Astaxanthin pretreatment attenuates hepatic ischemia reperfusion-induced apoptosis and autophagy via the ROS/MAPK pathway in mice

Marine Drugs

Volumn 13, Issue 6, 2015, Pages 3368-3387

  Li, Jingjing ^a   Wang, Fan ^a   Xia, Yujing ^a   Dai, Weiqi ^a   Chen, Kan ^a   Li, Sainan ^a   Liu, Tong ^a   Zheng, Yuanyuan ^a   Wang, Jianrong ^b   Lu, Wenxia ^b   Zhou, Yuqing ^c   Yin, Qin ^c   Lu, Jie ^a   Zhou, Yingqun ^a   Guo, Chuanyong ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

Astaxanthin; Hepatic ischemia reperfusion; Oxidative stress; Reactive oxygen species

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; ASTAXANTHIN; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT; AUTACOID; CYTOKINE; XANTHOPHYLL;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; AUTOPHAGY; BLOOD SAMPLING; CONTROLLED STUDY; CONVALESCENCE; DISEASE ASSOCIATION; DOWN REGULATION; DRUG EFFECT; ENZYME INACTIVATION; LIVER INJURY; LIVER ISCHEMIA; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; LIVER DISEASES; METABOLISM; REPERFUSION INJURY; TIME FACTOR;

MUS;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; AUTOPHAGY; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; INFLAMMATION MEDIATORS; LIVER DISEASES; MALE; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; TIME FACTORS; XANTHOPHYLLS;

EID: 84936777756     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13063368     Document Type: Article

References (68)

1. Li, Y.; Yang, Y.; Feng, Y.; Yan, J.; Fan, C.; Jiang, S.; Qu, Y. A review of melatonin in hepatic ischemia/reperfusion injury and clinical liver disease. Ann. Med. 2014, 46, 503-511.
2. Bhogal, R.H.; Sutaria, R.; Afford, S.C. Hepatic liver ischemia/reperfusion injury: Processes in inflammatory networks - A review. Liver Transpl. 2011, 17, 95-96.
3. Jennings, R.B.; Sommers, H.M.; Smyth, G.A.; Flack, H.A.; Linn, H. Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog. Arch. Pathol. 1960, 70, 68-78.
4. Guan, L. Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide. World J. Gastrointest. Surg. 2014, 6, 122-128.
5. Adam, A.N.I. Some mechanisms of the protective effect of ischemic preconditioning on rat liver ischemia-reperfusion injury. Int. J. Gen. Med. 2014, 7, 483-489.
6. Chu, M.J.; Hickey, A.J.; Phillips, A.R.; Bartlett, A.S. The impact of hepatic steatosis on hepatic ischemia-reperfusion injury in experimental studies: A systematic review. Biomed. Res. Int. 2013, 2013, doi:10.1155/2013/192029.
7. Rao, J.; Yue, S.; Fu, Y.; Zhu, J.; Wang, X.; Busuttil, R.W.; Kupiec-Weglinski, J.W.; Lu, L.; Zhai, Y. ATF6 mediates a pro-inflammatory synergy between ER stress and TLR activation in the pathogenesis of liver ischemia-reperfusion injury. Am. J. Transplant. 2014, 14, 1552-1561.
8. Park, S.W.; Kang, J.W.; Lee, S.M. Role of Kupffer cells in ischemic injury in alcoholic fatty liver. J. Surg. Res. 2015, 194, 91-100.
9. Nace, G.W.; Huang, H.; Klune, J.R.; Eid, R.E.; Rosborough, B.R.; Korff, S.; Li, S.; Shapiro, R.A.; Stolz, D.B.; Sodhi, C.P.; et al. Cellular-specific role of toll-like receptor 4 in hepatic ischemia-reperfusion injury in mice. Hepatology 2013, 58, 374-387.
10. Sanderson, T.H.; Reynolds, C.A.; Kumar, R.; Przyklenk, K.; Huttemann, M. Molecular mechanisms of ischemia-reperfusion injury in brain: Pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Mol. Neurobiol. 2013, 47, 9-23.
11. Sun, Y.; Pu, L.Y.; Lu, L.; Wang, X.H.; Zhang, F.; Rao, J.H. N-acetylcysteine attenuates reactive-oxygen-species-mediated endoplasmic reticulum stress during liver ischemia-reperfusion injury. World J. Gastroenterol. 2014, 20, 15289-15298.
12. Brass, C.A.; Roberts, T.G. Hepatic free radical production after cold storage: Kupffer cell-dependent and -independent mechanisms in rats. Gastroenterology 1995, 108, 1167-1175.
13. Schwabe, R.F.; Brenner, D.A. Mechanisms of Liver Injury. I. TNF-alpha-induced liver injury: Role of IKK, JNK, and ROS pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G583-G589.
14. Nakagawa, H.; Maeda, S. Molecular mechanisms of liver injury and hepatocarcinogenesis: Focusing on the role of stress-activated MAPK. Patholog. Res. Int. 2012, 2012, doi:10.1155/2012/172894.
15. Tiberio, L.; Tiberio, G.A.; Bardella, L.; Cervi, E.; Cerea, K.; Dreano, M.; Garotta, G.; Fra, A.; Montani, N.; Ferrari-Bravo, A.; et al. Mechanisms of interleukin-6 protection against ischemia-reperfusion injury in rat liver. Cytokine 2006, 34, 131-142.
16. Shen, M.; Lu, J.; Dai, W.; Wang, F.; Xu, L.; Chen, K.; He, L.; Cheng, P.; Zhang, Y.; Wang, C.; et al. Ethyl Pyruvate Ameliorates Hepatic Ischemia-Reperfusion Injury by Inhibiting Intrinsic Pathway of Apoptosis and Autophagy. Mediators Inflamm. 2013, 2013, 1-12.
17. Kohli, V.; Selzner, M.; Madden, J.F.; Bentley, R.C.; Clavien, P.A. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation 1999, 67, 1099-1105.
18. Imahashi, K.; Schneider, M.D.; Steenbergen, C.; Murphy, E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ. Res. 2004, 95, 734-741.
19. Selzner, M.; Rudiger, H.A.; Selzner, N.; Thomas, D.W.; Sindram, D.; Clavien, P.A. Transgenic mice overexpressing human Bcl-2 are resistant to hepatic ischemia and reperfusion. J. Hepatol. 2002, 36, 218-225.
20. Nikoletopoulou, V.; Markaki, M.; Palikaras, K.; Tavernarakis, N. Crosstalk between apoptosis, necrosis and autophagy. Biochim. Biophys. Acta 2013, 1833, 3448-3459.
21. Sybers, H.D.; Ingwall, J.; DeLuca, M. Autophagy in cardiac myocytes. Recent Adv. Stud. Cardiac. Struct. Metab. 1976, 12, 453-463.
22. Decker, R.S.; Wildenthal, K. Lysosomal alterations in hypoxic and reoxygenated hearts. I. Ultrastructural and cytochemical changes. Am. J. Pathol. 1980, 98, 425-444.
23. Liang, X.H.; Kleeman, L.K.; Jiang, H.H.; Gordon, G.; Goldman, J.E.; Berry, G.; Herman, B.; Levine, B. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 1998, 72, 8586-8596.
24. Naguib, Y.M. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 2000, 48, 1150-1154.
25. Shen, M.; Chen, K.; Lu, J.; Cheng, P.; Xu, L.; Dai, W.; Wang, F.; He, L.; Zhang, Y.; Chengfen, W.; et al. Protective Effect of Astaxanthin on Liver Fibrosis through Modulation of TGF-1 Expression and Autophagy. Mediators Inflamm. 2014, 2014, 1-14.
26. Ambati, R.; Moi, P.; Ravi, S.; Aswathanarayana, R. Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications - A review. Mar. Drugs 2014, 12, 128-152.
27. Li, J.; Xia, Y.; Liu, T.; Wang, J.; Dai, W.; Wang, F.; Zheng, Y.; Chen, K.; Li, S.; Abudumijiti, H.; et al. Protective effects of astaxanthin on ConA-induced autoimmune hepatitis by the JNK/p-JNK pathway-mediated inhibition of autophagy and apoptosis. PLoS ONE 2015, 10, e120440.
28. Kamath, B.S.; Srikanta, B.M.; Dharmesh, S.M.; Sarada, R.; Ravishankar, G.A. Ulcer preventive and antioxidative properties of astaxanthin from Haematococcus pluvialis. Eur. J. Pharmacol. 2008, 590, 387-395.
29. Yang, Y.; Kim, B.; Park, Y.K.; Koo, S.I.; Lee, J.Y. Astaxanthin prevents TGFβ1-induced pro-fibrogenic gene expression by inhibiting Smad3 activation in hepatic stellate cells. Biochim. Biophys. Acta 2015, 1850, 178-185.
30. Song, X.; Wang, B.; Lin, S.; Jing, L.; Mao, C.; Xu, P.; Lv, C.; Liu, W.; Zuo, J. Astaxanthin inhibits apoptosis in alveolar epithelial cells type II in vivo and in vitro through the ROS-dependent mitochondrial signalling pathway. J. Cell. Mol. Med. 2014, 18, 2198-2212.
31. 2-production. PLoS ONE 2014, 9, e88359.
32. Terazawa, S.; Nakajima, H.; Shingo, M.; Niwano, T.; Imokawa, G. Astaxanthin attenuates the UVB-induced secretion of prostaglandin E2 and interleukin-8 in human keratinocytes by interrupting MSK1 phosphorylation in a ROS depletion-independent manner. Exp. Dermatol. 2012, 21, 11-17.
33. Guerra, B.A.; Otton, R. Impact of the carotenoid astaxanthin on phagocytic capacity and ROS/RNS production of human neutrophils treated with free fatty acids and high glucose. Int. Immunopharmacol. 2011, 11, 2220-2226.
34. Marin, D.P.; Bolin, A.P.; Macedo, R.C.; Sampaio, S.C.; Otton, R. ROS production in neutrophils from alloxan-induced diabetic rats treated in vivo with astaxanthin. Int. Immunopharmacol. 2011, 11, 103-109.
35. 2-Induced neurotoxicity in vitro and on focal cerebral ischemia in vivo. Brain Res. 2010, 1360, 40-48.
36. Shen, H.; Kuo, C.C.; Chou, J.; Delvolve, A.; Jackson, S.N.; Post, J.; Woods, A.S.; Hoffer, B.J.; Wang, Y.; Harvey, B.K. Astaxanthin reduces ischemic brain injury in adult rats. FASEB J. 2009, 23, 1958-1968.
37. Lauver, D.A.; Lockwood, S.F.; Lucchesi, B.R. Disodium Disuccinate Astaxanthin (Cardax) attenuates complement activation and reduces myocardial injury following ischemia/reperfusion. J. Pharmacol. Exp. Ther. 2005, 314, 686-692.
38. Curek, G.D.; Cort, A.; Yucel, G.; Demir, N.; Ozturk, S.; Elpek, G.O.; Savas, B.; Aslan, M. Effect of astaxanthin on hepatocellular injury following ischemia/reperfusion. Toxicology 2010, 267, 147-153.
39. Sun, P.P.; Yuan, F.; Xu, J.; Sai, K.; Chen, J.; Guan, S. Cryptotanshinone ameliorates hepatic normothermic ischemia and reperfusion injury in rats by anti-mitochondrial apoptosis. Biol. Pharm. Bull. 2014, 37, 1758-1765.
40. Zhou, G.; Dada, L.A.; Wu, M.; Kelly, A.; Trejo, H.; Zhou, Q.; Varga, J.; Sznajder, J.I. Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297, L1120-L1130.
41. Boury, N.M.; Czuprynski, C.J. Listeria monocytogenes infection increases neutrophil adhesion and damage to a murine hepatocyte cell line in vitro. Immunol. Lett. 1995, 46, 111-116.
42. Gujral, J.S.; Bucci, T.J.; Farhood, A.; Jaeschke, H. Mechanism of cell death during warm hepatic ischemia-reperfusion in rats: Apoptosis or necrosis? Hepatology 2001, 33, 397-405.
43. Hamada, T.; Tsuchihashi, S.; Avanesyan, A.; Duarte, S.; Moore, C.; Busuttil, R.W.; Coito, A.J. Cyclooxygenase-2 deficiency enhances Th2 immune responses and impairs neutrophil recruitment in hepatic ischemia/reperfusion injury. J. Immunol. 2008, 180, 1843-1853.
44. Wang, J.; Kan, Q.; Li, J.; Zhang, X.; Qi, Y. Effect of neferine on liver ischemia-reperfusion injury in rats. Transplant. Proc. 2011, 43, 2536-2539.
45. Hussein, G.; Sankawa, U.; Goto, H.; Matsumoto, K.; Watanabe, H. Astaxanthin, a carotenoid with potential in human health and nutrition. J. Nat. Prod. 2006, 69, 443-449.
46. Goto, S.; Kogure, K.; Abe, K.; Kimata, Y.; Kitahama, K.; Yamashita, E.; Terada, H. Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid astaxanthin. Biochim. Biophys. Acta 2001, 1512, 251-258.
47. Zarubin, T.; Han, J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005, 15, 11-18.
48. Sturgill, T.W.; Ray, L.B. Muscle proteins related to microtubule associated protein-2 are substrates for an insulin-stimulatable kinase. Biochem. Biophys. Res. Commun. 1986, 134, 565-571.
49. Dufresne, S.D.; Bjorbaek, C.; El-Haschimi, K.; Zhao, Y.; Aschenbach, W.G.; Moller, D.E.; Goodyear, L.J. Altered extracellular signal-regulated kinase signaling and glycogen metabolism in skeletal muscle from p90 ribosomal S6 kinase 2 knockout mice. Mol. Cell. Biol. 2001, 21, 81-87.
50. Theodosiou, A.; Ashworth, A. MAP kinase phosphatases. Genome Biol. 2002, 3, doi:10.1186/gb-2002-3-7-reviews3009.
51. Kim, J. Astaxanthin Inhibits H2O2-Mediated Apoptotic Cell Death in Mouse Neural Progenitor Cells via Modulation of P38 and MEK Signaling Pathways. J. Microbiol. Biotech. 2009, 19, 1355-1363
52. Sanchez-Fidalgo, S.; Villegas, I.; Rosillo, M.A.; Aparicio-Soto, M.; de la Lastra, C.A. Dietary squalene supplementation improves DSS-induced acute colitis by downregulating p38 MAPK and NFkB signaling pathways. Mol. Nutr. Food Res. 2015, 59, 284-292.
53. Nick, J.A.; Young, S.K.; Arndt, P.G.; Lieber, J.G.; Suratt, B.T.; Poch, K.R.; Avdi, N.J.; Malcolm, K.C.; Taube, C.; Henson, P.M.; et al. Selective suppression of neutrophil accumulation in ongoing pulmonary inflammation by systemic inhibition of p38 mitogen-activated protein kinase. J. Immunol. 2002, 169, 5260-5269.
54. Zhang, D.; Wang, L.; Yan, L.; Miao, X.; Gong, C.; Xiao, M.; Ni, R.; Tang, Q. Vacuolar protein sorting 4B regulates apoptosis of intestinal epithelial cells via p38 MAPK in Crohn's disease. Exp. Mol. Pathol. 2014, 98, 55-64.
55. Brown, A.E.; Palsgaard, J.; Borup, R.; Avery, P.; Gunn, D.A.; De Meyts, P.; Yeaman, S.J.; Walker, M. p38 MAPK activation upregulates proinflammatory pathways in skeletal muscle cells from insulin-resistant type 2 diabetic patients. Am. J. Physiol. Endocrinol. Metab. 2015, 308, E63-E70.
56. Koike, N.; Takeyoshi, I.; Ohki, S.; Tokumine, M.; Matsumoto, K.; Morishita, Y. Effects of adding P38 mitogen-activated protein-kinase inhibitor to celsior solution in canine heart transplantation from non-heart-beating donors. Transplantation 2004, 77, 286-292.
57. Hashimoto, N.; Takeyoshi, I.; Tsutsumi, H.; Sunose, Y.; Tokumine, M.; Totsuka, O.; Ohwada, S.; Matsumoto, K.; Morishita, Y. Effects of a bradykinin B(2) receptor antagonist on ischemia-reperfusion injury in a canine lung transplantation model. J. Heart Lung Transplant. 2004, 23, 606-613.
58. Wang, H.; Sun, X.; Xu, Y.; Zhao, H.; Zhu, Q.; Zhu, C. Astaxanthin upregulates heme oxygenase-1 expression through ERK1/2 pathway and its protective effect against beta-amyloid-induced cytotoxicity in SH-SY5Y cells. Brain Res. 2010, 1360, 159-167.
59. Cheng, P.; Wang, F.; Chen, K.; Shen, M.; Dai, W.; Xu, L.; Zhang, Y.; Wang, C.; Li, J.; Yang, J.; et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm. 2014, 2014, doi:10.1155/2014/935251.
60. Wang, C.; Chen, K.; Xia, Y.; Dai, W.; Wang, F.; Shen, M.; Cheng, P.; Wang, J.; Lu, J.; Zhang, Y.; et al. N-Acetylcysteine Attenuates Ischemia-Reperfusion-Induced Apoptosis and Autophagy in Mouse Liver via Regulation of the ROS/JNK/Bcl-2 Pathway. PLoS ONE 2014, 9, e108855.
61. Park, G.B.; Choi, Y.; Kim, Y.S.; Lee, H.K.; Kim, D.; Hur, D.Y. ROS-mediated JNK/p38-MAPK activation regulates Bax translocation in Sorafenib-induced apoptosis of EBV-transformed B cells. Int. J. Oncol. 2014, 44, 977-985.
62. Park, G.B.; Kim, Y.S.; Lee, H.K.; Song, H.; Kim, S.; Cho, D.H.; Hur, D.Y. Reactive oxygen species and p38 MAPK regulate Bax translocation and calcium redistribution in salubrinal-induced apoptosis of EBV-transformed B cells. Cancer Lett. 2011, 313, 235-248.
63. Malik, S.; Suchal, K.; Gamad, N.; Dinda, A.K.; Arya, D.S.; Bhatia, J. Telmisartan ameliorates cisplatin-induced nephrotoxicity by inhibiting MAPK mediated inflammation and apoptosis. Eur. J. Pharmacol. 2014, 748, 54-60.
64. Ishiki, M.; Nishida, Y.; Ishibashi, H.; Wada, T.; Fujisaka, S.; Takikawa, A.; Urakaze, M.; Sasaoka, T.; Usui, I.; Tobe, K. Impact of divergent effects of astaxanthin on insulin signaling in L6 cells. Endocrinology 2013, 154, 2600-2612.
65. Camera, E.; Mastrofrancesco, A.; Fabbri, C.; Daubrawa, F.; Picardo, M.; Sies, H.; Stahl, W. Astaxanthin, canthaxanthin and beta-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp. Dermatol. 2009, 18, 222-231.
66. Gordy, C.; He, Y.W. The crosstalk between autophagy and apoptosis: Where does this lead? Protein Cell 2012, 3, 17-27.
67. Lin, X.; Li, S.; Zhao, Y.; Ma, X.; Zhang, K.; He, X.; Wang, Z. Interaction domains of p62: A bridge between p62 and selective autophagy. DNA Cell Biol. 2013, 32, 220-227.
68. Abe, Y.; Hines, I.N.; Zibari, G.; Pavlick, K.; Gray, L.; Kitagawa, Y.; Grisham, M.B. Mouse model of liver ischemia and reperfusion injury: Method for studying reactive oxygen and nitrogen metabolites in vivo. Free Radic. Biol. Med. 2009, 46, 1-7.