Protective effects of astaxanthin on conainduced autoimmune hepatitis by the JNK/p-JNK pathway-mediated inhibition of autophagy and apoptosis

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Li, Jingjing ^a   Xia, Yujing ^a   Liu, Tong ^a   Wang, Junshan ^a   Dai, Weiqi ^a   Wang, Fan ^a   Zheng, Yuanyuan ^a   Chen, Kan ^a   Li, Sainan ^a   Abudumijiti, Huerxidan ^a   Zhou, Zheng ^b   Wang, Jianrong ^b   Lu, Wenxia ^b   Zhu, Rong ^b   Yang, Jing ^a   Zhang, Huawei ^c   Yin, Qin ^c   Wang, Chengfen ^a   Zhou, Yuqing ^c   Lu, Jie ^a   Zhou, Yingqun ^a   Guo, Chuanyong ^a   more..

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ASTAXANTHIN; CONCANAVALIN A; CYTOKINE; LIVER ENZYME; MOLECULAR MARKER; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; XANTHOPHYLL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOIMMUNE HEPATITIS; AUTOPHAGY; DOWN REGULATION; ENZYME BLOOD LEVEL; HISTOPATHOLOGY; IN VITRO STUDY; LIVER CELL; LIVER INJURY; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; DRUG ADMINISTRATION; DRUG EFFECTS; ENZYMOLOGY; HEPATITIS, AUTOIMMUNE; IMMUNOLOGY; LIVER; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY;

MUS;

ADMINISTRATION, ORAL; ANIMALS; APOPTOSIS; AUTOPHAGY; CELLS, CULTURED; CONCANAVALIN A; CYTOKINES; DRUG ADMINISTRATION SCHEDULE; HEPATITIS, AUTOIMMUNE; HEPATOCYTES; LIVER; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; XANTHOPHYLLS;

EID: 84924362586     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120440     Document Type: Article

References (59)

1. Manns MP, Czaja AJ, Gorham JD, Krawitt EL, Mieli-Vergani G, Vergani D, et al. Diagnosis and management of autoimmune hepatitis. Hepatology. 2010; 51: 2193-2213. doi: 10.1002/hep.23584 PMID: 20513004
2. Czaja AJ. Diagnosis, pathogenesis, and treatment of autoimmune hepatitis after liver transplantation. Dig Dis Sci. 2012; 57: 2248-2266. doi: 10.1007/s10620-012-2179-3 PMID: 22562533
3. Liberal R, Longhi MS, Mieli-Vergani G, Vergani D. Pathogenesis of autoimmune hepatitis. Best Pract Res Clin Gastroenterol. 2011; 25: 653-664. doi: 10.1016/j.bpg.2011.09.009 PMID: 22117632
4. Strassburg CP, Manns MP. Therapy of autoimmune hepatitis. Best Pract Res Clin Gastroenterol. 2011; 25: 673-687. doi: 10.1016/j.bpg.2011.08.003 PMID: 22117634
5. Zhang NN, Huang NY, Zhou XK, Luo XL, Liu CY, Zhang Y, et al. Protective effects of il-4 on bacillus calmette-guerin and lipopolysaccharide induced immunological liver injury in mice. Inflamm Res. 2012; 61: 17-26. doi: 10.1007/s00011-011-0383-9 PMID: 21947361
6. Cho H, Park J, Choi H, Kwak JH, Lee D, Lee SK, et al. Protective mechanisms of acacetin against dgalactosamine and lipopolysaccharide-induced fulminant hepatic failure in mice. J Nat Prod. 2014: 1069052077.
7. Tiegs G, Hentschel J, Wendel A. A t cell-dependent experimental liver injury in mice inducible by concanavalin a. J Clin Invest. 1992; 90: 196-203. PMID: 1634608
8. Tiegs G. Cellular and cytokine-mediated mechanisms of inflammation and its modulation in immunemediated liver injury. Z Gastroenterol. 2007; 45: 63-70. PMID: 17236122
9. Mizuhara H, Uno M, Seki N, Yamashita M, Yamaoka M, Ogawa T, et al. Critical involvement of interferon gamma in the pathogenesis of t-cell activation-associated hepatitis and regulatory mechanisms of interleukin-6 for the manifestations of hepatitis. Hepatology. 1996; 23: 1608-1615. PMID: 8675184
10. Kusters S, Gantner F, Kunstle G, Tiegs G. Interferon gamma plays a critical role in t cell-dependent liver injury in mice initiated by concanavalin a. Gastroenterology. 1996; 111: 462-471. PMID: 8690213
11. Bozza M, Bliss JL, Maylor R, Erickson J, Donnelly L, Bouchard P, et al. Interleukin-11 reduces t-cell-dependent experimental liver injury in mice. Hepatology. 1999; 30: 1441-1447. PMID: 10573523
12. Tu CT, Han B, Liu HC, Zhang SC. Curcumin protects mice against concanavalin a-induced hepatitis by inhibiting intrahepatic intercellular adhesion molecule-1 (icam-1) and cxcl10 expression. Mol Cell Biochem. 2011; 358: 53-60. doi: 10.1007/s11010-011-0920-4 PMID: 21695461
13. Park A, Baichwal VR. Systematic mutational analysis of the death domain of the tumor necrosis factor receptor 1-associated protein tradd. J Biol Chem. 1996; 271: 9858-9862. PMID: 8621670
14. Wang HX, Liu M, Weng SY, Li JJ, Xie C, He HL, et al. Immune mechanisms of concanavalin a model of autoimmune hepatitis. World J Gastroenterol. 2012; 18: 119-125. doi: 10.3748/wjg.v18.i2.119 PMID: 22253517
15. Ksontini R, Colagiovanni DB, Josephs MD, Edwards CR, Tannahill CL, Solorzano CC, et al. Disparate roles for tnf-alpha and fas ligand in concanavalin a-induced hepatitis. J Immunol. 1998; 160: 4082-4089. PMID: 9558119
16. Wolf D, Hallmann R, Sass G, Sixt M, Kusters S, Fregien B, et al. Tnf-alpha-induced expression of adhesion molecules in the liver is under the control of tnfr1-relevance for concanavalin a-induced hepatitis. J Immunol. 2001; 166: 1300-1307. PMID: 11145713
17. Tiegs G, Wolter M, Wendel A. Tumor necrosis factor is a terminal mediator in galactosamine/endotox-in-induced hepatitis in mice. Biochem Pharmacol. 1989; 38: 627-631. PMID: 2465008
18. Gutowska I, Baranowska-Bosiacka I, Siwiec E, Szczuko M, Kolasa A, Kondarewicz A, et al. Lead enhances fluoride influence on apoptosis processes in liver cell line hepg2. Toxicol Ind Health. 2013:
19. Choi YS, Lee J, Lee HW, Chang DY, Sung PS, Jung MK, et al. Liver injury in acute hepatitis a is associated with decreased frequency of regulatory t cells caused by fas-mediated apoptosis. Gut. 2014:
20. Kou W, Li YD, Liu K, Sun SB, Dong YM, Wu ZH. Radix angelicae sinensis and radix hedysari enhance radiosensitivity of 12c6+ radiation in human liver cancer cells by modulating apoptosis protein. Saudi Med J. 2014; 35: 945-952. PMID: 25228175
21. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972; 26: 239-257. PMID: 4561027
22. Mizuhara H, O'Neill E, Seki N, Ogawa T, Kusunoki C, Otsuka K, et al. T cell activation-associated hepatic injury: mediation by tumor necrosis factors and protection by interleukin 6. J Exp Med. 1994; 179: 1529-1537. PMID: 8163936
23. Schwabe RF, Brenner DA. 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. PMID: 16537970
24. Ashford TP, Porter KR. Cytoplasmic components in hepatic cell lysosomes. J Cell Biol. 1962; 12: 198-202. PMID: 13862833
25. Cheng P, Wang F, Chen K, Shen M, Dai W, Xu L, et al. Hydrogen sulfide ameliorates ischemia/reperfu-sion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm. 2014; 2014: 935251. doi: 10.1155/2014/935251 PMID: 24966472
26. Shen M, Lu J, Dai W, Wang F, Xu L, Chen K, et al. Ethyl pyruvate ameliorates hepatic ischemiareperfusion injury by inhibiting intrinsic pathway of apoptosis and autophagy. Mediators Inflamm. 2013; 2013: 461536. doi: 10.1155/2013/461536 PMID: 24453420
27. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta. 2013; 1833: 3448-3459. doi: 10.1016/j.bbamcr.2013.06.001 PMID: 23770045
28. Ambati RR, Phang SM, Ravi S, Aswathanarayana RG. Astaxanthin: sources, extraction, stability, biological activities and its commercial applications-a review. Mar Drugs. 2014; 12: 128-152. doi: 10. 3390/md12010128 PMID: 24402174
29. Shen M, Chen K, Lu J, Cheng P, Xu L, Dai W, et al. Protective effect of astaxanthin on liver fibrosis through modulation of tgf-beta1 expression and autophagy. Mediators Inflamm. 2014; 2014: 954502. doi: 10.1155/2014/954502 PMID: 24860243
30. Liu X, Osawa T. Cis astaxanthin and especially 9-cis astaxanthin exhibits a higher antioxidant activity in vitro compared to the all-trans isomer. Biochem Biophys Res Commun. 2007; 357: 187-193. PMID: 17416351
31. Chew BP, Park JS, Wong MW, Wong TS. A comparison of the anticancer activities of dietary betacarotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res. 1999; 19: 1849-1853. PMID: 10470126
32. Nakao R, Nelson OL, Park JS, Mathison BD, Thompson PA, Chew BP. Effect of dietary astaxanthin at different stages of mammary tumor initiation in balb/c mice. Anticancer Res. 2010; 30: 2171-2175. PMID: 20651366
33. Bhuvaneswari S, Yogalakshmi B, Sreeja S, Anuradha CV. Astaxanthin reduces hepatic endoplasmic reticulum stress and nuclear factor-kappab-mediated inflammation in high fructose and high fat diet-fed mice. Cell Stress Chaperones. 2014; 19: 183-191. doi: 10.1007/s12192-013-0443-x PMID: 23852435
34. Nakao R, Nelson OL, Park JS, Mathison BD, Thompson PA, Chew BP. Effect of astaxanthin supplementation on inflammation and cardiac function in balb/c mice. Anticancer Res. 2010; 30: 2721-2725. PMID: 20683004
35. Ohgami K, Shiratori K, Kotake S, Nishida T, Mizuki N, Yazawa K, et al. Effects of astaxanthin on lipopoly-saccharide-induced inflammation in vitro and in vivo. Invest Ophthalmol Vis Sci. 2003; 44: 2694-2701. PMID: 12766075
36. Rao AR, Sindhuja HN, Dharmesh SM, Sankar KU, Sarada R, Ravishankar GA. Effective inhibition of skin cancer, tyrosinase, and antioxidative properties by astaxanthin and astaxanthin esters from the green alga haematococcus pluvialis. J Agric Food Chem. 2013; 61: 3842-3851. doi: 10.1021/jf304609j PMID: 23473626
37. Hama S, Takahashi K, Inai Y, Shiota K, Sakamoto R, Yamada A, et al. Protective effects of topical application of a poorly soluble antioxidant astaxanthin liposomal formulation on ultraviolet-induced skin damage. J Pharm Sci. 2012; 101: 2909-2916. doi: 10.1002/jps.23216 PMID: 22628205
38. Suzuki Y, Ohgami K, Shiratori K, Jin XH, Ilieva I, Koyama Y, et al. Suppressive effects of astaxanthin against rat endotoxin-induced uveitis by inhibiting the nf-kappab signaling pathway. Exp Eye Res. 2006; 82: 275-281. PMID: 16126197
39. Fassett RG, Healy H, Driver R, Robertson IK, Geraghty DP, Sharman JE, et al. Astaxanthin vs placebo on arterial stiffness, oxidative stress and inflammation in renal transplant patients (xanthin): a randomised controlled trial. BMC Nephrol. 2008; 9: 17. doi: 10.1186/1471-2369-9-17 PMID: 19091127
40. Fassett RG, Coombes JS. Astaxanthin, oxidative stress, inflammation and cardiovascular disease. Future Cardiol. 2009; 5: 333-342. doi: 10.2217/fca.09.19 PMID: 19656058
41. Tweedie D, Ferguson RA, Fishman K, Frankola KA, Van Praag H, Holloway HW, et al. Tumor necrosis factor-alpha synthesis inhibitor 3,6'-dithiothalidomide attenuates markers of inflammation, alzheimer pathology and behavioral deficits in animal models of neuroinflammation and alzheimer's disease. J Neuroinflammation. 2012; 9: 106. doi: 10.1186/1742-2094-9-106 PMID: 22642825
42. Lee SJ, Bai SK, Lee KS, Namkoong S, Na HJ, Ha KS, et al. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing i(kappa)b kinase-dependent nf-kappab activation. Mol Cells. 2003; 16: 97-105. PMID: 14503852
43. Tao YY, Yan XC, Zhou T, Shen L, Liu ZL, Liu CH. Fuzheng huayu recipe alleviates hepatic fibrosis via inhibiting tnf-alpha induced hepatocyte apoptosis. BMC Complement Altern Med. 2014; 14: 449. doi: 10.1186/1472-6882-14-449 PMID: 25407538
44. Shen M, Lu J, Cheng P, Lin C, Dai W, Wang F, et al. Ethyl pyruvate pretreatment attenuates concanavalin a-induced autoimmune hepatitis in mice. PLoS One. 2014; 9: e87977. doi: 10.1371/journal.pone. 0087977 PMID: 24498418
45. Dyson JK, Webb G, Hirschfield GM, Lohse A, Beuers U, Lindor K, et al. Unmet clinical need in autoimmune liver diseases. J Hepatol. 2014:
46. Speranza L, Pesce M, Patruno A, Franceschelli S, de Lutiis MA, Grilli A, et al. Astaxanthin treatment reduced oxidative induced pro-inflammatory cytokines secretion in u937: shp-1 as a novel biological target. Mar Drugs. 2012; 10: 890-899. doi: 10.3390/md10040890 PMID: 22690149
47. Davis RJ. Signal transduction by the jnk group of map kinases. Cell. 2000; 103: 239-252. PMID: 11057897
48. Schwabe RF, Uchinami H, Qian T, Bennett BL, Lemasters JJ, Brenner DA. Differential requirement for c-jun nh2-terminal kinase in tnfalpha- and fas-mediated apoptosis in hepatocytes. Faseb J. 2004; 18: 720-722. PMID: 14766793
49. Chen N, Nomura M, She QB, Ma WY, Bode AM, Wang L, et al. Suppression of skin tumorigenesis in cjun nh(2)-terminal kinase-2-deficient mice. Cancer Res. 2001; 61: 3908-3912. PMID: 11358804
50. Volk A, Li J, Xin J, You D, Zhang J, Liu X, et al. Co-inhibition of nf-kappab and jnk is synergistic in tnfexpressing human aml. J Exp Med. 2014; 211: 1093-1108. doi: 10.1084/jem.20130990 PMID: 24842373
51. Goda S, Kato Y, Domae E, Hayashi H, Tani-Ish NN, Iida J, et al. Effects of jnk1/2 on the inflammation cytokine tnf-alpha-enhanced production of mmp-3 in human dental pulp fibroblast-like cells. Int Endod J. 2014:
52. Lu Y, Jiang BC, Cao DL, Zhang ZJ, Zhang X, Ji RR, et al. Traf6 upregulation in spinal astrocytes maintains neuropathic pain by integrating tnf-alpha and il-1beta signaling. Pain. 2014:
53. Streetz K, Fregien B, Plumpe J, Korber K, Kubicka S, Sass G, et al. Dissection of the intracellular pathways in hepatocytes suggests a role for jun kinase and ifn regulatory factor-1 in con a-induced liver failure. J Immunol. 2001; 167: 514-523. PMID: 11418690
54. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote tnfalphainduced death and sustained jnk activation by inhibiting map kinase phosphatases. Cell. 2005; 120: 649-661. PMID: 15766528
55. Gordy C, He YW. The crosstalk between autophagy and apoptosis: where does this lead? Protein Cell. 2012; 3: 17-27. doi: 10.1007/s13238-011-1127-x PMID: 22314807
56. Renton JP, Xu N, Clark JJ, Hansen MR. Interaction of neurotrophin signaling with bcl-2 localized to the mitochondria and endoplasmic reticulum on spiral ganglion neuron survival and neurite growth. J Neurosci Res. 2010; 88: 2239-2251. doi: 10.1002/jnr.22381 PMID: 20209634
57. Yamamoto K, Ichijo H, Korsmeyer SJ. Bcl-2 is phosphorylated and inactivated by an ask1/jun nterminal protein kinase pathway normally activated at g(2)/m. Mol Cell Biol. 1999; 19: 8469-8478. PMID: 10567572
58. Wang C, Chen K, Xia Y, DaiW,Wang F, ShenM, et al. N-acetylcysteine attenuates ischemia-reperfusion-induced apoptosis and autophagy inmouse liver via regulation of the ros/jnk/bcl-2 pathway. PLoS One. 2014; 9: e108855. doi: 10.1371/journal.pone.0108855 PMID: 25264893
59. Cui J, Sim TH, Gong Z, Shen HM. Generation of transgenic zebrafish with liver-specific expression of egfp-lc3: a new in vivo model for investigation of liver autophagy. Biochem Biophys Res Commun. 2012; 422: 268-273. doi: 10.1016/j.bbrc.2012.04.145 PMID: 22580284