Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2017 (2017), Article ID 2432904, 12 pages
https://doi.org/10.1155/2017/2432904
Research Article

MCL Plays an Anti-Inflammatory Role in Mycobacterium tuberculosis-Induced Immune Response by Inhibiting NF-κB and NLRP3 Inflammasome Activation

1Department of Immunology and Microbiology, Shanghai University of Traditional Chinese Medicine, Shanghai, 201203, China
2Major in Biology, The University of British Columbia, Vancouver, Canada V6T 1Z4
3Department of Chemistry, School of Pharmacy, Fourth Military Medical University, Xi’an, Shaanxi 710034, China

Correspondence should be addressed to Yuejuan Zheng; moc.361@21467714631 and Xin Jiang; moc.361@oagnixgnaij

Received 6 December 2016; Accepted 28 March 2017; Published 31 May 2017

Academic Editor: Giuseppe Valacchi

Copyright © 2017 Qingwen Zhang 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. Y. Zhang, Y. Lu, L. Ma et al., “Activation of vascular endothelial growth factor receptor-3 in macrophages restrains TLR4-NF-κB signaling and protects against endotoxin shock,” Immunity, vol. 40, no. 4, pp. 501–514, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Nathan and A. Ding, “Nonresolving inflammation,” Cell, vol. 140, no. 6, pp. 871–882, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. C. A. Dinarello, “Role of interleukin-1 in infectious diseases,” Immunological Reviews, vol. 127, no. 1, pp. 119–146, 1992. View at Publisher · View at Google Scholar
  4. R. Korhonen, A. Lahti, H. Kankaanranta, and E. Moilanen, “Nitric oxide production and signaling in inflammation,” Current Drug Targets. Inflammation and Allergy, vol. 4, no. 4, pp. 471–479, 2005. View at Google Scholar
  5. M. Feldmann and R. N. Maini, “Lasker clinical medical research award. TNF defined as atherapeutic target for rheumatoid arthritis and other autoimmune diseases,” Nature Medicine, vol. 9, no. 10, pp. 1245–1250, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. J. G. Hakim, I. Ternouth, E. Mushangi, S. Siziya, V. Robertson, and A. Malin, “Double blind randomised placebo controlled trial of adjunctive prednisolone in the treatment of effusive tuberculous pericarditis in HIV seropositive patients,” Heart, vol. 84, no. 2, pp. 183–188, 2000. View at Publisher · View at Google Scholar
  7. K. Prasad, M. B. Singh, and H. Ryan, “Corticosteroids for managing tuberculous meningitis,” Cochrane Database of Systematic Reviews, no. 4, article CD0022444, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. J. A. Critchley, F. Young, L. Orton, and P. Garner, “Corticosteroids for prevention of mortality in people with tuberculosis: a systematic review and meta-analysis,” The Lancet Infectious Diseases, vol. 13, no. 3, pp. 223–237, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Dinarello, “Biologic basis for interleukin-1 in disease,” Blood, vol. 87, no. 6, pp. 2095–2147, 1996. View at Google Scholar
  10. A. K. Nussler and T. R. Billiar, “Inflammation, immunoregulation, and inducible nitric oxide synthase,” Journal of Leukocyte Biology, vol. 54, no. 2, pp. 171–178, 1993. View at Google Scholar
  11. L. G. Bekker, A. L. Moreira, A. Bertgold, S. Freeman, B. Ryffel, and G. Kaplan, “Immunopathologic effects of tumor necrosis factor α in murine mycobacterial infection are dose dependent,” Infection and Immunity, vol. 68, no. 12, pp. 6954–6961, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Kasahara, K. Kobayashi, Y. Shikama et al., “Direct evidence for granuloma inducing activity of interleukin-1: induction of experimental pulmonary granuloma formation in mice byinterleukin-1–coupled beads,” The American Journal of Pathology, vol. 130, no. 3, pp. 629–638, 1988. View at Google Scholar
  13. Y. He, H. Hara, and G. Núñez, “Mechanism and regulation of NLRP3 inflammasome activation,” Trends in Biochemical Sciences, vol. 41, no. 12, pp. 1012–1021, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Gasparini and M. Feldmann, “NF-κB as a target for modulating inflammatory responses,” Current Pharmaceutical Design, vol. 18, no. 35, pp. 5735–5745, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Lawrence and C. Fong, “The resolution of inflammation: anti-inflammatory roles for NF-kappaB,” The International Journal of Biochemistry & Cell Biology, vol. 42, no. 4, pp. 519–523, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. F. G. Bauernfeind, G. Horvath, A. Stutz et al., “Cuttingedge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression,” Journal of Immunology, vol. 183, no. 2, pp. 787–791, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Lamkanfi and V. M. Dixit, “Mechanisms and functions of inflammasomes,” Cell, vol. 157, no. 5, pp. 1013–1022, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. H. W. Kang, J. M. Kim, M. Y. Cha, H. C. Jung, I. S. Song, and J. S. Kim, “Deguelin, an Akt inhibitor, down-regulates NF-κB signaling and induces apoptosis in colon cancer cells and inhibits tumor growth in mice,” Digestive Diseases and Sciences, vol. 57, no. 11, pp. 2873–2882, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. X. Li, F. Chen, Q. Zhu et al., “Gli-1/PI3K/AKT/NF-kB pathway mediates resistance to radiation and is a target for reversion of responses in refractory acute myeloid leukemia cells,” Oncotarget, vol. 7, no. 22, pp. 33004–33015, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Guo, L. Yang, J. Luo et al., “Sophoraflavanone G from Sophora alopecuroides inhibits lipopolysaccharide-induced inflammation in RAW264.7 cells by targeting PI3K/Akt, JAK/STAT and Nrf2/HO-1 pathways,” International Immunopharmacology, vol. 38, pp. 349–356, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. WHO, Global Tuberculosis Report, World Health Organization, Geneva, Switzerland, 2015.
  22. A. M. Dannenberg Jr, “Pathogenesis of pulmonary Mycobacterium Bovis infection: basic principles established by the rabbit model,” Tuberculosis (Edinburgh, Scotland), vol. 81, no. 1-2, pp. 87–96, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. C. A. Dinarello, “Immunological and inflammatory functions of the interleukin-1 family,” Annual Review Immunology, vol. 27, pp. 519–550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Seiler, P. Aichele, S. Bandermann et al., “Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines,” European Journal of Immunology, vol. 33, no. 10, pp. 2676–2686, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. A. A. Chackerian, T. V. Perera, and S. M. Behar, “Gamma interferon-producing CD4+ T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis,” Infection and Immunity, vol. 69, no. 4, pp. 2666–2674, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Y. Eum, J. H. Kong, M. S. Hong et al., “Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB,” Chest, vol. 137, no. 1, pp. 122–128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. E. B. Eruslanov, I. V. Lyadova, T. K. Kondratieva et al., “Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice,” Infection and Immunity, vol. 73, no. 3, pp. 1744–1753, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. D. M. Tobin, “Host-directed therapies for tuberculosis,” Cold Spring Harbor Perspectives in Medicine, vol. 5, no. 10, article a021196, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Zumla, M. Maeurer, Host-Directed Therapies Network et al., “Towards host-directed therapies for tuberculosis,” Nature Reviews. Drug Discovery, vol. 14, no. 8, pp. 511-512, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Sachan, A. Srivastava, R. Ranjan, A. Gupta, S. Pandya, and A. Misra, “Opportunities and challenges for host-directed therapies in tuberculosis,” Current Pharmaceutical Design, vol. 22, no. 17, pp. 2599–2604, 2016. View at Publisher · View at Google Scholar
  31. B. Ivanescu, A. Miron, and A. Corciova, “Sesquiterpene lactones from Artemisia genus: biological activities and methods of analysis,” Journal of Analytical Methods in Chemistry, vol. 2015, Article ID 247685, 21 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. A. K. Picman, “Biological activities of sesquiterpene lactones,” Biochemical Systematics and Ecology, vol. 14, no. 3, pp. 255–281, 1986. View at Google Scholar
  33. A. Ghantous, H. Gali-Muhtasib, H. Vuorela, N. A. Saliba, and N. Darwiche, “What made sesquiterpene lactones reach cancer clinical trials?” Drug Discovery Today, vol. 15, no. 15-16, pp. 668–678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. X. Qin, X. Jiang, X. Jiang et al., “Micheliolide inhibits LPS-induced inflammatory response and protects mice from LPS challenge,” Scientific Reports, vol. 6, article 23240, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. L. P. Kane, V. S. Shapiro, D. Stokoe, and A. Weiss, “Induction of NF-κB by the Akt/PKB kinase,” Current Biology, vol. 9, no. 11, pp. 601–604, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. O. N. Ozes, L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner, “NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase,” Nature, vol. 401, no. 6748, pp. 82–85, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. J. D. Martins, J. Liberal, A. Silva, I. Ferreira, B. M. Neves, and M. T. Cruz, “Autophagy and inflammasome interplay,” DNA and Cell Biology, vol. 34, no. 4, pp. 274–281, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Tanida, “Autophagosome formation and molecular mechanism of autophagy,” Antioxidants & Redox Signaling, vol. 14, no. 11, pp. 2201–2214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Garza-Lombó and M. E. Gonsebatt, “Mammalian target of rapamycin: its role in early neural development and in adult and aged brain function,” Frontiers in Cellular Neuroscience, vol. 10, p. 157, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. F. Sun, X. Xu, X. Wang, and B. Zhang, “Regulation of autophagy by Ca+,” Tumour Biology, vol. 37, no. 12, pp. 15467–15476, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. S. H. Kaufmann and A. Dorhoi, “Inflammation in tuberculosis: interactions, imbalances and interventions,” Current Opinion in Immunology, vol. 25, no. 4, pp. 441–449, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. B. B. Mishra, V. A. Rathinam, G. W. Martens et al., “Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1β,” Nature Immunology, vol. 14, no. 1, pp. 52–60, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. K. W. Wong and W. R. Jacobs Jr, “Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis,” Cellular Microbiology, vol. 13, no. 9, pp. 1371–1384, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Dorhoi, G. Nouailles, S. Jörg et al., “Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis,” European Journal of Immunology, vol. 42, no. 2, pp. 374–384, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. H. J. Yoon, M. E. Moon, H. S. Park, S. Y. Im, and Y. H. Kim, “Chitosan oligosaccharide (COS) inhibits LPS-induced inflammatory effects in RAW264.7 macrophage cells,” Biochemical and Biophysical Research Communications, vol. 358, no. 3, pp. 954–959, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. D. M. Tobin, F. J. Roca, S. F. Oh et al., “Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections,” Cell, vol. 148, no. 3, pp. 434–446, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. F. J. Roca and L. Ramakrishnan, “TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species,” Cell, vol. 153, no. 3, pp. 521–534, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. R. M. R. M. Palmer, D. D. D. D. Rees, D. S. Ashton, and S. Moncada, “L-arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation,” Biochemical and Biophysical Research Communications, vol. 153, no. 3, pp. 1251–1256, 1988. View at Google Scholar
  49. P. Pacher, S. Joseph, J. S. Beckman, and L. Liaudet, “Nitric oxide and peroxynitrite in health and disease,” Physiological Reviews, vol. 87, no. 1, pp. 315–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Petros, D. Bennett, and P. Vallance, “Effect of nitric oxide synthase inhibitors on hypotension in patients with septic shock,” Lancet, vol. 338, no. 8782-8783, pp. 1557-1558, 1991. View at Google Scholar
  51. N. McCartney-Francis, J. B. Allen, D. E. Mizel et al., “Suppression of arthritis by an inhibitor of nitric oxide synthase,” The Journal of Experimental Medicine, vol. 178, no. 2, pp. 749–754, 1993. View at Google Scholar
  52. G. Pedruzzi, P. N. Das, K. V. Rao, and S. Chatterjee, “Understanding PGE2, LXA4 and LTB4 balance during Mycobacterium tuberculosis infection through mathematical model,” Journal of Theoretical Biology, vol. 389, pp. 159–170, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Panday, M. E. Inda, P. Bagam, M. K. Sahoo, D. Osorio, and S. Batra, “Transcription factor NF-κB: an update on intervention strategies,” Archivum Immunologiae et Therapiae Experimentalis (Warsz), vol. 64, no. 6, pp. 463–483, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Schuliga, “NF-kappaB signaling in chronic inflammatory airway disease,” Biomolecules, vol. 5, no. 3, pp. 1266–1283, 2015. View at Publisher · View at Google Scholar