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PPAR Research
Volume 2010, Article ID 352957, 17 pages
http://dx.doi.org/10.1155/2010/352957
Research Article

The Peroxisomal 3-keto-acyl-CoA thiolase B Gene Expression Is under the Dual Control of PPARα and HNF4α in the Liver

1Centre de Recherche, INSERM U866, LBMN 6, Boulevard Gabriel, 21000 Dijon, France
2Laboratoire de Biochimie Métabolique et Nutritionnelle (LBMN), Faculté des Sciences Gabriel, Université de Bourgogne, 21000 Dijon, France
3INSERM U744, Laboratoire d'Épidémiologie et Santé Publique, Institut Pasteur de Lille, 1 Rue du Professeur Calmette, BP 245, 59019 Lille Cedex, France
4Laboratory of Metabolism, Division of Basic Sciences, National Cancer Institute, Bethesda, MD 20892, USA
5Lady Davis Institute for Medical Research, McGill University, 3755 Côte Ste. Catherine Road, Montreal, QC, Canada H3T 1E2
6Department of Cell Biology, Neurobiology and Anatomy, Medical College of Wisconsin, Milwaukee, WI 53226-0509, USA
7Laboratoire de Pharmacologie et Toxicologie, UR66, INRA, 31931, Toulouse, France

Received 24 June 2010; Revised 1 December 2010; Accepted 9 December 2010

Academic Editor: Sander Kersten

Copyright © 2010 J. Chamouton et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. J. A. Wanders, S. Ferdinandusse, P. Brites, and S. Kemp, “Peroxisomes, lipid metabolism and lipotoxicity,” Biochimica et Biophysica Acta, vol. 1801, no. 3, pp. 272–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. V. D. Antonenkov, P. P. Van Veldhoven, E. Waelkens, and G. P. Mannaerts, “Comparison of the stability and substrate specificity of purified peroxisomal 3-oxoacyl-CoA thiolases A and B from rat liver,” Biochimica et Biophysica Acta, vol. 1437, no. 2, pp. 136–141, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Chevillard, M. C. Clémencet, P. Etienne et al., “Molecular cloning, gene structure and expression profile of two mouse peroxisomal 3-ketoacyl-CoA thiolase genes,” BMC Biochemistry, vol. 5, pp. 1–13, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Chevillard, M. C. Clémencet, N. Latruffe, and V. Nicolas-Francès, “Targeted disruption of the peroxisomal thiolase B gene in mouse: a new model to study disorders related to peroxisomal lipid metabolism,” Biochimie, vol. 86, no. 11, pp. 849–856, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Arnauld, M. Fidaleo, M. C. Clémencet et al., “Modulation of the hepatic fatty acid pool in peroxisomal 3-ketoacyl-CoA thiolase B-null mice exposed to the selective PPARalpha agonist Wy14,643,” Biochimie, vol. 91, no. 11-12, pp. 1376–1386, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Mandard, M. Müller, and S. Kersten, “Peroxisome proliferator-activated receptor α target genes,” Cellular and Molecular Life Sciences, vol. 61, no. 4, pp. 393–416, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Kersten, S. Mandard, P. Escher et al., “The peroxisome proliferator-activated receptor α regulates amino acid metabolism,” FASEB Journal, vol. 15, no. 11, pp. 1971–1978, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Patsouris, S. Mandard, P. J. Voshol et al., “PPARalpha governs glycerol metabolism,” Journal of Clinical Investigation, vol. 114, no. 1, pp. 94–103, 2004. View at Google Scholar
  9. S. Mandard, F. Zandbergen, N. S. Tan et al., “The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment,” Journal of Biological Chemistry, vol. 279, no. 33, pp. 34411–34420, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Genolet, S. Kersten, O. Braissant et al., “Promoter rearrangements cause species-specific hepatic regulation of the glyoxylate reductase/hydroxypyruvate reductase gene by the peroxisome proliferator-activated receptor a,” The Journal of Biological Chemistry, vol. 280, no. 25, pp. 24143–24152, 2005. View at Publisher · View at Google Scholar
  11. L. Burri, G. H. Thoresen, and R. K. Berge, “The role of PPAR activation in liver and muscle,” PPAR Research, vol. 2010, Article ID 542359, 11 pages, 2010. View at Publisher · View at Google Scholar
  12. F. Hansmannel, M. C. Clémencet, C. Le Jossic-Corcos, T. Osumi, N. Latruffe, and V. Nicolas-Francés, “Functional characterization of a peroxisome proliferator response-element located in the intron 3 of rat peroxisomal thiolase B gene,” Biochemical and Biophysical Research Communications, vol. 311, no. 1, pp. 149–155, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Mandard, R. Stienstra, P. Escher et al., “Glycogen synthase 2 is a novel target gene of peroxisome proliferator-activated receptors,” Cellular and Molecular Life Sciences, vol. 64, no. 9, pp. 1145–1157, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Dongol, Y. Shah, I. Kim, F. J. Gonzalez, and M. C. Hunt, “The acyl-CoA thioesterase I is regulated by PPARα and HNF4α via a distal response element in the promoter,” Journal of Lipid Research, vol. 48, no. 8, pp. 1781–1791, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Nicolas-Frances, V. K. Dasari, E. Abruzzi, T. Osumi, and N. Latruffe, “The peroxisome proliferator response element (PPRE) present at positions -681/-669 in the rat liver 3-ketoacyl-CoA thiolase B gene functionally interacts differently with PPARα and HNF-4,” Biochemical and Biophysical Research Communications, vol. 269, no. 2, pp. 347–351, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. G. P. Hayhurst, Y. H. Lee, G. Lambert, J. M. Ward, and F. J. Gonzalez, “Hepatocyte nuclear factor 4α (Nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis,” Molecular and Cellular Biology, vol. 21, no. 4, pp. 1393–1403, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Shin, I. Kim, Y. Inoue, S. Kimura, and F. J. Gonzalez, “Regulation of mouse hepatic α-amino-β-carboxymuconate-ε-semialdehyde decarboxylase, a key enzyme in the tryptophan-nicotinamide adenine dinucleotide pathway, by hepatocyte nuclear factor 4α and peroxisome proliferator-activated receptor α,” Molecular Pharmacology, vol. 70, no. 4, pp. 1281–1290, 2006. View at Publisher · View at Google Scholar
  18. S. S. T. Lee, T. Pineau, J. Drago et al., “Targeted disruption of the α isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators,” Molecular and Cellular Biology, vol. 15, no. 6, pp. 3012–3022, 1995. View at Google Scholar · View at Scopus
  19. F. Parviz, C. Matullo, W. D. Garrison et al., “Hepatocyte nuclear factor 4α controls the development of a hepatic epithelium and liver morphogenesis,” Nature Genetics, vol. 34, no. 3, pp. 292–296, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Fourcade, S. Savary, S. Albet et al., “Fibrate induction of the adrenoleukodystrophy-related gene (ABCD2): promoter analysis and role of the peroxisome proliferator-activated receptor PPARα,” European Journal of Biochemistry, vol. 268, no. 12, pp. 3490–3500, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Bardot, M. C. Clemencet, P. Passilly, and N. Latruffe, “The analysis or modified peroxisome proliferator responsive elements of the peroxisomal bifunctional enzyme in transfected HepG2 cells reveals two regulatory motifs,” FEBS Letters, vol. 360, no. 2, pp. 183–186, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. D. G. Taylor, S. Haubenwallner, and T. Leff, “Characterization of a dominant negative mutant form of the HNF-4 orphan receptor,” Nucleic Acids Research, vol. 24, no. 15, pp. 2930–2935, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Oxombre, E. Moerman, J. Eeckhoute, P. Formstecher, and B. Laine, “Mutations in hepatocyte nuclear factor 4α (HNF4α) gene associated with diabetes result in greater loss of HNF4α function in pancreatic β-cells than in nonpancreatic β-cells and in reduced activation of the apolipoprotein CIII promoter in hepatic cells,” Journal of Molecular Medicine, vol. 80, no. 7, pp. 423–430, 2002. View at Publisher · View at Google Scholar
  24. P. Spegelaere, B. van Hille, N. Spruyt, S. Faisst, J. J. Cornelis, and J. Rommelaere, “Initiation of transcription from the minute virus of mice P4 promoter is stimulated in rat cells expressing a c-Ha-ras oncogene,” Journal of Virology, vol. 65, no. 9, pp. 4919–4928, 1991. View at Google Scholar · View at Scopus
  25. G. Denis, S. Mandard, C. Humblet et al., “Nuclear localization of a new c-cbl related protein, CARP 90, during in vivo thymic apoptosis in mice,” Cell Death and Differentiation, vol. 6, no. 7, pp. 689–697, 1999. View at Google Scholar · View at Scopus
  26. C. Gondcaille, M. Depreter, S. Fourcade et al., “Phenylbutyrate up-regulates the adrenoleukodystrophy-related as a nonclassical peroxisome proliferator,” Journal of Cell Biology, vol. 169, no. 1, pp. 93–104, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Miyazawa, T. Osumi, and T. Hashimoto, “The presence of a new 3-oxoacyl-CoA thiolase in rat liver peroxisomes,” European Journal of Biochemistry, vol. 103, no. 3, pp. 589–596, 1980. View at Google Scholar · View at Scopus
  28. A. Kassam, C. J. Winrow, F. Fernandez-Rachubinski, J. P. Capone, and R. A. Rachubinski, “The peroxisome proliferator response element of the gene encoding the peroxisomal β-oxidation enzyme enoyl-CoA hydratase/3-hydroxyacyl-CoA dehydrogenase is a target for constitutive androstane receptor β/9-cis-retinoic acid receptor-mediated transactivation,” Journal of Biological Chemistry, vol. 275, no. 6, pp. 4345–4350, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. C. J. Winrow, J. P. Capone, and R. A. Rachubinski, “Cross-talk between orphan nuclear hormone receptor RZRα and peroxisome proliferator-activated receptor α in regulation of the peroxisomal hydratase-dehydrogenase gene,” Journal of Biological Chemistry, vol. 273, no. 47, pp. 31442–31448, 1998. View at Publisher · View at Google Scholar
  30. M. Podvinec, M. R. Kaufmann, C. Handschin, and U. A. Meyer, “NUBIScan, an in silico approach for prediction of nuclear receptor response elements,” Molecular Endocrinology, vol. 16, no. 6, pp. 1269–1279, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Rakhshandehroo, B. Knoch, M. Müller, and S. Kersten, “Peroxisome proliferator-activated receptor alpha target genes,” PPAR Research, vol. 2010, Article ID 612089, 20 pages, 2010. View at Publisher · View at Google Scholar
  32. D. T. Odom, N. Zizlsperger, D. B. Gordon et al., “Control of pancreas and liver gene expression by HNF transcription factors,” Science, vol. 303, no. 5662, pp. 1378–1381, 2004. View at Google Scholar
  33. A. Ribeiro, D. Pastier, D. Kardassis, J. Chambaz, and P. Cardot, “Cooperative binding of upstream stimulatory factor and hepatic nuclear factor 4 drives the transcription of the human apolipoprotein A-II gene,” Journal of Biological Chemistry, vol. 274, no. 3, pp. 1216–1225, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Wen, R. Ringseis, and K. Eder, “Mouse OCTN2 is directly regulated by peroxisome proliferator-activated receptor α (PPARα) via a PPRE located in the first intron,” Biochemical Pharmacology, vol. 79, no. 5, pp. 768–776, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Bolotin, H. Liao, T. C. Ta et al., “Integrated approach for the identification of human hepatocyte nuclear factor 4α target genes using protein binding microarrays,” Hepatology, vol. 51, no. 2, pp. 642–653, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. C. J. Winrow, S. L. Marcus, K. S. Miyata, B. Zhang, J. P. Capone, and R. A. Rachubinski, “Transactivation of the peroxisome proliferator-activated receptor is differentially modulated by hepatocyte nuclear factor-4,” Gene Expression, vol. 4, no. 1-2, pp. 53–62, 1994. View at Google Scholar · View at Scopus
  37. G. Jiang, L. Nepomuceno, K. Hopkins, and F. M. Sladek, “Exclusive homodimerization of the orphan receptor hepatocyte nuclear factor 4 defines a new subclass of nuclear receptors,” Molecular and Cellular Biology, vol. 15, no. 9, pp. 5131–5143, 1995. View at Google Scholar · View at Scopus
  38. F. Zandbergen, S. Mandard, P. Escher et al., “The G/G switch gene 2 is a novel PPAR target gene,” Biochemical Journal, vol. 392, no. 2, pp. 313–324, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Stienstra, S. Mandard, N. S. Tan et al., “The Interleukin-1 receptor antagonist is a direct target gene of PPARα in liver,” Journal of Hepatology, vol. 46, no. 5, pp. 869–877, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Patsouris, J. K. Reddy, M. Müller, and S. Kersten, “Peroxisome proliferator-activated receptor α mediates the effects of high-fat diet on hepatic gene expression,” Endocrinology, vol. 147, no. 3, pp. 1508–1516, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Stienstra, S. Mandard, D. Patsouris, C. Maass, S. Kersten, and M. Müller, “Peroxisome proliferator-activated receptor alpha protects against obesity-induced hepatic inflammation,” Endocrinology, vol. 148, no. 6, pp. 2753–2763, 2007. View at Google Scholar
  42. Y. Okuno, M. Matsuda, H. Kobayashi et al., “Adipose expression of catalase is regulated via a novel remote PPARγ-responsive region,” Biochemical and Biophysical Research Communications, vol. 366, no. 3, pp. 698–704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. T. C. Aldridge, J. D. Tugwood, and S. Green, “Identification and characterization of DNA elements implicated in the regulation of CYP4A1 transcription,” Biochemical Journal, vol. 306, no. 2, pp. 473–479, 1995. View at Google Scholar · View at Scopus
  44. M. Heinäniemi, J. O. Uski, T. Degenhardt, and C. Carlberg, “Meta-analysis of primary target genes of peroxisome proliferator-activated receptors,” Genome Biology, vol. 8, no. 7, article R147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Lopez, R. B. Irby, and M. P. McLean, “Peroxisome proliferator-activated receptor α induces rat sterol carrier protein x promoter activity through two peroxisome proliferator-response elements,” Molecular and Cellular Endocrinology, vol. 205, no. 1-2, pp. 169–184, 2003. View at Publisher · View at Google Scholar
  46. T. Hu, P. Foxworthy, A. Siesky et al., “Hepatic peroxisomal fatty acid β-oxidation is regulated by liver X receptor α,” Endocrinology, vol. 146, no. 12, pp. 5380–5387, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. K. A. R. Tobin, H. H. Steineger, S. Albert et al., “Cross-talk between fatty acid and cholesterol metabolism mediated by liver X receptor-α,” Molecular Endocrinology, vol. 14, no. 5, pp. 741–752, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. C. M. Klinge, D. L. Bodenner, D. Desai, R. M. Niles, and A. M. Traish, “Binding of type II nuclear receptors and estrogen receptor to full and half-site estrogen response elements in vitro,” Nucleic Acids Research, vol. 25, no. 10, pp. 1903–1912, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Juge-Aubry, A. Pernin, T. Favez et al., “DNA binding properties of peroxisome proliferator-activated receptor subtypes on various natural peroxisome proliferator response elements: importance of the 5'-flanking region,” Journal of Biological Chemistry, vol. 272, no. 40, pp. 25252–25259, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Nakshatri and P. Bhat-Nakshatri, “Multiple parameters determine the specificity of transcriptional response by nuclear receptors HNF-4, ARP-1, PPAR, RAR and RXR through common response elements,” Nucleic Acids Research, vol. 26, no. 10, pp. 2491–2499, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bugge, M. Siersbæk, M. S. Madsen, A. Göndör, C. Rougier, and S. Mandrup, “A novel intronic peroxisome proliferator-activated receptor γ enhancer in the Uncoupling Protein (UCP) 3 gene as a regulator of both UCP2 and -3 expression in adipocytes,” Journal of Biological Chemistry, vol. 285, no. 23, pp. 17310–17317, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. C. P. Martinez-Jimenez, I. Kyrmizi, P. Cardot, F. J. Gonzalez, and I. Talianidis, “Hepatocyte nuclear factor 4α coordinates a transcription factor network regulating hepatic fatty acid metabolism,” Molecular and Cellular Biology, vol. 30, no. 3, pp. 565–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Yamamoto, H. Shimano, Y. Nakagawa et al., “SREBP-1 interacts with hepatocyte nuclear factor-4α and interferes with PGC-1 recruitment to suppress hepatic gluconeogenic genes,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 12027–12035, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Misawa, T. Horiba, N. Arimura et al., “Sterol regulatory element-binding protein-2 interacts with hepatocyte nuclear factor-4 to enhance sterol isomerase gene expression in hepatocytes,” Journal of Biological Chemistry, vol. 278, no. 38, pp. 36176–36182, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Nishiyama, R. Hi, S. Osada, and T. Osumi, “Functional interactions between nuclear receptors recognizing a common sequence element, the direct repeat motif spaced by one nucleotide (DR-1),” Journal of Biochemistry, vol. 123, no. 6, pp. 1174–1179, 1998. View at Google Scholar · View at Scopus
  56. P. Rollini and R. E. K. Fournier, “The HNF-4/HNF-1α transactivation cascade regulates gene activity and chromatin structure of the human serine protease inhibitor gene cluster at 14q32.1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 18, pp. 10308–10313, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. M. G. Holloway, G. D. Miles, A. A. Dombkowski, and D. J. Waxman, “Liver-specific hepatocyte nuclear factor-4α deficiency: greater impact on gene expression in male than in female mouse liver,” Molecular Endocrinology, vol. 22, no. 5, pp. 1274–1286, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Palanker, J. M. Tennessen, G. Lam, and C. S. Thummel, “Drosophila HNF4 regulates lipid mobilization and β-oxidation,” Cell Metabolism, vol. 9, no. 3, pp. 228–239, 2009. View at Publisher · View at Google Scholar · View at Scopus