Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 8287125, 13 pages
https://doi.org/10.1155/2017/8287125
Research Article

Plant Proteinase Inhibitor BbCI Modulates Lung Inflammatory Responses and Mechanic and Remodeling Alterations Induced by Elastase in Mice

1Department of Medicine, School of Medicine, University of São Paulo, São Paulo, SP, Brazil
2Division of Pulmonary and Critical Care Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA
3Department of Biochemistry, Federal University of São Paulo, São Paulo, SP, Brazil
4Department of Biological Sciences, Federal University of São Paulo, São Paulo, SP, Brazil
5The Lovelace Respiratory Research Institute, Albuquerque, NM, USA

Correspondence should be addressed to Iolanda F. L. C. Tibério; rb.moc.lou@ovlacoi

Received 18 August 2016; Revised 20 February 2017; Accepted 9 March 2017; Published 30 March 2017

Academic Editor: Anastasia Kotanidou

Copyright © 2017 Rafael Almeida-Reis 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. L. Fromer and C. B. Cooper, “A review of the GOLD guidelines for the diagnosis and treatment of patients with COPD,” International Journal of Clinical Practice, vol. 62, no. 8, pp. 1219–1236, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. C.-B. Laurell and S. Eriksson, “The electrophoretic α;1-globulin pattern of serum in α;1-antitrypsin deficiency,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 15, no. 2, pp. 132–140, 1963. View at Publisher · View at Google Scholar · View at Scopus
  3. S. D. Shapiro, N. M. Goldstein, A. M. Houghton, D. K. Kobayashi, D. Kelley, and A. Belaaouaj, “Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice,” American Journal of Pathology, vol. 163, no. 6, pp. 2329–2335, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. R. A. Pauwels, A. S. Buist, P. M. A. Calverley, C. R. Jenkins, and S. S. Hurd, “Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) workshop summary,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 5, pp. 1256–1276, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Mahadeva and S. D. Shapiro, “Chronic obstructive pulmonary disease ∗ 3: experimental animal models of pulmonary emphysema,” Thorax, vol. 57, no. 10, pp. 908–914, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Turk, “Targeting proteases: successes, failures and future prospects,” Nature Reviews Drug Discovery, vol. 5, no. 9, pp. 785–799, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. P. J. Barnes and R. A. Stockley, “COPD: current therapeutic interventions and future approaches,” European Respiratory Journal, vol. 25, no. 6, pp. 1084–1106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. F. De Leo, M. Volpicella, F. Licciulli, S. Liuni, R. Gallerani, and L. R. Ceci, “PLANT-PIs: a database for plant protease inhibitors and their genes,” Nucleic Acids Research, vol. 30, no. 1, pp. 347–348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. M. L. Oliva and M. U. Sampaio, “Action of plant proteinase inhibitors on enzymes of physiopathological importance,” Anais da Academia Brasileira de Ciências, vol. 81, no. 3, pp. 615–621, 2009. View at Google Scholar
  10. M. L. Vilela Oliva and M. U. Sampaio, “Bauhinia Kunitz-type proteinase inhibitors: structural characteristics and biological properties,” Biological Chemistry, vol. 389, no. 8, pp. 1007–1013, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. A. P. Ulian Araújo, D. Hansen, D. F. Vieira et al., “Kunitz-type Bauhinia bauhinioides inhibitors devoid of disulfide bridges: isolation of the cDNAs, heterologous expression and structural studies,” Biological Chemistry, vol. 386, no. 6, pp. 561–568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Neuhof, M. L. V. Oliva, D. Maybauer, M. U. Sampaio, C. A. M. Sampaio, and H. Neuhof, “Effect of plant Kunitz from Bauhinia bauhinioides and Bauhinia rufa on pulmonary edema caused by activated neutrophils,” Biological Chemistry, vol. 384, no. 6, pp. 939–944, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Hantos, R. A. Collins, D. J. Turner, T. Z. Jánosi, and P. D. Sly, “Tracking of airway and tissue mechanics during TLC maneuvers in mice,” Journal of Applied Physiology, vol. 95, no. 4, pp. 1695–1705, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. A. C. Toledo, F. M. Arantes-Costa, M. Macchione et al., “Salbutamol improves markers of epithelial function in mice with chronic allergic pulmonary inflammation,” Respiratory Physiology and Neurobiology, vol. 177, no. 2, pp. 155–161, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. E. R. Weibel, “Morphological quantitation of emphysema: a debate,” Journal of Applied Physiology, vol. 100, no. 4, pp. 1419–1421, 2005. View at Publisher · View at Google Scholar
  16. A. Churg and J. L. Wright, “Proteases and emphysema,” Current Opinion in Pulmonary Medicine, vol. 11, no. 2, pp. 153–159, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. C. A. Owen, “Roles for proteinases in the pathogenesis of chronic obstructive pulmonary disease,” International Journal of Chronic Obstructive Pulmonary Disease, vol. 3, no. 2, pp. 253–268, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Shapiro, “Proteolysis in the lung,” European Respiratory Journal, vol. 44, pp. 30s–32s, 2003. View at Publisher · View at Google Scholar
  19. C. A. Owen and E. J. Campbell, “The cell biology of leukocyte-mediated proteolysis,” Journal of Leukocyte Biology, vol. 65, no. 2, pp. 137–150, 1999. View at Google Scholar · View at Scopus
  20. H. S. Deshmukh, L. M. Case, S. C. Wesselkamper et al., “Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation,” American Journal of Respiratory and Critical Care Medicine, vol. 171, no. 4, pp. 305–314, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Drag and G. S. Salvesen, “Emerging principles in protease-based drug discovery,” Nature Reviews Drug Discovery, vol. 9, no. 9, pp. 690–701, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Korkmaz, M. S. Horwitz, D. E. Jenne, and F. Gauthier, “Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases,” Pharmacological Reviews, vol. 62, no. 4, pp. 726–759, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Selman, J. Cisneros-Lira, M. Gaxiola et al., “Matrix metalloproteinases inhibition attenuates tobacco smoke-induced emphysema in guinea pigs,” Chest, vol. 123, no. 5, pp. 1633–1641, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. J. L. Wright, S. G. Farmer, and A. Churg, “A neutrophil elastase inhibitor reduces cigarette smoke-induced remodelling of lung vessels,” European Respiratory Journal, vol. 22, no. 1, pp. 77–81, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Guarnieri, J. L. Spencer, E. C. Lucey, M. A. Nugent, and P. J. Stone, “A human surfactant peptide-elastase inhibitor construct as a treatment for emphysema,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 23, pp. 10661–10666, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Luisetti, C. Sturani, D. Sella et al., “MR889, a neutrophil elastase inhibitor, in patients with chronic obstructive pulmonary disease: a double-blind, randomized, placebo-controlled clinical trial,” European Respiratory Journal, vol. 9, no. 7, pp. 1482–1486, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Fujie, Y. Shinguh, A. Yamazaki, H. Hatanaka, M. Okamoto, and M. Okuhara, “Inhibition of elastase-induced acute inflammation and pulmonary emphysema in hamsters by a novel neutrophil elastase inhibitor FR901277,” Inflammation Research, vol. 48, no. 3, pp. 160–167, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. L. V. Oliva, R. Almeida-Reis, O. Theodoro-Junior et al., “A plant proteinase inhibitor from Crataeva tapia (CrataBL) attenuates elastase-induced pulmonary inflammatory, remodeling, and mechanical alterations in mice,” Process Biochemistry, vol. 50, no. 11, pp. 1958–1965, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. B. T. Martins-Olivera, R. Almeida-Reis, O. A. Theodoro-Júnior et al., “The plant-derived Bauhinia bauhinioides Kallikrein proteinase inhibitor (rBbKI) attenuates elastase-induced emphysema in mice,” Mediators of Inflammation, vol. 2016, Article ID 5346574, 12 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Hantos, Á. Adamicza, T. Z. Jánosi, M. V. Szabari, J. Tolnai, and B. Suki, “Lung volumes and respiratory mechanics in elastase-induced emphysema in mice,” Journal of Applied Physiology, vol. 105, no. 6, pp. 1864–1872, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Ito, E. P. Ingenito, S. P. Arold et al., “Tissue heterogeneity in the mouse lung: effects of elastase treatment,” Journal of Applied Physiology, vol. 97, no. 1, pp. 204–212, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Scuri, R. Forteza, I. Lauredo et al., “Inhaled porcine pancreatic elastase causes bronchoconstriction via a bradykinin-mediated mechanism,” Journal of Applied Physiology, vol. 89, no. 4, pp. 1397–1402, 2000. View at Google Scholar · View at Scopus
  33. C. de Oliveira, L. A. Santana, A. K. Carmona et al., “Structure of cruzipain/cruzain inhibitors isolated from Bauhinia bauhinioides seeds,” Biological Chemistry, vol. 382, no. 5, pp. 847–852, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Suzuki, T. Betsuyaku, Y. Ito et al., “Curcumin attenuates elastase- and cigarette smoke-induced pulmonary emphysema in mice,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 296, no. 4, pp. L614–L623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Oliveira, R. A. Navarro-Xavier, E. A. Anjos-Vallota et al., “Effect of plant neutrophil elastase inhibitor on leucocyte migration, adhesion and cytokine release in inflammatory conditions,” British Journal of Pharmacology, vol. 161, no. 4, pp. 899–910, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. F. D. T. Q. S. Lopes, A. C. Toledo, C. R. Olivo et al., “A comparative study of extracellular matrix remodeling in two murine models of emphysema,” Histology and Histopathology, vol. 28, no. 2, pp. 269–276, 2013. View at Google Scholar · View at Scopus
  37. M. Hanaoka, Y. Droma, Y. Chen et al., “Carbocisteine protects against emphysema induced by cigarette smoke extract in rats,” Chest, vol. 139, no. 5, pp. 1101–1108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. R. D. Hautamaki, D. K. Kobayashi, R. M. Senior, and S. D. Shapiro, “Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice,” Science, vol. 277, no. 5334, pp. 2002–2004, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. C. M. Prado, E. A. Leick-Maldonado, V. Arata, D. I. Kasahara, M. A. Martins, and I. F. L. C. Tibério, “Neurokinins and inflammatory cell iNOS expression in guinea pigs with chronic allergic airway inflammation,” American Journal of Physiology-Lung Cellular and Molecular Physiology, vol. 288, no. 4, pp. L741–L748, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Kim and J. A. Nadel, “Role of neutrophils in mucus hypersecretion in COPD and implications for therapy,” Treatments in Respiratory Medicine, vol. 3, no. 3, pp. 147–159, 2004. View at Publisher · View at Google Scholar · View at Scopus