Loss of stearoyl-CoA desaturase activity leads to free cholesterol synthesis through increased Xbp-1 splicing

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 6, 2010, Pages

  Paton, Chad M ^a   Ntambi, James M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Acyl coenzyme A:cholesterol acyltransferase 1; Caveolin 1; Cell stress; Cholesterol metabolism; Fasting refeeding; X box binding protein 1

Indexed keywords

A 939572; ABC TRANSPORTER A1; ACYL COENZYME A DESATURASE; CHOLESTEROL; CHOLESTEROL ESTER; ENZYME INHIBITOR; LIVER X RECEPTOR; MONOUNSATURATED FATTY ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVITY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REFEEDING; RNA SPLICING; STEROL SYNTHESIS;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHOLESTEROL; DNA-BINDING PROTEINS; FATTY ACIDS, MONOUNSATURATED; FEMALE; LIVER; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; RNA SPLICING; STEAROYL-COA DESATURASE; TRANSCRIPTION FACTORS;

EID: 78649678445     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00388.2010     Document Type: Article

References (38)

1. Aja S, Landree LE, Kleman AM, Medghalchi SM, Vadlamudi A, McFadden JM, Aplasca A, Hyun J, Plummer E, Daniels K, Kemm M, Townsend CA, Thupari JN, Kuhajda FP, Moran TH, Ronnett GV. Pharmacological stimulation of brain carnitine palmitoyl-transferase-1 decreases food intake and body weight. Am J Physiol Regul Integr Comp Physiol 294: R352-R361, 2008.
2. Antalis C, Arnold T, Rasool T, Lee B, Buhman K, Siddiqui R. High ACAT1 expression in estrogen receptor negative basal-like breast cancer cells is associated with LDL-induced proliferation. Breast Cancer Res Treat 122: 661-670, 2009.
3. Attie AD. ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends Biochem Sci 32: 172-179, 2007.
4. Back SH, Lee K, Vink E, Kaufman RJ. Cytoplasmic IRE1alpha-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J Biol Chem 281: 18691-18706, 2006.
5. Brown JM, Chung S, Sawyer JK, Degirolamo C, Alger HM, Nguyen T, Zhu X, Duong MN, Wibley AL, Shah R, Davis MA, Kelley K, Wilson MD, Kent C, Parks JS, Rudel LL. Inhibition of stearoyl-coenzyme A desaturase 1 dissociates insulin resistance and obesity from atherosclerosis. Circulation 118: 1467-1475, 2008.
6. Chao WT, Tsai SH, Lin YC, Lin WW, Yang VC. Cellular localization and interaction of ABCA1 and caveolin-1 in aortic endothelial cells after HDL incubation. Biochem Biophys Res Commun 332: 743-749, 2005.
7. Choi Y, Park Y, Storkson JM, Pariza MW, Ntambi JM. Inhibition of stearoyl-CoA desaturase activity by the cis-9,trans-11 isomer and the trans-10,cis-12 isomer of conjugated linoleic acid in MDA-MB-231 and MCF-7 human breast cancer cells. Biochem Biophys Res Commun 294: 785-790, 2002.
8. Chu K, Miyazaki M, Man WC, Ntambi JM. Stearoyl-coenzyme A desaturase 1 deficiency protects against hypertriglyceridemia and increases plasma high-density lipoprotein cholesterol induced by liver X receptor activation. Mol Cell Biol 26: 6786-6798, 2006.
9. Chuu CP, Hiipakka RA, Kokontis JM, Fukuchi J, Chen RY, Liao S. Inhibition of tumor growth and progression of lncap prostate cancer cells in athymic mice by androgen and liver X receptor agonist. Cancer Res 66: 6482-6486, 2006.
10. Chuu CP, Kokontis J, Hiipakka R, Liao S. Modulation of liver X receptor signaling as novel therapy for prostate cancer. J Biomed Sci 14: 543-553, 2007.
11. Feng B, Yao PM, Li Y, Devlin CM, Zhang D, Harding HP, Sweeney M, Rong JX, Kuriakose G, Fisher EA, Marks AR, Ron D, Tabas I. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol 5: 781-792, 2003.
12. Flowers MT, Groen AK, Oler AT, Keller MP, Choi Y, Schueler KL, Richards OC, Lan H, Miyazaki M, Kuipers F, Kendziorski CM, Ntambi JM, Attie AD. Cholestasis and hypercholesterolemia in SCD1-deficient mice fed a low-fat, high-carbohydrate diet. J Lipid Res 47: 2668-2680, 2006.
13. Flowers MT, Keller MP, Choi Y, Lan H, Kendziorski C, Ntambi JM, Attie AD. Liver gene expression analysis reveals endoplasmic reticulum stress and metabolic dysfunction in SCD1-deficient mice fed a very low-fat diet. Physiol Genomics 33: 361-372, 2008. (Pubitemid 352755738)
14. Folch J, Lees M, Stanley GHS. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509, 1957.
15. Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, Lisanti MP. Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol 24: 98-105, 2004.
16. Fu Y, Hoang A, Escher G, Parton RG, Krozowski Z, Sviridov D. Expression of caveolin-1 enhances cholesterol efflux in hepatic cells. J Biol Chem 279: 14140-14146, 2004.
17. Fukuchi J, Kokontis JM, Hiipakka RA, Chuu Cp, Liao S. Antiproliferative effect of liver X receptor agonists on LNCaP human prostate cancer cells. Cancer Res 64: 7686-7689, 2004.
18. Goldstein JL, Dana SE, Faust JR, Beaudet AL, Brown MS. Role of lysosomal acid lipase in the metabolism of plasma low density lipoprotein. Observations in cultured fibroblasts from a patient with cholesteryl ester storage disease. J Biol Chem 250: 8487-8495, 1975.
19. Im SS, Hammond LE, Yousef L, Nugas-Selby C, Shin DJ, Seo YK, Fong LG, Young SG, Osborne TF. Sterol regulatory element binding protein 1a regulates hepatic fatty acid partitioning by activating acetyl coenzyme A carboxylase 2. Mol Cell Biol 29: 4864-4872, 2009.
20. Langer C, Huang Y, Cullen P, Wiesenh++tter B, Mahley RW, Assmann G, von Eckardstein A. Endogenous apolipoprotein E modulates cholesterol efflux and cholesteryl ester hydrolysis mediated by high-density lipoprotein-3 and lipid-free apolipoproteins in mouse peritoneal macrophages. J Mol Med 78: 217-227, 2000.
21. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459, 2003.
22. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320: 1492-1496, 2008.
23. Lin YC, Ma C, Hsu WC, Lo HF, Yang VC. Molecular interaction between caveolin-1 and ABCA1 on high-density lipoprotein-mediated cholesterol efflux in aortic endothelial cells. Cardiovasc Res 75: 575-583, 2007.
24. Miyazaki M, Flowers MT, Sampath H, Chu K, Otzelberger C, Liu X, Ntambi JM. Hepatic stearoyl-CoA desaturase-1 deficiency protects mice from carbohydrate-induced adiposity and hepatic steatosis. Cell Metab 6: 484-496, 2007.
25. Miyazaki M, Kim YC, Gray-Keller MP, Attie AD, Ntambi JM. The biosynthesis of hepatic cholesterol esters and triglycerides is impaired in mice with a disruption of the gene for stearoyl-CoA desaturase 1. J Biol Chem 275: 30132-30138, 2000.
26. Morgan-Lappe SE, Tucker LA, Huang X, Zhang Q, Sarthy AV, Zakula D, Vernetti L, Schurdak M, Wang J, Fesik SW. Identification of Ras-related nuclear protein, targeting protein for Xenopus kinesin-like protein 2, and stearoyl-CoA desaturase 1 as promising cancer targets from an RNAi-based screen. Cancer Res 67: 4390-4398, 2007.
27. Mulligan JD, Flowers MT, Tebon A, Bitgood JJ, Wellington C, Hayden MR, Attie AD. ABCA1 is essential for efficient basolateral cholesterol efflux during the absorption of dietary cholesterol in chickens. J Biol Chem 278: 13356-13366, 2003.
28. Przybytkowski E, Joly E, Nolan CJ, Hardy S, Francoeur AM, Langelier Y, Prentki M. Upregulation of cellular triacylglycerol-free fatty acid cycling by oleate is associated with long-term serum-free survival of human breast cancer cells. Biochem Cell Biol 85: 301-310, 2007. (Pubitemid 47025909)
29. Scaglia N, Igal RA. Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J Biol Chem 280: 25339-25349, 2005.
30. Seo T, Oelkers PM, Giattina MR, Worgall TS, Sturley SL, Deckelbaum RJ. Differential modulation of ACAT1 and ACAT2 transcription and activity by long chain free fatty acids in cultured cells. Biochemistry 40: 4756-4762, 2001.
31. Sha H, He Y, Chen H, Wang C, Zenno A, Shi H, Yang X, Zhang X, Qi L. The IRE1[alpha]-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab 9: 556-564, 2009.
32. Smaby JM, Schmid PC, Brockman HL. Phospholipid structure and the packing of cholesteryl oleate at the lipid/water interface. Biochemistry 23: 1955-1958, 1984.
33. Snow J, Phillips MC. Phase behavior of cholesteryl ester dispersions which model the inclusions of foam cells. Biochemistry 29: 2464-2471, 1990.
34. Sriburi R, Bommiasamy H, Buldak GL, Robbins GR, Frank M, Jackowski S, Brewer JW. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J Biol Chem 282: 7024-7034, 2007.
35. Sun Y, Hao M, Luo Y, Liang Cp Silver DL, Cheng C, Maxfield FR, Tall AR. Stearoyl-CoA desaturase inhibits ATP-binding cassette transporter A1-mediated cholesterol efflux and modulates membrane domain structure. J Biol Chem 278: 5813-5820, 2003.
36. Xie X, Liao H, Dang H, Pang W, Guan Y, Wang X, Shyy JYJ, Zhu Y, Sladek FM. Down-regulation of hepatic HNF4(alpha) gene expression during hyperinsulinemia via SREBPs. Mol Endocrinol 23: 434-443, 2009.
37. Xin Z, Zhao H, Serby MD, Liu B, Liu M, Szczepankiewicz BG, Nelson LTJ, Smith HT, Suhar TS, Janis RS, Cao N, Camp HS, Collins CA, Sham HL, Surowy TK, Liu G. Discovery of piperidine-aryl urea-based stearoyl-CoA desaturase 1 inhibitors. Bioorg Med Chem Lett 18: 4298-4302, 2008.
38. Zhou W, Simpson PJ, McFadden JM, Townsend CA, Medghalchi SM, Vadlamudi A, Pinn ML, Ronnett GV, Kuhajda FP. Fatty acid synthase inhibition triggers apoptosis during S phase in human cancer cells. Cancer Res 63: 7330-7337, 2003.