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Animal Models

Chickens from lines selected for high and low body weight show differences in fatty acid oxidation efficiency and metabolic flexibility in skeletal muscle and white adipose tissue

International Journal of Obesity volume 38, pages 1374–1382 (2014)Cite this article

Subjects

Abstract

Objective:

The Virginia lines of chickens have resulted from more than 55 generations of artificial selection for low (LWS) or high (HWS) juvenile body weight. We hypothesized that the relative hyperphagia and greater body weight in juvenile HWS chickens are associated with altered fatty acid oxidation efficiency and metabolic flexibility in tissues associated with energy sensing and storage, and relative cellular hypertrophy in white adipose tissue.

Methods:

Hypothalamus, liver, pectoralis major, gastrocnemius, abdominal fat, clavicular fat and subcutaneous fat were collected from the juvenile (56–65 days old) LWS and HWS chickens for metabolic, gene expression and histological assays.

Results:

The HWS chickens had reduced fatty acid oxidation efficiency in abdominal fat (P<0.0001) and reduced rates of oxidation in abdominal fat and gastrocnemius (P<0.0001) as compared with the LWS. There was reduced citrate synthase activity in white adipose tissue (P<0.0001) and greater metabolic inflexibility in skeletal muscle (P=0.006) of the HWS compared with the LWS. Greater pyruvate dehydrogenase kinase 4 (PDK4) and forkhead box O1A (FoxO1) mRNA were found in skeletal muscle and white adipose tissue of 56-day-old HWS than LWS. Expression of peroxisome proliferator-activated receptor γ (PPARγ) in all adipose tissue depots was greater (P<0.05) in LWS than in HWS chickens. The HWS chickens had larger (P<0.0001) and fewer (P<0.0001) adipocytes per unit area than the LWS.

Conclusion:

Compared with the LWS, the HWS chickens have impaired metabolic flexibility and fatty acid oxidation efficiency due to greater pyruvate dehydrogenase activity to accommodate the influx of acetyl-CoA from fatty acid oxidation in skeletal muscle and adipose tissue. These metabolic adaptations can be linked to differences in gene expression regulation, adipocyte cellularity and body composition between the lines, which may provide valuable insight into metabolic disorders in other species.

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References

  1. Dunnington EA, Siegel PB . Long-term divergent selection for eight-week body weight in white Plymouth rock chickens. Poult Sci 1996; 75:1168–1179.

    Article  CAS  Google Scholar 

  2. Zelenka DJ, Dunnington EA, Cherry JA, Siegel PB . Anorexia and sexual maturity in female white rock chickens. I. Increasing the feed intake. Behav Genet 1988; 18: 383–387.

    Article  CAS  Google Scholar 

  3. Dunnington EA, Siegel PB, Cherry JA, Jones DE, Zelenka DJ . Physiological traits in adult female chickens after selection and relaxation of selection for 8-week body weight. J Anim Breedg Genet 1986; 103: 51–58.

    Article  Google Scholar 

  4. Dunnington EA, Honaker CF, McGilliard ML, Siegel PB . Phenotypic responses of chickens to long-term, bidirectional selection for juvenile body weight—historical perspective. Poult Sci 2013; 92: 1724–1734.

    Article  CAS  Google Scholar 

  5. Katanbaf MN, Dunnington EA, Siegel PB . Allomorphic relationships from hatching to 56 days in parental lines and F1 crosses of chickens selected 27 generations for high or low body weight. Growth Dev Aging 1988; 52: 11–21.

    CAS  PubMed  Google Scholar 

  6. Burgener JA, Cherry JA, Siegel PB . The association between sartorial fat and fat deposition in meat-type chickens. Poultry Sci 1981; 60: 54–62.

    Article  Google Scholar 

  7. Zhang W, Sumners LH, Siegel PB, Cline MA, Gilbert ER . Quantity of glucose transporter and appetite-associated factor mRNA in various tissues after insulin injection in chickens selected for low or high body weight. Physiol Genomics 2013; 45: 1084–1094.

    Article  CAS  Google Scholar 

  8. Kuo AY, Cline MA, Werner E, Siegel PB, Denbow DM . Leptin effects on food and water intake in lines of chickens selected for high or low body weight. Physiol Behav 2005; 84: 459–464.

    Article  CAS  Google Scholar 

  9. Newmyer BA, Siegel PB, Cline MA . Neuropeptide AF differentially affects anorexia in lines of chickens selected for high or low body weight. J Neuroendocrinol 2010; 22: 593–598.

    Article  CAS  Google Scholar 

  10. Smith ML, Prall BC, Siegel PB, Cline MA . The threshold of insulin-induced hypophagia is lower in chicks selected for low rather than high juvenile body weight. Behav Brain Res 2011; 216: 719–722.

    Article  CAS  Google Scholar 

  11. Cline MA, Kuo AY, Smith ML, Nandar W, Prall BC, Siegel PB et al. Differential feed intake responses to central corticotrophin releasing factor in lines of chickens divergently selected for low or high body weight. Comp Biochem Physiol Part A Mol Integr Physiol 2009; 152: 130–134.

    Article  Google Scholar 

  12. Cline MA, Nandar W, Bowden C, Calchary W, Smith ML, Prall B et al. The threshold of amylin-induced anorexia is lower in chicks selected for low compared to high juvenile body weight. Behav Brain Res 2010; 208: 650–654.

    Article  CAS  Google Scholar 

  13. Cline MA, Nandar W, Bowden C, Hein PP, Denbow DM, Siegel PB . Differential feeding responses to central alpha-melanocyte stimulating hormone in genetically low and high body weight selected lines of chickens. Life Sci 2008; 83: 208–213.

    Article  CAS  Google Scholar 

  14. Cline MA, Prall BC, Smith ML, Calchary WA, Siegel PB . Differential appetite-related responses to central neuropeptide S in lines of chickens divergently selected for low or high body weight. J Neuroendocrinol 2008; 20: 904–908.

    Article  CAS  Google Scholar 

  15. Cline MA, Siders R, Newmyer BA, Smith ML, Siegel PB . Both calcitonin and calcitonin gene-related peptides' thresholds of hypophagia are considerably lower in chicks selected for high rather than low juvenile body weight. Physiol Behav 2010; 101: 254–259.

    Article  CAS  Google Scholar 

  16. Newmyer BA, Nandar W, Webster RI, Gilbert E, Siegel PB, Cline MA . Neuropeptide Y is associated with changes in appetite-associated hypothalamic nuclei but not food intake in a hypophagic avian model. Behav Brain Res 2013; 236: 327–331.

    Article  CAS  Google Scholar 

  17. Calabotta DF, Cherry JA, Siegel PB, Jones DE . Lipogenesis and lipolysis in fed and fasted chicks from high and low body weight lines. Poult Sci 1985; 64: 700–704.

    Article  CAS  Google Scholar 

  18. Robey WW, Van Krey HP, Cherry JA, Siegel PB, Bliss BA . Adipocyte dynamics in the retroperitioneal fat depot of genetically selected adult high- and low-weight line chickens. Arch. Gerflugelk 1992; 56: 68–72.

    Google Scholar 

  19. Robey WW, Cherry JA, Siegel PB, Van Krey HP . Hyperplastic response of adipose tissue to caloric overconsumption in sexually mature chickens. Poult Sci 1988; 67: 800–808.

    Article  CAS  Google Scholar 

  20. Sinsigalli NA, McMurtry JP, Cherry JA, Siegel PB . Glucose tolerance, plasma insulin and immunoreactive glucagon in chickens selected for high and low body weight. J Nutr 1987; 117: 941–947.

    Article  CAS  Google Scholar 

  21. Smith ML, Prall BC, Siegel PB, Cline MA . The threshold of insulin-induced hypophagia is lower in chicks selected for low rather than high juvenile body weight. Behav Brain Res 2011; 216: 719–722.

    Article  CAS  Google Scholar 

  22. Galgani JE, Moro C, Ravussin E . Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 2008; 295: E1009–E1017.

    Article  CAS  Google Scholar 

  23. Sugden MC . PDK4: a factor in fatness? Obes Res 2003; 11: 167–169.

    Article  Google Scholar 

  24. Sugden MC, Holness MJ . Interactive regulation of the pyruvate dehydrogenase complex and the carnitine palmitoyltransferase system. FASEB J 1994; 8: 54–61.

    Article  CAS  Google Scholar 

  25. Holness MJ, Kraus A, Harris RA, Sugden MC . Targeted upregulation of pyruvate dehydrogenase kinase (PDK)-4 in slow-twitch skeletal muscle underlies the stable modification of the regulatory characteristics of PDK induced by high-fat feeding. Diabetes 2000; 49: 775–781.

    Article  CAS  Google Scholar 

  26. Kwon HS, Harris RA . Mechanisms responsible for regulation of pyruvate dehydrogenase kinase 4 gene expression. Adv Enzyme Regul 2004; 44: 109–121.

    Article  CAS  Google Scholar 

  27. Gudi R, Bowker-Kinley MM, Kedishvili NY, Zhao Y, Popov KM . Diversity of the pyruvate dehydrogenase kinase gene family in humans. J Biol Chem 1995; 270: 28989–28994.

    Article  CAS  Google Scholar 

  28. Strumilo S . Short-term regulation of the mammalian pyruvate dehydrogenase complex. Acta Biochim Pol 2005; 52: 759–764.

    CAS  PubMed  Google Scholar 

  29. Wu P, Inskeep K, Bowker-Kinley MM, Popov KM, Harris RA . Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 1999; 48: 1593–1599.

    Article  CAS  Google Scholar 

  30. Constantin-Teodosiu D, Constantin D, Stephens F, Laithwaite D, Greenhaff PL . The role of FOXO and PPAR transcription factors in diet-mediated inhibition of PDC activation and carbohydrate oxidation during exercise in humans and the role of pharmacological activation of PDC in overriding these changes. Diabetes 2012; 61: 1017–1024.

    Article  CAS  Google Scholar 

  31. Guarente L, Kenyon C . Genetic pathways that regulate ageing in model organisms. Nature 2000; 408: 255–262.

    Article  CAS  Google Scholar 

  32. Gross DN, van den Heuvel AP, Birnbaum MJ . The role of FoxO in the regulation of metabolism. Oncogene 2008; 27: 2320–2336.

    Article  CAS  Google Scholar 

  33. Furuyama T, Kitayama K, Yamashita H, Mori N . Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 2003; 375: 365–371.

    Article  CAS  Google Scholar 

  34. Sears DD, Hsiao A, Ofrecio JM, Chapman J, He W, Olefsky JM . Selective modulation of promoter recruitment and transcriptional activity of PPARgamma. Biochem Biophys Res Commun 2007; 364: 515–521.

    Article  CAS  Google Scholar 

  35. Wan Z, Thrush AB, Legare M, Frier BC, Sutherland LN, Williams DB et al. Epinephrine-mediated regulation of PDK4 mRNA in rat adipose tissue. Am J Physiol Cell Physiol 2010; 299: C1162–C1170.

    Article  CAS  Google Scholar 

  36. Attia RR, Connnaughton S, Boone LR, Wang F, Elam MB, Ness GC et al. Regulation of pyruvate dehydrogenase kinase 4 (PDK4) by thyroid hormone: role of the peroxisome proliferator-activated receptor gamma coactivator (PGC-1 alpha). J Biol Chem 2010; 285: 2375–2385.

    Article  CAS  Google Scholar 

  37. Marquez GC, Speidel SE, Enns RM, Garrick DJ . Genetic diversity and population structure of American Red Angus cattle. J Anim Sci 2010; 88: 59–68.

    Article  CAS  Google Scholar 

  38. Puelles L . The Chick Brain in Stereotaxic Coordinates: An Atlas Featuring Neuromeric Subdivisions and Mammalian Homologies. 1st edn.Academic Press: Amsterdam; Boston, 2007.

    Google Scholar 

  39. Frisard MI, McMillan RP, Marchand J, Wahlberg KA, Wu Y, Voelker KA et al. Toll-like receptor 4 modulates skeletal muscle substrate metabolism. Am J Physiol Endocrinol Metab 2010; 298: E988–E998.

    Article  CAS  Google Scholar 

  40. Power RA, Hulver MW, Zhang JY, Dubois J, Marchand RM, Ilkayeva O et al. Carnitine revisited: potential use as adjunctive treatment in diabetes. Diabetologia 2007; 50: 824–832.

    Article  CAS  Google Scholar 

  41. Anderson AS, Roberts PC, Frisard MI, McMillan RP, Brown TJ, Lawless MH et al. Metabolic changes during ovarian cancer progression as targets for sphingosine treatment. Exp Cell Res 2013; 319: 1431–1442.

    Article  CAS  Google Scholar 

  42. Lopaschuk GD, Ussher JR, Jaswal JS . Targeting intermediary metabolism in the hypothalamus as a mechanism to regulate appetite. Pharmacol Rev 2010; 62: 237–264.

    Article  CAS  Google Scholar 

  43. Lopez M, Vidal-Puig A . Brain lipogenesis and regulation of energy metabolism. Curr Opin Clin Nutr Metab Care 2008; 11: 483–490.

    Article  CAS  Google Scholar 

  44. Serra D, Mera P, Malandrino MI, Mir JF, Herrero L . Mitochondrial fatty acid oxidation in obesity. Antioxid Redox Signal 2013; 19: 269–284.

    Article  CAS  Google Scholar 

  45. Ashmore CR, Doerr L . Postnatal development of fiber types in normal and dystrophic skeletal muscle of the chick. Exp Neurol 1971; 30: 431–446.

    Article  CAS  Google Scholar 

  46. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 2012; 590: 3349–3360.

    Article  CAS  Google Scholar 

  47. Jeong JY, Jeoung NH, Park KG, Lee IK . Transcriptional regulation of pyruvate dehydrogenase kinase. Diabetes Metab J 2012; 36: 328–335.

    Article  Google Scholar 

  48. Maffeis C, Silvagni D, Bonadonna R, Grezzani A, Banzato C, Tato L . Fat cell size, insulin sensitivity, and inflammation in obese children. J Pediatr 2007; 151: 647–652.

    Article  CAS  Google Scholar 

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Acknowledgements

We wish to acknowledge the Paul B Siegel Poultry Center Farm Manager, Mike Graham, for his outstanding support in the chicken trials.

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Authors and Affiliations

  1. Department of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA, USA

    S Zhang, P B Siegel, L H Sumners, W Zhang, M A Cline & E R Gilbert

  2. Department of Human Nutrition, Foods and Exercise and Metabolic Phenotyping Core, Virginia Tech, Blacksburg, VA, USA

    R P McMillan & M W Hulver

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  1. S Zhang
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  2. R P McMillan
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Correspondence to E R Gilbert.

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Zhang, S., McMillan, R., Hulver, M. et al. Chickens from lines selected for high and low body weight show differences in fatty acid oxidation efficiency and metabolic flexibility in skeletal muscle and white adipose tissue. Int J Obes 38, 1374–1382 (2014). https://doi.org/10.1038/ijo.2014.8

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