Biochemical disorders associated with antiproliferative effect of dehydroepiandrosterone in hepatoma cells as revealed by LC-based metabolomics

Biochemical Pharmacology

Volumn 82, Issue 11, 2011, Pages 1549-1561

  Cheng, Mei Ling ^a,b   Shiao, Ming Shi ^a   Chiu, Daniel Tsun Yee ^a,b   Weng, Shiue Fen ^a   Tang, Hsiang Yu ^a   Ho, Hung Yao ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Dehydroepiandrosterone; Metabolomics; Mitochondria; Oxidative stress; s Adenosylmethionine

Indexed keywords

CARDIOLIPIN; CARNITINE; FATTY ACID; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; LYSINE; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 2A; METHIONINE ADENOSYLTRANSFERASE 2B; PHOSPHATIDYLCHOLINE; PRASTERONE; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

ARTICLE; CATABOLISM; CELL GROWTH; CELL METABOLISM; CONTROLLED STUDY; DRUG ACTIVITY; DRUG MECHANISM; GENE EXPRESSION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; LIVER CELL CARCINOMA; METABOLOMICS; OXIDATIVE STRESS; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY;

ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CHROMATOGRAPHY, LIQUID; DEHYDROEPIANDROSTERONE; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; LIVER NEOPLASMS; METABOLOME; METHIONINE ADENOSYLTRANSFERASE; MITOCHONDRIA; OXIDATIVE STRESS; PHOSPHATIDYLCHOLINES; PHOSPHORYLCHOLINE; S-ADENOSYLMETHIONINE;

EID: 80255131071     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.07.104     Document Type: Article

References (93)

1. C.R. Parker Jr. Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging Steroids 64 1999 640 647 (Pubitemid 29424103)
2. S.S. Yen, and G.A. Laughlin Aging and the adrenal cortex Exp Gerontol 33 1998 897 910 (Pubitemid 29019344)
3. M.P. Cleary The antiobesity effect of dehydroepiandrosterone in rats Proc Soc Exp Biol Med 196 1991 8 16
4. M.K. McIntosh, and C.D. Berdanier Antiobesity effects of dehydroepiandrosterone are mediated by futile substrate cycling in hepatocytes of BHE/cdb rats J Nutr 121 1991 2037 2043
5. D.L. Coleman, E.H. Leiter, and R.W. Schwizer Therapeutic effects of dehydroepiandrosterone (DHEA) in diabetic mice Diabetes 31 1982 830 833 (Pubitemid 12062875)
6. D.L. Coleman, R.W. Schwizer, and E.H. Leiter Effect of genetic background on the therapeutic effects of dehydroepiandrosterone (DHEA) in diabetes-obesity mutants and in aged normal mice Diabetes 33 1984 26 32 (Pubitemid 14187198)
7. G.B. Gordon, D.E. Bush, and H.F. Weisman Reduction of atherosclerosis by administration of dehydroepiandrosterone. A study in the hypercholesterolemic New Zealand white rabbit with aortic intimal injury J Clin Invest 82 1988 712 720
8. A.N. Nafziger, D.M. Herrington, and T.L. Bush Dehydroepiandrosterone and dehydroepiandrosterone sulfate: their relation to cardiovascular disease Epidemiol Rev 13 1991 267 293
9. K. Wojtal, M.K. Trojnar, and S.J. Czuczwar Endogenous neuroprotective factors: neurosteroids Pharmacol Rep 58 2006 335 340 (Pubitemid 44111068)
10. B. Zumoff, J. Levin, R.S. Rosenfeld, M. Markham, G.W. Strain, and D.K. Fukushima Abnormal 24-hr mean plasma concentrations of dehydroisoandrosterone and dehydroisoandrosterone sulfate in women with primary operable breast cancer Cancer Res 41 1981 3360 3363 (Pubitemid 11063603)
11. G.B. Gordon, K.J. Helzlsouer, and G.W. Comstock Serum levels of dehydroepiandrosterone and its sulfate and the risk of developing bladder cancer Cancer Res 51 1991 1366 1369
12. S.D. Hursting, S.N. Perkins, D.C. Haines, J.M. Ward, and J.M. Phang Chemoprevention of spontaneous tumorigenesis in p53-knockout mice Cancer Res 55 1995 3949 3953
13. M.A. Moore, W. Thamavit, A. Ichihara, K. Sato, and N. Ito Influence of dehydroepiandrosterone, diaminopropane and butylated hydroxyanisole treatment during the induction phase of rat liver nodular lesions in a short-term system Carcinogenesis 7 1986 1059 1063 (Pubitemid 17127469)
14. R. Garcea, L. Daino, R. Pascale, S. Frassetto, P. Cozzolino, and M.E. Ruggiu Inhibition by dehydroepiandrosterone of liver preneoplastic foci formation in rats after initiation-selection in experimental carcinogenesis Toxicol Pathol 15 1987 164 169
15. M. Simile, R.M. Pascale, M.R. De Miglio, A. Nufris, L. Daino, and M.A. Seddaiu Inhibition by dehydroepiandrosterone of growth and progression of persistent liver nodules in experimental rat liver carcinogenesis Int J Cancer 62 1995 210 215
16. J.W. Nyce, P.N. Magee, G.C. Hard, and A.G. Schwartz Inhibition of 1,2-dimethylhydrazine-induced colon tumorigenesis in Balb/c mice by dehydroepiandrosterone Carcinogenesis 5 1984 57 62 (Pubitemid 14197927)
17. A.G. Schwartz, and R.H. Tannen Inhibition of 7,12-dimethylbenz[a] anthracene- and urethan-induced lung tumor formation in A/J mice by long-term treatment with dehydroepiandrosterone Carcinogenesis 2 1981 1335 1337 (Pubitemid 12131940)
18. T.A. Ratko, C.J. Detrisac, R.G. Mehta, G.J. Kelloff, and R.C. Moon Inhibition of rat mammary gland chemical carcinogenesis by dietary dehydroepiandrosterone or a fluorinated analogue of dehydroepiandrosterone Cancer Res 51 1991 481 486
19. W.S. Melvin, L.G. Boros, P. Muscarella, J.L. Brandes, J.A. Johnson, and W.E. Fisher Dehydroepiandrosterone-sulfate inhibits pancreatic carcinoma cell proliferation in vitro and in vivo Surgery 121 1997 392 397 (Pubitemid 27184962)
20. M.S. Rao, and V. Subbarao Dehydroepiandrosterone inhibits DNA synthesis of rat hepatocytes induced by partial hepatectomy or mitogen (ciprofibrate) Cell Prolif 30 1997 1 5 (Pubitemid 27374591)
21. R. Lopez-Marure, P.G. Contreras, and J.S. Dillon Effects of dehydroepiandrosterone on proliferation, migration, and death of breast cancer cells Eur J Pharmacol 660 2011 268 274
22. F. Svec, and J.R. Porter The actions of exogenous dehydroepiandrosterone in experimental animals and humans Proc Soc Exp Biol Med 218 1998 174 191
23. Y. Matsuzaki, and A. Honda Dehydroepiandrosterone and its derivatives: potentially novel anti-proliferative and chemopreventive agents Curr Pharm Des 12 2006 3411 3421 (Pubitemid 44375466)
24. R.C. Klann, C.T. Holbrook, and J.W. Nyce Chemotherapy of murine colorectal carcinoma with cisplatin and cisplatin plus 3'-deoxy-3'- azidothymidine Anticancer Res 12 1992 781 787
25. P. Muscarella, L.G. Boros, W.E. Fisher, C. Rink, and W.S. Melvin Oral dehydroepiandrosterone inhibits the growth of human pancreatic cancer in nude mice J Surg Res 79 1998 154 157 (Pubitemid 28467351)
26. J.E. Green, M.A. Shibata, E. Shibata, R.C. Moon, M.R. Anver, and G. Kelloff 2-difluoromethylornithine and dehydroepiandrosterone inhibit mammary tumor progression but not mammary or prostate tumor initiation in C3(1)/SV40 T/t-antigen transgenic mice Cancer Res 61 2001 7449 7455 (Pubitemid 32995033)
27. S. Taniguchi, T. Yanase, M. Haji, K. Ishibashi, R. Takayanagi, and H. Nawata The antiobesity effect of dehydroepiandrosterone in castrated or noncastrated obese Zucker male rats Obesity Res 3 Suppl 5 1995 639S 643S
28. D.L. Coleman, E.H. Leiter, and N. Applezweig Therapeutic effects of dehydroepiandrosterone metabolites in diabetes mutant mice (C57BL/KsJ-db/db) Endocrinology 115 1984 239 243 (Pubitemid 14086816)
29. W.N. Tian, L.D. Braunstein, J. Pang, K.M. Stuhlmeier, Q.C. Xi, and X. Tian Importance of glucose-6-phosphate dehydrogenase activity for cell growth J Biol Chem 273 1998 10609 10617 (Pubitemid 28227673)
30. G. Boccuzzi, M. Di Monaco, E. Brignardello, L. Leonardi, V. Gatto, and A. Pizzini Dehydroepiandrosterone antiestrogenic action through androgen receptor in MCF-7 human breast cancer cell line Anticancer Res 13 1993 2267 2272 (Pubitemid 24036361)
31. S. Yoshida, A. Honda, Y. Matsuzaki, S. Fukushima, N. Tanaka, and A. Takagiwa Anti-proliferative action of endogenous dehydroepiandrosterone metabolites on human cancer cell lines Steroids 68 2003 73 83 (Pubitemid 35418305)
32. J.E. Biaglow, I.S. Ayene, C.J. Koch, J. Donahue, T.D. Stamato, and S.W. Tuttle G6PD deficient cells and the bioreduction of disulfides: effects of DHEA, GSH depletion and phenylarsine oxide Biochem Biophys Res Commun 273 2000 846 852 (Pubitemid 30481042)
33. H.P. Ng, Y.F. Wang, C.Y. Lee, and M.L. Hu Toxicological and antioxidant effects of short-term dehydroepiandrosterone injection in young rats fed diets deficient or adequate in vitamin E Food Chem Toxicol 37 1999 503 508 (Pubitemid 29306915)
34. K. Izumo, M. Horiuchi, M. Komatsu, K. Aoyama, K. Bandow, and T. Matsuguchi Dehydroepiandrosterone increased oxidative stress in a human cell line during differentiation Free Radic Res 43 2009 922 931
35. H.Y. Ho, M.L. Cheng, H.Y. Chiu, S.F. Weng, and D.T. Chiu Dehydroepiandrosterone induces growth arrest of hepatoma cells via alteration of mitochondrial gene expression and function Int J Oncol 33 2008 969 977
36. R.H. Barton A decade of advances in metabonomics Expert Opin Drug Metab Toxicol 7 2011 129 136
37. J.C. Lindon, E. Holmes, and J.K. Nicholson So what's the deal with metabonomics? Anal Chem 75 2003 384A 391A (Pubitemid 37082218)
38. I.D. Wilson, R. Plumb, J. Granger, H. Major, R. Williams, and E.M. Lenz HPLC-MS-based methods for the study of metabonomics J Chromatogr B 817 2005 67 76 (Pubitemid 40174790)
39. J. Yang, G. Xu, Y. Zheng, H. Kong, C. Wang, and X. Zhao Strategy for metabonomics research based on high-performance liquid chromatography and liquid chromatography coupled with tandem mass spectrometry J Chromatogr A 1084 2005 214 221 (Pubitemid 40966931)
40. J.L. Griffin, and A.W. Nicholls Metabolomics as a functional genomic tool for understanding lipid dysfunction in diabetes, obesity and related disorders Pharmacogenomics 7 2006 1095 1107 (Pubitemid 44649115)
41. J.K. Nicholson, J.C. Lindon, and E. Holmes 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data Xenobiotica 29 1999 1181 1189
42. O. Fiehn Metabolomics - the link between genotypes and phenotypes Plant Mol Biol 48 2002 155 171 (Pubitemid 34128498)
43. O. Fiehn Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks Comp Funct Genomics 2 2001 155 168 (Pubitemid 32590962)
44. N.J. Serkova, and K. Glunde Metabolomics of cancer Meth Mol Biol 520 2009 273 295
45. K. Kim, P. Aronov, S.O. Zakharkin, D. Anderson, B. Perroud, and I.M. Thompson Urine metabolomics analysis for kidney cancer detection and biomarker discovery Mol Cell Proteomics 8 2009 558 570
46. P.F. Pradat, and M. Dib Biomarkers in amyotrophic lateral sclerosis: facts and future horizons Mol Diagn Ther 13 2009 115 125
47. E.J. Saude, I.P. Obiefuna, R.L. Somorjai, F. Ajamian, C. Skappak, and T. Ahmad Metabolomic biomarkers in a model of asthma exacerbation: urine nuclear magnetic resonance Am J Respir Crit Care Med 179 2009 25 34
48. E.Y. Xu, W.H. Schaefer, and Q. Xu Metabolomics in pharmaceutical research and development: metabolites, mechanisms and pathways Curr Opin Drug Discov Devel 12 2009 40 52
49. J.C. Lindon, E. Holmes, and J.K. Nicholson Metabonomics: systems biology in pharmaceutical research and development Curr Opin Mol Therapeut 6 2004 265 272 (Pubitemid 38997127)
50. H.Y. Ho, M.L. Cheng, Y.H. Wang, and D.T. Chiu Flow cytometry for assessment of the efficacy of siRNA Cytometry A 69 2006 1054 1061 (Pubitemid 44570200)
51. L.P. Gao, M.L. Cheng, H.J. Chou, Y.H. Yang, H.Y. Ho, and D.T. Chiu Ineffective GSH regeneration enhances G6PD-knockdown Hep G2 cell sensitivity to diamide-induced oxidative damage Free Radic Biol Med 47 2009 529 535
52. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J Biol Chem 226 1957 497 509
53. M. Kanehisa, and S. Goto KEGG: kyoto encyclopedia of genes and genomes Nucleic Acids Res 28 2000 27 30 (Pubitemid 30047706)
54. M. Kanehisa, S. Goto, M. Furumichi, M. Tanabe, and M. Hirakawa KEGG for representation and analysis of molecular networks involving diseases and drugs Nucleic Acids Res 38 2010 D355 D360
55. D.S. Wishart, C. Knox, A.C. Guo, R. Eisner, N. Young, and B. Gautam HMDB: a knowledgebase for the human metabolome Nucleic Acids Res 37 2009 D603 D610
56. H.Y. Ho, M.L. Cheng, S.F. Weng, Y.L. Leu, and D.T. Chiu Antiviral effect of epigallocatechin gallate on enterovirus 71 J Agric Food Chem 57 2009 6140 6147
57. H.Y. Ho, M.L. Cheng, S.F. Weng, L. Chang, T.T. Yeh, and S.R. Shih Glucose-6-phosphate dehydrogenase deficiency enhances enterovirus 71 infection J Gen Virol 89 2008 2080 2089
58. H.A. Newman, S.E. Gordesky, C. Hoppel, and C. Cooper The action of digitonin on rat liver mitochondria. Phospholipid content Biochem J 107 1968 381 385
59. G. Daum Lipids of mitochondria Biochim Biophys Acta 822 1985 1 42 (Pubitemid 15042024)
60. C. Kent Eukaryotic phospholipid biosynthesis Annu Rev Biochem 64 1995 315 343
61. T. Hirao, Y. Urata, K. Kageyama, M. Ikezaki, M. Kawakatsu, and M. Matsuse Dehydroepiandrosterone augments sensitivity to gamma-ray irradiation in human H4 neuroglioma cells through down-regulation of Akt signaling Free Radic Res 42 2008 957 965
62. H. Shinno, C. Noda, K. Tanaka, and A. Ichihara Induction of l-lysine-2-oxoglutarate reductase by glucagon and glucocorticoid in developing and adult rats: in vivo and in vitro studies Biochim Biophys Acta 633 1980 310 316 (Pubitemid 11162546)
63. Yang H, Li TW, Peng J, Mato JM, Lu SC. Insulin-like growth factor 1 activates methionine adenosyltransferase 2A transcription by multiple pathways in human colon cancer cells. Biochem J 2011. doi:10.1042/BJ20101754.
64. H.Z. Sun, T.W. Yang, W.J. Zang, and S.F. Wu Dehydroepiandrosterone- induced proliferation of prostatic epithelial cell is mediated by NFKB via PI3 K/AKT signaling pathway J Endocrinol 204 2010 311 318
65. R. Dashtaki, A.R. Whorton, T.M. Murphy, P. Chitano, W. Reed, and T.P. Kennedy Dehydroepiandrosterone and analogs inhibit DNA binding of AP-1 and airway smooth muscle proliferation J Pharmacol Exp Ther 285 1998 876 883 (Pubitemid 28237474)
66. M.L. Martinez-Chantar, E.R. Garcia-Trevijano, M.U. Latasa, A. Martin-Duce, P. Fortes, and J. Caballeria Methionine adenosyltransferase II beta subunit gene expression provides a proliferative advantage in human hepatoma Gastroenterology 124 2003 940 948 (Pubitemid 36389797)
67. Q. Wang, Q.Y. Liu, Z.S. Liu, Q. Qian, Q. Sun, and D.Y. Pan Lentivirus mediated shRNA interference targeting MAT2B induces growth-inhibition and apoptosis in hepatocelluar carcinoma World J Gastroenterol 14 2008 4633 4642
68. K. Kapyaho, H. Poso, and J. Janne Role of propylamine transferases in hormone-induced stimulation of polyamine biosynthesis Biochem J 192 1980 59 63 (Pubitemid 11207911)
69. Y. Ikeguchi, M.C. Bewley, and A.E. Pegg Aminopropyltransferases: function, structure and genetics J Biochem 139 2006 1 9 (Pubitemid 43258840)
70. K. Igarashi, and K. Kashiwagi Modulation of cellular function by polyamines Int J Biochem Cell Biol 42 2010 39 51
71. R.F. Coburn Polyamine effects on cell function: Possible central role of plasma membrane PI(4,5)P2 J Cell Physiol 221 2009 544 551
72. R.M. Ray, B.J. Zimmerman, S.A. McCormack, T.B. Patel, and L.R. Johnson Polyamine depletion arrests cell cycle and induces inhibitors p21(Waf1/Cip1), p27(Kip1), and p53 in IEC-6 cells Am J Physiol 276 1999 C684 C691
73. S.H. Choi, S.W. Kim, D.H. Choi, B.H. Min, and B.G. Chun Polyamine-depletion induces p27Kip1 and enhances dexamethasone-induced G1 arrest and apoptosis in human T lymphoblastic leukemia cells Leuk Res 24 2000 119 127
74. F.M. Vaz, and R.J. Wanders Carnitine biosynthesis in mammals Biochem J 361 2002 417 429 (Pubitemid 34177810)
75. R.C. Noland, T.R. Koves, S.E. Seiler, H. Lum, R.M. Lust, and O. Ilkayeva Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control J Biol Chem 284 2009 22840 22852
76. S.H. Zeisel, and J.K. Blusztajn Choline and human nutrition Annu Rev Nutr 14 1994 269 296 (Pubitemid 24261839)
77. M.S. Sharpley, R.J. Shannon, F. Draghi, and J. Hirst Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria Biochemistry 45 2006 241 248 (Pubitemid 43054102)
78. A.T. Baykal, M.R. Jain, and H. Li Aberrant regulation of choline metabolism by mitochondrial electron transport system inhibition in neuroblastoma cells Metabolomics 4 2008 347 356
79. F.L. Hoch Cardiolipins and biomembrane function Biochim Biophys Acta 1113 1992 71 133
80. M. Schlame, and D. Otten Analysis of cardiolipin molecular species by high-performance liquid chromatography of its derivative 1,3-bisphosphatidyl-2- benzoyl-sn-glycerol dimethyl ester Anal Biochem 195 1991 290 295
81. M. Schlame, M. Ren, Y. Xu, M.L. Greenberg, and I. Haller Molecular symmetry in mitochondrial cardiolipins Chem Phys Lipids 138 2005 38 49 (Pubitemid 41579001)
82. E. Mileykovskaya, M. Zhang, and W. Dowhan Cardiolipin in energy transducing membranes Biochemistry (Mosc) 70 2005 154 158 (Pubitemid 40512322)
83. C. Lange, J.H. Nett, B.L. Trumpower, and C. Hunte Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure Embo J 20 2001 6591 6600 (Pubitemid 33134190)
84. E.K. Tuominen, C.J. Wallace, and P.K. Kinnunen Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage J Biol Chem 277 2002 8822 8826 (Pubitemid 34952948)
85. M. Schlame, D. Rua, and M.L. Greenberg The biosynthesis and functional role of cardiolipin Prog Lipid Res 39 2000 257 288 (Pubitemid 30224706)
86. M. Zhang, E. Mileykovskaya, and W. Dowhan Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane J Biol Chem 277 2002 43553 43556 (Pubitemid 36157767)
87. E. Mileykovskaya, and W. Dowhan Cardiolipin membrane domains in prokaryotes and eukaryotes Biochim Biophys Acta 1788 2009 2084 2091
88. Y. Xu, A. Malhotra, M. Ren, and M. Schlame The enzymatic function of tafazzin J Biol Chem 281 2006 39217 39224 (Pubitemid 46041881)
89. S.M. Claypool, P. Boontheung, J.M. McCaffery, J.A. Loo, and C.M. Koehler The cardiolipin transacylase, tafazzin, associates with two distinct respiratory components providing insight into Barth syndrome Mol Biol Cell 19 2008 5143 5155
90. M.I. Panayiotidis, S.P. Stabler, R.H. Allen, A. Pappa, and C.W. White Oxidative stress-induced regulation of the methionine metabolic pathway in human lung epithelial-like (A549) cells Mutat Res 674 2009 23 30
91. M.J. Hitchler, and F.E. Domann An epigenetic perspective on the free radical theory of development Free Radic Biol Med 43 2007 1023 1036 (Pubitemid 47302657)
92. I. Wiswedel, A. Gardemann, A. Storch, D. Peter, and L. Schild Degradation of phospholipids by oxidative stress - exceptional significance of cardiolipin Free Radic Res 44 2010 135 145
93. J. Kim, P.E. Minkler, R.G. Salomon, V.E. Anderson, and C.L. Hoppel Cardiolipin: characterization of distinct oxidized molecular species J Lipid Res 52 2011 125 135