7-Ketocholesterol induces P-glycoprotein through PI3K/mTOR signaling in hepatoma cells

Biochemical Pharmacology

Volumn 86, Issue 4, 2013, Pages 548-560

  Wang, Sheng Fan ^a,b,c   Chou, Yueh Ching ^b,c,f   Mazumder, Nirmal ^b   Kao, Fu Jen ^b   Nagy, Eslie D ^d,e   Guengerich, Peter ^d   Huang, Cheng ^a   Lee, Hsin Chen ^b   Lai, Ping Shan ^e   Ueng, Yune Fang ^a,b,f  

^a NATIONAL RESEARCH INSTITUTE OF CHINESE MEDICINE   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

7 Ketocholesterol; Glycolysis; Hepatoma; P Glycoprotein; PI3K mTOR

Indexed keywords

7 OXOCHOLESTEROL; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; DOXORUBICIN; INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN; MULTIDRUG RESISTANCE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; CELL KILLING; CELL LYSATE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DENSITY GRADIENT; ELECTROPHORETIC MOBILITY; ENZYME ACTIVATION; GLYCOLYSIS; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; LIPID RAFT; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84884903837     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.06.006     Document Type: Article

References (46)

1. Luqmani YA. Mechanisms of drug resistance in cancer chemotherapy. Med Princ Pract 2005;14(Suppl. 1):35-48. (Pubitemid 41161048)
2. Lencioni R, Chen XP, Dagher L, Venook AP. Treatment of intermediate/advanced hepatocellular carcinoma in the clinic: how can outcomes be improved. Oncologist 2010;15(Suppl. 4):42-52.
3. Tong AW, Su D, Mues G, Tillery GW, Goldstein R, Klintmalm G, et al. Chemosensitization of human hepatocellular carcinoma cells with cyclosporine A in poat-liver transplant patient plasma. Clin Cancer Res 1996;2:531-9. (Pubitemid 26099173)
4. Soini Y, Virkajarvi N, Raunio H, Paakko P. Expression of P-glycoprotein in hepatocellular carcinoma: a potential marker of prognosis. J Clin Pathol 1994;49: 470-3.
5. Itsubo M, Ishikawa T, Toda G, Tanaka M. Immunohistochemical study of expression and cellular localization of the multidrug resistance gene product P-glycoprotein in primary liver carcinoma. Cancer 1994;73:298-303. (Pubitemid 24030605)
6. Grude P, Conti F, Mennecier D, Louvel A, Houssin D, Weill B, et al. MDR1 gene expression in hepatocellular carcinoma and the peritumoral liver of patients with and without cirrhosis. Cancer Lett 2002;186:107-13. (Pubitemid 35245333)
7. Nagasue N, Dhar DK, Makino Y, Yoshimura H, Nakamura T. Overexpression of P-glycoprotein in adenomatous hyperplasia of human liver with cirrhosis. J Hepatol 1995;22:197-201.
8. Meyer dos Santos S, Weber CC, Franke C, Muller WE, Eckert GP. Cholesterol: coupling between membrane microenvironment and ABC transporter activity. Biochem Biophys Res Commun 2007;354:216-21. (Pubitemid 46137959)
9. Hwang SJ, Lee SD, Chang CF, Wu JC, Tsay SH, Lui WY, et al. Hypercholesterolaemia in patients with hepatocellular carcinoma. J Gastroenterol Hepatol 1992;7:491-6.
10. Vejux A, Malvitte L, Lizard G. Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis. Braz J Med Biol Res 2008;41:545-56.
11. Corradini SG, Micheletta F, Natoli S, Iappelli M, Angelantonio ED, Marco RD, et al. High preoperative recipient plasma 7b-hydroxycholesterol is associated with initial poor graft function after liver transplantation. Liver Transplant 2005;11:1494-504. (Pubitemid 43072625)
12. Saito H, Kitame F, Uemura Y, Ishida N. The regulating effect of cholesterol derivatives isolated from human sera on lymphocyte response to phytohemagglutinin. Tohoku J Exp Med 1983;140:245-58. (Pubitemid 13006042)
13. Ryzlak MT, Fales HM, Russell WL, Schaffner CP. Oxysterols and alcoholic liver disease. Alcohol Clin Exp Res 1990;14:490-5. (Pubitemid 20195135)
14. Overmoyer BA, McLaren CE, Brittenham GM. Uniformity of liver density and nonheme (storage) iron distribution. Arch Pathol Lab Med 1987;111:549-54. (Pubitemid 17085985)
15. Hirayama T, Honda A, Matsuzaki Y, Miyazaki T, Ikegami T, Doy M, et al. Hypercholesterolemia in rats with hepatomas: increased oxysterols accelerate efflux but do not inhibit biosynthesis of cholesterol. Hepatology 2006;44:602-11. (Pubitemid 44433716)
16. Arca M, Natoli S, Micheletta F, Riggi S, Angelantonio ED, Montali A, et al. Increased plasma levels of oxysterols, in vivo markers of oxidative stress, in patients with familial combined hyperlipidemia: reduction during atorvastatin and fenofibrate therapy. Free Rad Biol Med 2007;42:698-705. (Pubitemid 46205153)
17. Rodrigues AC, Curi R, Britto LR, Rebbechi IM, Hirata MH, Bertolami MC, et al. Down-regulation of ABCB1 transporter by atorvastatin in a human hepatoma cell line and in human peripheral blood mononuclear cells. Biochim Biophys Acta 2006;1760:1866-73. (Pubitemid 44692371)
18. Reyes JM, Fermanian S, Yang F, Zhou SY, Herretes S, Murphy DB, et al. Metabolic changes in mesenchymal stem cells in osteogenic medium measured by autofluorescence spectroscopy. Stem Cells 2006;245:1213-7. (Pubitemid 44464689)
19. Bird DK, Yan L, Vrotsos KM, Eliceiri KW, Vaughan EM, Keely PJ, et al. Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH. Cancer Res 2005;65:8766-73. (Pubitemid 41377365)
20. Aly HH, Watashi K, Hijikata M, Kaneko H, Takada Y, Egawa H, et al. Serumderived hepatitis C virus infectivity in interferon regulatory factor-7-suppressed human primary hepatocytes. J Hepatol 2007;46:26-36. (Pubitemid 44827421)
21. Shieh MJ, Hsu CY, Huang LY, Chen HY, Huang FH, Lai PS. Reversal of doxorubicin-resistance by multifunctional nanoparticles in MCF-7/ADR cells. J Control Release 2011;152:418-25.
22. Lee YC, Tang YC, Chen YH, Wong CM, Tsou AP. Selenite-induced survival of HuH7 hepatoma cells involves activation of focal adhesion kinase- phosphatidylinositol 3-kinase-Akt pathway and Rac1. J Biol Chem 2003;278:39615-24.
23. Pan WC, Chen RM, Shen YC, Chen CC, Ueng YF. Suppressive effect of tobacco smoke extracts on oral P-glycoprotein function and its impact in smokeinduced insult to oral epidermal cells. Toxicol Lett 2009;185:116-23.
24. Royer MC, Lemaire-Ewing S, Desrumaux C, Monier S, deBarros JPP, Athias A, et al. 7-Ketocholesterol incorporation into sphingolipid/cholesterol-enriched (lipid raft) domains is impaired by vitamin E. J Biol Chem 2009;284:15826-34.
25. Shinkyo R, Xu L, Tallman KA, Cheng Q, Porter NA, Guengerich FP. Conversion of 7-dehydrocholesterol to 7-ketocholesterol is catalyzed by human cytochrome P450 7A1 and occurs by direct oxidation without an epoxide intermediate. J Biol Chem 2011;286:33021-28.
26. Rothe G, Valet G. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 20,70-dichlorofluorescein. J Leukoc Biol 1990;47:440-8. (Pubitemid 20155877)
27. Ghukasyan V, Hsu YY, Kung HS, Kao FJ. Application of fluorescence resonance energy transfer resolved by fluorescence lifetime imaging microscopy for the detection of enterovirus 71 infection in cells. J Biomed Opt 2007;12:024016-24023.
28. Dordal MS, Winter JN, Atkinson Jr AJ. Kinetic analysis of p-glycoproteinmediated doxorubicin efflux. J Pharmacol Exp Ther 1992;263:762-6.
29. Massey JB, Pownall HJ. The polar nature of 7-ketocholesterol determines its location within membrane domains and the kinetics of membrane microsolubilization by apolipoprotein A-I. Biochemistry 2005;44:10423-33. (Pubitemid 41076838)
30. Aye ILMH, Waddell BJ, Mark PJ, Keelan JA. Oxysterols inhibit differentiation and fusion of term primary trophoblasts by activating liver X receptors. Placenta 2011;32:183-91.
31. Huwait EA, Greenow KR, Singh NN, Ramji DP. A novel role for c-Jun N-terminal kinase and phosphoinositide 3-kinase in the liver X receptor-mediated induction of macrophage gene expression. Cell Signal 2011;23:542-9.
32. Pommier AJC, Alves G, Viennois E, Bernard S, Communal Y, Sion B, et al. Liver X receptor activation downregulates AKT survival signaling in lipid rafts and induces apoptosis of prostate cancer cells. Oncogene 2010;29:2712-23.
33. Arcaro A, Aubert M, Espinosa del Hierro ME, Khanzada UK, Angelidou S, Tetley TD, et al. Critical role for lipid raft-associated Src kinases in activation of PI3KAkt signaling. Cell Signal 2007;19:1081-92. (Pubitemid 46437438)
34. Phillips JE, Geng YJ, Mason RP. 7-Ketocholesterol forms crystalline domains in model membranes and murine aortic smooth muscle cells. Atherosclerosis 2001;159:125-35. (Pubitemid 33016629)
35. Garc?a MG, Alaniz LD, Russo RIC, Alvarez E, Hajos SE. PI3K/Akt inhibition modulates multidrug resistance and activates NF-kB in murine lymphoma cell lines. Leukemia Res 2009;33:288-96.
36. Katayama K, Yoshioka S, Tsukahara S, Mitsuhashi J, Sugimoto Y. Inhibition of the mitogen-activated protein kinase pathway results in the down-regulation of P-glycoprotein. Mol Cancer Ther 2007;6:2092-102. (Pubitemid 47052500)
37. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, et al. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 2007;282: 14056-64. (Pubitemid 47100467)
38. Breier A, Gibalova L, Seres M, Barancik M, Sulova Z. New insight into Pglycoprotein as a drug target. Anti-cancer Agent Med Chem 2013;13:159-70.
39. Jazirehi AR, Wenn PB, Damavand M. Therapeutic implications of targeting the PI3Kinase/AKT/mTOR signaling module in melanoma therapy. Am J Cancer Res 2012;2:178-91.
40. Hsu IC, Tokiwa T, Metcalf RA, Welsh JA, Sun T, Harris CC. p53 gene mutation and integrated hepatitis B viral DNA sequences in human liver cancer cell lines. Carcinogenesis 1993;14:987-92. (Pubitemid 23169159)
41. Mathieu MC, Lapierre I, Brault K, Raymond M. Aromatic hydrocarbon receptor (AhR)-, AhR nuclear translocator-and p53-mediated induction of murine multidrug resistance mdr1 gene by 3-methylcholanthrene and benzo(a)pyrene in hepatoma cells. J Biol Chem 2001;276:4819-27.
42. Ros JE, Schuetz JD, Geuken M, Streetz K, Moshage H, Kuipers F, et al. Induction of Mdr1b expression by tumor necrosis factor-a in rat liver cells is independent of p53 but requires NF-kB signaling. Hepatology 2001;33:1425-31. (Pubitemid 32496979)
43. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X, et al. Mammalian target of rapamycin up-regulation of pyruvate kinase type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci U S A 2011;108: 4129-34.
44. Skala MC, Riching KM, Bird DK, Gendron-Fitzpatrick A, Eickhoff J, Eliceiri KW, et al. In vivo multiphoton fluorescence lifetime imaging of protein-bound and free NADH in normal and pre-cancerous epithelia. J Biomed Opt 2007;12: 1-19.
45. Warburg O. On the origin of cancer cells. Science 1956;324:1029-33.
46. Wartenberg M, Richter M, Datchev A, Gunther S, Milosevic N, Bekhite MN, et al. Glycolytic pyruvate regulates p-glycoprotein expression in multicellular tumor spheroids via modulation of the intracellular redox state. J Cell Biochem 2010;109:434-46.