Dietary energy sources affect the partition of body lipids and the hierarchy of energy metabolic pathways in growing pigs differing in feed efficiency

Journal of Animal Science

Volumn 92, Issue 11, 2014, Pages 4865-4877

  Gondret, F ^a   Louveau, I ^a   Mourot, J ^a   Duclos, M J ^c   Lagarrigue, S ^a   Gilbert, H ^b   Van Milgen, J ^a  

^a PEGASE   (France)

^b UMR1388 GenPhySE   (France)

^c STATION DE RECHERCHES AVICOLES   (France)

Author keywords

Feed efficiency; Fiber; Glucokinase; Lipid partition; Lipogenesis

Indexed keywords

FAT INTAKE; FATTY ACID SYNTHASE;

ADIPOSE TISSUE; ANIMAL; BODY COMPOSITION; BODY WEIGHT; CALORIC INTAKE; COMPARATIVE STUDY; DIET; DIETARY FIBER; DRUG EFFECTS; ENERGY METABOLISM; FAT INTAKE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; LIVER; MALE; METABOLISM; PHARMACOLOGY; PHYSIOLOGY; PIG; SKELETAL MUSCLE; VETERINARY;

ADIPOSE TISSUE; ANIMALS; BODY COMPOSITION; BODY WEIGHT; DIET; DIETARY FATS; DIETARY FIBER; DRUG EFFECTS; ENERGY INTAKE; ENERGY METABOLISM; FATTY ACID SYNTHASES; GENETICS; GROWTH AND DEVELOPMENT; LIPID METABOLISM; LIVER; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLISM; MUSCLE, SKELETAL; PHARMACOLOGY; PHYSIOLOGY; SWINE; VETERINARY;

EID: 84908261878     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2014-7995     Document Type: Article

References (44)

1. Barea, R., S. Dubois, H. Gilbert, P. Sellier, J. van Milgen, and J. Noblet. 2010. Energy utilization in pigs selected for high and low residual feed intake. J. Anim. Sci. 88:2062–2072. doi:10.2527/ jas.2009-2395
2. Bass, A., D. Brdiczka, P. Eyer, S. Hofer, and D. Pette. 1969. Metabolic differentiation of distinct muscle types at the level of enzymatic organization. Eur. J. Biochem. 10:198–206. doi:10.1111/j.1432-1033.1969.tb00674.x
3. Bazin, R., and P. Ferré. 2001. Assays of lipogenic enzymes. Methods Mol. Biol. 155:121–127.
4. Benmansour, N. M., Y. Demarne, M. J. Lecourtier, and C. Lhuillery. 1991. Effects of dietary fat and adipose tissue location on insulin action in young boar adipocytes. Int. J. Biochem. 23:499–506. doi:10.1016/0020-711X(91)90180-U
5. Birkett, S., and C. F. M. de Lange. 2001. A computational framework for a nutrient flow representation of energy utilization by growing monogastric animals. Br. J. Nutr. 86:647–659. doi:10.1079/BJN2001441
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254. doi:10.1016/0003-2697(76)90527-3
7. Cho, S. Y., P. J. Park, E. S. Shin, J. H. Lee, H. K. Chang, and T. R. Lee. 2009. Proteomic analysis of mitochondrial proteins of basal and lipolytically (isoproterenol and TNF-alpha)-stimulated adipocytes. J. Cell. Biochem. 106:257–266. doi:10.1002/jcb.21998
8. Cruzen, S. M., A. J. Harris, K. Hollinger, R. M. Punt, J. K. Grubbs, J. T. Selsby, J. C. Dekkers, N. K. Gabler, S. M. Lonergan, and E. Huff-Lonergan. 2013. Evidence of decreased muscle protein turnover in gilts selected for low residual feed intake. J. Anim. Sci. 91:4007–4016. doi:10.2527/jas.2013-6413
9. De Lange, C., J. van Milgen, S. Dubois, and J. Noblet. 2006. Energy cost of ingesting and excreting indigestible material in growing pigs is minimal. Anim. Res. 55:551–562. doi:10.1051/animres:2006041
10. Faure, J., L. Lefaucheur, N. Bonhomme, P. Ecolan, K. Meteau, S. M. Coustard, M. Kouba, H. Gilbert, and B. Lebret. 2013. Consequences of divergent selection for residual feed intake in pigs on muscle energy metabolism and meat quality. Meat Sci. 93:37–45. doi:10.1016/j.meatsci.2012.07.006
11. Flachs, P., M. Rossmeisl, O. Kuda, and J. Kopecky. 2013. Stimulation of mitochondrial oxidative capacity in white fat independent of UCP1: A key to lean phenotype. Biochim. Biophys. Acta 1831:986–1003. doi:10.1016/j.bbalip.2013.02.003
12. Gilbert, H., J. P. Bidanel, J. Gruand, J. C. Caritez, Y. Billon, P. Guillouet, H. Lagant, J. Noblet, and P. Sellier. 2007. Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits. J. Anim. Sci. 85:3182–3188. doi:10.2527/jas.2006-590
13. Good, C. A., H. Kramer, and M. Somogyi. 1933. The determination of glycogen. J. Biol. Chem. 100:485–491.
14. Grubbs, J. K., A. N. Fritchen, E. Huff-Lonergan, N. K. Gabler, and S. M. Lonergan. 2013. Selection for residual feed intake alters the mitochondria protein profile in pigs. J. Proteomics 80:334–345. doi:10.1016/j.jprot.2013.01.017
15. Harris, A. J., J. F. Patience, S. M. Lonergan, J. M. Dekkers, and N. K. Gabler. 2012. Improved nutrient digestibility and retention partially explains feed efficiency gains in pigs selected for low residual feed intake. J. Anim. Sci. 90(S4):164–166. doi:10.2527/ jas.53855
16. Kerr, B. J., and G. C. Shurson. 2013. Strategies to improve fiber utilization in swine. J. Anim. Sci. Biotechnol. doi: 10.1186/2049- 1891-4-11.
17. Koch, R. M., L. A. Swiger, D. Chambers, and K. E. Gregory. 1963. Efficiency of feed use in beef cattle. J. Anim. Sci. 22:486–494.
18. Lefaucheur, L., B. Lebret, P. Ecolan, I. Louveau, M. Damon, A. Prunier, Y. Billon, P. Sellier, and H. Gilbert. 2011. Muscle characteristics and meat quality traits are affected by divergent selection on residual feed intake in pigs. J. Anim. Sci. 89:996–1010. doi:10.2527/jas.2010-3493
19. Le Naou, T., N. Le Floc’h, I. Louveau, H. Gilbert, and F. Gondret. 2012. Metabolic changes and tissue responses to selection on residual feed intake in growing pigs. J. Anim. Sci. 90:4771–4780. doi:10.2527/jas.2012-5226
20. Lkhagvadorj, S., L. Qu, W. Cai, O. P. Couture, C. R. Barb, G. J. Hausman, D. Nettleton, L. L. Anderson, J. C. Dekkers, and C. K. Tuggle. 2010. Gene expression profiling of the short-term adaptive response to acute caloric restriction in liver and adipose tissues of pigs differing in feed efficiency. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298:R494–R507. doi:10.1152/ ajpregu.00632.2009
21. Matschinsky, F. M. 1990. Glucokinase as glucose sensor and metabolic signal generator in pancreatic beta-cells and hepatocytes. Diabetes 39:647–652. doi:10.2337/diab.39.6.647
22. Millet, S., S. Kumar, J. De Boever, T. Meyns, M. Aluwé, D. De Brabander, and R. Ducatelle. 2012. Effect of particle size distribution and dietary crude fibre content on growth performance and gastric mucosa integrity of growing-finishing pigs. Vet. J. 192:316–321. doi:10.1016/j.tvjl.2011.06.037
23. Mithieux, G. 1996. Role of glucokinase and glucose-6 phosphatase in the nutritional regulation of endogenous glucose production. Reprod. Nutr. Dev. 36:357–362. doi:10.1051/rnd:19960402
24. Monin, G., and P. Sellier. 1985. Pork of low technological quality with a normal rate of muscle pH fall in the immediate postmortem period: The case of the Hampshire breed. Meat Sci. 13:49–63. doi:10.1016/S0309-1740(85)80004-8
25. Montagne, L., F. Loisel, T. Le Naou, F. Gondret, H. Gilbert, and M. Le Gall. 2014. Difference in short-term responses to a high fiber diet in pigs divergently selected on residual feed intake. J. Anim. Sci. 92:1512–1523. doi:10.2527/jas.2013-6623
26. Morrison and Smith. 1964. Preparation of fatty acid methyl esters and dimethyl acetals from lipids with boron fluoride-methanol. J. Lipid Res. 5:600–608.
27. Munoz, R., J. Estany, M. Tor, and O. Doran. 2013. Hepatic lipogenic enzyme expression in pigs is affected by selection for decreased backfat thickness at constant intramuscular fat content. Meat Sci. 93:746–751. doi:10.1016/j.meatsci.2012.11.045
28. Myer, R. O., and G. E. Combs. 1991. Fat supplementation of diets containing a high level of oats for growing-finishing swine. J. Anim. Sci. 69:4665–4669.
29. Panserat, S., F. Medale, C. Blin, J. Breque, C. Vachot, E. Plagnes- Juan, E. Gomes, R. Krishnamoorthy, and S. Kaushik. 2000. Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R1164–R1170.
30. Ponsuksili, S., E. Murani, C. Walz, M. Schwerin, and K. Wimmers. 2007. Pre- and postnatal hepatic gene expression profiles of two pig breeds differing in body composition: Insight into pathways of metabolic regulation. Physiol. Genomics 29:267–279. doi:10.1152/physiolgenomics.00178.2006
31. Printz, R. L., M. A. Magnuson, and D. K. Granner. 1993. Mammalian glucokinase. Annu. Rev. Nutr. 13:463–496. doi:10.1146/ annurev.nu.13.070193.002335
32. Quemeneur, B., M. Le Roux, and M. Magnin. 2013. Characterization and interest of the feed swelling capacity for the weaned piglets. Journées Rech. Porcine 45:197–198.
33. Quiniou, N., and J. Noblet. 2012. Effect of the dietary net energy concentration on feed intake and performance of growing-finishing pigs housed individually. J. Anim. Sci. 90:4362–4372. doi:10.2527/jas.2011-4004
34. Sahena, F., I. S. M. Zaidul, S. Jinap, A. A. Karim, K. A. Abbas, N. A. N. Norulaini, and A. K. M. Omar. 2009. Application of supercritical CO2 in lipid extraction. J. Food Eng. 95:240–253. doi:10.1016/j.jfoodeng.2009.06.026
35. Simoneau, J. A., and D. E. Kelley. 1997. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 83:166–171.
36. Smith, R. M., N. K. Gabler, J. M. Young, W. Cai, N. J. Boddicker, M. J. Anderson, E. Huff-Lonergan, J. C. Dekkers, and S. M. Lonergan. 2011. Effects of selection for decreased residual feed intake on composition and quality of fresh pork. J. Anim. Sci. 89:192–200. doi:10.2527/jas.2010-2861
37. Srere, P. A. 1969. Citrate synthase: EC 4.1.3.7. Citrate oxaloacetatelyase (CoA-acetylating). Methods Enzymol. 13:3–11.
38. Tranulis, M. A., O. Dregni, B. Christophersen, A. Krogdahl, and B. Borrebaek. 1996. A glucokinase-like-enzyme in the liver of Atlantic salmon (Salmo salar). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 114:35–39. doi:10.1016/0305- 0491(95)02119-1
39. van Soest, P. J., and R. H. Wine. 1967. Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J. Assoc. Off. Anal. Chem. 50:50–55.
40. Varel, V. H., and J. T. Yen. 1997. Microbial perspective on fiber utilization by swine. J. Anim. Sci. 75:2715–2722.
41. Vincent, A., I. Louveau, F. Gondret, B. Lebret, and M. Damon. 2012. Mitochondrial function, fatty acid metabolism, and immune system are relevant features of pig adipose tissue development. Physiol. Genomics 44:1116–1124. doi:10.1152/physiolgenomics. 00098.2012
42. Whittemore, E. C., I. Kyriazakis, B. J. Tolkamp, and G. C. Emmans. 2002. The short-term feeding behavior of growing pigs fed foods differing in bulk content. Physiol. Behav. 76:131–141. doi:10.1016/S0031-9384(02)00686-8
43. Wilson-Fritch, L., S. Nicoloro, M. Chouinard, M. A. Lazar, P. C. Chui, J. Leszyk, J. Straubhaar, M. P. Czech, and S. Corvera. 2004. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114:1281–1289. doi:10.1172/JCI200421752
44. Yan, H., R. Potu, H. Lu, V. Vezzoni de Almeida, T. Stewart, D. Ragland, A. Armstrong, O. Adeola, C. H. Nakatsu, and K. M. Ajuwon. 2013. Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig. PLoS ONE 8:e59581. doi:10.1371/journal.pone.0059581