Skip to main content
Erschienen in: Inflammation 6/2016

02.09.2016 | ORIGINAL ARTICLE

Therapeutic Effects of Resveratrol in a Mouse Model of LPS and Cigarette Smoke-Induced COPD

verfasst von: Jinlong Chen, Xu Yang, Weiya Zhang, Danhua Peng, Yanan Xia, Yi Lu, Xiaodong Han, Guangjie Song, Jing Zhu, Renping Liu

Erschienen in: Inflammation | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

This study was designed to examine whether resveratrol exerts the protective effects on LPS and cigarette smoke (LC)-induced COPD in a murine model. In lung histopathological studies, H&E, Masson’s trichrome, and AB-PAS staining were performed. The cytokines (IL-6, IL-17, TGF-β, and TNF-α) and inflammatory cells in BALF were determined. The Beclin1 level in the lungs of mouse was analyzed. Compared with the LC-induced mouse, the level of inflammatory cytokines (IL-17, IL-6, TNF-α, and TGF-β) of the BALF in the resveratrol + cigarette smoke-treated mouse had obviously decreased. Histological examination of the lung tissue revealed that the resveratrol treatment attenuated the fibrotic response and mucus hypersecretion. In addition, resveratrol inhibited the expression of the Beclin1 protein in mouse lungs. The presented findings collectively suggest that resveratrol has a therapeutic effect on mouse LC-induced COPD, and its mechanism of action might be related to reducing the production of the Beclin1 protein.
Literatur
1.
Zurück zum Zitat Wollin, L., and M.P. Pieper. 2010. Tiotropium bromide exerts anti-inflammatory activity in a cigarette smoke mouse model of COPD. Pulmonary Pharmacology & Therapeutics 23(2010): 345–354.CrossRef Wollin, L., and M.P. Pieper. 2010. Tiotropium bromide exerts anti-inflammatory activity in a cigarette smoke mouse model of COPD. Pulmonary Pharmacology & Therapeutics 23(2010): 345–354.CrossRef
2.
Zurück zum Zitat Tamini, A., D. Serdarevic, and N.A. Hanania. 2012. The effects of cigarette smoke on airway inflammation in asthma and COPD: therapeutic implications. Respiratory Medicine 106(2012): 319–328.CrossRef Tamini, A., D. Serdarevic, and N.A. Hanania. 2012. The effects of cigarette smoke on airway inflammation in asthma and COPD: therapeutic implications. Respiratory Medicine 106(2012): 319–328.CrossRef
3.
Zurück zum Zitat Busse, P.J., T.F. Zhang, K. Srivastava, B.P. Lin, B. Schofield, S.C. Sealfon, and X.M. Li. 2005. Chronic exposure to TNF-alpha increases airway mucus gene expression in vivo. Journal of Allergy and Clinical Immunology 116(6): 1256–1263.CrossRefPubMed Busse, P.J., T.F. Zhang, K. Srivastava, B.P. Lin, B. Schofield, S.C. Sealfon, and X.M. Li. 2005. Chronic exposure to TNF-alpha increases airway mucus gene expression in vivo. Journal of Allergy and Clinical Immunology 116(6): 1256–1263.CrossRefPubMed
4.
Zurück zum Zitat Numasaki, M., Y. Tomioka, H. Takahashi, and H. Sasaki. 2004. IL-17 and IL-17F modulate GM-CSF production by lung microvascular endothelial cells stimulated with IL-1beta and/or TNF-alpha. Immunology Letters 95(2): 175–184.CrossRefPubMed Numasaki, M., Y. Tomioka, H. Takahashi, and H. Sasaki. 2004. IL-17 and IL-17F modulate GM-CSF production by lung microvascular endothelial cells stimulated with IL-1beta and/or TNF-alpha. Immunology Letters 95(2): 175–184.CrossRefPubMed
5.
Zurück zum Zitat Friedrichs, B., U. Neumann, J. Schuller, and M.J. Peck. 2014. Cigarette-smoke-induced priming of neutrophils from smokers and non-smokers for increased oxidative burst response is mediated by TNF-alpha. Toxicology In Vitro : An International Journal Published in Association with BIBRA 28(7): 1249–1258.CrossRef Friedrichs, B., U. Neumann, J. Schuller, and M.J. Peck. 2014. Cigarette-smoke-induced priming of neutrophils from smokers and non-smokers for increased oxidative burst response is mediated by TNF-alpha. Toxicology In Vitro : An International Journal Published in Association with BIBRA 28(7): 1249–1258.CrossRef
6.
Zurück zum Zitat Kohri, K., R.F. Ueki, and A.A. Nadel. 2002. Neutrophil elastase induces mucin production by ligand-dependent pidermal growth factor receptor activation. American Journal of Physiology Lung Cellular and Molecular Physiology 283(3): 531–540.CrossRef Kohri, K., R.F. Ueki, and A.A. Nadel. 2002. Neutrophil elastase induces mucin production by ligand-dependent pidermal growth factor receptor activation. American Journal of Physiology Lung Cellular and Molecular Physiology 283(3): 531–540.CrossRef
7.
Zurück zum Zitat Ryter, S.W., S.-J. Lee, and A.M. Choi. 2010. Autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. Expert Review of Respiratory Medicine 4(5): 573–584.CrossRefPubMedPubMedCentral Ryter, S.W., S.-J. Lee, and A.M. Choi. 2010. Autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. Expert Review of Respiratory Medicine 4(5): 573–584.CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Wang, X., Y. Wang, X. Zhao, R. Andersson, Z. Song, D. Yang, and C. Bai. 2009. Potential effects of peroxisome proliferator-activated receptor activator on LPS-induced lung injury in rats. Pulmonary Pharmacology & Therapeutics 22(4): 318–325.CrossRef Wang, X., Y. Wang, X. Zhao, R. Andersson, Z. Song, D. Yang, and C. Bai. 2009. Potential effects of peroxisome proliferator-activated receptor activator on LPS-induced lung injury in rats. Pulmonary Pharmacology & Therapeutics 22(4): 318–325.CrossRef
9.
Zurück zum Zitat Hardaker, E.L., M.S. Freeman, N. Dale, P. Bahra, F. Raza, K.H. Banner, and C. Poll. 2010. Exposing rodents to a combination of tobacco smoke and lipopolysaccharide results in an exaggerated inflammatory response in the lung. British Journal of Pharmacology 160(8): 1985–1996.CrossRefPubMedPubMedCentral Hardaker, E.L., M.S. Freeman, N. Dale, P. Bahra, F. Raza, K.H. Banner, and C. Poll. 2010. Exposing rodents to a combination of tobacco smoke and lipopolysaccharide results in an exaggerated inflammatory response in the lung. British Journal of Pharmacology 160(8): 1985–1996.CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Ryu, H.W., H.-H. Song, I.-S. Shin, B.O. Cho, S.H. Jeong, D.-Y. Kim, K.-S. Ahn, and S.-R. Oh. 2015. Suffruticosol A isolated from Paeonia lactiflora seedcases attenuates airway inflammation in mice induced by cigarette smoke and LPS exposure. Journal of Functional Foods 17: 774–784.CrossRef Ryu, H.W., H.-H. Song, I.-S. Shin, B.O. Cho, S.H. Jeong, D.-Y. Kim, K.-S. Ahn, and S.-R. Oh. 2015. Suffruticosol A isolated from Paeonia lactiflora seedcases attenuates airway inflammation in mice induced by cigarette smoke and LPS exposure. Journal of Functional Foods 17: 774–784.CrossRef
11.
Zurück zum Zitat Milara, J., J. Lluch, P. Almudever, J. Freire, Q. Xiaozhong, and J. Cortijo. 2014. Roflumilast N-oxide reverses corticosteroid resistance in neutrophils from patients with chronic obstructive pulmonary disease. Journal of Allergy and Clinical Immunology 134(2): 314–322.CrossRefPubMed Milara, J., J. Lluch, P. Almudever, J. Freire, Q. Xiaozhong, and J. Cortijo. 2014. Roflumilast N-oxide reverses corticosteroid resistance in neutrophils from patients with chronic obstructive pulmonary disease. Journal of Allergy and Clinical Immunology 134(2): 314–322.CrossRefPubMed
12.
Zurück zum Zitat Bellaver, Bruna, D.G. Souza, D.O. Souza, and A. Quincozes-Santos. 2014. Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicology in Vitro 28(4): 479–484.CrossRefPubMed Bellaver, Bruna, D.G. Souza, D.O. Souza, and A. Quincozes-Santos. 2014. Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicology in Vitro 28(4): 479–484.CrossRefPubMed
13.
Zurück zum Zitat Wang, D.-G., W.-Y. Liu, and G.-T. Chen. 2013. A simple method for the isolation and purification of resveratrol from Polygonum cuspidatum. Journal of Pharmaceutical Analysis 3(4): 241–247.CrossRef Wang, D.-G., W.-Y. Liu, and G.-T. Chen. 2013. A simple method for the isolation and purification of resveratrol from Polygonum cuspidatum. Journal of Pharmaceutical Analysis 3(4): 241–247.CrossRef
14.
Zurück zum Zitat Tang, W., J. Xie, S. Xu, H. Lv, M. Lin, S. Yuan, J. Bai, Q. Hou, and S. Yu. 2014. Novel nitric oxide-releasing derivatives of brusatol as anti- inflammatory agents: design, synthesis, biological evaluation, and nitric oxide release studies. Journal of Medicinal Chemistry 57(18): 7600–7612.CrossRefPubMed Tang, W., J. Xie, S. Xu, H. Lv, M. Lin, S. Yuan, J. Bai, Q. Hou, and S. Yu. 2014. Novel nitric oxide-releasing derivatives of brusatol as anti- inflammatory agents: design, synthesis, biological evaluation, and nitric oxide release studies. Journal of Medicinal Chemistry 57(18): 7600–7612.CrossRefPubMed
15.
Zurück zum Zitat Voynow, J.A., B.M. Fischer, D.E. Malarkey, L.H. Burch, T. Wong, M. Longphre, S.B. Ho, and W.M. Foster. 2004. Neutrophil elastase induces mucus cell metaplasia in mouse lung. American Journal of Physiology Lung Cellular and Molecular Physiology 287(6): L1293–1302.CrossRefPubMed Voynow, J.A., B.M. Fischer, D.E. Malarkey, L.H. Burch, T. Wong, M. Longphre, S.B. Ho, and W.M. Foster. 2004. Neutrophil elastase induces mucus cell metaplasia in mouse lung. American Journal of Physiology Lung Cellular and Molecular Physiology 287(6): L1293–1302.CrossRefPubMed
16.
Zurück zum Zitat Chen, J., H. Zhou, J. Wang, B. Zhang, F. Liu, J. Huang, J. Li, J. Lin, J. Bai, and R. Liu. 2015. Therapeutic effects of resveratrol in a mouse model of HDM-induced allergic asthma. International Immunopharmacology 25(1): 43–48.CrossRefPubMed Chen, J., H. Zhou, J. Wang, B. Zhang, F. Liu, J. Huang, J. Li, J. Lin, J. Bai, and R. Liu. 2015. Therapeutic effects of resveratrol in a mouse model of HDM-induced allergic asthma. International Immunopharmacology 25(1): 43–48.CrossRefPubMed
17.
Zurück zum Zitat Klopfleisch, R. 2013. Multiparametric and semiquantitative scoring systems for the evaluation of mouse model histopathology—a systematic review. BMC Veterinary Research 123(9): 1–15. Klopfleisch, R. 2013. Multiparametric and semiquantitative scoring systems for the evaluation of mouse model histopathology—a systematic review. BMC Veterinary Research 123(9): 1–15.
18.
Zurück zum Zitat Churg, A., M. Cosio, and J.L. Wright. 2008. Mechanisms of cigarette smoke-induced COPD: insights from animal models. American Journal of Physiology Lung Cellular and Molecular Physiology 83(4): 1385–1396. Churg, A., M. Cosio, and J.L. Wright. 2008. Mechanisms of cigarette smoke-induced COPD: insights from animal models. American Journal of Physiology Lung Cellular and Molecular Physiology 83(4): 1385–1396.
19.
Zurück zum Zitat Makinde, T., R.F. Murphy, and D.K. Agrawal. 2007. The regulatory role of TGF-beta in airway remodeling in asthma. Immunology and Cell Biology 85(5): 348–356.CrossRefPubMed Makinde, T., R.F. Murphy, and D.K. Agrawal. 2007. The regulatory role of TGF-beta in airway remodeling in asthma. Immunology and Cell Biology 85(5): 348–356.CrossRefPubMed
20.
Zurück zum Zitat Liu, R., J. Bai, G. Xu, L. Xuan, T. Zhang, A. Meng, and Q. Hou. 2013. Multi-allergen challenge stimulates steriod-resistant airway inflammation via NF-kappaB-mediated IL-8 expression. Inflammation 36(4): 845–854.CrossRefPubMed Liu, R., J. Bai, G. Xu, L. Xuan, T. Zhang, A. Meng, and Q. Hou. 2013. Multi-allergen challenge stimulates steriod-resistant airway inflammation via NF-kappaB-mediated IL-8 expression. Inflammation 36(4): 845–854.CrossRefPubMed
21.
Zurück zum Zitat Chakir, Jamila, Joanne Shannon, Sophie Molet, Motonori Fukakusa, Jack Elias, Michel Laviolette, Louis-Philippe Boulet, and Q. Hamid. 2003. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-β, IL-11, IL-17, and type I and type III collagen expression. Journal of Allergy and Clinical Immunology 111(6): 1293–1298.CrossRefPubMed Chakir, Jamila, Joanne Shannon, Sophie Molet, Motonori Fukakusa, Jack Elias, Michel Laviolette, Louis-Philippe Boulet, and Q. Hamid. 2003. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-β, IL-11, IL-17, and type I and type III collagen expression. Journal of Allergy and Clinical Immunology 111(6): 1293–1298.CrossRefPubMed
22.
Zurück zum Zitat Neveu, W.A., J.L. Allard, D.M. Raymond, L.M. Bourassa, S.M. Burns, J.Y. Bunn, C.G. Irvin, D.A. Kaminsky, and M. Rincon. 2010. Elevation of IL-6 in the allergic asthmatic airway is independent of inflammation but associates with loss of central airway function. Respiratory Research 28(11): 1–10. Neveu, W.A., J.L. Allard, D.M. Raymond, L.M. Bourassa, S.M. Burns, J.Y. Bunn, C.G. Irvin, D.A. Kaminsky, and M. Rincon. 2010. Elevation of IL-6 in the allergic asthmatic airway is independent of inflammation but associates with loss of central airway function. Respiratory Research 28(11): 1–10.
23.
Zurück zum Zitat Linden, A., and M. Adachi. 2002. Neutrophilic airway inflammation and IL-17. Allergy 57(9): 769–775.CrossRefPubMed Linden, A., and M. Adachi. 2002. Neutrophilic airway inflammation and IL-17. Allergy 57(9): 769–775.CrossRefPubMed
24.
Zurück zum Zitat Neveu, W.A., J.L. Allard, D.M. Raymond, L.M. Bourassa, S.M. Burns, J.Y. Bunn, C.G. Irvin, D.A. Kaminsky, and M. Rincon. 2010. Elevation of IL-6 in the allergic asthmatic airway is independent of inflammation but associates with loss of central airway function. Respiratory Research 11: 28.CrossRefPubMedPubMedCentral Neveu, W.A., J.L. Allard, D.M. Raymond, L.M. Bourassa, S.M. Burns, J.Y. Bunn, C.G. Irvin, D.A. Kaminsky, and M. Rincon. 2010. Elevation of IL-6 in the allergic asthmatic airway is independent of inflammation but associates with loss of central airway function. Respiratory Research 11: 28.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Fischer, B.M., E. Pavlisko, and J.A. Voynow. 2011. Pathogenic triad in COPD: oxidative stress, protease-antiprotease imbalance, and inflammation. International Journal of COPD 1(6): 413–421.CrossRef Fischer, B.M., E. Pavlisko, and J.A. Voynow. 2011. Pathogenic triad in COPD: oxidative stress, protease-antiprotease imbalance, and inflammation. International Journal of COPD 1(6): 413–421.CrossRef
26.
Zurück zum Zitat Kim, H.P., X. Wang, S.-J. Lee, M.-H. Huang, Y. Wan, S.W. Ryter, and A.M.K. Choi. 2008. Autophagic proteins regulate cigarette smoke induced apoptosis: protective role of heme oxygenase-1. Autophagy 4(7): 887–895.CrossRefPubMed Kim, H.P., X. Wang, S.-J. Lee, M.-H. Huang, Y. Wan, S.W. Ryter, and A.M.K. Choi. 2008. Autophagic proteins regulate cigarette smoke induced apoptosis: protective role of heme oxygenase-1. Autophagy 4(7): 887–895.CrossRefPubMed
28.
Zurück zum Zitat Shi, J., N. Yin, L.L. Xuan, C.S. Yao, A.M. Meng, and Q. Hou. 2012. Vam3, a derivative of resveratrol, attenuates cigarette smoke-induced autophagy. Acta Pharmacologica Sinica 33(7): 888–896.CrossRefPubMedPubMedCentral Shi, J., N. Yin, L.L. Xuan, C.S. Yao, A.M. Meng, and Q. Hou. 2012. Vam3, a derivative of resveratrol, attenuates cigarette smoke-induced autophagy. Acta Pharmacologica Sinica 33(7): 888–896.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Knobloch, J., B. Sibbing, D. Jungck, Y. Lin, K. Urban, E. Stoelben, J. Strauch, and A. Koch. 2010. Resveratrol impairs the release of steroid-resistant inflammatory cytokines from human airway smooth muscle cells in chronic obstructive pulmonary disease. The Journal of Pharmacology and Experimental Therapeutics 335(3): 788–798.CrossRefPubMed Knobloch, J., B. Sibbing, D. Jungck, Y. Lin, K. Urban, E. Stoelben, J. Strauch, and A. Koch. 2010. Resveratrol impairs the release of steroid-resistant inflammatory cytokines from human airway smooth muscle cells in chronic obstructive pulmonary disease. The Journal of Pharmacology and Experimental Therapeutics 335(3): 788–798.CrossRefPubMed
30.
Zurück zum Zitat Wood, Lisa G., P.A.B. Wark, and M.L. Garg. 2009. Antioxidant and anti-inflammatory effects of resveratrol in airway disease. Antioxidants & Redox Signaling 13(10): 1535–1548.CrossRef Wood, Lisa G., P.A.B. Wark, and M.L. Garg. 2009. Antioxidant and anti-inflammatory effects of resveratrol in airway disease. Antioxidants & Redox Signaling 13(10): 1535–1548.CrossRef
31.
Zurück zum Zitat Mikula-Pietrasik, J., A. Kuczmarska, M. Kucinska, M. Murias, M. Wierzchowski, M. Winckiewicz, R. Staniszewski, A. Breborowicz, and K. Ksiazek. 2012. Resveratrol and its synthetic derivatives exert opposite effects on mesothelial cell-dependent angiogenesis via modulating secretion of VEGF and IL-8/CXCL8. Angiogenesis 15(3): 361–376.CrossRefPubMedPubMedCentral Mikula-Pietrasik, J., A. Kuczmarska, M. Kucinska, M. Murias, M. Wierzchowski, M. Winckiewicz, R. Staniszewski, A. Breborowicz, and K. Ksiazek. 2012. Resveratrol and its synthetic derivatives exert opposite effects on mesothelial cell-dependent angiogenesis via modulating secretion of VEGF and IL-8/CXCL8. Angiogenesis 15(3): 361–376.CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Lee, K.Y., J.Y. Jung, M.Y. Lee, D. Jung, E.S. Cho, and H.Y. Son. 2012. Diospyros blancoi attenuates asthmatic effects in a mouse model of airway inflammation. Inflammation 35(2): 623–632.CrossRefPubMed Lee, K.Y., J.Y. Jung, M.Y. Lee, D. Jung, E.S. Cho, and H.Y. Son. 2012. Diospyros blancoi attenuates asthmatic effects in a mouse model of airway inflammation. Inflammation 35(2): 623–632.CrossRefPubMed
Metadaten
Titel
Therapeutic Effects of Resveratrol in a Mouse Model of LPS and Cigarette Smoke-Induced COPD
verfasst von
Jinlong Chen
Xu Yang
Weiya Zhang
Danhua Peng
Yanan Xia
Yi Lu
Xiaodong Han
Guangjie Song
Jing Zhu
Renping Liu
Publikationsdatum
02.09.2016
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 6/2016
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-016-0430-3

Weitere Artikel der Ausgabe 6/2016

Inflammation 6/2016 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.