Ketogenic HMGCS2 is a c-Myc target gene expressed in differentiated cells of human colonic epithelium and down-regulated in colon cancer

Molecular Cancer Research

Volumn 4, Issue 9, 2006, Pages 645-653

  Camarero, Nurla ^a   Mascaró, Cristina ^a   Mayordomo, Cristina ^a   Vilardell, Felip ^b   Haro, Diego ^a   Marrero, Pedro F ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CATALAN INSTITUTE OF ONCOLOGY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HYDROXYMETHYLGLUTARYL COENZYME A SYNTHASE; KETONE BODY; MYC PROTEIN; TRANSCRIPTION FACTOR SP1;

ACETYLATION; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN CACO 2; CHROMATIN IMMUNOPRECIPITATION; COLON CANCER; COLON TUMOR; COLORECTAL CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM TUMOR; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KETOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECTUM TUMOR; SMALL INTESTINE;

ACETYLATION; ADENOCARCINOMA; CACO-2 CELLS; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; COLONIC NEOPLASMS; DNA-BINDING PROTEINS; DOWN-REGULATION; EPITHELIUM; GENES, MYC; HISTONE DEACETYLASES; HISTONES; HUMANS; HYDROXYMETHYLGLUTARYL-COA SYNTHASE; IMMUNOHISTOCHEMISTRY; KETONE BODIES; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-MYC; TRANSCRIPTION FACTORS;

EID: 33749347347     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-05-0267     Document Type: Article

References (52)

1. Williamson DH, Bates MW, Krebs HA. Activity and intracellular distribution of enzymes of ketone-body metabolism in rat liver. Biochem J 1968;108:353-61.
2. Baird GD, Hibbitt KG. Lee J. Enzymes involved in acetoacetate formation in various bovine tissues. Biochem J 1970;117:703-9.
3. Dashti N, Ontko JA. Rate-limiting function of 3-hydroxy-3-methylglutaryl- coenzyme A synthase in ketogenesis. Biochem Med 1979;22:365-74.
4. Girard J, Ferre P, Pegorier JP, Duee PH. Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiol Rev 1992;72:507-62.
5. McGarry JD, Foster DW. Regulation of hepatic fatty acid oxidation and ketone body production. Annu Rev Biochem 1980;49:395-420.
6. Hegardt FG. Mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase: a control enzyme in ketogenesis. Biochem J 1999;338:569-82.
7. Thumelin S, Forestier M, Girard J, Pegorier JP. Developmental changes in mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene expression in rat liver, intestine and kidney. Biochem J 1993;292:493-6.
8. Quant PA. Activity and expression of hepatic mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase during the starved-to-fed transition. Biochem Soc Trans 1990;18:994-5.
9. Quant PA, Tubbs PK, Brand MD. Glucagon activates mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase in vivo by decreasing the extent of succinylation of the enzyme. Eur J Biochem 1990;187:169-74.
10. Hegardt FG, Serra D, Asins G. Influence of etomoxir on the expression of several genes in liver, testis and heart. Gene Pharmacol 1995;26:897-904.
11. Gil-Gómez G, Ayté J, Hegardt FG. The rat mitochondrial 3-hydroxy-3-methylglutaryl-coenzyme-A-synthase gene contains elements that mediate its multihormonal regulation and tissue specificity. Eur J Biochem 1993;213:773 -9.
12. Nadal A, Marrero PF, Haro D. Down-regulation of the mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene by insulin: the role of the forkhead transcription factor FKHRL1. Biochem J 2002;366:289-97.
13. Rodriguez JC, Gil-Gomez G, Hegardt FG, Haro D. Peroxisome proliferator-activated receptor mediates induction of the mitochondrial 3-hydroxy-3-methyl-glutaryl-CoA synthase gene by fatty acids. J Biol Chem 1994;269:18767-72.
14. Camarero N, Nadal A, Barrero MJ, Haro D, Marrero PF. Histone deacetylase inhibitors stimulate mitochondrial HMG-CoA synthase gene expression via a promoter proximal Sp1 site. Nucleic Acids Res 2003;31:1693-703.
15. Hsu MH, Savas U, Griffin KJ, Johnson EF. Identification of peroxisome proliferator-responsive human genes by elevated expression of the peroxisome proliferator-activated receptor α in HepG2 cells. J Biol Chem 2001;276:27950-8.
16. Mascaro C, Acosta E, Ortiz JA, et al. Characterization of a response element for peroxisomal proliferator activated receptor (PPRE) in human muscle-type carnitine palmitoyltransferase I. Adv Exp Med Biol 1999;466:79-85.
17. Cullingford TE, Dolphin CT, Bhakoo KK, Peuchen S, Canevari L, Clark JB. Molecular cloning of rat mitochondrial 3-hydroxy-3-methylglutaryl-CoA lyase and detection of the corresponding tnRNA and of those encoding the remaining enzymes comprising the ketogenic 3-hydroxy-3-methylglutaryl-CoA cycle in central nervous system of suckling rat. Biochem J 1998;329:373-81.
18. Cherbuy C, Darcy-Vrillon B, Morel MT, Pegorier JP, Duee PH. Effect of germfree state on the capacities of isolated rat colonocytes to metabolize n-butyrate, glucose, and glutamine. Gastroenterology 1995;109:1890-9.
19. Curi R, Williams JF, Newsholme EA. Formation of ketone bodies by resting lymphocytes. Int J Biochem 1989;21:1133-6.
20. Mascaro C, Buesa C, Ortiz JA, Haro D, Hegardt FG. Molecular cloning and tissue expression of human mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase. Arch Biochem Biophys 1995;317:385-90.
21. Le May C, Pineau T, Bigot K, Kohl C, Girard J, Pegorier JP. Reduced hepatic fatty acid oxidation in fasting PPARα null mice is due to impaired mitochondrial hydroxymethylglutaryl-CoA synthase gene expression. FEBS Lett 2000;475:163-6.
22. Cherbuy C, Andrieux C, Honvo-Houeto E, et al. Expression of mitochondrial HMGCoA synthase and glutaminase in the colonic mucosa is modulated by bacterial species. Eur J Biochem 2004;271:87-95.
23. Hass R, Busche R, Luciano L, Reale E, Engelhardt WV. Lack of butyrate is associated with induction of Bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology 1997;112:875-81.
24. Hague A, Singh B, Paraskeva C. Butyrate acts as a survival factor for colonic epithelial cells: further fuel for the in vivo versus in vitro debate. Gastroenterology 1997;112:1036-40.
25. Heerdt BG, Houston MA, Augenlicht LH. Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res 1994;54:3288-94.
26. Jass JR. Diet, butyric acid and differentiation of gastrointestinal tract tumours. Med Hypotheses 1985;18:113-8.
27. Mariadason JM, Velcich A, Wilson AJ, Augenlicht LH, Gibson PR. Resistance to butyrate-induced cell differentiation and apoptosis during spontaneous Caco-2 cell differentiation. Gastroenterology 2001;120:889-99.
28. van de Wetering M, Sancho E, Verweij C, et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002;111:241-50.
29. Kim JW, Zeller KI, Wang Y, et al. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitaion assays. Mol Cell Biol 2004;24:5923-36.
30. Li F, Wang Y, Zeller KI, et al. Myc stimulates nuclearly encoded mitochondrial genes and mictochondrial biogenesis. Mol Cell Biol 2005;25:6225-34.
31. Riu E, Bosch F, Valera A. Prevention of diabetic alterations in transgenic mice overexpressing Myc in the liver. Proc Natl Acad Sci U S A 1996;93:2198-202.
32. Peukert K, Staller P, Schneider A, Carmichael G, Hanel F, Eilers M. An alternative pathway for gene regulation by Myc. EMBO J 1997;16:5672-86.
33. Staller P, Peukert K, Kiermaier A, et al. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol 2001;3:392-9.
34. Wanzel M, Herold S, Eilers M. Transcriptional repression by Myc. Trends Cell Biol 2003;13:146-50.
35. Gartel AL, Ye X, Goufman E, et al. Myc represses the p21 (WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proc Natl Acad Sci U S A 2001;98:4510-5.
36. Gartel AL, Shchors K. Mechanisms of c-myc-mediated transcriptional repression of growth arrest genes. Exp Cell Res 2003;283:17-21.
37. Luo Q, Li J, Cenkci B, Kretzner L. Autorepression of c-myc requires both initiator and E2F-binding site elements and cooperation with the p107 gene product. Oncogene 2004;23:1088-97.
38. Bowen H, Lapham A, Phillips E, et al. Characterization of the murine Nramp1 promoter: requirements for transactivation by Miz-1. J Biol Chem 2003;278:36017-26.
39. Ortiz JA, Gil-Gomez G, Casaroli-Marano RP, Vilaro S, Hegardt FG, Haro D. Transfection of the ketogenic mitochondrial 3-hydroxy-3-methylglutaryl-coenzyme A synthase cDNA into Mev-1 cells corrects their auxotrophy for mevalonate. J Biol Chem 1994;269:28523-6.
40. Adhikary S, Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 2005;6:635-45.
41. Ortiz JA, Mallolas J, Nicot C, et al. Isolation of pig mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene promoter: characterization of a peroxisome proliferator-responsive element. Biochem J 1999;337:329-35.
42. Zhu P, Martin E, Mengwasser J, Schlag P, Janssen KP, Gottlicher M. Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell 2004;5:455-63.
43. Fujiwara K, Ochiai M, Ohta T, et al. Global gene expression analysis of rat colon cancers induced by a food-borne carcinogen, 2-amino-1-methyl-6-phenyl- imidazo[4,5-b]pyridine. Carcinogenesis 2004;25:1495-505.
44. Asins G, Rosa JL, Serra D, et al. Gene expression of enzymes regulating ketogenesis and fatty acid metabolism in regenerating rat liver. Biochem J 1994;299:65-9.
45. Uehara Y, Engel T, Li Z, et al. Polyunsaturated fatty acids and acetoacetate downregulate the expression of the ATP-binding cassette transporter A1. Diabetes 2002;51:2922-8.
46. Jain SK, Kannan K, Lim G. Ketosis (acetoacetate) can generate oxygen radicals and cause increased lipid peroxidation and growth inhibition in human endothelial cells. Free Radic Biol Med 1998;25:1083-8.
47. Abdelmegeed MA, Kim SK, Woodcraft KJ, Novak RF. Acetoacetate activation of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in primary cultured rat hepatocytes: role of oxidative stress. J Pharmacol Exp Ther 2004;310:728-36.
48. Rodriguez JC, Ortiz JA, Hegardt FG, Haro D. Chicken ovalbumin upstream-promoter transcription factor (COUP-TF) could act as a transcriptional activator or repressor of the mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene. Biochem J 1997;326:587-92.
49. Vaque JP, Navascues J, Shiio Y, et al. Myc antagonizes Ras-mediated growth arrest in leukemia cells through the inhibition of the Ras-ERK-p21Cip1 pathway. J Biol Chem 2005;280:1112-22.
50. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1989.
51. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
52. Altomonte J, Richter A, Harbaran S, et al. Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. Am J Physiol Endocrinol Metab 2003;285:E718-28.