee, B. Ma, S. Takyar et al., “Studies of vascular endothelial growth factor in asthma and chronic obstructive pulmonary disease,” Proceedings of the American Thoracic Society, vol. 8, no. 6, pp. 512–515, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. S. S. Sidhu, S. Yuan, A. L. Innes et al., “Roles of epithelial cell-derived periostin in TGF-β activation, collagen production, and collagen gel elasticity in asthma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 32, pp. 14170–14175, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Al-Muhsen, J. R. Johnson, and Q. Hamid, “Remodeling in asthma,” Journal of Allergy and Clinical Immunology, vol. 128, no. 3, pp. 451–462, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. H. L. Chua, P. Bhat-Nakshatri, S. E. Clare, A. Morimiya, S. Badve, and H. Nakshatri, “NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2,” Oncogene, vol. 26, no. 5, pp. 711–724, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. H. J. Kim, B. C. Litzenburger, X. Cui et al., “Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-κB and snail,” Molecular and Cellular Biology, vol. 27, no. 8, pp. 3165–3175, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Barberà, I. Puig, D. Domínguez et al., “Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells,” Oncogene, vol. 23, no. 44, pp. 7345–7354, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Wu, J. Deng, P. G. Rychahou, S. Qiu, B. M. Evers, and B. P. Zhou, “Stabilization of Snail by NF-κB Is Required for inflammation-induced cell migration and invasion,” Cancer Cell, vol. 15, no. 5, pp. 416–428, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. R. Brasier, A. Garcia-Sastre, and S. M. Lemon, Cellular Signaling and Innate Immune Response to RNA Virus Infections, ASM Press, Washington, DC, USA, 2008.
  58. R. J. Sims III, R. Belotserkovskaya, and D. Reinberg, “Elongation by RNA polymerase II: the short and long of it,” Genes and Development, vol. 18, no. 20, pp. 2437–2468, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. B. M. Peterlin and D. H. Price, “Controlling the elongation phase of transcription with P-TEFb,” Molecular Cell, vol. 23, no. 3, pp. 297–305, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Tourdot, S. Mathie, T. Hussell et al., “Respiratory syncytial virus infection provokes airway remodelling in allergen-exposed mice in absence of prior allergen sensitization,” Clinical and Experimental Allergy, vol. 38, no. 6, pp. 1016–1024, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. L. S. van Rijt, N. Vos, M. Willart et al., “Persistent activation of dendritic cells after resolution of allergic airway inflammation breaks tolerance to inhaled allergens in mice,” American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 3, pp. 303–311, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Kaltenborn, S. Kern, S. Frixel et al., “Respiratory syncytial virus potentiates ABCA3 mutation-induced loss of lung epithelial cell differentiation,” Human Molecular Genetics, vol. 21, pp. 2793–2806, 2012. View at Publisher · View at Google Scholar
  63. C. Palena, D. E. Polev, K. Y. Tsang et al., “The human T-box mesodermal transcription factor Brachyury is a candidate target for T-cell—mediated cancer immunotherapy,” Clinical Cancer Research, vol. 13, no. 8, pp. 2471–2478, 2007. View at Publisher · View at Google Scholar · View at Scopus