Tissue-specific gene expression and functional regulation of uncoupling protein 2 (UCP2) by hypoxia and nutrient availability in gilthead sea bream (Sparus aurata): Implications on the physiological significance of UCP1-3 variants

Fish Physiology and Biochemistry

Volumn 40, Issue 3, 2014, Pages 751-762

  Bermejo Nogales, Azucena ^a   Calduch Giner, Josep Alvar ^a   Pérez Sánchez, Jaume ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

Author keywords

Antioxidant activity; Blood chemistry; Feed restriction; Fish; Hypoxia; Mitochondria; Oxidative capacity; Respiration uncoupling

Indexed keywords

ARCHOSARGUS RHOMBOIDALIS; SPARUS AURATA;

FISH PROTEIN; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2;

AMINO ACID SEQUENCE; ANIMAL; ANOXIA; BLOOD; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; METABOLISM; MOLECULAR GENETICS; NUTRITIONAL STATUS; SEA BREAM; SKELETAL MUSCLE;

AMINO ACID SEQUENCE; ANIMALS; ANOXIA; FISH PROTEINS; GENE EXPRESSION REGULATION; ION CHANNELS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOCARDIUM; NUTRITIONAL STATUS; SEA BREAM;

EID: 84900327148     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-013-9882-7     Document Type: Article

References (48)

1. Alán L, Smolková K, Kronusová E, Šantorová J, Ježek P (2009) Absolute levels of transcripts for mitochondrial uncoupling proteins UCP2, UCP3, UCP4, and UCP5 show different patterns in rat and mice tissues. J Bioenerg Biomembr 41: 71-78.
2. Barazzoni R, Zanetti M, Bosutti A, Biolo G, Vitali-Serdoz L, Stebel M, Guarnieri G (2005) Moderate caloric restriction, but not physiological hyperleptinemia per se, enhances mitochondrial oxidative capacity in rat liver and skeletal muscle-tissue-specific impact on tissue triglyceride content and AKT activation. Endocrinology 146: 2098-2106.
3. Bermejo-Nogales A, Calduch-Giner J, Pérez-Sánchez J (2010) Gene expression survey of mitochondrial uncoupling proteins (UCP1/UCP3) in gilthead sea bream (Sparus aurata L.). J Comp Physiol B 180: 685-694.
4. Bermejo-Nogales A, Benedito-Palos L, Calduch-Giner JA, Pérez-Sánchez J (2011) Feed restriction up-regulates uncoupling protein 3 (UCP3) gene expression in heart and red muscle tissues of gilthead sea bream (Sparus aurata L.): new insights in substrate oxidation and energy expenditure. Comp Biochem Physiol A Physiol 159: 296-302.
5. Bo H, Jiang N, Ma G, Qu J, Zhang G, Cao D, Wen L, Liu S, Ji LL, Zhang Y (2008) Regulation of mitochondrial uncoupling respiration during exercise in rat heart: role of reactive oxygen species (ROS) and uncoupling protein 2. Free Radic Biol Med 44: 1373-1381.
6. Bordone L, Motta MC, Picard F, Robinson A, Jhala US, Apfeld J, McDonagh T, Lemieux M, McBurney M, Szilvasi A, Easlon EJ, Lin SJ, Guarente L (2005) Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic β cells. PLoS Biol 4: e31.
7. Cabrera JA, Ziemba EA, Colbert R, Kelly RF, Kuskowski M, Arriaga EA, Sluiter W, Duncker DJ, Ward HB, McFalls EO (2012) Uncoupling protein-2 expression and effects on mitochondrial membrane potential and oxidant stress in heart tissue. Transl Res 159: 383-390.
8. Calduch-Giner JA, Mingarro M, Vega-Rubín de Celis S, Boujard D, Pérez-Sánchez J (2003) Molecular cloning and characterization of gilthead sea bream, (Sparus aurata) growth hormone receptor (GHR). Assessment of alternative splicing. Comp Biochem Physiol B-Biochem Mol Biol 136: 1-13.
9. Calduch-Giner J, Bermejo-Nogales A, Benedito-Palos L, Estensoro I, Ballester-Lozano G, Sitjà-Bobadilla A, Pérez-Sánchez J (2013) Deep sequencing for de novo construction of a marine fish (Sparus aurata) transcriptome database with a large coverage of protein-coding transcripts. BMC Genomics 14: 178.
10. Coulibaly I, Gahr SA, Palti Y, Yao J, Rexroad CE (2006) Genomic structure and expression of uncoupling protein 2 genes in rainbow trout (Oncorhynchus mykiss). BMC Genomics 7: 203.
11. Dridi S, Onagbesan O, Swennen Q, Buyse J, Decuypere E, Taouis M (2004) Gene expression, tissue distribution and potential physiological role of uncoupling protein in avian species. Comp Biochem Physiol A-Physiol 139: 273-283.
12. Emre Y, Hurtaud C, Ricquier D, Bouillaud F, Hughes J, Criscuolo F (2007) Avian UCP: the killjoy in the evolution of the mitochondrial uncoupling proteins. J Mol Evol 65: 392-402.
13. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, LeviMeyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15: 269-272.
14. Frezza C, Zheng L, Tennant DA, Papkovsky DB, Hedley BA, Kalna G, Watson DG, Gottlieb E (2011) Metabolic profiling of hypoxic cells revealed a catabolic signature required for cell survival. PLoS One 6: e24411.
15. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, Sartorelli V (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661-673.
16. Gao Q, Wolin MS (2008) Effects of hypoxia on relationships between cytosolic and mitochondrial NAD(P)H redox and superoxide generation in coronary arterial smooth muscle. Am J Physiol Heart Circul Physiol 295: H978-H989.
17. Heaton GM, Wagenvoord RJ, Kemp A, Nicholls DG (1978) Brown adipose tissue mitochondria: photoaffinity labelling of the regulatory site of energy dissipation. Eur J Biochem 82: 515-521.
18. Huang QS, Dong SJ, Fang C, Wu XL, Ye T, Lin Y (2012) Deep sequencing-based transcriptome profiling analysis of Oryzias melastigma exposed to PFOS. Aquat Toxicol 120: 54-58.
19. Hughes J, Criscuolo F (2008) Evolutionary history of the UCP gene family: gene duplication and selection. BMC Evol Biol 8: 306.
20. Jastroch M, Wuertz S, Kloas W, Klingenspor M (2005) Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol Genomics 22: 150-156.
21. Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, Fromme T, Hirschberg V, Heldmaier G, McAllan BM, Firth BT, Burmester T, Platzer M, Klingenspor M (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genomics 32: 161-169.
22. Jin Y, Chen R, Liu W, Fu Z (2010a) Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol 28: 854-861.
23. Jin Y, Zhang X, Shu L, Chen L, Sun L, Qian H, Liu W, Fu Z (2010b) Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 78: 846-852.
24. Kim T-H, Zhao Y, Ding W-X, Shin JN, He X, Seo Y-W, Chen J, Rabinowich H, Amoscato AA, Yin X-M (2004) Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome c release. Mol Biol Cell 15: 3061-3072.
25. Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6: 248-261.
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
27. Liang XF, Ogata HY, Oku H, Chen J, Hwang F (2003) Abundant and constant expression of uncoupling protein 2 in the liver of red sea bream Pagrus major. Comp Biochem Physiol A-Physiol 136: 655-661.
28. Liao WQ, Liang XF, Wang L, Fang L, Lin XT, Bai JJ, Jian Q (2006) Structural conservation and food habit-related liver expression of uncoupling protein 2 gene in five major Chinese carps. J Biochem Mol Biol 39: 346-354.
29. Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1α. Mol Cell 38: 864-878.
30. Liu Y, Wang J, Wei Y, Zhang H, Xu M, Dai J (2008) Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver. Aquatic Toxicol 89: 242-250.
31. -ΔΔC method. Methods 25: 402-408.
32. Ljubicic V, Joseph A-M, Saleem A, Uguccioni G, Collu-Marchese M, Lai RYJ, Nguyen LMD, Hood DA (2010) Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. BBA-Gen Subjects 1800: 223-234.
33. Lushchak VI, Bagnyukova TV (2006) Effects of different environmental oxygen levels on free radical processes in fish. Comp Biochem Physiol B-Biochem Mol Biol 144: 283-289.
34. Mark FC, Lucassen M, Pörtner HO (2006) Thermal sensitivity of uncoupling protein expression in polar and temperate fish. Comp Biochem Phys D Genomics Proteomics 1: 365-374.
35. Modrianský M, Murdza-Inglis DL, Patel HV, Freemann KB, Garlid KD (1997) Identification by site-directed mutagenesis of three arginines in uncoupling protein that are essential for nucleotide binding and inhibition. J Biol Chem 272: 24759-24762.
36. Nabben M, Hoeks J (2008) Mitochondrial uncoupling protein 3 and its role in cardiac- and skeletal muscle metabolism. Physiol Behav 94: 259-269.
37. Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64: 1-64.
38. Pérez-Jiménez A, Peres H, Rubio VC, Oliva-Teles A (2012) The effect of hypoxia on intermediary metabolism and oxidative status in gilthead sea bream (Sparus aurata) fed on diets supplemented with methionine and white tea. Comp Biochem Physiol C-Toxicol Pharmacol 155: 506-516.
39. Rial E, Zardoya R (2009) Oxidative stress, thermogenesis and evolution of uncoupling proteins. J Biol 8: 58.
40. Rupprecht A, Bräuer AU, Smorodchenko A, Goyn J, Hilse KE, Shabalina IG, Infante-Duarte C, Pohl EE (2012) Quantification of uncoupling protein 2 reveals its main expression in immune cells and selective up-regulation during T-Cell proliferation. PLoS One 7: 8.
41. Samec S, Seydoux J, Russell AP, Montani JP, Dulloo AG (2002) Skeletal muscle heterogeneity in fasting-induced upregulation of genes encoding UCP2, UCP3, PPAR gamma and key enzymes of lipid oxidation. Pflugers Arch EJP 445: 80-86.
42. Soane L, Cho H-J, Niculescu F, Rus H, Shin ML (2001) C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway. J Immunol 167: 2305-2311.
43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
44. Tiano L, Ballarini P, Santoni G, Wozniak M, Falcioni G (2000) Morphological and functional changes of mitochondria from density separated trout erythrocytes. BBA Bioenerg 1457: 118-128.
45. Tine M, Kuhl H, Jastroch M, Reinhardt R (2012) Genomic characterization of the European sea bass Dicentrarchus labrax reveals the presence of a novel uncoupling protein (UCP) gene family member in the teleost fish lineage. BMC Evol Biol 12: 62.
46. Torstensen BE, Nanton DA, Olsvik PA, Sundvold H, Stubhaug I (2009) Gene expression of fatty acid-binding proteins, fatty acid transport proteins (cd36 and FATP) and β-oxidation-related genes in Atlantic salmon (Salmo salar L.) fed fish oil or vegetable oil. Aquacult Nutr 15: 440-451.
47. Tseng Y-C, Chen R-D, Lucassen M, Schmidt MM, Dringen R, Abele D, Hwang P-P (2011) Exploring uncoupling proteins and antioxidant mechanisms under acute cold exposure in brains of fish. PLoS One 6: e18180.
48. Wang L, Liang XF, Liao WQ, Lei LM, Han BP (2006) Structural and functional characterization of microcystin detoxification-related liver genes in a phytoplanktivorous fish, Nile tilapia (Oreochromis niloticus). Comp Biochem Physiol C-Toxicol Pharmacol 144: 216-227.