Astaxanthin prevents TGFβ1-induced pro-fibrogenic gene expression by inhibiting Smad3 activation in hepatic stellate cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 1, 2015, Pages 178-185

  Yang, Yue ^a   Kim, Bohkyung ^a   Park, Young Ki ^a   Koo, Sung I ^a   Lee, Ji Young ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Astaxanthin; Hepatic stellate cell; Liver fibrosis; Non alcoholic steatohepatitis; Smad3; Transforming growth factor 1

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ASTAXANTHIN; COLLAGEN TYPE 1; MESSENGER RNA; SMAD3 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; ACTIN; FIBRINOLYTIC AGENT; XANTHOPHYLL;

ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL IMMORTALIZATION; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; FIBROGENESIS; FIBROGENIC GENE; GENE; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STELLATE CELL; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CELL NUCLEUS; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SMOOTH MUSCLE;

ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CELLS, CULTURED; COLLAGEN TYPE I; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBRINOLYTIC AGENTS; FIBROSIS; GENE EXPRESSION REGULATION; HEPATIC STELLATE CELLS; HUMANS; MICE, INBRED C57BL; MUSCLE, SMOOTH; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; XANTHOPHYLLS;

EID: 84910029457     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.10.014     Document Type: Article

References (62)

1. M. Lazo, J.M. Clark, The epidemiology of nonalcoholic fatty liver disease: a global perspective, Semin. Liver Dis. 28 (2008) 339-350.
2. J.P. Ong, Z.M. Younossi, Epidemiology and natural history of NAFLD and NASH, Clin. Liver Dis. 11 (2007) 1-16.
3. Y.-S. Lim, W.R. Kim, The global impact of hepatic fibrosis and end-stage liver disease, Clin. Liver Dis. 12 (2008) 733-746.
4. J.K. Reddy, M.S. Rao, Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation, Am. J. Physiol. Gastrointest. Liver Physiol. 290 (2006) G852-G858.
5. J. Ludwig, T.R. Viggiano, D.B. McGill, B.J. Oh, Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease, Mayo Clin. Proc. 55 (1980) 434-438.
6. E.M. Brunt, Pathology of nonalcoholic steatohepatitis, Hepatol. Res. 33 (2005) 68-71.
7. E.E. Powell, W.G. Cooksley, R. Hanson, J. Searle, J.W. Halliday, L.W. Powell, The natural history of nonalcoholic steatohepatitis: a follow-up study of forty-two patients for up to 21 years, Hepatology 11 (1990) 74-80.
8. A.J. Sanyal, C. Campbell-Sargent, F. Mirshahi, W.B. Rizzo, M.J. Contos, R.K. Sterling, V.A. Luketic, M.L. Shiffman, J.N. Clore, Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities, Gastroenterology 120 (2001) 1183-1192.
9. M. Ekstedt, L.E. Franzén, U.L. Mathiesen, L. Thorelius, M. Holmqvist, G. Bodemar, S. Kechagias, Long-term follow-up of patientswith NAFLD and elevated liver enzymes, Hepatology 44 (2006) 865-873.
10. G. Vernon, A. Baranova, Z.M. Younossi, Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults, Aliment. Pharmacol. Ther. 34 (2011) 274-285.
11. V. Hernandez-Gea, S.L. Friedman, Pathogenesis of liver fibrosis, Annu. Rev. Pathol. 6 (2011) 425-456.
12. S.L. Friedman, Stellate cell activation in alcoholic fibrosis - an overview, Alcohol. Clin. Exp. Res. 23 (1999) 904-910.
13. M. Parola, G. Robino, Oxidative stress-relatedmolecules and liver fibrosis, J. Hepatol. 35 (2001) 297-306.
14. E. Williams, J. Iredale, Hepatic regeneration and TGF-β: growing to a prosperous perfection, Gut 46 (2000) 593-594.
15. S.L. Friedman, Mechanisms of disease: mechanisms of hepatic fibrosis and therapeutic implications, Nat. Clin. Pract. Gastroenterol. Hepatol. 1 (2004) 98-105.
16. J. Gauldie, P. Bonniaud, P. Sime, K. Ask, M. Kolb, TGF-beta, Smad3 and the process of progressive fibrosis, Biochem. Soc. Trans. 35 (2007) 661-664.
17. I. Higuera-Ciapara, L. Felix-Valenzuela, F.M. Goycoolea, Astaxanthin: a review of its chemistry and applications, Crit. Rev. Food Sci. Nutr. 46 (2006) 185-196.
18. G. Hussein, U. Sankawa, H. Goto, K. Matsumoto, H. Watanabe, Astaxanthin, a carotenoid with potential in human health and nutrition, J. Nat. Prod. 69 (2005) 443-449.
19. F.J. Pashkow, D.G. Watumull, C.L. Campbell, Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease, Am. J. Cardiol. 101 (2008) 58D-68D.
20. H.D. Choi, J.H. Kim, M.J. Chang, Y. Kyu-Youn, W.G. Shin, Effects of astaxanthin on oxidative stress in overweight and obese adults, Phytother. Res. 25 (2011) 1813-1818.
21. K. Ohgami, K. Shiratori, S. Kotake, T. Nishida, N. Mizuki, K. Yazawa, S. Ohno, Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo, Invest. Ophthalmol. Vis. Sci. 44 (2003) 2694-2701.
22. G. Hussein, M. Nakamura, Q. Zhao, T. Iguchi, H. Goto, U. Sankawa, H. Watanabe, Antihypertensive and neuroprotective effects of astaxanthin in experimental animals, Biol. Pharm. Bull. 28 (2005) 47-52.
23. K. Uchiyama, Y. Naito, G. Hasegawa, N. Nakamura, J. Takahashi, T. Yoshikawa, Astaxanthin protects beta-cells against glucose toxicity in diabetic db/db mice, Redox Rep. 7 (2002) 290-293.
24. W. Li, A. Hellsten, L.S. Jacobsson, H.M. Blomqvist, A.G. Olsson, X.M. Yuan, Alpha-tocopherol and astaxanthin decrease macrophage infiltration, apoptosis and vulnerability in atheroma of hyperlipidaemic rabbits, J. Mol. Cell. Cardiol. 37 (2004) 969-978.
25. Y. Yang, J.M. Seo, A. Nguyen, T.X. Pham, H.J. Park, Y. Park, B. Kim, R.S. Bruno, J. Lee, Astaxanthin-rich extract from the green alga Haematococcus pluvialis lowers plasma lipid concentrations and enhances antioxidant defense in apolipoprotein E knockout mice, J. Nutr. 141 (2011) 1611-1617.
26. R. Weiskirchen, A.M. Gressner, Isolation and Culture of Hepatic Stellate Cells, vol. 1172005. 99-113.
27. Y. Kamada, K. Mori, H. Matsumoto, S. Kiso, Y. Yoshida, S. Shinzaki, N. Hiramatsu, M. Ishii, K. Moriwaki, N. Kawada, T. Takehara, E. Miyoshi, N-Acetylglucosaminyltransferase V regulates TGF-β response in hepatic stellate cells and the progression of steatohepatitis, Glycobiology 22 (2012) 778-787.
28. J.M. Graham, Fractionation of hepatic nonparenchymal cells, ScientificWorldJournal 2 (2002) 1347-1350.
29. Y. Yang, Y. Park, D.A. Cassada, D.D. Snow, D.G. Rogers, J. Lee, In vitro and in vivo safety assessment of edible blue-green algae, Nostoc commune var. sphaeroides Kützing and Spirulina plantensis, Food Chem. Toxicol. 49 (2011) 1560-1564.
30. S.G. Lee, B. Kim, Y. Yang, T.X. Pham, Y.K. Park, J. Manatou, S.I. Koo, O.K. Chun, J.Y. Lee, Berry anthocyanins suppress the expression and secretion of proinflammatory mediators in macrophages by inhibiting nuclear translocation of NF-kappaB independent of NRF2-mediated mechanism, J. Nutr. Biochem. 25 (4) (2013) 404-411.
31. Y.K. Park, H.E. Rasmussen, S.J. Ehlers, K.R. Blobaum, F. Lu, V.L. Schlegal, T.P. Carr, J.Y. Lee, Repression of proinflammatory gene expression by lipid extract of Nostoc commune var sphaeroides Kutzing, a blue-green alga, via inhibition of nuclear factor-kappaB in RAW 264.7 macrophages, Nutr. Res. 28 (2008) 83-91.
32. H.E. Rasmussen, K.R. Blobaum, Y.K. Park, S.J. Ehlers, F. Lu, J.Y. Lee, Lipid extract of Nostoc commune var. sphaeroides Kutzing, a blue-green alga, inhibits the activation of sterol regulatory element binding proteins in HepG2 cells, J. Nutr. 138 (2008) 476-481.
33. C.S. Ku, T.X. Pham, Y. Park, B. Kim, M.S. Shin, I. Kang, J. Lee, Edible blue-green algae reduce the production of pro-inflammatory cytokines by inhibiting NF-κB pathway in macrophages and splenocytes, Biochim. Biophys. Acta Gen. Subj. 1830 (2013) 2981-2988.
34. P. Angulo, Nonalcoholic fatty liver disease, N. Engl. J. Med. 346 (2002) 1221-1231.
35. V. Proell, I. Carmona-Cuenca, M. Murillo, H. Huber, I. Fabregat, W. Mikulits, TGF-beta dependent regulation of oxygen radicals during transdifferentiation of activated hepatic stellate cells to myofibroblastoid cells, Comp. Hepatol. 6 (2007) 1.
36. M. Guerin, M.E. Huntley, M. Olaizola, Haematococcus astaxanthin: applications for human health and nutrition, Trends Biotechnol. 21 (2003) 210-216.
37. X. Liu, H. Hu, J.Q. Yin, Therapeutic strategies against TGF-beta signaling pathway in hepatic fibrosis, Liver Int. 26 (2006) 8-22.
38. Y. Inagaki, R. Higashiyama, K. Higashi, Novel anti-fibrotic modalities for liver fibrosis: molecular targeting and regenerative medicine in fibrosis therapy, J. Gastroenterol. Hepatol. 27 (Suppl. 2) (2012) 85-88.
39. R.P. Nagarajan, J. Zhang, W. Li, Y. Chen, Regulation of Smad7 promoter by direct association with Smad3 and Smad4, J. Biol. Chem. 274 (1999) 33412-33418.
40. L. Xu, A.Y. Hui, E. Albanis, M.J. Arthur, S.M. O'Byrne, W.S. Blaner, P. Mukherjee, S.L. Friedman, F.J. Eng, Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis, Gut 54 (2005) 142-151.
41. M. Lazo, R. Hernaez, M.S. Eberhardt, S. Bonekamp, I. Kamel, E. Guallar, A. Koteish, F.L. Brancati, J.M. Clark, Prevalence of nonalcoholic fatty liver disease in the United States: the third national health and nutrition examination survey, 1988-1994, Am. J. Epidemol. 178 (2013) 38-45.
42. S. Bellentani, F. Scaglioni, M. Marino, G. Bedogni, Epidemiology of non-alcoholic fatty liver disease, Dig. Dis. 28 (2010) 155-161.
43. S. Weber, O.A. Gressner, R. Hall, F. Grünhage, F. Lammert, Genetic determinants in hepatic fibrosis: from experimental models to fibrogenic gene signatures in humans, Clin. Liver Dis. 12 (2008) 747-757.
44. A. Galli, G. Svegliati-Baroni, E. Ceni, S. Milani, F. Ridolfi, R. Salzano, M. Tarocchi, C. Grappone, G. Pellegrini, A. Benedetti, C. Surrenti, A. Casini, Oxidative stress stimulates proliferation and invasiveness of hepatic stellate cells via a MMP2-mediated mechanism, Hepatology 41 (2005) 1074-1084.
45. D.P. Jones, Radical-free biology of oxidative stress, Am. J. Physiol. Cell Physiol. 295 (2008) C849-C868.
46. E. Rodrigues, L.R. Mariutti, A.Z. Mercadante, Scavenging capacity of marine carotenoids against reactive oxygen and nitrogen species in a membrane-mimicking system, Mar. Drugs 10 (2012) 1784-1798.
47. P. Sancho, J. Mainez, E. Crosas-Molist, C. Roncero, C.M. Fernández-Rodriguez, F. Pinedo, H. Huber, R. Eferl, W. Mikulits, I. Fabregat, NADPH oxidase NOX4 mediates stellate cell activation and hepatocyte cell death during liver fibrosis development, PLoS ONE 7 (2012) e45285.
48. B. Hu, Z. Wu, S.H. Phan, Smad3 mediates transforming growth factor-beta-induced alpha-smooth muscle actin expression, Am. J. Respir. Cell Mol. Biol. 29 (2003) 397-404.
49. S. Kim, Y. Lee, J.E. Seo, K.H. Cho, J.H. Chung, Caveolin-1 increases basal and TGF-beta1-induced expression of type I procollagen through PI-3 kinase/Akt/mTOR pathway in human dermal fibroblasts, Cell. Signal. 20 (2008) 1313-1319.
50. D.A. Mann, D.E. Smart, Transcriptional regulation of hepatic stellate cell activation, Gut 50 (2002) 891-896.
51. V. Ellenrieder, TGFbeta regulated gene expression by Smads and Sp1/KLF-like transcription factors in cancer, Anticancer Res. 28 (2008) 1531-1539.
52. Y. Kim, V. Ratziu, S.-G. Choi, A. Lalazar, G. Theiss, Q. Dang, S.-J. Kim, S.L. Friedman, Transcriptional activation of transforming growth factor β1 and its receptors by the Kruppel-like Factor Zf9/Core promoter-binding protein and Sp1: potential mechanisms for autocrine fibrogenesis in response to injury, J. Biol. Chem. 273 (1998) 33750-33758.
53. A. Biernacka, M. Dobaczewski, N.G. Frangogiannis, TGF-beta signaling in fibrosis, Growth Factors 29 (2011) 196-202.
54. A. LEASK, D.J. ABRAHAM, TGF-β signaling and the fibrotic response, FASEB J. 18 (2004) 816-827.
55. K. Matsuzaki, Smad phosphoisoform signaling specificity: the right place at the right time, Carcinogenesis 32 (2011) 1578-1588.
56. M. Centrella, C. Ji, S. Casinghino, T. McCarthy, Rapid flux in transforming growth factor-beta receptors on bone cells, J. Biol. Chem. 271 (1996) 18616-18622.
57. K. Takahashi, M. Watanabe, T. Takimoto, Y. Akiba, Uptake and distribution of astaxanthin in several tissues and plasma lipoproteins in male broiler chickens fed a yeast (Phaffia rhodozyma ) with a high concentration of astaxanthin, Br. Poult. Sci. 45 (2004) 133-138.
58. H.P. McNulty, J. Byun, S.F. Lockwood, R.F. Jacob, R.P. Mason, Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis, Biochim. Biophys. Acta 1768 (2007) 167-174.
59. F. Huang, Y.G. Chen, Regulation of TGF-beta receptor activity, Cell Biosci. 2 (2012) 9.
60. J. Herrmann, A.M. Gressner, R. Weiskirchen, Immortal hepatic stellate cell lines: useful tools to study hepatic stellate cell biology and function? J. Cell. Mol. Med. 11 (2007) 704-722.
61. E. Guimaraes, J. Best, L. Dolle, M. Najimi, E. Sokal, L. van Grunsven, Mitochondrial uncouplers inhibit hepatic stellate cell activation, BMC Gastroenterol. 12 (2012) 68.
62. H. Senoo, K. Yoshikawa, M. Morii, M. Miura, K. Imai, Y. Mezaki, Hepatic stellate cell (vitamin A-storing cell) and its relative - past, present and future, Cell Biol. Int. 34 (2010) 1247-1272.