Activation of a novel c-Myc-miR27-prohibitin 1 circuitry in cholestatic liver injury inhibits glutathione synthesis in mice

Antioxidants and Redox Signaling

Volumn 22, Issue 3, 2015, Pages 259-274

  Yang, Heping ^a   Li, Tony W H ^a   Zhou, Yu ^a   Peng, Hui ^a   Liu, Ting ^b   Zandi, Ebrahim ^a,c   Martínez Chantar, Mariá Luz ^d   Mato, José M ^d   Lu, Shelly C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE CYSTEINE LIGASE; LITHOCHOLIC ACID; MESSENGER RNA; MICRORNA; MICRORNA 27A; MICRORNA 27B; MYC PROTEIN; PROHIBITIN; S ADENOSYLMETHIONINE; TRANSCRIPTION FACTOR MAFG; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID; GLUTATHIONE; MIRN27 MICRORNA, MOUSE; MYC PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; PROTEIN BINDING; REPRESSOR PROTEIN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CHOLESTASIS; CONTROLLED STUDY; GLUTATHIONE METABOLISM; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; WESTERN BLOTTING; ANIMAL; BINDING SITE; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION; GENETICS; HUMAN; INTRAHEPATIC CHOLESTASIS; METABOLISM; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; TUMOR CELL LINE;

MUS;

ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CHOLESTASIS, INTRAHEPATIC; GENE EXPRESSION; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMANS; MALE; MICE, INBRED C57BL; MICRORNAS; NF-E2-RELATED FACTOR 2; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; RNA INTERFERENCE;

EID: 84921048652     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.6027     Document Type: Article

References (35)

1. Adachi R, Honma Y, Masuno H, Kawana K, Shimomura I, Yamada S, and Makishima M. Selective activation of vitamin D receptor by lithocholic acid acetate, a bile acid derivative. J Lipid Res 46: 46-57, 2005.
2. Bea F, Hudson FN, Neff-LaFord H, White CC, Kavanagh TJ, Kreuzer J, Preusch MR, Blessing E, Katus HA, and Rosenfeld ME. Homocysteine stimulates antioxidant response element-mediated expression of glutamate-cysteine ligase in mouse macrophages. Atherosclerosis 203: 105-111, 2009.
3. Benassi A, Fanciulli M, Fiorentino F, Porrello A, Chiorino G, Loda M, Zupi G, and Biroccio A. c-Myc phosphorylation is required for cellular response to oxidative stress. Mol Cells 21: 509-519, 2006.
4. Dhakshinamoorthy S, and Jaiswal AK. Small Maf (MafG and MafK) proteins negatively regulate antioxidant response element-mediated expression and antioxidant induction of the NAD(P)H:Quinone oxidoreductase 1 gene. J Biol Chem 275: 40134-40141, 2000.
5. Dhakshinamoorthy S, and Jaiswal AK. C-Maf negatively regulates ARE-mediated detoxifying enzyme genes expression and anti-oxidant induction. Oncogene 21: 5301-5312, 2002.
6. Fimia GM. Prohibitins in human diseases: diagnostic and therapeutic applications. Gastroenterol Hepatol 2: S19-S26, 2009.
7. Fusaro G, Dasgupta P, Rastogi S, Joshi B, and Chellappan S. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. J Biol Chem 278: 47853-47861, 2003.
8. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36: 1199-1207, 2004.
9. Kang T, Lu W, Xu W, Anderson L, Bacanamwo M, Thompson W, Chen E, and Liu D. MicroRNA-27 (miR-27) targets prohibitin and impairs adipocytes differentiation and mitochondrial function in human adipose-derived stem cells. J Biol Chem 288: 34394-34402, 2013.
10. Kensler TW, Wakabayashi N, and Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
11. Kloek JJ, Maréchal X, Roelofsen J, Houtkooper RH, van Kuilenburg ABP, Kulik W, Bezemer R, Nevière R, van Gulik TM, and Heger M. Cholestasis is associated with hepatic microvascular dysfunction and aberrant energy metabolism before and during ischemia-reperfusion. Antioxid Redox Signal 17: 1109-1123, 2012.
12. Ko K, Iglesias-Ara A, French BA, French SW, Ramani K, Tomasi ML, Lozano JJ, Oh P, He L, Stiles BL, Li TWH, Yang HP, Martńez-Chantar ML, Mato JM, and Lu SC. Liver-specific deletion of prohibitin 1 results in spontaneous liver injury, fibrosis and hepatocellular carcinoma in mice. Hepatology 52: 2096-2108, 2010.
13. Kreamer BL, Staecker JL, Sawada N, Sattler GL, Hsia MT, and Pitot HC. Use of a low-speed, iso-density percoll centrifugation method to increase the viability of isolated rat hepatocyte preparations. In Vitro Cell Dev Biol 22: 201-211, 1986.
14. Kumar D, and Tandon RK. Use of ursodeoxycholic acid in liver disease. J Gastroenterol Hepatol 16: 3-14, 2001.
15. Kwak MK, Itoh K, Yamamoto M, and Kensler TW. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol Cell Biol 22: 2883-2892, 2002.
16. Levy S, and Forman HJ. C-Myc is a Nrf2 interacting protein that negatively regulates phase II genes through their electrophile responsive elements. IUBMB Life 62: 237-246, 2010.
17. Li X, Liu X, Xu W, Zhou P, Gao P, Jiang S, Lobie PE, and Zhou T. C-Myc-regulated miR-23a/24-2/27a cluster promotes mammary carcinoma cell invasion and hepatic metastasis by targeting sprouty2. J Biol Chem 288: 18121-18133, 2013.
18. Lu SC. Glutathione synthesis. BBA-Gen 1830: 3143-3153, 2013.
19. Mishra S, Murphy LC, and Murphy LJ. The prohibitins: emerging roles in diverse functions. J Cell Mol Med 10: 353-363, 2006.
20. Narasimhan M, Patel D, Vedpathak D, Rathinam M, Henderson G, and Mahimainathan L. Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells. PLoS One 7: e51111, 2012.
21. Nijtmans LGJ, Sanz MA, Grivell LA, and Coates PJ. The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 59: 143-155, 2002.
22. Okada K, Shoda J, Taguchi K, Maher JM, Ishizaki K, Inoue Y, Ohtsuki M, Goto N, Sugimoto H, Utsunomiya H, Oda K, Warabi E, Ishii T, and Yamamoto M. Nrf2 counteracts cholestatic liver injury via stimulation of hepatic defense systems. Biochem Biophys Res Commun 389: 431-436, 2009.
23. Ramani K, Tomasi ML, Yang HP, Ko K, and Lu SC. Mechanism and significance of changes in glutamatecysteine ligase expression during hepatic fibrogenesis. J Biol Chem 287: 36341-36355, 2012.
24. Silveira MG, and Lindor KD. Treatment of primary biliary cirrhosis: therapy with choleretic and immunosuppressive agents. Clin Liver Dis 12: 425-443, 2008.
25. Tan KP, Wood GA, Yang M, and Ito S. Participation of nuclear factor (erythroid 2-related), factor 2 in ameliorating lithocholic acid-induced cholestatic liver injury in mice. Br J Pharmacol 161: 1111-1121, 2010.
26. Tan KP, Yang M, and Ito S. Activation of nuclear factor (erythroid-2 like) factor 2 by toxic bile acids provokes adaptive defense responses to enhance cell survival at the emergence of oxidative stress. Mol Pharmacol 72: 1380-1390, 2007.
27. Theiss AL, Vijay-Kumar M, Obertone TS, Jones DP, Hansen JM, Gewirtz AT, Merlin D, and Sitaraman SV. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology 137: 199-208, 2009.
28. Tomasi ML, Ryoo M, Yang HP, Iglesia Ara A, Ko K, and Lu SC. Molecular mechanisms of lipopolysaccharidemediated inhibition of glutathione synthesis in mice. Free Radic Biol Med 68: 148-158, 2014.
29. Wang S, Fusaro G, Padmanabhan J, and Chellappan SP. Prohibitin co-localizes with Rb in the nucleus and recruits N-CoR and HDAC1 for transcriptional repression. Oncogene 21: 8388-8396, 2002.
30. Weerachayaphorn J, Mennone A, Soroka CJ, Harry K, Hagey LR, Kensler TW, and Boyer JL. Nuclear factor-E2-related factor 2 is a major determinant of bile acid homeostasis in the liver and intestine. Am J Physiol Gastrointest Liver Physiol 302: G925-G936, 2012.
31. Yang HP, Ko K, Xia M, Li TWH, Oh P, Li J, and Lu SC. Induction of avian musculoaponeurotic fibrosarcoma proteins by toxic bile acid inhibits expression of GSH synthetic enzymes and contributes to cholestatic liver injury in mice. Hepatology 51: 1291-1301, 2010.
32. Yang HP, Li TWH, Ko KS, Xia M, and Lu SC. Switch from Mnt-Max to Myc-Max induces p53 and cyclin D1 expression and apoptosis during cholestasis in mice and human hepatocytes. Hepatology 49: 860-870, 2009.
33. Yang HP, Ramani K, Xia M, Ko KS, Li TWH, Oh P, Li J, and Lu SC. Dysregulation of glutathione synthesis during cholestasis in mice: molecular mechanisms and therapeutic implications. Hepatology 49: 1982-1991, 2009.
34. Yang H, Zheng Y, Li TW, Peng H, Fernandez-Ramos D, Martńez-Chantar ML, Rojas AL, Mato JM, and Lu SC. Methionine adenosyltransferase 2B, HuR, and sirtuin 1 protein cross-talk impacts on the effect of resveratrol on apoptosis and growth in liver cancer cells. J Biol Chem 288: 23161-23170, 2013.
35. Zhou Y, Yi T, Park SS, Chadwick W, Shen RF, Wu WW, Martin B, and Maudsley S. Rapid and enhanced proteolytic digestion using electric-field-oriented enzyme reactor. J Proteomics 74: 1030-1035, 2011.