Regulation of fatty acid oxidation in chicken (Gallus gallus): Interactions between genotype and diet composition

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 153, Issue 2, 2009, Pages 171-177

  Collin, A ^a   Swennen, Q ^b,c   Skiba Cassy, S ^d   Buyse, J ^b   Chartrin, P ^a   Le Bihan Duval, E ^a   Crochet, S ^a   Duclos, M J ^a   Joubert, R ^a   Decuypere, E ^b   Tesseraud, S ^a  

^a STATION DE RECHERCHES AVICOLES   (France)

^b LABORATORY OF GENE TECHNOLOGY   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

^d Unite mixte INRA IFREMER Universite Bordeaux 1 UMR Nuage   (France)

Author keywords

Avian uncoupling protein; Fat and lean chickens; Fatty acid utilization; Liver; Muscle; PGC 1 ; PPAR

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CARNITINE PALMITOYLTRANSFERASE I; COMPLEMENTARY DNA; CYTOCHROME C OXIDASE; FATTY ACID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RNA 18S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY FAT; CHICKEN; CONTROLLED STUDY; DIET; DIETARY INTAKE; ENERGY METABOLISM; ENZYME ACTIVITY; FATTY ACID OXIDATION; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; GENOTYPE; LIPID DIET; LIPOGENESIS; LIVER; LIVER MITOCHONDRION; LOW FAT DIET; MALE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PRIORITY JOURNAL; PROTEIN DIET; PROTEIN RESTRICTION; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ANIMALIA; AVES; GALLUS GALLUS;

EID: 67349240944     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2009.02.012     Document Type: Article

References (63)

1. Abe T., Mujahid A., Sato K., Akiba Y., and Toyomizu M. Possible role of avian uncoupling protein in down-regulating mitochondrial superoxide production in skeletal muscle of fasted chickens. FEBS Lett. 580 20 (2006) 4815-4822
2. Alam N., and Saggerson E.D. Malonyl-CoA and the regulation of fatty acid oxidation in soleus muscle. Biochem. J. 34 (1998) 233-241
3. Alleman, F., 1999. Amino acids catabolism of genetically lean and fat broiler chickens. PhD Thesis. Université François Rabelais de Tours.
4. Bartlett K., and Eaton S. Mitochondrial beta-oxidation. Eur. J. Biochem. 271 3 (2004) 462-469
5. Bass A., Brdiczka D., Eyer P., Hofer S., and Pette D. Metabolic differentiation of distinct muscle types at the level of enzymatic organization. Eur. J. Biochem. 10 2 (1969) 198-206
6. Bourneuf E., Hérault F., Chicault C., Carré W., Assaf S., Monnier A., Mottier S., Lagarrigue S., Douaire M., Mosser J., and Diot C. Microarray analysis of differential gene expression in the liver of lean and fat chickens. Gene 372 (2006) 162-170
7. Britton C.H., Mackey D.W., Esser V., Foster D.W., Burns D.K., Yarnall D.P., Froguel P., and McGarry J.D. Fine chromosome mapping of the genes for human liver and muscle carnitine palmitoyltransferase I (CPT1A and CPT1B). Genomics 40 1 (1997) 209-211
8. Cassy S., Metayer S., Crochet S., Rideau N., Collin A., and Tesseraud S. Leptin receptor in the chicken ovary: potential involvement in ovarian dysfunction of ad libitum-fed broiler breeder hens. Reprod. Biol. Endocrinol. 2 (2004) 72
9. Català-Niell A., Estrany M., Proenza A., Gianotti M., and Lladó I. Skeletal muscle and liver oxidative metabolism in response to a voluntary isocaloric intake of a high fat diet in male and female rats. Cell. Physiol. Biochem. 22 (2008) 327-336
10. Cha S.H., Rodgers J.T., Puigserver P., Chohnan S., and Lane M.D. Hypothalamic malonyl-CoA triggers mitochondrial biogenesis and oxidative gene expression in skeletal muscle: Role of PGC-1alpha. Proc. Natl. Acad. Sci. USA 103 (2006) 15410-15415
11. Chan L.L., Chen Q., Go A.G., Lam E.K., and Li E.T. Reduced adiposity in bitter melon (Momordica charantia)-fed rats is associated with increased lipid oxidative enzyme activities and uncoupling protein expression. J. Nutr. 135 (2005) 2517-2523
12. Colberg S.R., Simoneau J.A., Thaete F.L., and Kelley D.E. Skeletal muscle utilization of free fatty acids in women with visceral obesity. J. Clin. Invest. 95 (1995) 1846-1853
13. Collin A., Buyse J., Van As P., Darras V.M., Malheiros R.D., Moraes V.M.B., Reyns G.E., Taouis M., and Decuypere E. Cold-induced enhancement of avian uncoupling protein expression, heat production and triiodothyronine concentrations in broiler chicks. Gen. Comp. Endocrinol. 130 (2003) 70-77
14. Collin A., Malheiros R.D., Moraes V.M., Van As P., Darras V.M., Taouis M., Decuypere E., and Buyse J. Effects of dietary macronutrient content on energy metabolism and uncoupling protein mRNA expression in broiler chickens. Br. J. Nutr. 90 (2003) 261-269
15. Collin A., Taouis M., Buyse J., Ifuta N.B., Darras V.M., Van As P., Malheiros R.D., Moraes V.M., and Decuypere E. Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken. Am. J. Physiol., Endocrinol. Metab. 284 (2003) E771-777
16. 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
17. Collin A., Berri C., Tesseraud S., Rodón F.E., Skiba-Cassy S., Crochet S., Duclos M.J., Rideau N., Tona K., Buyse J., Bruggeman V., Decuypere E., Picard M., and Yahav S. Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens. Poult. Sci. 86 (2007) 795-800
18. Criscuolo F., Gonzalez-Barroso M.M., Le Maho Y., Ricquier D., and Bouillaud F. Avian uncoupling protein expressed in yeast mitochondria prevents endogenous free radical damage. Proc. Biol. Sci. 272 (2005) 803-810
19. Daval S., Lagarrigue S., and Douaire M. Messenger RNA levels and transcription rates of hepatic lipogenesis genes in genetically lean and fat chickens. Genet. Sel. Evol. 32 (2000) 521-531
20. Dupont J., Chen J., Derouet M., Simon J., Leclercq B., and Taouis M. Metabolic differences between genetically lean and fat chickens are partly attributed to alteration of insulin signaling in liver. J. Nutr. 129 (1999) 1937-1944
21. Dupont J., Tesseraud S., Derouet M., Collin A., Rideau N., Crochet S., Godet E., Cailleau-Audouin E., Métayer-Coustard S., Duclos M.J., Gespach C., Porter T.E., Cogburn L.A., and Simon J. Insulin immuno-neutralization in chicken: effects on insulin signaling and gene expression in liver and muscle. J. Endocrinol. 197 (2008) 531-542
22. Eaton S. Control of mitochondrial beta-oxidation flux. Prog. Lipid Res. 41 (2002) 197-239
23. Emre Y., Hurtaud C., Ricquier D., Bouillaud F., Hughes J., and Criscuolo F. Avian UCP: the killjoy in the evolution of the mitochondrial uncoupling proteins. J. Mol. Evol. 65 (2007) 392-402
24. Evock-Clover C.M., Poch S.M., Richards M.P., Ashwell C.M., and McMurtry J.P. Expression of an uncoupling protein gene homolog in chickens. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133 (2002) 345-358
25. Geraert P.A., MacLeod M.G., and Leclercq B. Energy metabolism in genetically fat and lean chickens: diet- and cold-induced thermogenesis. J. Nutr. 118 (1988) 1232-1239
26. Gilde A.J., and Van Bilsen M. Peroxisome proliferator-activated receptors (PPARS): regulators of gene expression in heart and skeletal muscle. Acta Physiol. Scand. 178 (2003) 425-434
27. Grimaldi P.A. Peroxisome proliferator-activated receptors as sensors of fatty acids and derivatives. Cell. Mol. Life Sci. 64 (2007) 2459-2464
28. Hermier D., Quignard-Boulange A., Dugail I., Guy G., Salichon M.R., Brigant L., Ardouin B., and Leclercq B. Evidence of enhanced storage capacity in adipose tissue of genetically fat chickens. J. Nutr. 119 (1989) 1369-1375
29. Holst D., Luquet S., Nogueira V., Kristiansen K., Leverve X., and Grimaldi P.A. Nutritional regulation and role of peroxisome proliferator-activated receptor delta in fatty acid catabolism in skeletal muscle. Biochim. Biophys. Acta 1633 (2003) 43-50
30. 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
31. Kim J.Y., Hickner R.C., Cortright R.L., Dohm G.L., and Houmard J.A. Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279 (2000) E1039-1044
32. Kim S., Sohn I., Ahn J.I., Lee K.H., Lee Y.S., and Lee Y.S. Hepatic gene expression profiles in a long-term high-fat diet-induced obesity mouse model. Gene 340 (2004) 99-109
33. Kolditz C., Borthaire M., Richard N., Corraze G., Panserat S., Vachot C., Lefèvre F., and Médale F. Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 294 (2008) R1154-1164
34. Lanni A., Mancini F.P., Sabatino L., Silvestri E., Franco R., De Rosa G., Goglia F., and Colantuoni V. De novo expression of uncoupling protein 3 is associated to enhanced mitochondrial thioesterase-1 expression and fatty acid metabolism in liver of fenofibrate-treated rats. FEBS Lett. 525 (2002) 7-12
35. Larrouy D., Laharrague P., Carrera G., Viguerie-Bascands N., Levi-Meyrueis C., Fleury C., Pecqueur C., Nibbelink M., André M., Casteilla L., and Ricquier D. Kupffer cells are a dominant site of uncoupling protein 2 expression in rat liver. Biochem. Biophys. Res. Commun. 235 (1997) 760-764
36. Leclercq B., Blum J.C., and Boyer J.P. Selecting broilers for low or high abdominal fat: initial observations. Br. Poult. Sci. 21 (1980) 107-113
37. Legrand P., and Hermier D. Hepatic delta 9 desaturation and plasma VLDL level in genetically lean and fat chickens. Int. J. Obes. Relat. Metab. Disord. 16 (1992) 289-294
38. Liu S., Wang S.Z., Li Z.H., and Li H. Association of single nucleotide polymorphism of chicken uncoupling protein gene with muscle and fatness traits. J. Anim. Breed. Genet. 124 (2007) 230-235
39. Marques-Lopes I., Ansorena D., Astiasaran I., Forga L., and Martinez J.A. Postprandial de novo lipogenesis and metabolic changes induced by a high-carbohydrate, low-fat meal in lean and overweight men. Am. J. Clin. Nutr. 73 (2001) 253-261
40. McGarry J.D., Woeltje K.F., Kuwajima M., and Foster D.W. Regulation of ketogenesis and the renaissance of carnitine palmitoyltransferase. Diabetes Metab. Rev. 5 (1989) 271-284
41. Matsuda J., Hosoda K., Itoh H., Son C., Doi K., Tanaka T., Fukunaga Y., Inoue G., Nishimura H., Yoshimasa Y., Yamori Y., and Nakao K. Cloning of rat uncoupling protein-3 and uncoupling protein-2 cDNAs: their gene expression in rats fed high-fat diet. FEBS Lett. 418 (1997) 200-204
42. Mostyn A., Litten J.C., Perkins K.S., Alves-Guerra M.C., Pecqueur C., Miroux B., Symonds M.E., and Clarke L. 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 1 (2004) 121-131
43. Mozo J., Emre Y., Bouillaud F., Ricquier D., and Criscuolo F. Thermoregulation: what role for UCPs in mammals and birds?. Biosci. Rep. 25 3-4 (2005) 227-249
44. Mujahid A., Sato K., Akiba Y., and Toyomizu M. Acute heat stress stimulates mitochondrial superoxide production in broiler skeletal muscle, possibly via downregulation of uncoupling protein content. Poult. Sci. 85 (2006) 1259-1265
45. Nunn A.V., Bell J., and Barter P. The integration of lipid-sensing and anti-inflammatory effects: how the PPARs play a role in metabolic balance. Nucl. Recept. 5 (2007) 1
46. Ojano-Dirain C., Toyomizu M., Wing T., Cooper M., and Bottje W.G. Gene expression in breast muscle and duodenum from low and high feed efficient broilers. Poult. Sci. 86 (2007) 372-381
47. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
48. Pecqueur C., Alves-Guerra M.C., Gelly C., Levi-Meyrueis C., Couplan E., Collins S., Ricquier D., Bouillaud F., and Miroux B. Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J. Biol. Chem. 276 (2001) 8705-8712
49. Raimbault S., Dridi S., Denjean F., Lachuer J., Couplan E., Bouillaud F., Bordas A., Duchamp C., Taouis M., and Ricquier D. An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem. J. 353 (2001) 441-444
50. Ramsay T.G., and Mitchell A.D. Impact of dietary protein content on uncoupling protein mRNA abundance in swine. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 149 (2008) 562-571
51. Rey B., Halsey L.G., Dolmazon V., Rouanet J.L., Roussel D., Handrich Y., Butler P.J., and Duchamp C. Long-term fasting decreases mitochondrial avian UCP-mediated oxygen consumption in hypometabolic king penguins. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008) R92-R100
52. Saito S., Saito C.T., and Shingai R. Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene 408 (2008) 37-44
53. Sibut V., Le Bihan-Duval E., Tesseraud S., Godet E., Bordeau T., Cailleau-Audouin E., Chartrin P., Duclos M.J., and Berri C. AMP-activated protein kinase involved in the variations of muscle glycogen and breast meat quality between lean and fat chickens. J. Anim. Sci. 86 (2008) 2888-2896
54. Silvestri E., de Lange P., Moreno M., Lombardi A., Ragni M., Feola A., Schiavo L., Goglia F., and Lanni A. Fenofibrate activates the biochemical pathways and the de novo expression of genes related to lipid handling and uncoupling protein-3 functions in liver of normal rats. Biochim. Biophys. Acta 1757 (2006) 486-495
55. Skiba-Cassy S., Collin A., Chartrin P., Medale F., Simon J., Duclos M.J., and Tesseraud S. Chicken liver and muscle carnitine palmitoyltransferase 1: nutritional regulation of messengers. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 147 (2007) 278-287
56. Swennen Q., Janssens G.P.J., Collin A., Le Bihan-Duval E., Verbeke K., Decuypere E., and Buyse J. Diet-induced thermogenesis and glucose oxidation in broiler chickens: influence of genotype and diet composition. Poult. Sci. 85 (2006) 731-742
57. Talbot D.A., Hanuise N., Rey B., Rouanet J.L., Duchamp C., and Brand M.D. Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus). Biochem. Biophys. Res. Commun. 312 (2003) 983-988
58. Taouis M., De Basilio V., Mignon-Grasteau S., Crochet S., Bouchot C., Bigot K., Collin A., and Picard M. Early-age thermal conditioning reduces uncoupling protein messenger RNA expression in pectoral muscle of broiler chicks at seven days of age. Poult. Sci. 81 (2002) 1640-1643
59. Toyomizu M., Ueda M., Sato S., Seki Y., Sato K., and Akiba Y. Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. FEBS Lett. 529 (2002) 313-318
60. Turner N., Bruce C.R., Beale S.M., Hoehn K.L., So T., Rolph M.S., and Cooney G.J. Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56 (2007) 2085-2092
61. Vianna C.R., Hagen T., Zhang C.Y., Bachman E., Boss O., Gereben B., Moriscot A.S., Lowell B.B., Bicudo J.E., and Bianco A.C. Cloning and functional characterization of an uncoupling protein homolog in hummingbirds. Physiol. Genomics 5 (2001) 137-145
62. Villarroya F., Iglesias R., and Giralt M. PPARs in the control of uncoupling proteins gene expression. PPAR Res. 2007 (2007) 74364
63. Young M.E., Guthrie P.H., Razeghi P., Leighton B., Abbasi S., Patil S., Youker K.A., and Taegtmeyer H. Impaired long-chain fatty acid oxidation and contractile dysfunction in the obese Zucker rat heart. Diabetes 51 (2002) 2587-2595