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Cloning and ontogenetic expression of the uncoupling protein 1 gene UCP1 in sheep

  • Animal Genetics • Original Paper
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Abstract

The uncoupling protein 1 (UCP1) is an indicator of brown adipocytes and is involved in the control of body temperature and regulation of energy balance. It abundantly expresses in newborns and has important functions in adults. However, little information was known on UCP1 gene expression in young and adolescent sheep. In this study, we cloned and identified the full-length DNA and cDNA sequences of the ovine UCP1 gene, which were 6659 bp and 1621 bp, respectively, and predicted the location of the gene on chromosome 17. Forty-eight animals with an equal number of males and females each for both Guangling Large Tail sheep (GLT) and Small Tail sheep Han (STH) sheep were used to study the ontogenetic expression of UCP1 mRNA in eight adipose tissues by quantitative real-time polymerase chain reaction (PCR). The results showed that the mRNA was expressed in all tissues studied and at all stages from 2 to 12 months of age. Nevertheless, the mRNA in perirenal fat was expressed significantly higher than that in other tissues and lower in superficial fat than in deep deposits. The highest expression was observed in animals at 2 months of age and then decreased gradually with age. Global expression in GLT was significantly higher than that in STH. Interactions between tissue and breed and age also influenced the mRNA expression significantly. In addition, the mRNA expression was associated with the single nucleotide polymorphism (SNP) haplotypes detected in the cDNA of the gene.

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References

  • Au-Yong IT, Thorn N, Ganatra R, Perkins AC, Symonds ME (2009) Brown adipose tissue and seasonal variation in humans. Diabetes 58:2583–2587

    Article  PubMed  CAS  Google Scholar 

  • Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, Giacobino JP, De Matteis R, Cinti S (2010) The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab 298:E1244–E1253

    Article  PubMed  CAS  Google Scholar 

  • Bassett JM, Bomford J, Mott JC (1988) Photoperiod: an important regulator of plasma prolactin concentration in fetal lambs during late gestation. Q J Exp Physiol 73:241–244

    PubMed  CAS  Google Scholar 

  • Budge H, Edwards LJ, McMillen IC, Bryce A, Warnes K, Pearce S, Stephenson T, Symonds ME (2004) Nutritional Manipulation of Fetal Adipose Tissue Deposition and Uncoupling Protein 1 Messenger RNA Abundance in the Sheep: Differential Effects of Timing and Duration. Biol Reprod 71:359–365

    Article  PubMed  CAS  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    Article  PubMed  CAS  Google Scholar 

  • Clarke L, Bryant MJ, Lomax MA, Symonds ME (1997a) Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. Br J Nutr 77:871–883

    Article  PubMed  CAS  Google Scholar 

  • Clarke L, Buss DS, Juniper DT, Lomax MA, Symonds ME (1997b) Adipose tissue development during early postnatal life in ewe-reared lambs. Exp Physiol 82:1015–1027

    Article  PubMed  CAS  Google Scholar 

  • Dahl GE (2008) Effects of short day photoperiod on prolactin signaling in dry cows: a common mechanism among tissues and environments? J Anim Sci 86:10–14

    Article  PubMed  CAS  Google Scholar 

  • de Vooght KM, van Wijk R, van Solinge WW (2009) Management of gene promoter mutations in molecular diagnostics. Clin Chem 55:698–708

    Article  PubMed  Google Scholar 

  • Demas GE, Bowers RR, Bartness TJ, Gettys TW (2002) Photoperiodic regulation of gene expression in brown and white adipose tissue of Siberian hamsters (Phodopus sungorus). Am J Physiol Regul Integr Comp Physiol 282:R114–R121

    PubMed  CAS  Google Scholar 

  • Festuccia WT, Blanchard PG, Richard D, Deshaies Y (2010) Basal adrenergic tone is required for maximal stimulation of rat brown adipose tissue UCP1 expression by chronic PPAR-gamma activation. Am J Physiol Regul Integr Comp Physiol 299:R159–R167

    Article  PubMed  CAS  Google Scholar 

  • Finn D, Lomax MA, Trayhurn P (1998) An immunohistochemical and in situ hybridisation study of the postnatal development of uncoupling protein-1 and uncoupling protein-1 mRNA in lamb perirenal adipose tissue. Cell Tissue Res 294:461–466

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Cazarin ML, Gamboa JL, Andrade FH (2011) Rat diaphragm mitochondria have lower intrinsic respiratory rates than mitochondria in limb muscles. Am J Physiol Regul Integr Comp Physiol 300:R1311–R1315

    Article  PubMed  CAS  Google Scholar 

  • Gnanalingham M, Hyatt M, Bispham J, Mostyn A, Clarke L, Budge H, Symonds M, Stephenson T (2008) Maternal dexamethasone administration and the maturation of perirenal adipose tissue of the neonatal sheep. Organog 4:188–194

    Article  Google Scholar 

  • Henry BA, Blache D, Rao A, Clarke IJ, Maloney SK (2008) Profiling postprandial thermogenesis in muscle and fat of sheep and the central effect of leptin administration. Endocrinology 149:2019–2026

    Article  PubMed  CAS  Google Scholar 

  • Henry BA, Blache D, Rao A, Clarke IJ, Maloney SK (2010) Disparate effects of feeding on core body and adipose tissue temperatures in animals selectively bred for Nervous or Calm temperament. Am J Physiol Regul Integr Comp Physiol 299:907–917

    Article  Google Scholar 

  • Hu J, Zhou H, Smyth A, Luo Y, Hickford JG (2010) Polymorphism of the bovine ADRB3 gene. Mol Biol Rep 37:3389–3392

    Article  PubMed  CAS  Google Scholar 

  • Hyatt MA, Keisler DH, Budge H, Symonds ME (2010) Maternal parity and its effect on adipose tissue deposition and endocrine sensitivity in the postnatal sheep. J Endocrinol 204:173–179

    Article  PubMed  CAS  Google Scholar 

  • Iritani N, Sugimoto T, Fukuda H, Tomoe K (2002) Changes in UCP Family Expressions in Rat Tissues Due to Diet and Aging. J Nutr Sci Vitaminol Tokyo 48:410–416

    Article  PubMed  CAS  Google Scholar 

  • Jia JJ, Tian YB, Cao ZH, Tao LL, Zhang X, Gao SZ, Ge CR, Lin QY, Jois M (2010) The polymorphisms of UCP1 genes associated with fat metabolism, obesity and diabetes. Mol Biol Rep 37:1513–1522

    Article  PubMed  CAS  Google Scholar 

  • Klingenspor M, Fromme T, Hughes DA Jr, Manzke L, Polymeropoulos E, Riemann T, Trzcionka M, Hirschberg V, Jastroch M (2008) An ancient look at UCP1. Biochimica et Biophysica Acta (BBA). Bioenergetics 1777:637–641

    Article  CAS  Google Scholar 

  • Lomax MA, Sadiq F, Karamanlidis G, Karamitri A, Trayhurn P, Hazlerigg DG (2006) Ontogenic Loss of Brown Adipose Tissue Sensitivity to -Adrenergic Stimulation in the Ovine. Endocrinology 148:461–468

    Article  PubMed  Google Scholar 

  • Mori H, Okazawa H, Iwamoto K, Maeda E, Hashiramoto M, Kasuga M (2001) A polymorphism in the 5' untranslated region and a Met229– > Leu variant in exon 5 of the human UCP1 gene are associated with susceptibility to type II diabetes mellitus. Diabetologia 44:373–376

    Article  PubMed  CAS  Google Scholar 

  • Mostyn A, Bispham J, Pearce S, Evens Y, Raver N, Keisler DH, Webb R, Stephenson T, Symonds ME (2002) Differential effects of leptin on thermoregulation and uncoupling protein abundance in the neonatal lamb. FASEB J 16:1438–1440

    PubMed  CAS  Google Scholar 

  • Myers DA, Hanson K, Mlynarczyk M, Kaushal KM, Ducsay CA (2008) Long-term hypoxia modulates expression of key genes regulating adipose function in the late-gestation ovine fetus. Am J Physiol Regul Integr Comp Physiol 294:R1312–R1318

    Article  PubMed  CAS  Google Scholar 

  • Nagai N, Sakane N, Tsuzaki K, Moritani T (2011) UCP1 genetic polymorphism (−3826 A/G) diminishes resting energy expenditure and thermoregulatory sympathetic nervous system activity in young females. Int J Obes Lond 35:1050–1055

    Article  PubMed  CAS  Google Scholar 

  • Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293:E444–E452

    Article  PubMed  CAS  Google Scholar 

  • Nedergaard J, Bengtsson T, Cannon B (2010) Three years with adult human brown adipose tissue. Ann N Y Acad Sci 1212:E20–E36

    Article  PubMed  Google Scholar 

  • Oliver P, Picó C, Palou A (2001) Differential expression of genes for uncoupling proteins 1, 2 and 3 in brown and white adipose tissue depots during rat development. Cell Mol Life Sci 58:470–476

    Article  PubMed  CAS  Google Scholar 

  • Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531

    Article  PubMed  CAS  Google Scholar 

  • Shin HD, Kim KS, Cha MH, Yoon Y (2005) The effects of UCP-1 polymorphisms on obesity phenotypes among Korean female subjects. Biochem Biophys Res Commun 335:624–630

    Article  PubMed  CAS  Google Scholar 

  • Sonstegard TS, Kappes SM (1999) Mapping of the ucp1 locus to bovine chromosome 17. Anim Genet 30:462–478

    Google Scholar 

  • Svensson PA, Jernås M, Sjöholm K, Hoffmann JM, Nilsson BE, Hansson M, Carlsson LM (2011) Gene expression in human brown adipose tissue. Int J Mol Med 27:227–232

    Article  PubMed  CAS  Google Scholar 

  • Symonds ME, Budge H, Perkins AC, Lomax MA (2011) Adipose tissue development - Impact of the early life environment. Prog Biophys Mol Biol 106:300–306

    Article  PubMed  CAS  Google Scholar 

  • Viengchareun S, Servel N, Fève B, Freemark M, Lombès M, Binart N (2008) Prolactin receptor signaling is essential for perinatal brown adipocyte function: a role for insulin-like growth factor-2. PLoS One 3:e1535

    Article  PubMed  Google Scholar 

  • Watanabe M, Yamamoto T, Mori C, Okada N, Yamazaki N, Kajimoto K, Kataoka M, Shinohara Y (2008) Cold-induced changes in gene expression in brown adipose tissue: implications for the activation of thermogenesis. Biol Pharm Bull 31:775–784

    Article  PubMed  CAS  Google Scholar 

  • Wolf G (2009) Brown adipose tissue: the molecular mechanism of its formation. Nutr Rev 67:167–171

    Article  PubMed  Google Scholar 

  • Wu JL, Liu WZ, Liu JH, Qiao LY, Yuan YN (2011) Distribution and quantification of β-3 adrenergic receptor in tissues of sheep. Animal 5:88–93

    Article  PubMed  CAS  Google Scholar 

  • Xue B, Rim JS, Hogan JC, Coulter AA, Koza RA, Kozak LP (2007) Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J Lipid Res 48:41–51

    Article  PubMed  CAS  Google Scholar 

  • Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, Nedergaard J, Cinti S (2009) The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J 23:3113–3120

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the staff of the Laboratory of Animal Genetics, Breeding and Reproduction, Shanxi Agricultural University. This study was supported by the project of the Chinese National Natural Science Foundation (no. 30972084), the Program for New Century Excellent Talents in University, Ministry of Education of China (no. NCET-05-0269) and the Excellent Innovation Project for Graduate in Shanxi Province (no. 20103042).

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Correspondence to Wen-Zhong Liu.

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Yuan, YN., Liu, WZ., Liu, JH. et al. Cloning and ontogenetic expression of the uncoupling protein 1 gene UCP1 in sheep. J Appl Genetics 53, 203–212 (2012). https://doi.org/10.1007/s13353-012-0086-0

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  • DOI: https://doi.org/10.1007/s13353-012-0086-0

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