Skip to main content
Top
Published in: Inflammation 5/2014

01-10-2014

Oxidative Stress and Inflammation Are Differentially Affected by Atorvastatin, Pravastatin, Rosuvastatin, and Simvastatin on Lungs from Mice Exposed to Cigarette Smoke

Authors: Thiago Santos Ferreira, Manuella Lanzetti, Marina Valente Barroso, Carlos Romualdo Rueff-Barroso, Cláudia Farias Benjamim, Lycia de Brito-Gitirana, Luís Cristóvão Porto, Samuel Santos Valença

Published in: Inflammation | Issue 5/2014

Login to get access

Abstract

Our aim was to investigate the effects of four different statins on acute lung inflammation induced by cigarette smoke (CS). C57BL/6 male mice were divided into a control group (sham-smoked) and mice exposed to CS from 12 cigarettes/day for 5 days. Mice exposed to CS were grouped and treated with vehicle (i.p.), atorvastatin (10 mg/kg), pravastatin (10 mg/kg), rosuvastatin (5 mg/kg), or simvastatin (20 mg/kg). Treatment with statins differentially improved the pulmonary response when compared to the CS group. Atorvastatin and pravastatin demonstrated slightly effects on inflammation and oxidative stress. Rosuvastatin demonstrated the best anti-inflammatory effect, whereas simvastatin demonstrated the best antioxidant response.
Literature
1.
go back to reference Brody, J.S., and A. Spira. 2006. State of the art. Chronic obstructive pulmonary disease, inflammation, and lung cancer. Proceedings of the American Thoracic Society 3: 535–7.PubMedCrossRef Brody, J.S., and A. Spira. 2006. State of the art. Chronic obstructive pulmonary disease, inflammation, and lung cancer. Proceedings of the American Thoracic Society 3: 535–7.PubMedCrossRef
3.
4.
go back to reference Takahashi, S., H. Nakamura, M. Seki, Y. Shiraishi, M. Yamamoto, M. Furuuchi, et al. 2008. Reversal of elastase-induced pulmonary emphysema and promotion of alveolar epithelial cell proliferation by simvastatin in mice. American Journal of Physiology. Lung Cellular and Molecular Physiology 294: L882–90.PubMedCrossRef Takahashi, S., H. Nakamura, M. Seki, Y. Shiraishi, M. Yamamoto, M. Furuuchi, et al. 2008. Reversal of elastase-induced pulmonary emphysema and promotion of alveolar epithelial cell proliferation by simvastatin in mice. American Journal of Physiology. Lung Cellular and Molecular Physiology 294: L882–90.PubMedCrossRef
6.
go back to reference Lapperre, T.S., J.K. Sont, A. van Schadewijk, M.M. Gosman, D.S. Postma, I.M. Bajema, et al. 2007. Smoking cessation and bronchial epithelial remodelling in COPD: a cross-sectional study. Respiratory Research 8: 85.PubMedCrossRefPubMedCentral Lapperre, T.S., J.K. Sont, A. van Schadewijk, M.M. Gosman, D.S. Postma, I.M. Bajema, et al. 2007. Smoking cessation and bronchial epithelial remodelling in COPD: a cross-sectional study. Respiratory Research 8: 85.PubMedCrossRefPubMedCentral
7.
go back to reference Pryor, W.A., and K. Stone. 1993. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Annals of the New York Academy of Sciences 686: 12–27. discussion 27-8.PubMedCrossRef Pryor, W.A., and K. Stone. 1993. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Annals of the New York Academy of Sciences 686: 12–27. discussion 27-8.PubMedCrossRef
8.
go back to reference Spurzem, J.R., and S.I. Rennard. 2005. Pathogenesis of COPD. Seminars in Respiratory and Critical Care Medicine 26: 142–53.PubMedCrossRef Spurzem, J.R., and S.I. Rennard. 2005. Pathogenesis of COPD. Seminars in Respiratory and Critical Care Medicine 26: 142–53.PubMedCrossRef
9.
go back to reference Lanzetti, M., F.S. Bezerra, B. Romana-Souza, A.C. Brando-Lima, V.L. Koatz, L.C. Porto, et al. 2008. Mate tea reduced acute lung inflammation in mice exposed to cigarette smoke. Nutrition 24: 375–81.PubMedCrossRef Lanzetti, M., F.S. Bezerra, B. Romana-Souza, A.C. Brando-Lima, V.L. Koatz, L.C. Porto, et al. 2008. Mate tea reduced acute lung inflammation in mice exposed to cigarette smoke. Nutrition 24: 375–81.PubMedCrossRef
10.
go back to reference Rahman, I., and I.M. Adcock. 2006. Oxidative stress and redox regulation of lung inflammation in COPD. European Respiratory Journal 28: 219–42.PubMedCrossRef Rahman, I., and I.M. Adcock. 2006. Oxidative stress and redox regulation of lung inflammation in COPD. European Respiratory Journal 28: 219–42.PubMedCrossRef
11.
go back to reference Valenca, S.S., W.A. Pimenta, C.R. Rueff-Barroso, T.S. Ferreira, A.C. Resende, R.S. Moura, et al. 2009. Involvement of nitric oxide in acute lung inflammation induced by cigarette smoke in the mouse. Nitric Oxide 20: 175–81.PubMedCrossRef Valenca, S.S., W.A. Pimenta, C.R. Rueff-Barroso, T.S. Ferreira, A.C. Resende, R.S. Moura, et al. 2009. Involvement of nitric oxide in acute lung inflammation induced by cigarette smoke in the mouse. Nitric Oxide 20: 175–81.PubMedCrossRef
12.
go back to reference Helen, A., and P.L. Vijayammal. 1997. Effect of vitamin A supplementation on cigarette smoke-induced lipid peroxidation. Veterinary and Human Toxicology 39: 18–21.PubMed Helen, A., and P.L. Vijayammal. 1997. Effect of vitamin A supplementation on cigarette smoke-induced lipid peroxidation. Veterinary and Human Toxicology 39: 18–21.PubMed
13.
go back to reference Bar-Shai, M., E. Hasnis, Z. Wiener-Megnazi, and A.Z. Reznick. 2006. The role of reactive nitrogen species and cigarette smoke in activation of transcription factor NF-kappaB and implication to inflammatory processes. Journal of Physiology and Pharmacology 57(Suppl 4): 39–44.PubMed Bar-Shai, M., E. Hasnis, Z. Wiener-Megnazi, and A.Z. Reznick. 2006. The role of reactive nitrogen species and cigarette smoke in activation of transcription factor NF-kappaB and implication to inflammatory processes. Journal of Physiology and Pharmacology 57(Suppl 4): 39–44.PubMed
14.
go back to reference Maron, D.J., S. Fazio, and M.F. Linton. 2000. Current perspectives on statins. Circulation 101: 207–13.PubMedCrossRef Maron, D.J., S. Fazio, and M.F. Linton. 2000. Current perspectives on statins. Circulation 101: 207–13.PubMedCrossRef
15.
go back to reference Jacobson, J.R., J.W. Barnard, D.N. Grigoryev, S.F. Ma, R.M. Tuder, and J.G. Garcia. 2005. Simvastatin attenuates vascular leak and inflammation in murine inflammatory lung injury. American Journal of Physiology. Lung Cellular and Molecular Physiology 288: L1026–32.PubMedCrossRef Jacobson, J.R., J.W. Barnard, D.N. Grigoryev, S.F. Ma, R.M. Tuder, and J.G. Garcia. 2005. Simvastatin attenuates vascular leak and inflammation in murine inflammatory lung injury. American Journal of Physiology. Lung Cellular and Molecular Physiology 288: L1026–32.PubMedCrossRef
16.
go back to reference Morikawa, S., W. Takabe, C. Mataki, T. Kanke, T. Itoh, Y. Wada, et al. 2002. The effect of statins on mRNA levels of genes related to inflammation, coagulation, and vascular constriction in HUVEC. Human umbilical vein endothelial cells. Journal of Atherosclerosis and Thrombosis 9: 178–83.PubMedCrossRef Morikawa, S., W. Takabe, C. Mataki, T. Kanke, T. Itoh, Y. Wada, et al. 2002. The effect of statins on mRNA levels of genes related to inflammation, coagulation, and vascular constriction in HUVEC. Human umbilical vein endothelial cells. Journal of Atherosclerosis and Thrombosis 9: 178–83.PubMedCrossRef
17.
go back to reference Sezer, E.D., E.Y. Sozmen, D. Nart, and T. Onat. 2011. Effect of atorvastatin therapy on oxidant-antioxidant status and atherosclerotic plaque formation. Vascular Health and Risk Management 7: 333–43.PubMedCrossRefPubMedCentral Sezer, E.D., E.Y. Sozmen, D. Nart, and T. Onat. 2011. Effect of atorvastatin therapy on oxidant-antioxidant status and atherosclerotic plaque formation. Vascular Health and Risk Management 7: 333–43.PubMedCrossRefPubMedCentral
18.
go back to reference Heeba, G., M.E. Moselhy, M. Hassan, M. Khalifa, R. Gryglewski, and T. Malinski. 2009. Anti-atherogenic effect of statins: role of nitric oxide, peroxynitrite and haem oxygenase-1. British Journal of Pharmacology 156: 1256–66.PubMedCrossRefPubMedCentral Heeba, G., M.E. Moselhy, M. Hassan, M. Khalifa, R. Gryglewski, and T. Malinski. 2009. Anti-atherogenic effect of statins: role of nitric oxide, peroxynitrite and haem oxygenase-1. British Journal of Pharmacology 156: 1256–66.PubMedCrossRefPubMedCentral
19.
go back to reference Moura, R.S., T.S. Ferreira, A.A. Lopes, K.M. Pires, R.T. Nesi, A.C. Resende, et al. 2012. Effects of Euterpe oleracea Mart. (ACAI) extract in acute lung inflammation induced by cigarette smoke in the mouse. Phytomedicine 19: 262–9.PubMedCrossRef Moura, R.S., T.S. Ferreira, A.A. Lopes, K.M. Pires, R.T. Nesi, A.C. Resende, et al. 2012. Effects of Euterpe oleracea Mart. (ACAI) extract in acute lung inflammation induced by cigarette smoke in the mouse. Phytomedicine 19: 262–9.PubMedCrossRef
20.
go back to reference Pires, K.M., S.S. Valenca, A.C. Resende, L.C. Porto, E.F. Queiroz, D.D. Moreira, et al. 2011. Grape skin extract reduced pulmonary oxidative response in mice exposed to cigarette smoke. Medical Science Monitor 17: BR187–195.PubMedCrossRefPubMedCentral Pires, K.M., S.S. Valenca, A.C. Resende, L.C. Porto, E.F. Queiroz, D.D. Moreira, et al. 2011. Grape skin extract reduced pulmonary oxidative response in mice exposed to cigarette smoke. Medical Science Monitor 17: BR187–195.PubMedCrossRefPubMedCentral
21.
go back to reference Silva Bezerra, F., S.S. Valenca, M. Lanzetti, W.A. Pimenta, P. Castro, V.L. Goncalves Koatz, et al. 2006. Alpha-tocopherol and ascorbic acid supplementation reduced acute lung inflammatory response by cigarette smoke in mouse. Nutrition 22: 1192–201.PubMedCrossRef Silva Bezerra, F., S.S. Valenca, M. Lanzetti, W.A. Pimenta, P. Castro, V.L. Goncalves Koatz, et al. 2006. Alpha-tocopherol and ascorbic acid supplementation reduced acute lung inflammatory response by cigarette smoke in mouse. Nutrition 22: 1192–201.PubMedCrossRef
22.
go back to reference Valenca, S.S., F. Silva Bezerra, A.A. Lopes, B. Romana-Souza, M.C. Marinho Cavalcante, A.B. Lima, et al. 2008. Oxidative stress in mouse plasma and lungs induced by cigarette smoke and lipopolysaccharide. Environmental Research 108: 199–204.PubMedCrossRef Valenca, S.S., F. Silva Bezerra, A.A. Lopes, B. Romana-Souza, M.C. Marinho Cavalcante, A.B. Lima, et al. 2008. Oxidative stress in mouse plasma and lungs induced by cigarette smoke and lipopolysaccharide. Environmental Research 108: 199–204.PubMedCrossRef
23.
go back to reference Rakotoniaina, Z., P. Guerard, F. Lirussi, F. Goirand, L. Rochette, M. Dumas, et al. 2006. The protective effect of HMG-CoA reductase inhibitors against monocrotaline-induced pulmonary hypertension in the rat might not be a class effect: comparison of pravastatin and atorvastatin. Naunyn-Schmiedeberg's Archives of Pharmacology 374: 195–206.PubMedCrossRef Rakotoniaina, Z., P. Guerard, F. Lirussi, F. Goirand, L. Rochette, M. Dumas, et al. 2006. The protective effect of HMG-CoA reductase inhibitors against monocrotaline-induced pulmonary hypertension in the rat might not be a class effect: comparison of pravastatin and atorvastatin. Naunyn-Schmiedeberg's Archives of Pharmacology 374: 195–206.PubMedCrossRef
24.
go back to reference Yao, H.W., L.G. Mao, and J.P. Zhu. 2006. Protective effects of pravastatin in murine lipopolysaccharide-induced acute lung injury. Clinical and Experimental Pharmacology and Physiology 33: 793–7.PubMedCrossRef Yao, H.W., L.G. Mao, and J.P. Zhu. 2006. Protective effects of pravastatin in murine lipopolysaccharide-induced acute lung injury. Clinical and Experimental Pharmacology and Physiology 33: 793–7.PubMedCrossRef
25.
go back to reference Zaitone, S.A., and N.M. Abo-Gresha. 2012. Rosuvastatin promotes angiogenesis and reverses isoproterenol-induced acute myocardial infarction in rats: role of iNOS and VEGF. European Journal of Pharmacology 691: 134–42.PubMedCrossRef Zaitone, S.A., and N.M. Abo-Gresha. 2012. Rosuvastatin promotes angiogenesis and reverses isoproterenol-induced acute myocardial infarction in rats: role of iNOS and VEGF. European Journal of Pharmacology 691: 134–42.PubMedCrossRef
26.
go back to reference Muller, H.C., K. Hellwig, S. Rosseau, T. Tschernig, A. Schmiedl, B. Gutbier, et al. 2010. Simvastatin attenuates ventilator-induced lung injury in mice. Critical Care 14: R143.PubMedCrossRefPubMedCentral Muller, H.C., K. Hellwig, S. Rosseau, T. Tschernig, A. Schmiedl, B. Gutbier, et al. 2010. Simvastatin attenuates ventilator-induced lung injury in mice. Critical Care 14: R143.PubMedCrossRefPubMedCentral
27.
go back to reference Suzuki, K., H. Ota, S. Sasagawa, T. Sakatani, and T. Fujikura. 1983. Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Analytical Biochemistry 132: 345–52.PubMedCrossRef Suzuki, K., H. Ota, S. Sasagawa, T. Sakatani, and T. Fujikura. 1983. Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Analytical Biochemistry 132: 345–52.PubMedCrossRef
28.
go back to reference Green, L.C., D.A. Wagner, J. Glogowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15 N]nitrate in biological fluids. Analytical Biochemistry 126: 131–8.PubMedCrossRef Green, L.C., D.A. Wagner, J. Glogowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15 N]nitrate in biological fluids. Analytical Biochemistry 126: 131–8.PubMedCrossRef
29.
go back to reference Kerkweg, U., F. Petrat, H.G. Korth, and H. de Groot. 2007. Disruption of skeletal myocytes initiates superoxide release: contribution of NADPH oxidase. Shock 27: 552–8.PubMedCrossRef Kerkweg, U., F. Petrat, H.G. Korth, and H. de Groot. 2007. Disruption of skeletal myocytes initiates superoxide release: contribution of NADPH oxidase. Shock 27: 552–8.PubMedCrossRef
30.
go back to reference Bannister, J.V., and L. Calabrese. 1987. Assays for superoxide dismutase. Methods of Biochemical Analysis 32: 279–312.PubMedCrossRef Bannister, J.V., and L. Calabrese. 1987. Assays for superoxide dismutase. Methods of Biochemical Analysis 32: 279–312.PubMedCrossRef
31.
32.
go back to reference Rahman, I., A. Kode, and S.K. Biswas. 2006. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature Protocols 1: 3159–65.PubMedCrossRef Rahman, I., A. Kode, and S.K. Biswas. 2006. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature Protocols 1: 3159–65.PubMedCrossRef
33.
go back to reference Kovala-Demertzi, D., D. Hadjipavlou-Litina, A. Primikiri, M. Staninska, C. Kotoglou, and M.A. Demertzis. 2009. Anti-inflammatory, antiproliferative, and radical-scavenging activities of tolfenamic acid and its metal complexes. Chemistry and Biodiversity 6: 948–60.PubMedCrossRef Kovala-Demertzi, D., D. Hadjipavlou-Litina, A. Primikiri, M. Staninska, C. Kotoglou, and M.A. Demertzis. 2009. Anti-inflammatory, antiproliferative, and radical-scavenging activities of tolfenamic acid and its metal complexes. Chemistry and Biodiversity 6: 948–60.PubMedCrossRef
34.
go back to reference Hermes-Lima, M., W.G. Willmore, and K.B. Storey. 1995. Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation. Free Radical Biology and Medicine 19: 271–80.PubMedCrossRef Hermes-Lima, M., W.G. Willmore, and K.B. Storey. 1995. Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation. Free Radical Biology and Medicine 19: 271–80.PubMedCrossRef
35.
go back to reference Kim, D.Y., S.Y. Ryu, J.E. Lim, Y.S. Lee, and J.Y. Ro. 2007. Anti-inflammatory mechanism of simvastatin in mouse allergic asthma model. European Journal of Pharmacology 557: 76–86.PubMedCrossRef Kim, D.Y., S.Y. Ryu, J.E. Lim, Y.S. Lee, and J.Y. Ro. 2007. Anti-inflammatory mechanism of simvastatin in mouse allergic asthma model. European Journal of Pharmacology 557: 76–86.PubMedCrossRef
36.
go back to reference Wang, C.Y., P.Y. Liu, and J.K. Liao. 2008. Pleiotropic effects of statin therapy: molecular mechanisms and clinical results. Trends in Molecular Medicine 14: 37–44.PubMedCrossRefPubMedCentral Wang, C.Y., P.Y. Liu, and J.K. Liao. 2008. Pleiotropic effects of statin therapy: molecular mechanisms and clinical results. Trends in Molecular Medicine 14: 37–44.PubMedCrossRefPubMedCentral
37.
go back to reference Wright, J.L., S. Zhou, O. Preobrazhenska, C. Marshall, D.D. Sin, I. Laher, et al. 2011. Statin reverses smoke-induced pulmonary hypertension and prevents emphysema but not airway remodeling. American Journal of Respiratory and Critical Care Medicine 183: 50–8.PubMedCrossRef Wright, J.L., S. Zhou, O. Preobrazhenska, C. Marshall, D.D. Sin, I. Laher, et al. 2011. Statin reverses smoke-induced pulmonary hypertension and prevents emphysema but not airway remodeling. American Journal of Respiratory and Critical Care Medicine 183: 50–8.PubMedCrossRef
38.
go back to reference Rise, P., S. Ghezzi, C. Manzoni, C. Colombo, and C. Galli. 2009. The in vitro effects of cigarette smoke on fatty acid metabolism are partially counteracted by simvastatin. Prostaglandins, Leukotrienes, and Essential Fatty Acids 80: 71–5.PubMedCrossRef Rise, P., S. Ghezzi, C. Manzoni, C. Colombo, and C. Galli. 2009. The in vitro effects of cigarette smoke on fatty acid metabolism are partially counteracted by simvastatin. Prostaglandins, Leukotrienes, and Essential Fatty Acids 80: 71–5.PubMedCrossRef
39.
go back to reference Rose Jr., C.E., S.S. Sung, and S.M. Fu. 2003. Significant involvement of CCL2 (MCP-1) in inflammatory disorders of the lung. Microcirculation 10: 273–88.PubMedCrossRef Rose Jr., C.E., S.S. Sung, and S.M. Fu. 2003. Significant involvement of CCL2 (MCP-1) in inflammatory disorders of the lung. Microcirculation 10: 273–88.PubMedCrossRef
40.
go back to reference Fildes, J.E., S.M. Shaw, A. Mitsidou, K. Rogacev, C.T. Leonard, S.G. Williams, et al. 2008. HMG-CoA reductase inhibitors deplete circulating classical and non-classical monocytes following human heart transplantation. Transplant Immunology 19: 152–7.PubMedCrossRef Fildes, J.E., S.M. Shaw, A. Mitsidou, K. Rogacev, C.T. Leonard, S.G. Williams, et al. 2008. HMG-CoA reductase inhibitors deplete circulating classical and non-classical monocytes following human heart transplantation. Transplant Immunology 19: 152–7.PubMedCrossRef
41.
go back to reference Teupser, D., M. Bruegel, O. Stein, Y. Stein, and J. Thiery. 2001. HMG-CoA reductase inhibitors reduce adhesion of human monocytes to endothelial cells. Biochemical and Biophysical Research Communications 289: 838–44.PubMedCrossRef Teupser, D., M. Bruegel, O. Stein, Y. Stein, and J. Thiery. 2001. HMG-CoA reductase inhibitors reduce adhesion of human monocytes to endothelial cells. Biochemical and Biophysical Research Communications 289: 838–44.PubMedCrossRef
42.
go back to reference Montecucco, F., F. Burger, G. Pelli, N.K. Poku, C. Berlier, S. Steffens, et al. 2009. Statins inhibit C-reactive protein-induced chemokine secretion, ICAM-1 upregulation and chemotaxis in adherent human monocytes. Rheumatology (Oxford) 48: 233–42.CrossRef Montecucco, F., F. Burger, G. Pelli, N.K. Poku, C. Berlier, S. Steffens, et al. 2009. Statins inhibit C-reactive protein-induced chemokine secretion, ICAM-1 upregulation and chemotaxis in adherent human monocytes. Rheumatology (Oxford) 48: 233–42.CrossRef
44.
go back to reference Togbe, D., S. Schnyder-Candrian, B. Schnyder, E. Doz, N. Noulin, L. Janot, et al. 2007. Toll-like receptor and tumour necrosis factor dependent endotoxin-induced acute lung injury. International Journal of Experimental Pathology 88: 387–91.PubMedCrossRefPubMedCentral Togbe, D., S. Schnyder-Candrian, B. Schnyder, E. Doz, N. Noulin, L. Janot, et al. 2007. Toll-like receptor and tumour necrosis factor dependent endotoxin-induced acute lung injury. International Journal of Experimental Pathology 88: 387–91.PubMedCrossRefPubMedCentral
45.
go back to reference McDonald, P.P., S.R. McColl, P.H. Naccache, and P. Borgeat. 1992. Activation of the human neutrophil 5-lipoxygenase by leukotriene B4. British Journal of Pharmacology 107: 226–32.PubMedCrossRefPubMedCentral McDonald, P.P., S.R. McColl, P.H. Naccache, and P. Borgeat. 1992. Activation of the human neutrophil 5-lipoxygenase by leukotriene B4. British Journal of Pharmacology 107: 226–32.PubMedCrossRefPubMedCentral
47.
go back to reference Lysgaard, C., M.S. Nielsen, J.H. Christensen, S. Lundbye-Christensen, S. Riahi, and E.B. Schmidt. 2012. No effect of high-dose atorvastatin on leukotriene B(4) formation from neutrophils in patients treated with coronary bypass surgery: a randomized placebo-controlled double-blinded trial with a crossover design. Prostaglandins, Leukotrienes, and Essential Fatty Acids 87: 185–8.PubMedCrossRef Lysgaard, C., M.S. Nielsen, J.H. Christensen, S. Lundbye-Christensen, S. Riahi, and E.B. Schmidt. 2012. No effect of high-dose atorvastatin on leukotriene B(4) formation from neutrophils in patients treated with coronary bypass surgery: a randomized placebo-controlled double-blinded trial with a crossover design. Prostaglandins, Leukotrienes, and Essential Fatty Acids 87: 185–8.PubMedCrossRef
48.
go back to reference Chen, L.W., C.M. Hsu, J.S. Wang, H.L. Chen, and J.S. Chen. 2001. Inhibition of inducible nitric oxide synthase (iNOS) prevents lung neutrophil deposition and damage in burned rats. Shock 15: 151–6.PubMedCrossRef Chen, L.W., C.M. Hsu, J.S. Wang, H.L. Chen, and J.S. Chen. 2001. Inhibition of inducible nitric oxide synthase (iNOS) prevents lung neutrophil deposition and damage in burned rats. Shock 15: 151–6.PubMedCrossRef
49.
go back to reference Gabbay, E., E. Haydn Walters, B. Orsida, H. Whitford, C. Ward, T.C. Kotsimbos, et al. 1999. In stable lung transplant recipients, exhaled nitric oxide levels positively correlate with airway neutrophilia and bronchial epithelial iNOS. American Journal of Respiratory and Critical Care Medicine 160: 2093–9.PubMedCrossRef Gabbay, E., E. Haydn Walters, B. Orsida, H. Whitford, C. Ward, T.C. Kotsimbos, et al. 1999. In stable lung transplant recipients, exhaled nitric oxide levels positively correlate with airway neutrophilia and bronchial epithelial iNOS. American Journal of Respiratory and Critical Care Medicine 160: 2093–9.PubMedCrossRef
50.
go back to reference Harkin, D.W., B.B. Rubin, A. Romaschin, and T.F. Lindsay. 2004. Selective inducible nitric oxide synthase (iNOS) inhibition attenuates remote acute lung injury in a model of ruptured abdominal aortic aneurysm. Journal of Surgical Research 120: 230–41.PubMedCrossRef Harkin, D.W., B.B. Rubin, A. Romaschin, and T.F. Lindsay. 2004. Selective inducible nitric oxide synthase (iNOS) inhibition attenuates remote acute lung injury in a model of ruptured abdominal aortic aneurysm. Journal of Surgical Research 120: 230–41.PubMedCrossRef
51.
go back to reference Igawa, S., I. Hayashi, N. Tanaka, H. Hiruma, M. Majima, T. Kawakami, et al. 2004. Nitric oxide generated by iNOS reduces deformability of Lewis lung carcinoma cells. Cancer Science 95: 342–7.PubMedCrossRef Igawa, S., I. Hayashi, N. Tanaka, H. Hiruma, M. Majima, T. Kawakami, et al. 2004. Nitric oxide generated by iNOS reduces deformability of Lewis lung carcinoma cells. Cancer Science 95: 342–7.PubMedCrossRef
52.
go back to reference Wang, L.F., S. Mehta, S. Weicker, J.A. Scott, M. Joseph, H.M. Razavi, et al. 2001. Relative contribution of hemopoietic and pulmonary parenchymal cells to lung inducible nitric oxide synthase (inos) activity in murine endotoxemia. Biochemical and Biophysical Research Communications 283: 694–9.PubMedCrossRef Wang, L.F., S. Mehta, S. Weicker, J.A. Scott, M. Joseph, H.M. Razavi, et al. 2001. Relative contribution of hemopoietic and pulmonary parenchymal cells to lung inducible nitric oxide synthase (inos) activity in murine endotoxemia. Biochemical and Biophysical Research Communications 283: 694–9.PubMedCrossRef
53.
go back to reference Zhao, H., J.K. Ma, M.W. Barger, R.R. Mercer, L. Millecchia, D. Schwegler-Berry, et al. 2009. Reactive oxygen species- and nitric oxide-mediated lung inflammation and mitochondrial dysfunction in wild-type and iNOS-deficient mice exposed to diesel exhaust particles. Journal of Toxicology and Environmental Health A 72: 560–70.CrossRef Zhao, H., J.K. Ma, M.W. Barger, R.R. Mercer, L. Millecchia, D. Schwegler-Berry, et al. 2009. Reactive oxygen species- and nitric oxide-mediated lung inflammation and mitochondrial dysfunction in wild-type and iNOS-deficient mice exposed to diesel exhaust particles. Journal of Toxicology and Environmental Health A 72: 560–70.CrossRef
54.
go back to reference Dodd, O.J., and D.B. Pearse. 2000. Effect of the NADPH oxidase inhibitor apocynin on ischemia-reperfusion lung injury. American Journal of Physiology. Heart and Circulatory Physiology 279: H303–12. Dodd, O.J., and D.B. Pearse. 2000. Effect of the NADPH oxidase inhibitor apocynin on ischemia-reperfusion lung injury. American Journal of Physiology. Heart and Circulatory Physiology 279: H303–12.
55.
go back to reference Segal, B.H., B.A. Davidson, A.D. Hutson, T.A. Russo, B.A. Holm, B. Mullan, et al. 2007. Acid aspiration-induced lung inflammation and injury are exacerbated in NADPH oxidase-deficient mice. American Journal of Physiology. Lung Cellular and Molecular Physiology 292: L760–8.PubMedCrossRef Segal, B.H., B.A. Davidson, A.D. Hutson, T.A. Russo, B.A. Holm, B. Mullan, et al. 2007. Acid aspiration-induced lung inflammation and injury are exacerbated in NADPH oxidase-deficient mice. American Journal of Physiology. Lung Cellular and Molecular Physiology 292: L760–8.PubMedCrossRef
56.
go back to reference Xiang, M., L. Yin, Y. Li, G. Xiao, Y. Vodovotz, T.R. Billiar, et al. 2011. Hemorrhagic shock activates lung endothelial reduced nicotinamide adenine dinucleotide phosphate (NADPH) oxidase via neutrophil NADPH oxidase. American Journal of Respiratory Cell and Molecular Biology 44: 333–40.PubMedCrossRefPubMedCentral Xiang, M., L. Yin, Y. Li, G. Xiao, Y. Vodovotz, T.R. Billiar, et al. 2011. Hemorrhagic shock activates lung endothelial reduced nicotinamide adenine dinucleotide phosphate (NADPH) oxidase via neutrophil NADPH oxidase. American Journal of Respiratory Cell and Molecular Biology 44: 333–40.PubMedCrossRefPubMedCentral
57.
go back to reference Terblanche, M., Y. Almog, R.S. Rosenson, T.S. Smith, and D.G. Hackam. 2007. Statins and sepsis: multiple modifications at multiple levels. Lancet Infectious Diseases 7: 358–68.CrossRef Terblanche, M., Y. Almog, R.S. Rosenson, T.S. Smith, and D.G. Hackam. 2007. Statins and sepsis: multiple modifications at multiple levels. Lancet Infectious Diseases 7: 358–68.CrossRef
58.
go back to reference Chen, W., S. Pendyala, V. Natarajan, J.G. Garcia, and J.R. Jacobson. 2008. Endothelial cell barrier protection by simvastatin: GTPase regulation and NADPH oxidase inhibition. American Journal of Physiology Lung Cellular and Molecular Physiology 295: L575–83.PubMedCrossRefPubMedCentral Chen, W., S. Pendyala, V. Natarajan, J.G. Garcia, and J.R. Jacobson. 2008. Endothelial cell barrier protection by simvastatin: GTPase regulation and NADPH oxidase inhibition. American Journal of Physiology Lung Cellular and Molecular Physiology 295: L575–83.PubMedCrossRefPubMedCentral
59.
go back to reference Bargagli, E., C. Olivieri, D. Bennett, A. Prasse, J. Muller-Quernheim, and P. Rottoli. 2009. Oxidative stress in the pathogenesis of diffuse lung diseases: a review. Respiratory Medicine 103: 1245–56.PubMedCrossRef Bargagli, E., C. Olivieri, D. Bennett, A. Prasse, J. Muller-Quernheim, and P. Rottoli. 2009. Oxidative stress in the pathogenesis of diffuse lung diseases: a review. Respiratory Medicine 103: 1245–56.PubMedCrossRef
60.
go back to reference Bast, A., A.R. Weseler, G.R. Haenen, and G.J. den Hartog. 2010. Oxidative stress and antioxidants in interstitial lung disease. Current Opinion in Pulmonary Medicine 16: 516–20.PubMedCrossRef Bast, A., A.R. Weseler, G.R. Haenen, and G.J. den Hartog. 2010. Oxidative stress and antioxidants in interstitial lung disease. Current Opinion in Pulmonary Medicine 16: 516–20.PubMedCrossRef
61.
go back to reference Ward, P.A. 2010. Oxidative stress: acute and progressive lung injury. Annals of the New York Academy of Sciences 1203: 53–9.PubMedCrossRef Ward, P.A. 2010. Oxidative stress: acute and progressive lung injury. Annals of the New York Academy of Sciences 1203: 53–9.PubMedCrossRef
62.
go back to reference Chow, C.K. 1993. Cigarette smoking and oxidative damage in the lung. Annals of the New York Academy of Sciences 686: 289–98.PubMedCrossRef Chow, C.K. 1993. Cigarette smoking and oxidative damage in the lung. Annals of the New York Academy of Sciences 686: 289–98.PubMedCrossRef
63.
go back to reference Paz-Elizur, T., M. Krupsky, D. Elinger, E. Schechtman, and Z. Livneh. 2005. Repair of the oxidative DNA damage 8-oxoguanine as a biomarker for lung cancer risk. Cancer Biomarkers 1: 201–5.PubMed Paz-Elizur, T., M. Krupsky, D. Elinger, E. Schechtman, and Z. Livneh. 2005. Repair of the oxidative DNA damage 8-oxoguanine as a biomarker for lung cancer risk. Cancer Biomarkers 1: 201–5.PubMed
64.
go back to reference Al-Shabrawey, M., M. Bartoli, A.B. El-Remessy, G. Ma, S. Matragoon, T. Lemtalsi, et al. 2008. Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Investigative Ophthalmology & Visual Science 49: 3231–8.CrossRef Al-Shabrawey, M., M. Bartoli, A.B. El-Remessy, G. Ma, S. Matragoon, T. Lemtalsi, et al. 2008. Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Investigative Ophthalmology & Visual Science 49: 3231–8.CrossRef
65.
go back to reference Antoniades, C., M. Demosthenous, S. Reilly, M. Margaritis, M.H. Zhang, A. Antonopoulos, et al. 2012. Myocardial redox state predicts in-hospital clinical outcome after cardiac surgery effects of short-term pre-operative statin treatment. Journal of the American College of Cardiology 59: 60–70.PubMedCrossRef Antoniades, C., M. Demosthenous, S. Reilly, M. Margaritis, M.H. Zhang, A. Antonopoulos, et al. 2012. Myocardial redox state predicts in-hospital clinical outcome after cardiac surgery effects of short-term pre-operative statin treatment. Journal of the American College of Cardiology 59: 60–70.PubMedCrossRef
66.
go back to reference Bartoli, M., M. Al-Shabrawey, M. Labazi, M.A. Behzadian, M. Istanboli, A.B. El-Remessy, et al. 2009. HMG-CoA reductase inhibitors (statin) prevents retinal neovascularization in a model of oxygen-induced retinopathy. Investigative Ophthalmology & Visual Science 50: 4934–40.CrossRef Bartoli, M., M. Al-Shabrawey, M. Labazi, M.A. Behzadian, M. Istanboli, A.B. El-Remessy, et al. 2009. HMG-CoA reductase inhibitors (statin) prevents retinal neovascularization in a model of oxygen-induced retinopathy. Investigative Ophthalmology & Visual Science 50: 4934–40.CrossRef
67.
go back to reference Key, P.B., J. Hoguet, L.A. Reed, K.W. Chung, and M.H. Fulton. 2008. Effects of the statin antihyperlipidemic agent simvastatin on grass shrimp, Palaemonetes pugio. Environmental Toxicology 23: 153–60.PubMedCrossRef Key, P.B., J. Hoguet, L.A. Reed, K.W. Chung, and M.H. Fulton. 2008. Effects of the statin antihyperlipidemic agent simvastatin on grass shrimp, Palaemonetes pugio. Environmental Toxicology 23: 153–60.PubMedCrossRef
68.
go back to reference Riad, A., S. Bien, D. Westermann, P.M. Becher, K. Loya, U. Landmesser, et al. 2009. Pretreatment with statin attenuates the cardiotoxicity of doxorubicin in mice. Cancer Research 69: 695–9.PubMedCrossRef Riad, A., S. Bien, D. Westermann, P.M. Becher, K. Loya, U. Landmesser, et al. 2009. Pretreatment with statin attenuates the cardiotoxicity of doxorubicin in mice. Cancer Research 69: 695–9.PubMedCrossRef
69.
go back to reference da Silva, P.M. 2011. Are all statins the same? Focus on the efficacy and tolerability of pitavastatin. American Journal of Cardiovascular Drugs 11: 93–107.PubMedCrossRef da Silva, P.M. 2011. Are all statins the same? Focus on the efficacy and tolerability of pitavastatin. American Journal of Cardiovascular Drugs 11: 93–107.PubMedCrossRef
70.
go back to reference Ohshima, K., M. Mogi, H. Nakaoka, F. Jing, J. Iwanami, L.J. Min, et al. 2012. Inhibition of MCP-1/CCR2 signaling pathway is involved in synergistic inhibitory effects of irbesartan with rosuvastatin on vascular remodeling. Journal of the American Society of Hypertension 6: 375–84.PubMedCrossRef Ohshima, K., M. Mogi, H. Nakaoka, F. Jing, J. Iwanami, L.J. Min, et al. 2012. Inhibition of MCP-1/CCR2 signaling pathway is involved in synergistic inhibitory effects of irbesartan with rosuvastatin on vascular remodeling. Journal of the American Society of Hypertension 6: 375–84.PubMedCrossRef
71.
go back to reference Sultana, C., Y. Shen, V. Rattan, and V.K. Kalra. 1996. Lipoxygenase metabolites induced expression of adhesion molecules and transendothelial migration of monocyte-like HL-60 cells is linked to protein kinase C activation. Journal of Cellular Physiology 167: 477–87.PubMedCrossRef Sultana, C., Y. Shen, V. Rattan, and V.K. Kalra. 1996. Lipoxygenase metabolites induced expression of adhesion molecules and transendothelial migration of monocyte-like HL-60 cells is linked to protein kinase C activation. Journal of Cellular Physiology 167: 477–87.PubMedCrossRef
72.
go back to reference Belli, S., O. Basaran, B.H. Ozdemir, S. Turkoglu, G. Karabay, A. Kut, et al. 2011. Protective role of simvastatin on lung damage caused by burn and cotton smoke inhalation in rats. Journal of Surgical Research 167: e283–90.PubMedCrossRef Belli, S., O. Basaran, B.H. Ozdemir, S. Turkoglu, G. Karabay, A. Kut, et al. 2011. Protective role of simvastatin on lung damage caused by burn and cotton smoke inhalation in rats. Journal of Surgical Research 167: e283–90.PubMedCrossRef
73.
go back to reference Al-Otaibi KE, Al Elaiwi AM, Tariq M, Al-Asmari AK. 2012. Simvastatin attenuates contrast-induced nephropathy through modulation of oxidative stress, proinflammatory myeloperoxidase, and nitric oxide. Oxidative Medicine and Cellular Longevity doi:10.1155/2012/831748 Al-Otaibi KE, Al Elaiwi AM, Tariq M, Al-Asmari AK. 2012. Simvastatin attenuates contrast-induced nephropathy through modulation of oxidative stress, proinflammatory myeloperoxidase, and nitric oxide. Oxidative Medicine and Cellular Longevity doi:10.​1155/​2012/​831748
74.
go back to reference Gill, L., J. Santa, D.L. Peter, and J. Keehn. 2012. Lipitor goes generic: business as usual or more big business? Annals of Internal Medicine 156: 892–3. W313.PubMedCrossRef Gill, L., J. Santa, D.L. Peter, and J. Keehn. 2012. Lipitor goes generic: business as usual or more big business? Annals of Internal Medicine 156: 892–3. W313.PubMedCrossRef
75.
go back to reference Bezerra, F.S., S.S. Valenca, K.M. Pires, M. Lanzetti, W.A. Pimenta, A.C. Schmidt, et al. 2011. Long-term exposure to cigarette smoke impairs lung function and increases HMGB-1 expression in mice. Respiratory Physiology & Neurobiology 177: 120–6.CrossRef Bezerra, F.S., S.S. Valenca, K.M. Pires, M. Lanzetti, W.A. Pimenta, A.C. Schmidt, et al. 2011. Long-term exposure to cigarette smoke impairs lung function and increases HMGB-1 expression in mice. Respiratory Physiology & Neurobiology 177: 120–6.CrossRef
76.
go back to reference da Hora, K., S.S. Valenca, and L.C. Porto. 2005. Immunohistochemical study of tumor necrosis factor-alpha, matrix metalloproteinase-12, and tissue inhibitor of metalloproteinase-2 on alveolar macrophages of BALB/c mice exposed to short-term cigarette smoke. Experimental Lung Research 31: 759–70.PubMedCrossRef da Hora, K., S.S. Valenca, and L.C. Porto. 2005. Immunohistochemical study of tumor necrosis factor-alpha, matrix metalloproteinase-12, and tissue inhibitor of metalloproteinase-2 on alveolar macrophages of BALB/c mice exposed to short-term cigarette smoke. Experimental Lung Research 31: 759–70.PubMedCrossRef
77.
go back to reference de Moura, R.S., K.M. Pires, T. Santos Ferreira, A.A. Lopes, R.T. Nesi, A.C. Resende, et al. 2011. Addition of acai (Euterpe oleracea) to cigarettes has a protective effect against emphysema in mice. Food and Chemical Toxicology 49: 855–63.PubMedCrossRef de Moura, R.S., K.M. Pires, T. Santos Ferreira, A.A. Lopes, R.T. Nesi, A.C. Resende, et al. 2011. Addition of acai (Euterpe oleracea) to cigarettes has a protective effect against emphysema in mice. Food and Chemical Toxicology 49: 855–63.PubMedCrossRef
78.
go back to reference Valenca, S.S., K. da Hora, P. Castro, V.G. Moraes, L. Carvalho, and L.C. Porto. 2004. Emphysema and metalloelastase expression in mouse lung induced by cigarette smoke. Toxicologic Pathology 32: 351–6.PubMedCrossRef Valenca, S.S., K. da Hora, P. Castro, V.G. Moraes, L. Carvalho, and L.C. Porto. 2004. Emphysema and metalloelastase expression in mouse lung induced by cigarette smoke. Toxicologic Pathology 32: 351–6.PubMedCrossRef
79.
go back to reference Valenca, S.S., and L.C. Porto. 2008. Immunohistochemical study of lung remodeling in mice exposed to cigarette smoke*. Jornal Brasileiro de Pneumologia 34: 787–95.PubMedCrossRef Valenca, S.S., and L.C. Porto. 2008. Immunohistochemical study of lung remodeling in mice exposed to cigarette smoke*. Jornal Brasileiro de Pneumologia 34: 787–95.PubMedCrossRef
80.
go back to reference Valenca, S.S., C.R. Rueff-Barroso, W.A. Pimenta, A.C. Melo, R.T. Nesi, M.A. Silva, et al. 2011. L-NAME and l-arginine differentially ameliorate cigarette smoke-induced emphysema in mice. Pulmonary Pharmacology & Therapeutics 24: 587–94.CrossRef Valenca, S.S., C.R. Rueff-Barroso, W.A. Pimenta, A.C. Melo, R.T. Nesi, M.A. Silva, et al. 2011. L-NAME and l-arginine differentially ameliorate cigarette smoke-induced emphysema in mice. Pulmonary Pharmacology & Therapeutics 24: 587–94.CrossRef
Metadata
Title
Oxidative Stress and Inflammation Are Differentially Affected by Atorvastatin, Pravastatin, Rosuvastatin, and Simvastatin on Lungs from Mice Exposed to Cigarette Smoke
Authors
Thiago Santos Ferreira
Manuella Lanzetti
Marina Valente Barroso
Carlos Romualdo Rueff-Barroso
Cláudia Farias Benjamim
Lycia de Brito-Gitirana
Luís Cristóvão Porto
Samuel Santos Valença
Publication date
01-10-2014
Publisher
Springer US
Published in
Inflammation / Issue 5/2014
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-014-9860-y

Other articles of this Issue 5/2014

Inflammation 5/2014 Go to the issue