Uncoupling protein expression in skeletal muscle and adipose tissue in response to in vivo porcine somatotropin treatment

Domestic Animal Endocrinology

Volumn 35, Issue 2, 2008, Pages 130-141

  Ramsay, T G ^a   Mitchell, A D ^a   Richards, M P ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

IGF I; PPAR; Somatotropin; Swine; Uncoupling protein

Indexed keywords

GROWTH HORMONE; HYDROCORTISONE; INSULIN; ION CHANNEL; LIOTHYRONINE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; MITOCHONDRIAL UNCOUPLING PROTEIN 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; SOMATOMEDIN C;

ANIMAL; ANIMAL DISEASE; ARTICLE; BIOSYNTHESIS; BLOOD; CAPILLARY ELECTROPHORESIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE BLOOD LEVEL; MALE; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SUBCUTANEOUS FAT; SWINE;

ANIMALS; BLOOD GLUCOSE; ELECTROPHORESIS, CAPILLARY; GENE EXPRESSION REGULATION; GROWTH HORMONE; HYDROCORTISONE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; ION CHANNELS; MALE; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUBCUTANEOUS FAT; SWINE; TRIIODOTHYRONINE;

SUIDAE; SUS;

EID: 47049097376     PISSN: 07397240     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.domaniend.2007.12.001     Document Type: Article

References (63)

1. Ricquier D., and Bouillaud F. Mitochondrial uncoupling proteins: from mitochondria to the regulation of energy balance. J Physiol 529 Pt 1 (2000) 3-10
2. Nicholls D.G., and Locke R.M. Thermogenic mechanisms in brown fat. Physiol Rev 64 (1984) 1-64
3. Trayhurn P., Temple N.J., and Van Aerde J. Evidence from immunoblotting studies on uncoupling protein that brown adipose tissue is not present in the domestic pig. Can J Physiol Pharmacol 67 (1989) 1480-1485
4. Boss O., Samec S., Paoloni-Giacobino A., Rossier C., Dulloo A., Seydoux J., et al. Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408 (1997) 39-42
5. Fleury C., Neverova M., Collins S., Raimbault S., Champigny O., Levi-Meyrueis C., et al. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15 (1997) 269-272
6. Esteves T.C., and Brand M.D. The reactions catalysed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim Biophys Acta 1709 (2005) 35-44
7. Jezek P., and Garlid K.D. Mammalian mitochondrial uncoupling proteins. Int J Biochem Cell Biol 30 (1998) 1163-1168
8. Cline G.W., Vidal-Puig A.J., Dufour S., Cadman K.S., Lowell B.B., and Shulman G.I. In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J Biol Chem 276 (2001) 20240-20244
9. Erlanson-Albertsson C. The role of uncoupling proteins in the regulation of metabolism. Acta Physiol Scand 178 (2003) 405-412
10. Schrauwen P., Hoeks J., and Hesselink M.K. Putative function and physiological relevance of the mitochondrial uncoupling protein-3: involvement in fatty acid metabolism?. Prog Lipid Res 45 (2006) 17-41
11. Damon M., Vincent A., Lombardi A., and Herpin P. First evidence of uncoupling protein-2 (UCP-2) and -3 (UCP-3) gene expression in piglet skeletal muscle and adipose tissue. Gene 246 (2000) 133-141
12. Spurlock M.E., Ji S.Q., Godat R.L., Kuske J.L., Willis G.M., Frank G.R., et al. Changes in the expression of uncoupling proteins and lipases in porcine adipose tissue and skeletal muscle during feed deprivation. J Nutr Biochem 12 (2001) 81-87
13. Ramsay T.G., and Rosebrough R.W. Regulation of uncoupling proteins 2 and 3 in porcine adipose tissue. Domest Anim Endocrinol 28 (2005) 351-366
14. Dunshea F.R. Effect of metabolism modifiers on lipid metabolism in the pig. J Anim Sci 71 (1993) 1966-1977
15. Brown-Borg H.M., Rakoczy S.G., Romanick M.A., and Kennedy M.A. Effects of growth hormone and insulin-like growth factor-1 on hepatocyte antioxidative enzymes. Exp Biol Med (Maywood) 227 (2002) 94-104
16. Pedersen S.B., Kristensen K., Fisker S., Jorgensen J.O., Christiansen J.S., and Richelsen B. Regulation of uncoupling protein-2 and -3 by growth hormone in skeletal muscle and adipose tissue in growth hormone-deficient adults. J Clin Endocrinol Metab 84 (1999) 4073-4078
17. Pedersen S.B., Borglum J.D., Kristensen K., Norrelund H., Otto J., Jorgensen L., et al. Regulation of uncoupling protein (UCP) 2 and 3 in adipose and muscle tissue by fasting and growth hormone treatment in obese humans. Int J Obes Relat Metab Disord 24 (2000) 968-975
18. Hioki C., Yoshida T., Kogure A., Takakura Y., Umekawa T., Yoshioka K., et al. Effects of growth hormone (GH) on mRNA levels of uncoupling proteins 1, 2 and 3 in brown and white adipose tissues and skeletal muscle in obese mice. Horm Metab Res 36 (2004) 607-613
19. Lentes K.U., Tu N., Chen H., Winnikes U., Reinert I., Marmann G., et al. Genomic organization and mutational analysis of the human UCP2 gene, a prime candidate gene for human obesity. J Recept Signal Transduct Res 19 (1999) 229-244
20. Sbraccia P., D'Adamo M., Leonetti F., Buongiorno A., Silecchia G., Basso M.S., et al. Relationship between plasma free fatty acids and uncoupling protein-3 gene expression in skeletal muscle of obese subjects: in vitro evidence of a causal link. Clin Endocrinol (Oxf) 57 (2002) 199-207
21. Muoio D.M., MacLean P.S., Lang D.B., Li S., Houmard J.A., Way J.M., et al. Fatty acid homeostasis and induction of lipid regulatory genes in skeletal muscles of peroxisome proliferator-activated receptor (PPAR) alpha knock-out mice. Evidence for compensatory regulation by PPAR delta. J Biol Chem 277 (2002) 26089-26097
22. Ramsay T.G., and Richards M.P. Leptin and leptin receptor expression in skeletal muscle and adipose tissue in response to in vivo porcine somatotropin treatment. J Anim Sci 83 (2005) 2501-2508
23. Campbell R.G., Steele N.C., Caperna T.J., McMurtry J.P., Solomon M.B., and Mitchell A.D. Interrelationships between energy intake and endogenous porcine growth hormone administration on the performance, body composition and protein and energy metabolism of growing pigs weighing 25 to 55 kilograms live weight. J Anim Sci 66 (1988) 1643-1650
24. Steele N.C., McMurtry J.P., Campbell R.G., Caperna T.J., and Rosebrough R.W. Effect of dietary energy intake and exogenous porcine growth hormone administration on circulating porcine growth hormone concentration and response to human growth hormone-releasing factor administration in growing swine. Domest Anim Endocrinol 12 (1995) 293-298
25. ARC. The nutrient requirements of pigs (1981), Commonwealth Agricultural Bureaux, Slough, UK
26. Anderson D.B., Kauffman R.G., and Kastenschmidt L.L. Lipogenic enzyme activities and cellularity of porcine adipose tissue from various anatomical locations. J Lipid Res 13 (1972) 593-599
27. Ono Y., Solomon M.B., Evock-Clover C.M., Steele N.C., and Maruyama K. Effects of porcine somatotropin administration on porcine muscles located within different regions of the body. J Anim Sci 73 (1995) 2282-2288
28. Balaji R., Wright K.J., Hill C.M., Dritz S.S., Knoppel E.L., and Minton J.E. Acute phase responses of pigs challenged orally with Salmonella typhimurium. J Anim Sci 78 (2000) 1885-1891
29. Lord E., Murphy B.D., Desmarais J.A., Ledoux S., Beaudry D., and Palin M.F. Modulation of peroxisome proliferator-activated receptor delta and gamma transcripts in swine endometrial tissue during early gestation. Reproduction 131 (2006) 929-942
30. Richards M.P., and Poch S.M. Quantitative analysis of gene expression by reverse transcription polymerase chain reaction and capillary electrophoresis with laser-induced fluorescence detection. Mol Biotechnol 21 (2002) 19-37
31. Winer J., Jung C.K., Shackel I., and Williams P.M. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270 (1999) 41-49
32. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
33. Chung C.S., Etherton T.D., and Wiggins J.P. Stimulation of swine growth by porcine growth hormone. J Anim Sci 60 (1985) 118-130
34. Etherton T.D., Wiggins J.P., Chung C.S., Evock C.M., Rebbun J.F., and Walton P.E. Stimulation of pig growth performance by porcine growth hormone and growth hormone-releasing factor. J Anim Sci 63 (1986) 1389-1399
35. Etherton T.D., Wiggins J.P., Evock C.M., Chung C.S., Rebbun J.F., Walton P.E., et al. Stimulation of pig growth performance by porcine growth hormone: determination of the dose-response relationship. J Anim Sci 64 (1987) 433-443
36. Novakofski J., Brenner K.V., McKeith F.K., McLaren D.G., Easter R.A., Grebner G.L., et al. Performance enhancement by natural porcine somatotropin (PST): hematology and endocrinology. J Anim Sci 65 Suppl. l (1987) 246 (Abstr.)
37. Pedersen S.B., Lund S., Buhl E.S., and Richelsen B. Insulin and contraction directly stimulate UCP2 and UCP3 mRNA expression in rat skeletal muscle in vitro. Biochem Biophys Res Commun 283 (2001) 19-25
38. Collin A., Cassy S., Buyse J., Decuypere E., and Damon M. Potential involvement of mammalian and avian uncoupling proteins in the thermogenic effect of thyroid hormones. Domest Anim Endocrinol 29 (2005) 78-87
39. Teruel T., Valverde A.M., Navarro P., Benito M., and Lorenzo M. Inhibition of PI 3-kinase and RAS blocks IGF-I and insulin-induced uncoupling protein 1 gene expression in brown adipocytes. J Cell Physiol 176 (1998) 99-109
40. Gaskins H.R., Kim J.W., Wright J.T., Rund L.A., and Hausman G.J. Regulation of insulin-like growth factor-I ribonucleic acid expression, polypeptide secretion, and binding protein activity by growth hormone in porcine preadipocyte cultures. Endocrinology 126 (1990) 622-630
41. Lanni A., Moreno M., Lombardi A., and Goglia F. Thyroid hormone and uncoupling proteins. FEBS Lett 543 (2003) 5-10
42. Hishikawa D., Hong Y.H., Roh S.G., Miyahara H., Nishimura Y., Tomimatsu A., et al. Identification of genes expressed differentially in subcutaneous and visceral fat of cattle, pig, and mouse. Physiol Genom 21 (2005) 343-350
43. Carlsson L., Nilsson I., and Oscarsson J. Hormonal regulation of liver fatty acid-binding protein in vivo and in vitro: effects of growth hormone and insulin. Endocrinology 139 (1998) 2699-2709
44. Jump D.B., Botolin D., Wang Y., Xu J., Christian B., and Demeure O. Fatty acid regulation of hepatic gene transcription. J Nutr 135 (2005) 2503-2506
45. Tugwood J.D., Issemann I., Anderson R.G., Bundell K.R., McPheat W.L., and Green S. The mouse peroxisome proliferator activated receptor recognizes a response element in the 5′ flanking sequence of the rat acyl CoA oxidase gene. EMBO J 11 (1992) 433-439
46. Reddy J.K., and Hashimoto T. Peroxisomal beta-oxidation and peroxisome proliferator-activated receptor alpha: an adaptive metabolic system. Annu Rev Nutr 21 (2001) 193-230
47. Jaburek M., Miyamoto S., Di Mascio P., Garlid K.D., and Jezek P. Hydroperoxy fatty acid cycling mediated by mitochondrial uncoupling protein UCP2. J Biol Chem 279 (2004) 53097-53102
48. Mostyn A., Litten J.C., Perkins K.S., Euden P.J., Corson A.M., Symonds M.E., et al. Influence of size at birth on the endocrine profiles and expression of uncoupling proteins in subcutaneous adipose tissue, lung, and muscle of neonatal pigs. Am J Physiol Regul Integr Comp Physiol 288 (2005) R1536-R1542
49. Gong D.W., He Y., Karas M., and Reitman M. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin. J Biol Chem 272 (1997) 24129-24132
50. Hwang C.S., and Lane M.D. Up-regulation of uncoupling protein-3 by fatty acid in C2C12 myotubes. Biochem Biophys Res Commun 258 (1999) 464-469
51. Mostyn A., Litten J.C., Perkins K.S., Alves-Guerra M.C., Pecqueur C., Miroux B., et al. Influence of genotype on the differential ontogeny of uncoupling protein 2 and 3 in subcutaneous adipose tissue and muscle in neonatal pigs. J Endocrinol 183 (2004) 121-131
52. Pecqueur C., Alves-Guerra M.C., Gelly C., Levi-Meyrueis C., Couplan E., Collins S., et al. Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 276 (2001) 8705-8712
53. Ricquier D. Respiration uncoupling and metabolism in the control of energy expenditure. Proc Nutr Soc 64 (2005) 47-52
54. Krauss S., Zhang C.Y., and Lowell B.B. The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6 (2005) 248-261
55. Negre-Salvayre A., Hirtz C., Carrera G., Cazenave R., Troly M., Salvayre R., et al. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11 (1997) 809-815
56. Jezek P., Zackova M., Ruzicka M., Skobisova E., and Jaburek M. Mitochondrial uncoupling proteins-facts and fantasies. Physiol Res 53 Suppl. 1 (2004) S199-S211
57. Cannon B., Shabalina I.G., Kramarova T.V., Petrovic N., and Nedergaard J. Uncoupling proteins: a role in protection against reactive oxygen species-or not?. Biochim Biophys Acta 1757 (2006) 449-458
58. MacLellan J.D., Gerrits M.F., Gowing A., Smith P.J., Wheeler M.B., and Harper M.E. Physiological increases in uncoupling protein 3 augment fatty acid oxidation and decrease reactive oxygen species production without uncoupling respiration in muscle cells. Diabetes 54 (2005) 2343-2350
59. Himms-Hagen J., and Harper M.E. Physiological role of UCP3 may be export of fatty acids from mitochondria when fatty acid oxidation predominates: an hypothesis. Exp Biol Med 226 (2001) 78-84
60. Son C., Hosoda K., Matsuda J., Fujikura J., Yonemitsu S., Iwakura H., et al. Up-regulation of uncoupling protein 3 geneexpression by fatty acids and agonists for PARs in L6myotubes. Endocrinology 142 (2001) 4189-4194
61. Solanes G., Pedraza N., Iglesias R., Giralt M., and Villarroya F. 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 (2003) 1944-1958
62. Hunt M.C., Nousiainen S.E., Huttunen M.K., Orii K.E., Svensson L.T., and Alexson S.E. Peroxisome proliferatorinduced long chain acyl-CoA thioesterases comprise a highly conserved novel multi-gene family involved in lipid metabolism. J Biol Chem 274 (1999) 34317-34326
63. Svensson L.T., Engberg S.T., Aoyama T., Usuda N., Alexson S.E., and Hashimoto T. Molecular cloning and characterization of a mitochondrial peroxisome proliferator induced acyl-CoA thioesterase from rat liver. Biochem J 329 (1998) 601-608