Abstract
This paper reviews aspects concerning the genetic regulation of the expression of the well studied peroxisomal genes including those of fatty acid β‐oxidation enzymes; acyl‐CoA oxidase, multifunctional enzyme and thiolase from different tissues and species. An important statement is PPARα, which is now long known to be in rodents the key nuclear receptor orchestrating liver peroxisome proliferation and enhanced peroxisomal β‐oxidation, does not appear to control so strongly in man the expression of genes involved in peroxisomal fatty acid β‐oxidation related enzymes. In this respect, the present review strengthens among others the emerging concept that, in the humans, the main genes whose expression is up‐regulated by PPARα are mitochondrial and less peroxisomal genes. A special emphasis is also made on the animal cold adaptation and on need for sustained study of peroxisomal enzymes and genes; challenging that some essential roles of peroxisomes in cell function and regulation still remain to be discovered.
Keywords: peroxisome, gene, β‐oxidation, biogenesis, PPAR, fibrates, fatty acids, hormones
References
- 1. Roels F., Baes M., De Bie S, Peroxisomal disorders and regulation of genes, Kluwer Academic Plenum Press, 2003, in press. [Google Scholar]
- 2. Issemann I., Green S., Activation of a member of the steroid hormone superfamily by peroxisome proliferators, Nature, 347: 645–650, 1990. [DOI] [PubMed] [Google Scholar]
- 3. Reddy J.K., Hashimoto T., Peroxisomal β‐oxidation and Peroxisome Proliferator‐Activated Receptors α: an adaptative metabolic system, Ann. Rev. Nutr., 21: 193–230, 2001. [DOI] [PubMed] [Google Scholar]
- 4. Ferdinandusse S., Denis S., Mooijer P.A., Zhang Z., Reddy J.K., Spector A.A., Wanders R.J., Identification of the peroxisomal beta‐oxidation enzymes involved in the biosynthesis of docosahexaenic acid, J. Lipid Res., 42: 1987–1995, 2001. [PubMed] [Google Scholar]
- 5. Stolz D.B., Zamora R., Vodovotz Y., Loughran P.A., Billiar T.R., Kim Y.M., Simmons R.L., Watkins S.C., Peroxisomal localization of inducible nitric oxide synthase in hepatocytes, Hepatology, 36: 81–93, 2002. [DOI] [PubMed] [Google Scholar]
- 6. Chang C.C., South S., Warren D., Jones J., Moser A.B., Moser H.W., Gould S.J., Metabolic control of peroxisome abundance, J. Cell Sci., 112: 1579–1590, 1999. [DOI] [PubMed] [Google Scholar]
- 7. Latruffe N., Vamecq J., Evolutionary aspects of peroxisomes as cell organelles and genes encoding peroxisomal proteins, Biol. Cell, 92: 389–395, 2000. [DOI] [PubMed] [Google Scholar]
- 8. Petriv O.I., Pilgrim D.B., Rachubinski R.A., Titorenko V.I., RNA interference of peroxisome‐related genes in C. elegans: a new model for human peroxisomal disorders, Physiol. Genomics, 10: 79–91, 2002. [DOI] [PubMed] [Google Scholar]
- 9. Berteaux‐Lecellier V., Picard M., Thompson‐Coffe C., Zickler D., Panvier‐Adoutte A., Simonet J.M., A nonmammalian homolog of the PAF1 gene (Zellweger syndrome) discovered as a gene involved in caryogamy in the fungus Podospora anserina, Cell, 81: 1043–1051, 1995. [DOI] [PubMed] [Google Scholar]
- 10. Liu L.X., Janvier K., Berteaux‐Lecellier V., Cartier N., Benarous R., Aubourg P., Homo‐ and heterodimerization of peroxisomal ATP‐binding cassette half‐transporters, J. Biol. Chem., 274: 32738–32743, 1999. [DOI] [PubMed] [Google Scholar]
- 11. Duclos S., Bride J., Ramirez L.C., Bournot P., Peroxisome proliferation and beta‐oxidation in Fao and MH1C1 rat hepatoma cells, HepG2 human hepatoblastoma cells and cultured human hepatocytes: effect of ciprofibrate, Eur. J. Cell Biol., 72: 314–323, 1997. [PubMed] [Google Scholar]
- 12. El Kebbaj M.S., Malki M.C., Latruffe N., Properties of peroxisomes from jerboa (Jaculus orientalis), Eur. J. Cell Biol., 70: 150–156, 1996. [PubMed] [Google Scholar]
- 13. Kabine M., Cherkaoui‐Malki M., Clémencet M.‐C., El Kebbaj M.S. and Latruffe N., Peroxisomal Changes During Hibernation of Jerboa (Jaculus orientalis), J. Am. Oil Chem. Soc., 75: 275–280, 1998. [Google Scholar]
- 14. Cimini A., Cristiano L., Bernardo A., Farioli‐Vecchioli S., Stefanini S., Ceru M.P., Presence and inducibility of peroxisomes in a human glioblastoma cell line, Biochim. Biophys. Acta., 1474: 397–409, 2000. [DOI] [PubMed] [Google Scholar]
- 15. Kobayashi T, Shinnoh N, Kondo A, Yamada T. Adrenoleukodystrophy protein‐deficient mice represent abnormality of very long chain fatty acid metabolism, Biochem. Biophys. Res. Commun., 232: 631–636, 1997. [DOI] [PubMed] [Google Scholar]
- 16. Fan C‐Y., Pan J., Chu R., Lee D., Kluckman K.D., Usuda N., Singh I., Yeldandi A.V., Rao M.S., Maeda N., Reddy J.K., Hepatocellular and hepatic peroxisomal alterations in mice with a disrupted peroxisomal fatty acylcoenzyme A oxidase gene, J. Biol. Chem., 271: 24689–24710, 1996. [DOI] [PubMed] [Google Scholar]
- 17. Qi Q., Zhu Y., Pan J., Usuda N., Maeda N., Yeldandi A.V., Rao M.S., Hashimoto T., Reddy J.K., Absence of spontaneous peroxisome proliferation in enoyl‐CoA hydratase/L‐3‐hydroxyacyl‐CoA dehydrogenase‐deficient mouse liver. Further support for the role of fatty acyl CoA oxidase in PPARα ligand metabolism, J. Biol. Chem., 274: 15775–15780, 1999. [DOI] [PubMed] [Google Scholar]
- 18. Baes M., Huyghe S., Cameliet P., Declercq P.E., Collen D., Mannaerts G.P., Van Veldhoven P.P., Inactivation of the peroxisomal multifunctional protein‐2 in mice impedes the degradation of not only 2‐methyl‐branched fatty acids and bile acid intermediates but also very long chain fatty acids, J. Biol. Chem., 275: 16329–16336, 2000. [DOI] [PubMed] [Google Scholar]
- 19. Seedorf U., Raabe M., Ellinghaus P., Kannenberg F., Fobker M., Engel T., Denis S., Wouters F., Wirtz K.W., Wanders R.J.A., Defective peroxisomal catabolism of branched fatty acyl coenzyme A in mice lacking the sterol carrier protein2/sterol carrier protein‐x gene function, Genes Dev., 12: 1189–1201, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Lee S.S.T., Pineau T., Drago J., Lee E.J., Owens J.W., Kroetz D.I., Fernandez‐Salguero P.M., Westphal H., Gonzalez F.J., Targeted disruption of the α isoform of the peroxisome proliferator‐activated receptor gene in mice results in abolishement of the pleiotropic effect of peroxisome proliferators, Mol. Cell. Biol., 15: 312–322, 1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Michalik L, Desvergne B, Tan NS, Basu‐Modak S, Escher P, Rieusset J, Peters JM, Kaya G, Gonzalez FJ, Zakany J, Metzger D, Chambon P, Duboule D, Wahli W. Impaired skin wound healing in peroxisome proliferator‐activated receptor (PPAR)alpha and PPARbeta mutant mice, J. Cell Biol., 154: 799–814, 2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Akiyama T.E., Sakai S., Lambert G., Nicol C.J., Matsusue K., Pimp S., Lee Y.H., Ricote M., Glass C.K., Brewer H.B., Gonzalez F.J., Conditional disruption of the peroxisome proliferator‐activated receptor gamma gene in mice results in lowered expression of ABCA1, ABCG1, and apoE in macrophages and reduced cholesterol efflux, Mol. Cell Biol., 22: 2607–2619, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Baes M., Gressens P., Baumgart E., Carmeliet P., Casteels M., Fransen M., Evrard P., Fahimi D., Declercq P, Collen D., et al, A mouse model for Zellweger syndrome, Nature Genet., 17: 49–56, 1997. [DOI] [PubMed] [Google Scholar]
- 24. Faust PL, Hatten ME. Targeted deletion of the PEX2 peroxisome assembly gene in mice provides a model for Zellweger syndrome, a human neuronal migration disorder, J. Cell Biol., 139: 1293–1305, 1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Baes M, Dewerchin M, Janssen A, Collen D, Carmeliet P. Generation of Pex5‐loxP mice allowing the conditional elimination of peroxisomes, Genesis, 32: 177–178, 2002. [DOI] [PubMed] [Google Scholar]
- 26. Bjorkman J, Tonks I, Maxwell MA, Paterson C, Kay GF, Crane DI. Conditional inactivation of the peroxisome biogenesis Pex13 gene by Cre‐loxP excision, Genesis, 32: 179–80, 2002. [DOI] [PubMed] [Google Scholar]
- 27. Nilakatan V., LIX. , Glauert H.P., Spear B.T., Increased liver‐specific catalase activty in transgenic mice, DNA and Cell Biology, 15: 625–630, 1996. [DOI] [PubMed] [Google Scholar]
- 28. Kiema T.R., Taskinen J.P., Pirila P.L., Koivuranta K.T., Wierenga R.K., Hiltunen J.K., Organization of the multifunctional enzyme type 1: interaction between N‐and C‐terminal domains is required for the hydratase1/isomerase activity, Biochem. J., 367: 433–441, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Cherkaoui‐Malki M., Meyer K., Cao W.Q., Latruffe N., Yeldandi A.V., Rao M.S., Bradfield C.A., Reddy J.K., Identification of novel peroxisome proliferator‐activated receptor alpha (PPARalpha) target genes in mouse liver using cDNA microarray analysis, Gene Expr., 9: 291–304, 2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Zipper J., Proliferation of myocardial peroxisomes caused by several agents and conditions, J. Mol. Cell Cardiol., 29: 149–161, 1997. [DOI] [PubMed] [Google Scholar]
- 31. Fan C.Y., Pan L., Usuda N., Yeldandi A.V., Rao M.S., Reddy J.K., Steatohepatitis, spontaneaous peroxisome proliferation and liver tumors in mice lacking peroxisomal fatty acyl‐CoA oxidase, J. Biol. Chem., 273: 15639–15645, 1998. [DOI] [PubMed] [Google Scholar]
- 32. Tobin K.A., Steineger H.H., Alberti S., Spydevold O., Auwerx J., Gustafsson J.A., Nebb H.I., Cross‐talk between fatty acid and cholesterol metabolism mediated by liver X receptor‐alpha, Mol. Endocrinol., 14: 741–752, 2000. [DOI] [PubMed] [Google Scholar]
- 33. Chao P.M., Chao C.Y., Lin F.J., Huang C., Oxidized frying oil up‐regulates hepatic acyl‐CoA oxidase and cytochrome P450 4 A1 genes in rats and activates PPARalpha, J. Nutr., 131: 3166–3174, 2001. [DOI] [PubMed] [Google Scholar]
- 34. Moya‐Camarena S.Y., Vanden Heuvel J.P., Blanchard S.G., Leesnitzer L.A., Belury M.A., Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARalpha, J. Lipid Res., 40: 1426–1433, 1999. [PubMed] [Google Scholar]
- 35. Zomer A.W., van Der Burg B., Jansen G.A., Wanders R.J., Poll‐The B.T., van Der Saag P.T., Pristanic acid and phytanic acid: naturally occurring ligands for the nuclear receptor peroxisome proliferator‐activated receptor alpha, J. Lipid Res., 41: 1801–1807, 2000. [PubMed] [Google Scholar]
- 36. Vamecq J., Latruffe N., Medical significance of peroxisome proliferator‐activated receptors, Lancet, 354(9173): 141–148, 1999. [DOI] [PubMed] [Google Scholar]
- 37. Kabine M., Clémencet M.‐C., El Kebbaj M.S. and Latruffe N, Cherkaoui‐Malki M. Changes of peroxisomal fatty acid metabolism during cold acclimatization in hibernating Jerboa (jaculus orientalis), Biochimie (in press), 2003. [DOI] [PubMed] [Google Scholar]
- 38. Goglia F., Liverini G., Lanni A., Iossa S., Barletta A., Morphological and functional modifications of rat liver peroxisomal subpopulations during cold expusure, Exp. Biol., 48: 127–133, 1989. [PubMed] [Google Scholar]
- 39. Xia T., Mostafa N., Bhat B.G., Florant G.L., Coleman R.A., Selective retention of essential fatty acids: the role of hepatic monoacylglycerol acyltranferase, Am. J. Physiol., 265: 414–419, 1993. [DOI] [PubMed] [Google Scholar]
- 40. Nedergaard J., Alexon S., Cannon B., Cold adaptation in the rat: increased brown fat peroxisomal β‐oxidation related to maximal mitochondrial oxidative capacity, Am. J. Physiol., 239: C208–C216, 1980. [DOI] [PubMed] [Google Scholar]
- 41. Guardiola‐Diaz H.M., Rehnmark S., Usuda N., Albrektsen T., Feltkamp D., Gustafsson J.A., Alexson S.E., Rat peroxisome proliferator‐activated receptors and brown adipose tissue function during cold acclimatization, J. Biol. Chem., 274: 23368–23377, 1999. [DOI] [PubMed] [Google Scholar]
- 42. Yu S., Cao W‐Q., Kashireddy P., Meyer K., Jia Y., Hughes D.E., Tan Y., Feng J., Yeldandi A.V., Rao M.S., Costa R.H., Gonzalez F.J., Reddy J.K., Human peroxisome proliferator‐activated receptor α (PPARα) supports the induction of peroxisome proliferation in PPARa‐deficient mouse liver, J. Biol. Chem., 276: 42485–42491, 2001. [DOI] [PubMed] [Google Scholar]
- 43. Hsu M.H., Savas U., Griffin K.J., Johnson E.F., Identification of peroxisome proliferator‐responsive human genes by elevated expression of the peroxisome proliferator‐activated receptor alpha in HepG2 cells, J. Biol. Chem., 276: 27950–27958, 2001. [DOI] [PubMed] [Google Scholar]
- 44. Lawrence J.W., Li Y., Chen S., DeLuca J.G., Berger J.P., Umbenhauer D.R., Moller D.E., Zhou G., Differential gene regulation in human versus rodent hepatocytes by peroxisome proliferator‐activated receptor (PPAR) alpha. PPAR alpha fails to induce peroxisome proliferation‐associated genes in human cells independently of the level of receptor expresson, J. Biol. Chem., 276: 31521–31527, 2001. [DOI] [PubMed] [Google Scholar]
- 45. Mascaro C., Acosta E., Ortiz J.A., Marrero P.F., Hegardt F.G., Haro D., Control of human muscle‐type carnitine palmitoyltransferase I gene transcription by peroxisome proliferator‐activated receptor, J. Biol. Chem., 273: 8560–8563, 1998. [DOI] [PubMed] [Google Scholar]
- 46. Zhang X., Chen L., Hardwick J.P., Promoter activity and regulation of the CYP4F2 leukotriene B(4) omegahydroxylase gene by peroxisomal proliferators and retinoic acid in HepG2 cells, Arch. Biochem. Biophys., 378: 364–376, 2000. [DOI] [PubMed] [Google Scholar]
- 47. Chu R., Madison L.D., Lin Y., Kopp P., Rao M.S., Jameson J.L., Reddy J.K., Thyroid hormone (T3) inhibits ciprofibrate‐induced transcription of genes encoding beta‐oxidation enzymes: cross talk between peroxisome proliferator and T3 signaling pathways, Proc. Natl. Acad. Sci. USA, 92: 11593–11597, 1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Miyata K.S., McCaw S.E., Patel H.V., Rachubinski R.A., Capone J.P., The orphan nuclear hormone receptor LXR alpha interacts with the peroxisome proliferator‐activated receptor and inhibits peroxisome proliferator signaling, J. Biol. Chem., 271: 9189–9192, 1996. [DOI] [PubMed] [Google Scholar]
- 49. Sinal C.J., Yoon M., Gonzalez F.J., Antagonism of the actions of peroxisome proliferator‐activated receptor‐alpha by bile acids, J. Biol. Chem., 276: 47154–47162, 2001. [DOI] [PubMed] [Google Scholar]
- 50. Kassam A., Winrow C.J., Fernandez‐Rachubinski F., Capone J.P., Rachubinski R.A., The peroxisome proliferator response element of the gene encoding the peroxisomal beta‐oxidation enzyme enoyl‐CoA hydratase/3‐hydroxyacyl‐CoA dehydrogenase is a target for constitutive androstane receptor beta/9‐cis‐retinoic acid receptor‐mediated transactivation, J. Biol. Chem., 275: 4345–4350, 2000. [DOI] [PubMed] [Google Scholar]
- 51. Shy Y., Hon M., Evans R.M., The peroxisome proliferator‐activated receptor delta, an integrator of transcriptional repression and nuclear receptor signaling, Proc. Natl. Acad. Sci. USA, 99: 2613–2618, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52. Kassam A., Capone J.P., Rachubinski R.A., The short heterodimer partner receptor differentially modulates peroxisome proliferator‐activated receptor alpha‐mediated transcription from the peroxisome proliferator‐response elements of the genes encoding the peroxisomal beta‐oxidation enzymes acyl‐CoA oxidase and hydratase‐dehydrogenase, Mol. Cell Endocrinol., 176: 49–56, 2001. [DOI] [PubMed] [Google Scholar]
- 53. Zhou Y.C., Davey H.W., McLachlan M.J., Xie T., Waxman D.J., Elevated basal expression of liver peroxisomal beta‐oxidation enzymes and CYP4A microsomal fatty acid omega‐hydroxylase in STAT5b(‐/‐) mice: cross‐talk in vivo between peroxisome proliferator‐activated receptor and signal transducer and activator of transcription signaling pathways, Toxicol. Appl. Pharmacol., 182: 1–10, 2002. [DOI] [PubMed] [Google Scholar]
- 54. Miyata K.S., McCaw S.E., Meertens L.M., Patel H.V., Rachubinski R.A., Capone J.P., Receptor‐interacting protein 140 interacts with and inhibits transactivation by, peroxisome proliferator‐activated receptor alpha and liver‐X‐receptor alpha, Mol. Cell Endocrinol., 146: 69–76, 1998. [DOI] [PubMed] [Google Scholar]
- 55. Mochizuki K., Suruga K., Sakaguchi N., Takase S., Goda T., Major intestinal coactivator p300 strongly activates peroxisome proliferator‐activated receptor in intestinal cell line, Caco‐2, Gene, 291: 271–277, 2002. [DOI] [PubMed] [Google Scholar]
- 56. Surapureddi S., Yu S., Bu H., Hashimoto T., Yeldandi A.V., Kashireddy P., Cherkaoui‐Malki M., Qi C., Zhu Y.J., Rao M.S., Reddy J.K., Identification of a transcriptionally active peroxisome proliferator‐activated receptor alpha ‐interacting cofactor complex in rat liver and characterization of PRIC285 as a coactivator, Proc. Natl. Acad. Sci. USA, 99: 11836–11841, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57. Latruffe N., Cherkaoui‐Malki M., Nicolas‐Frances V., Clemencet M.C., Jannin B., Berlot J.P., Regulation of the peroxisomal beta‐oxidation‐dependent pathway by peroxisome proliferator‐activated receptor alpha and kinases, Biochem Pharmacol., 60: 1027–1032, 2000. [DOI] [PubMed] [Google Scholar]
- 58. Lazennec G., Canaple L., Saugy D., Wahli W., Activation of peroxisome proliferator‐activated receptors (PPARs) by their ligands and protein kinase A activators, Mol. Endocrinol., 14: 1962–1975, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Barger P.M., Browning A.C., Garner A.N., Kelly DP., p38 mitogen‐activated protein kinase activates peroxisome proliferator‐activated receptor alpha: a potential role in the cardiac metabolic stress response, J. Biol. Chem., 276: 44495–44501, 2001. [DOI] [PubMed] [Google Scholar]
- 60. Beier K., Volkl A., Fahimi H.D., TNF‐alpha downregulates the peroxisome proliferator activated receptor‐alpha and the mRNAs encoding peroxisomal proteins in rat liver, FEBS Lett., 412: 385–387, 1997. [DOI] [PubMed] [Google Scholar]
- 61. Meertens L.M., Miyata K.S., Cechetto J.D., Rachubinski R.A., Capone J.P., A mitochondrial ketogenic enzyme regulates its gene expression by association with the nuclear hormone receptor PPARalpha, EMBO J., 17: 6972–6978, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Juge‐Aubry C.E., Kuenzli S., Sanchez J.C., Hochstrasser D., Meier C.A., Peroxisomal bifunctional enzyme binds and activates the activation function‐1 region of the peroxisome proliferator‐activated receptor alpha, Biochem J., 353: 253–258, 2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63. Tan N.S., Shaw N.S., Vinkenbosch N., Yasmin R., Desvergne B., Walhi W., Noy N., Selective cooperation between fatty acid binding protein and peroxisome proliferator‐activated receptor in regulating transcription, Mol. Cell Biol., 22: 5114–5127, 2002, and Mol. Cell Biol., 22: 6318, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Powers J.M., Moser H.W., Peroxisomal disorders: genotype, phenotype, major neuropathologic lesions, and pathogenesis, Brain Pathol., 8: 101–120, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65. Wanders R.J.A., Vreken P., Ferdinandusse S., Janssen G.A., Waterham H.R., Van Roermund C.W.T. and Van Grunsven E.G. Peroxisomal fatty acid α‐ and β‐oxidation in humans: enzymology, peroxisomal metabolite transporters and peroxisomal diseases, Biochem. Soc. Trans., 29(Part 2): 250–267, 2001. [DOI] [PubMed] [Google Scholar]
- 66. Fourcade S., Savary S. Gondcaille C., Berger J., Netik A., Cadepond F., El Etr M., Molzer B., Bugaut M. Thyroid hormone induction of the ABCD2 gene: prospect of a therapy for X‐linked adrenoleukodystrophy, Mol. Pharmacol., 63: 1296–1303, 2003. [DOI] [PubMed] [Google Scholar]
- 67. Caira F., Clemencet M‐C., Cherkaoui‐Malki M., Dieuaide‐Noubhani M., Pacot C., Van Veldhoven P.P., Latruffe N., Differential regulation by a peroxisome proliferator of the different multifunctional proteins in guinea pig: cDNA cloning of the guinea pig D‐specific multifunctional protein 2, Biochem. J., 330: 1361–1368, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68. Motojima K., Passilly P., Peters J.M., Gonzalez F.J., Latruffe N., Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator‐activated receptor alpha and gamma activators in a tissue ‐ and inducer‐specific manner, J. Biol. Chem., 273: 16710–16714, 1998. [DOI] [PubMed] [Google Scholar]
- 69. Le Jossic‐Corcos C., Bournot P., Regulation of farnesyl pyrophosphate synthase gene expression by fatty acids in “Peroxisomal Disorders and Regulation of Genes” (Roels F., De Baes M., De Bie S. eds) Kluwer Academic Plenum press; (in preparation), 2003. [Google Scholar]
- 70. Nicolas‐Frances V., Dasari V.K., Abruzzi E., Osumi T., Latruffe N., 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 PPARalpha and HNF‐4, Biochem. Biophys. Res. Commun., 269: 347–351, 2000. [DOI] [PubMed] [Google Scholar]