Transcription of the human uncoupling protein 3 gene is governed by a complex interplay between the promoter and intronic sequences

Diabetologia

Volumn 52, Issue 8, 2009, Pages 1638-1646

  Girousse, A ^a,b   Tavernier, G ^a,b,e   Tiraby, C ^a,b   Lichtenstein, L ^a,b   Iacovoni, J S ^a,b   Mairal, A ^a,b   Villarroya, F ^c,d   Langin, D ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF BARCELONA   (Spain)

^d Instituto de Salud Carlos III   (Spain)

^e TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

Diabetes; Fasting; Regulatory sequences; Transgenic; UCP3; Uncoupling protein

Indexed keywords

CIS ACTING ELEMENT; FATTY ACID; MESSENGER RNA; THYROID HORMONE; UNCOUPLING PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DIET RESTRICTION; ENERGY; FAST MUSCLE; FATTY ACID METABOLISM; GENE; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; INSULIN SENSITIVITY; INTRON; MITOCHONDRIAL MEMBRANE; MOLECULAR BIOLOGY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REGULATORY SEQUENCE; REPORTER GENE; SKELETAL MUSCLE; TRANSGENIC MOUSE; UCP GENE;

ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; HUMANS; INSULIN; INTRONS; ION CHANNELS; MICE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 67650682553     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-009-1385-9     Document Type: Article

References (42)

1. D Ricquier F Bouillaud 2000 The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP Biochem J 345 161 179 (Pubitemid 30077154)
2. S Krauss CY Zhang BB Lowell 2005 The mitochondrial uncoupling-protein homologues Nat Rev Mol Cell Biol 6 248 261 (Pubitemid 40314925)
3. MD Brand TC Esteves 2005 Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3 Cell Metab 2 85 93
4. MKC Hesselink HA Keizer LB Borghouts 2001 Protein expression of UCP3 differs between human type 1, type 2a, and type 2b fibers FASEB J 15 1071 1073
5. AJ Vidal-Puig D Grujic C-Y Zhang 2000 Energy metabolism in uncoupling protein 3 gene knockout mice J Biol Chem 275 16258 16266 (Pubitemid 30366939)
6. P Schrauwen J Hoeks MK Hesselink 2006 Putative function and physiological relevance of the mitochondrial uncoupling protein-3: involvement in fatty acid metabolism? Prog Lipid Res 45 17 41 (Pubitemid 43170803)
7. V Bezaire EL Seifert ME Harper 2007 Uncoupling protein-3: clues in an ongoing mitochondrial mystery Faseb J 21 312 324 (Pubitemid 46213479)
8. C Garcia-Martinez B Sibille G Solanes 2001 Overexpression of UCP3 in cultured human muscle lowers mitochondrial membrane potential, raises ATP/ADP ratio, and favors fatty acid versus glucose oxidation FASEB J 15 2003 2035
9. CS Choi JJ Fillmore JK Kim 2007 Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance J Clin Invest 117 1995 2003 (Pubitemid 47036334)
10. C Tiraby G Tavernier F Capel 2007 Resistance to high-fat-diet-induced obesity and sexual dimorphism in the metabolic responses of transgenic mice with moderate uncoupling protein 3 overexpression in glycolytic skeletal muscles Diabetologia 50 2190 2199 (Pubitemid 47373849)
11. SR Costford SN Chaudhry SA Crawford M Salkhordeh ME Harper 2008 Long-term high-fat feeding induces greater fat storage in mice lacking UCP3 Am J Physiol Endocrinol Metab 295 E1018 E1024
12. N Guigal M Rodriguez RN Cooper 2002 Uncoupling protein-3 (UCP3) mRNA expression in reconstituted human muscle after myoblast transplantation in RAG2-/-/gamma c/C5- immunodeficient mice J Biol Chem 277 47407 47411 (Pubitemid 36159256)
13. L Millet H Vidal F Andreelli 1997 Increased uncoupling protein-2 and -3 mRNA expression during fasting in obese and lean humans J Clin Invest 100 2665 2670 (Pubitemid 28007533)
14. DW Gong Y He M Karas M Reitman 1997 Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin J Biol Chem 272 24129 24132 (Pubitemid 27418606)
15. N Pedraza M Rosell J Villarroya 2006 Developmental and tissue-specific involvement of peroxisome proliferator-activated receptor-alpha in the control of mouse uncoupling protein-3 gene expression Endocrinology 147 4695 4704 (Pubitemid 44402177)
16. S Larkin E Mull W Miao 1997 Regulation of the third member of the uncoupling protein family UCP3 by cold and thyroid hormone Biochem Biophys Res Commun 240 222 227 (Pubitemid 27503779)
17. P Barbe D Larrouy C Boulanger 2001 Triiodothyronine-mediated upregulation of UCP2 and UCP3 gene expression in human skeletal muscle without coordinated induction of mitochondrial respiratory chain genes FASEB J 15 13 15
18. G Solanes A Vidal-Puig D Grujic JS Flier BB Lowell 1997 The human uncoupling protein-3 gene. Genomic structure, chromosomal localization, and genetic basis for short and long form transcripts J Biol Chem 272 25433 25436 (Pubitemid 27438845)
19. A Acín M Rodriguez H Rique E Canet JA Boutin J-P Galizzi 1999 Cloning and characterization of the 5? flanking region of the human uncoupling protein 3 (UCP3) gene Biochem Biophys Res Commun 258 278 283 (Pubitemid 29287042)
20. G Solanes N Pedraza R Iglesias M Giralt F Villarroya 2000 The human uncoupling protein-3 gene promoter requires MyoD and is induced by retinoic acid in muscle cells FASEB J 14 2141 2143 (Pubitemid 30843907)
21. G Solanes N Pedraza R Iglesias M Giralt F Villarroya 2003 Functional relationship between MyoD and peroxisome proliferator-activated receptor-dependent regulatory pathways in the control of the human uncoupling protein-3 gene transcription Mol Endocrinol 17 1944 1958 (Pubitemid 37281788)
22. G Solanes N Pedraza V Calvo A Vidal-Puig BB Lowell F Villarroya 2005 Thyroid hormones directly activate the expression of the human and mouse uncoupling protein-3 genes through a thyroid response element in the proximal promoter region Biochem J 386 505 513 (Pubitemid 40445875)
23. PG Cassell PJ Saker SJ Huxtable 2000 Evidence that single nucleotide polymorphism in the uncoupling protein 3 (UCP3) gene influences fat distribution in women of European and Asian origin Diabetologia 43 1558 1564 (Pubitemid 32734864)
24. DR Gable JW Stephens JA Cooper GJ Miller SE Humphries 2006 Variation in the UCP2-UCP3 gene cluster predicts the development of type 2 diabetes in healthy middle-aged men Diabetes 55 1504 1511 (Pubitemid 44195394)
25. S Otabe K Clement C Dina 2000 A genetic variation in the 5? flanking region of the UCP3 gene is associated with body mass index in humans in interaction with physical activity Diabetologia 43 245 249 (Pubitemid 30126832)
26. R Blaise J Grober P Rouet G Tavernier D Daegelen D Langin 1999 Testis expression of hormone-sensitive lipase is conferred by a specific promoter that contains four regions binding testicular nuclear proteins J Biol Chem 274 9327 9334
27. A Mazzucotelli N Viguerie C Tiraby 2007 The transcriptional coactivator PGC-1alpha and the nuclear receptor PPARalpha control the expression of glycerol kinase and metabolism genes independently of PPARgamma activation in human white adipocytes Diabetes 56 2467 2475
28. Ausubel FM, Brent R, Kingston RE et al (1996) Current protocols in molecular biology. Wiley, New York
29. CS Hwang MD Lane 1999 Up-regulation of uncoupling protein-3 by fatty acid in C2C12 myotubes Biochem Biophys Res Commun 258 464 469 (Pubitemid 29287074)
30. I Nagase S Yoshida X Canas 1999 Up-regulation of uncoupling protein 3 by thyroid hormone, peroxisome proliferator-activated receptor ligands and 9-cis retinoic acid in L6 myotubes FEBS Lett 461 319 322 (Pubitemid 29533355)
31. E Chevillotte J Rieusset M Roques M Desage H Vidal 2001 The regulation of uncoupling protein-2 gene expression by omega-6 polyunsaturated fatty acids in human skeletal muscle cells involves multiple pathways, including the nuclear receptor peroxisome proliferator-activated receptor beta J Biol Chem 276 10853 10860 (Pubitemid 38089262)
32. O Boss S Samec A Paoloni-Giacobino 1997 Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression FEBS Lett 408 39 42 (Pubitemid 27216458)
33. H Esterbauer H Oberkofler F Krempler AD Strosberg W Patsch 2000 The uncoupling protein-3 gene is transcribed from tissue-specific promoters in humans but not in rodents J Biol Chem 275 36394 36399 (Pubitemid 30841195)
34. R Chan C Boudreau-Larivière L Angus F Mankal B Jasmin 1999 An intronic enhancer containing an N-box motif is required for synapse- and tissue-specific expression of the acetylcholinesterase gene in skeletal muscle fibers Proc Natl Acad Sci U S A 96 4627 4632 (Pubitemid 29190387)
35. P Marshall N Chartrand Y de Repentigny 2002 Mouse dystrophin enhancer preferentially targets lacZ expression in skeletal and cardiac muscle Dev Dyn 224 30 38 (Pubitemid 34464930)
36. DS Weigle LE Selfridge MW Schwartz 1998 Elevated free fatty acids induce uncoupling protein 3 expression in muscle. A potential explanation for the effect of fasting Diabetes 47 298 302 (Pubitemid 28079993)
37. H Vidal D Langin F Andreelli L Millet D Larrouy M Laville 1999 Lack of skeletal muscle uncoupling protein 2 and 3 mRNA induction during fasting in type-2 diabetic subjects Am J Physiol 277 E830 E837
38. Y Khalfallah S Fages M Laville D Langin H Vidal 2000 Regulation of uncoupling protein-2 and uncoupling protein-3 mRNA expression during lipid infusion in human skeletal muscle and subcutaneous adipose tissue Diabetes 49 25 31 (Pubitemid 30022920)
39. S Brun MC Carmona T Mampel 1999 Activators of peroxisome proliferator-activated receptor-alpha induce the expression of the uncoupling protein-3 gene in skeletal muscle: a potential mechanism for the lipid intake-dependent activation of uncoupling protein-3 gene expression at birth Diabetes 48 1217 1222 (Pubitemid 29241017)
40. A Krook J Digby S O'Rahilly J Zierath H Wallberg-Henriksson 1998 Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients Diabetes 47 1528 1531 (Pubitemid 28396961)
41. P Schrauwen MKC Hesselink EE Blaak 2001 Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes Diabetes 50 2870 2873 (Pubitemid 33733141)
42. P Schrauwen M Mensink G Schaart 2006 Reduced skeletal muscle uncoupling protein-3 content in prediabetic subjects and type 2 diabetic patients: restoration by rosiglitazone treatment J Clin Endocrinol Metab 91 1520 1525