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Astaxanthin suppresses cigarette smoke and lipopolysaccharide-induced airway inflammation through induction of heme oxygenase-1
Corresponding Author(s) : Liu Zhiguang
Cellular and Molecular Biology,
Vol. 65 No. 1: Issue 1
Abstract
The present study was carried out to evolve an effective treatment strategy for chronic obstructive pulmonary disease (COPD). Astaxanthin (AS) is abundantly present in red pigments of crustaceans, and has also been proven to have considerable biological activities. The anti-inflammatory effect of AS was evaluated in lipopolysaccharide (LPS)-exposed RAW264.7 macrophages. It was found that AS markedly inhibited elevation of NO and pro-inflammatory mediators. Moreover, it downregulated iNOS in LPS-stimulated RAW264.7 cells, suppressed the release of pro-inflammatory cytokines, and decreased ROS levels in mice exposed to cigarette smoke (CS) and LPS. These results imply that AS has therapeutic and prophylactic potential in the airway inflammatory response associated with COPD.
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- O'Donnell DE, Aaron S, Bourbeau J, Hernandez P, Marciniuk DD, Balter M, et al. Canadian Thoracic Society recommendations for management of chronic obstructive pulmonary disease - 2007 update. Can Respir J 2016; 10: 11.
- Russell R, Norcliffe J, Bafadhel M. Chronic obstructive pulmonary disease: management of chronic disease. Med 2016; 44: 310-313.
- Pouwels SD, Hesse L, Faiz A, Lubbers J, Bodha PK, Ten Hacken NH, et al. Susceptibility for cigarette smoke-induced DAMP release and DAMP-induced inflammation in COPD. Am J Physiol Lung Cell Mol Physiol 2016; 311: 881-892.
- Gerrit J, Katrin K, Jürgen O, Reda A, Schnelle-Kreis J, Zimmermann R, et al. The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clin Sci 2014; 126: 207-221.
- Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, Butler K, et al. Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 2004; 31: 633-642.
- Peralta JG, Barnard ML, Turrens JF. Characteristics of neutrophil influx in rat lungs following fecal peritonitis. Inflammation 1993; 17: 263-271.
- Cavarra E, Martorana PA, De SM, Bartalesi B, Cortese S, Gambelli F, et al. Neutrophil influx into the lungs of beige mice is followed by elastolytic damage and emphysema. Am J Respir Cell Mol Biol 1999; 20: 264-269.
- Gordon S, Martinez FO. Alternative Activation of Macrophages: Mechanism and Functions. Immunity 2010; 32: 593-604.
- Bai X, Chen Y, Chen W, Lei H, Gao F, Qin Y, et al. The effect of black coral extraction on acute lung inflammation induced by cigarette smoke in mice. Exp Lung Res 2011; 37: 627-632.
- Miravitlles M, Soler-Cataluña JJ, Calle M, Soriano JB. Treatment of COPD by clinical phenotypes: putting old evidence into clinical practice. Eur Respir J 2013; 41: 1252-1256.
- Bernardo I, Bozinovski S, Vlahos R. Targeting oxidant-dependent mechanisms for the treatment of COPD and its comorbidities. Pharmacol Ther 2015; 155: 60-79.
- Guerin M, Huntley ME, Olaizola M. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 2003; 21: 210-216.
- Pashkow FJ, Watumull DG, Campbell CL. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol 2008; 101: 58-68.
- Hussein G, Goto H, Oda S, Sankawa U, Matsumoto K, Watanabe H. Antihypertensive potential and mechanism of action of astaxanthin: III. Antioxidant and histopathological effects in spontaneously hypertensive rats. Biol Pharm Bull 2006; 29: 684-688.
- Lee JW, Park JW, Shin NR, Park SY, Kwon OK, Park HA, et al. Picrasma quassiodes (D. Don) Benn. attenuates lipopolysaccharide (LPS)-induced acute lung injury. Int J Mol Med 2016; 38: 834.
- Shin IS, Park JW, Shin NR, Jeon CM, Kwon OK, Lee MY, et al. Melatonin inhibits MUC5AC production via suppression of MAPK signaling in human airway epithelial cells. J Pineal Res 2014; 56: 398-407.
- Ham YM, Yoon WJ, Park SY, Song G, Jung YH, Jeon YJ, et al. Quercitrin protects against oxidative stress-induced injury in lung fibroblast cells via up-regulation of Bcl-xL. J Funct Foods 2012; 4: 253-262.
- O'Donnell R, Breen D, Wilson S, Djukanovic R. Inflammatory cells in the airways in COPD. Thorax 2006; 61: 448.
- Hoenderdos K, Condliffe A. The neutrophil in chronic obstructive pulmonary disease. American Am J Respir Cell Mol Biol 2013; 48: 531-539.
- Yadav UCS, Ramana KV, Srivastava SK. Aldose reductase inhibition suppresses airway inflammation. Chem Biol Interact 2011; 191: 339-345.
- Stämpfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 2009; 9: 377-384.
- Onizawa S, Aoshiba K, Kajita M, Miyamoto Y, Nagai A. Platinum nanoparticle antioxidants inhibit pulmonary inflammation in mice exposed to cigarette smoke. Pulm Pharmacol Ther 2009; 22: 340-349.
- Hsu CL, Fang SC, Huang HW, Yen GC. Anti-inflammatory effects of triterpenes and steroid compounds isolated from the stem bark of Hiptage benghalensis. J Funct Foods 2015; 12: 420-427.
- Zhang H, Wu MY, Guo DJ, Chanet SW, Lau CC, Chan CO, et al. Gui-ling-gao (turtle jelly), a traditional Chinese functional food, exerts anti-inflammatory effects by inhibiting iNOS and pro-inflammatory cytokine expressions in splenocytes isolated from BALB/c mice. J Funct Foods 2013; 5: 625-632.
- Wu X, Song M, Rakariyatham K, Zheng J, Guo S, Tang Z, et al. Anti-inflammatory effects of 4'-demethylnobiletin, a major metabolite of nobiletin. J Funct Foods 2015; 19: 278-287.
- Li RJ, Gao CY, Guo C, Zhou MM, Luo J, Kong LY. The Anti-inflammatory Activities of Two Major Withanolides from Physalis minima Via Acting on NF-κB, STAT3, and HO-1 in LPS-Stimulated RAW264.7 Cells. Inflammation 2016; 40: 1-13.
- Lee JW, Park HA, Kwon OK, Jang YG, Kim JY, Choi BK, et al. Asiatic acid inhibits pulmonary inflammation induced by cigarette smoke. Int Immunopharmacol 2016; 39: 208-217.
References
O'Donnell DE, Aaron S, Bourbeau J, Hernandez P, Marciniuk DD, Balter M, et al. Canadian Thoracic Society recommendations for management of chronic obstructive pulmonary disease - 2007 update. Can Respir J 2016; 10: 11.
Russell R, Norcliffe J, Bafadhel M. Chronic obstructive pulmonary disease: management of chronic disease. Med 2016; 44: 310-313.
Pouwels SD, Hesse L, Faiz A, Lubbers J, Bodha PK, Ten Hacken NH, et al. Susceptibility for cigarette smoke-induced DAMP release and DAMP-induced inflammation in COPD. Am J Physiol Lung Cell Mol Physiol 2016; 311: 881-892.
Gerrit J, Katrin K, Jürgen O, Reda A, Schnelle-Kreis J, Zimmermann R, et al. The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clin Sci 2014; 126: 207-221.
Marwick JA, Kirkham PA, Stevenson CS, Danahay H, Giddings J, Butler K, et al. Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 2004; 31: 633-642.
Peralta JG, Barnard ML, Turrens JF. Characteristics of neutrophil influx in rat lungs following fecal peritonitis. Inflammation 1993; 17: 263-271.
Cavarra E, Martorana PA, De SM, Bartalesi B, Cortese S, Gambelli F, et al. Neutrophil influx into the lungs of beige mice is followed by elastolytic damage and emphysema. Am J Respir Cell Mol Biol 1999; 20: 264-269.
Gordon S, Martinez FO. Alternative Activation of Macrophages: Mechanism and Functions. Immunity 2010; 32: 593-604.
Bai X, Chen Y, Chen W, Lei H, Gao F, Qin Y, et al. The effect of black coral extraction on acute lung inflammation induced by cigarette smoke in mice. Exp Lung Res 2011; 37: 627-632.
Miravitlles M, Soler-Cataluña JJ, Calle M, Soriano JB. Treatment of COPD by clinical phenotypes: putting old evidence into clinical practice. Eur Respir J 2013; 41: 1252-1256.
Bernardo I, Bozinovski S, Vlahos R. Targeting oxidant-dependent mechanisms for the treatment of COPD and its comorbidities. Pharmacol Ther 2015; 155: 60-79.
Guerin M, Huntley ME, Olaizola M. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 2003; 21: 210-216.
Pashkow FJ, Watumull DG, Campbell CL. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol 2008; 101: 58-68.
Hussein G, Goto H, Oda S, Sankawa U, Matsumoto K, Watanabe H. Antihypertensive potential and mechanism of action of astaxanthin: III. Antioxidant and histopathological effects in spontaneously hypertensive rats. Biol Pharm Bull 2006; 29: 684-688.
Lee JW, Park JW, Shin NR, Park SY, Kwon OK, Park HA, et al. Picrasma quassiodes (D. Don) Benn. attenuates lipopolysaccharide (LPS)-induced acute lung injury. Int J Mol Med 2016; 38: 834.
Shin IS, Park JW, Shin NR, Jeon CM, Kwon OK, Lee MY, et al. Melatonin inhibits MUC5AC production via suppression of MAPK signaling in human airway epithelial cells. J Pineal Res 2014; 56: 398-407.
Ham YM, Yoon WJ, Park SY, Song G, Jung YH, Jeon YJ, et al. Quercitrin protects against oxidative stress-induced injury in lung fibroblast cells via up-regulation of Bcl-xL. J Funct Foods 2012; 4: 253-262.
O'Donnell R, Breen D, Wilson S, Djukanovic R. Inflammatory cells in the airways in COPD. Thorax 2006; 61: 448.
Hoenderdos K, Condliffe A. The neutrophil in chronic obstructive pulmonary disease. American Am J Respir Cell Mol Biol 2013; 48: 531-539.
Yadav UCS, Ramana KV, Srivastava SK. Aldose reductase inhibition suppresses airway inflammation. Chem Biol Interact 2011; 191: 339-345.
Stämpfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 2009; 9: 377-384.
Onizawa S, Aoshiba K, Kajita M, Miyamoto Y, Nagai A. Platinum nanoparticle antioxidants inhibit pulmonary inflammation in mice exposed to cigarette smoke. Pulm Pharmacol Ther 2009; 22: 340-349.
Hsu CL, Fang SC, Huang HW, Yen GC. Anti-inflammatory effects of triterpenes and steroid compounds isolated from the stem bark of Hiptage benghalensis. J Funct Foods 2015; 12: 420-427.
Zhang H, Wu MY, Guo DJ, Chanet SW, Lau CC, Chan CO, et al. Gui-ling-gao (turtle jelly), a traditional Chinese functional food, exerts anti-inflammatory effects by inhibiting iNOS and pro-inflammatory cytokine expressions in splenocytes isolated from BALB/c mice. J Funct Foods 2013; 5: 625-632.
Wu X, Song M, Rakariyatham K, Zheng J, Guo S, Tang Z, et al. Anti-inflammatory effects of 4'-demethylnobiletin, a major metabolite of nobiletin. J Funct Foods 2015; 19: 278-287.
Li RJ, Gao CY, Guo C, Zhou MM, Luo J, Kong LY. The Anti-inflammatory Activities of Two Major Withanolides from Physalis minima Via Acting on NF-κB, STAT3, and HO-1 in LPS-Stimulated RAW264.7 Cells. Inflammation 2016; 40: 1-13.
Lee JW, Park HA, Kwon OK, Jang YG, Kim JY, Choi BK, et al. Asiatic acid inhibits pulmonary inflammation induced by cigarette smoke. Int Immunopharmacol 2016; 39: 208-217.