Improved hepatoprotective effect of liposome-encapsulated astaxanthin in lipopolysaccharide-induced acute hepatotoxicity

International Journal of Molecular Sciences

Volumn 17, Issue 7, 2016, Pages

  Chiu, Chun Hung ^a   Chang, Chun Chao ^b,c   Lin, Shiang Ting ^a   Chyau, Charng Cherng ^a   Peng, Robert Y ^a,d  

^a HUNGKUANG UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Antioxidant enzymes; Astaxanthin; Hepatotoxicity; Inflammation; Liposome encapsulation

Indexed keywords

ACETYLCYSTEINE; ASTAXANTHIN; CATALASE; COLLAGEN; CREATININE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LIPOSOME; MALONALDEHYDE; NITRITE; SMOOTH MUSCLE ACTIN; STAT3 PROTEIN; SUPEROXIDE DISMUTASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; ANTIOXIDANT; FIBRINOLYTIC AGENT; GLUTATHIONE; NANOCAPSULE; PROTECTIVE AGENT; XANTHOPHYLL;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BODY WEIGHT; CELL SURVIVAL; CONTROLLED STUDY; DRUG BIOAVAILABILITY; ENCAPSULATION; ENZYME ACTIVITY; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOPATHOLOGY; KIDNEY MASS; LIVER PROTECTION; LIVER TOXICITY; LIVER WEIGHT; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; UREA NITROGEN BLOOD LEVEL; ANIMAL; CHEMICAL AND DRUG INDUCED LIVER INJURY; CHEMISTRY; DRUG EFFECTS; METABOLISM; ORGAN SIZE; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; BODY WEIGHT; CHEMICAL AND DRUG INDUCED LIVER INJURY; FIBRINOLYTIC AGENTS; GLUTATHIONE; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LIPOSOMES; MALE; MALONDIALDEHYDE; NANOCAPSULES; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; ORGAN SIZE; OXIDATIVE STRESS; PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; XANTHOPHYLLS;

EID: 84978516929     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17071128     Document Type: Article

References (41)

1. Ambati, R. R.; Phang, S. M.; Ravi, S.; Aswathanarayana, R. G. Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications-A review. Mar. Drugs 2014, 12, 128-152. [CrossRef] [PubMed].
2. Dose, J.; Matsugo, S.; Yokokawa, H.; Koshida, Y.; Okazaki, S.; Seidel, U.; Eggersdorfer, M.; Rimbach, G.; Esatbeyoglu, T. Free radical scavenging and cellular antioxidant properties of astaxanthin. Int. J. Mol. Sci. 2016, 17, 103. [CrossRef] [PubMed].
3. Naguib, Y. M. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 2000, 48, 1150-1154. [CrossRef] [PubMed].
4. Rao, A. R.; Sarada, R.; Ravishankar, G. A. Stabilization of astaxanthine in edible oils and its use as an antioxidant. J. Sci. Food Agric. 2007, 87, 957-965. [CrossRef].
5. Yuan, J. P.; Peng, J.; Yin, K.; Wang, J. H. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol. Nutr. Food Res. 2011, 55, 150-165. [CrossRef] [PubMed].
6. Ikeda, Y.; Tsuji, S.; Satoh, A.; Ishikura, M.; Shirasawa, T.; Shimizu, T. Protective effects of astaxanthine on 6-hydroxydopamine-induced apoptosis in human neuroblastoma SH-SY5Y cells. J. Neurochem. 2008, 107, 1730-1740. [CrossRef] [PubMed].
7. Kistler, A.; Liechti, H.; Pichard, L.; Wolz, E.; Oesterhelt, G.; Hayes, A.; Maurel, P. Metabolism and CYP-inducer properties of astaxanthine in man and primary human hepatocytes. Arch. Toxicol. 2002, 75, 665-675. [CrossRef] [PubMed].
8. Jyonouchi, H.; Sun, S.; Iijima, K.; Gross, M. D. Antitumor activity of astaxanthin and its mode of action. Nutr. Cancer 2000, 36, 59-65. [CrossRef] [PubMed].
9. Franceschelli, S.; Pesce, M.; Ferrone, A.; de Lutiis, M. A.; Patruno, A.; Grilli, A.; Felaco, M.; Speranza, L. Astaxanthin treatment confers protection against oxidative stress in U937 cells stimulated with lipopolysaccharide reducing O2+ production. PLoS ONE 2014, 9, e88359. [CrossRef] [PubMed].
10. 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-β1 expression and autophagy. Mediat. Inflamm. 2014, 2014, 954502. [CrossRef] [PubMed].
11. 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, e0120440. [CrossRef] [PubMed].
12. Elpek, G. Ö. Cellular and molecular mechanisms in the pathogenesis of liver fibrosis: An update. World J. Gastroenterol. 2014, 20, 7260-7276. [CrossRef] [PubMed].
13. Yang, Y.; Pham, T. X.; Wegner, C. J.; Kim, B.; Ku, C. S.; Park, Y. K.; Lee, J. Y. Astaxanthin lowers plasma TAG concentrations and increases hepatic antioxidant gene expression in diet-induced obesity mice. Br. J. Nutr. 2014, 112, 1797-1804. [CrossRef] [PubMed].
14. Amar, E. C.; Kiron, V.; Satoh, S.; Watanabe, T. Enhancement of innate immunity in rainbow trout (Oncorhynchus mykiss Walbaum) associated with dietary intake of carotenoids from natural products. Fish Shellfish Immunol. 2004, 16, 527-537. [CrossRef] [PubMed].
15. Peng, C. H.; Chang, C. H.; Peng, R. Y.; Chyau, C. C. Improved membrane transport of astaxanthine by liposomal encapsulation. Eur. J. Pharm. Biopharm. 2010, 75, 154-161. [CrossRef] [PubMed].
16. Akira, S.; Taga, T.; Kishimoto, T. Interleukin-6 in biology and medicine. Adv. Immunol. 1993, 54, 1-78. [PubMed].
17. Gao, B. Hepatoprotective and anti-inflammatory cytokines in alcoholic liver disease. J. Gastroenterol. Hepatol. 2012, 27, 89-93. [CrossRef] [PubMed].
18. Damas, P.; Ledoux, D.; Nys, M.; Vrindts, Y.; de Groote, D.; Franchimont, P.; Lamy, M. Cytokine serum levels during severe sepsis in human: IL-6 as a marker of severity. Ann. Surg. 1992, 15, 362-365. [CrossRef].
19. Osawa, Y.; Hoshi, M.; Yasuda, I.; Saibara, T.; Moriwaki, H.; Kozawa, O. Tumor necrosis factor-β promotes cholestasis-induced liver fibrosis in the mouse through tissue inhibitor of metalloproteinase-1 production in hepatic stellate cells. PLoS ONE 2013, 8, e65251. [CrossRef] [PubMed].
20. Chastre, A.; Be'langer, M.; Beauchesne, E.; Nguyen, B. N.; Desjardins, P.; Butterworth, R. F. Inflammatory cascades driven by tumor necrosis factor-β play a major role in the progression of acute liver failure and its neurological complications. PLoS ONE 2012, 7, e49670. [CrossRef] [PubMed].
21. Braithwaite, M. C.; Tyagi, C.; Tomar, L. K.; Kumar, P.; Choonara, Y. E.; Pillay, V. Nutraceutical-based therapeutics and formulation strategies augmenting their efficiency to complement modern medicine: An overview. J. Funct. Foods 2014, 6, 82-99. [CrossRef].
22. Lorenz, R. T.; Cysewski, G. R. Commercial potential for Haematococcus microalgae as a natural source of astaxanthine. Trends Biotechnol. 2000, 18, 160-167. [CrossRef].
23. Green, S. J.; Scheller, L. F.; Marletta, M. A.; Seguin, M. C.; Klotz, F. W.; Slayter, M.; Nelson, B. J.; Nacy, C. A. Nitric oxide: Cytokine-regulation of nitric oxide in host resistance to intracellular pathogens. Immunol. Lett. 1994, 43, 87-94. [CrossRef].
24. Mungrue, I. N.; Husain, M.; Stewart, D. J. The role of NOS in heart failure: Lessons from murine genetic models. Heart Fail. Rev. 2002, 7, 407-422. [CrossRef] [PubMed].
25. Brown, G. C. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim. Biophys. Acta 2001, 1504, 46-57. [CrossRef].
26. Mateo, J.; Garcia-Lecea, M.; Cadenas, S.; Hernandez, C.; Moncada, S. Regulation of hypoxia-inducible factor-1+ by nitric oxide through mitochondria-dependent and-independent pathways. Biochem. J. 2003, 376, 537-544. [CrossRef] [PubMed].
27. Moncada, S.; Higgs, E. A. The discovery of nitric oxide and its role in vascular biology. Br. J. Pharmacol. 2006, 147 (Suppl. 1), S193-S201. [CrossRef] [PubMed].
28. Xu, W.; Charles, I. G.; Moncada, S. Nitric oxide: Orchestrating hypoxia regulation through mitochondrial respiration and the endoplasmic reticulum stress response. Cell Res. 2005, 15, 63-65. [CrossRef] [PubMed].
29. Zelickson, B. R.; Benavides, G. A.; Johnson, M. S.; Chacko, B. K.; Venkatraman, A.; Landar, A.; Betancourt, A. M.; Bailey, S. M.; Darley-Usmar, V. M. Nitric oxide and hypoxia exacerbate alcohol-induced mitochondrial dysfunction in hepatocytes. Biochim. Biophys. Acta 2011, 1807, 1573-1582. [CrossRef] [PubMed].
30. Wei, T.; Chen, C.; Hou, J.; Zhao, B.; Xin, W.; Mori, A. The antioxidant EPC-K1 attenuates NO-induced mitochondrial dysfunction, lipid peroxidation and apoptosis in cerebellar granule cells. Toxicology 1999, 134, 117-126. [CrossRef].
31. Stewart, V. C.; Heales, S. J. Nitric oxide-induced mitochondrial dysfunction: Implications for neurodegeneration. Free Radic. Biol. Med. 2003, 34, 287-303. [CrossRef].
32. Wei, Y. H.; Lu, C. Y.; Lee, H. C.; Pang, C. Y.; Ma, Y. S. Oxidative damage and mutation to mitochondrial DNA and age dependent decline of mitochondrial respiratory function. Ann. N. Y. Acad. Sci. 1998, 854, 155-170. [CrossRef] [PubMed].
33. Matés, J. M.; Pérez-Gómez, C.; Núñez de Castro, I. Antioxidant enzymes and human diseases. Clin. Biochem. 1999, 32, 595-603. [CrossRef].
34. Breimer, L. H. Molecular mechanisms of oxygen radical carcinogenesis and mutagenesis: The role of DNA base damage. Mol. Carcinog. 1990, 3, 188-197. [CrossRef] [PubMed].
35. Pajović, S. B.; Saičić, Z. S.; Pejić, S.; Kasapović, J.; Stojiljković, V.; Kanazir, D. T. Antioxidative biomarkers and cancerogenesis. Jugosl. Med. Biohem. 2006, 25, 397-402. [CrossRef].
36. Miranda, K. M.; Espey, M. G.; Wink, D. A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001, 1, 62-71. [CrossRef] [PubMed].
37. Buege, J. A.; Aust, S. D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52, 302-310. [PubMed].
38. Bradford, M. M. A rapid and sensitive method for the quantitation of microquantities of protein utilizing the principle of protein-dye binding. Anal. Chem. 1976, 72, 248-254.
39. Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47, 469-474. [CrossRef] [PubMed].
40. Aebi, H. Catalase in vitro. Methods Enzymol. 1984, 105, 121-126. [PubMed].
41. Lawrence, R. A.; Burk, R. F. Glutathione peroxidase activity in selenium deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71, 952-958. [CrossRef].