Acute cold and exercise training up-regulate similar aspects of fatty acid transport and catabolism in house sparrows (Passer domesticus)

Journal of Experimental Biology

Volumn 218, Issue 24, 2015, Pages 3885-3893

  Zhang, Yufeng ^a   Carter, Travis ^a   Eyster, Kathleen ^b   Swanson, David L ^a  

^a University of South Dakota   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Carnitine palmitoyl transferase; Citrate synthase; Cold training; Exercise training; Fatty acid binding protein; Fatty acid translocase; Phenotypic flexibility; Hydroxyacyl CoA dehydrogenase

Indexed keywords

FATTY ACID;

ADAPTATION; ANIMAL; ANIMAL EXPERIMENT; BASAL METABOLIC RATE; CARDIAC MUSCLE; COLD; ENERGY METABOLISM; GENE EXPRESSION; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; SPARROW; THERMOGENESIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASAL METABOLISM; COLD TEMPERATURE; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION; LIPID METABOLISM; MUSCLE, SKELETAL; MYOCARDIUM; PHYSICAL CONDITIONING, ANIMAL; SPARROWS; THERMOGENESIS;

EID: 84963706201     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.126128     Document Type: Article

References (69)

1. Arendt, D. H., Smith, J. P., Bastida, C. C., Prasad, M. S., Oliver, K. D., Eyster, K. M., Summers, T. R., Delville, Y. and Summers, C. H. (2012). Contrasting hippocampal and amygdalar expression of genes related to neural plasticity during escape from social aggression. Physiol. Behav. 107, 670-679.
2. Bonen, A., Miskovic, D. and Kiens, B. (1999). Fatty acid transporters (FABPpm, FAT, FATP) in human muscle. Can. J. Appl. Physiol. 24, 515-523.
3. Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Rasbach, K. A., Boström, E. A., Choi, J. H., Long, J. Z. et al. (2012). A PGC1α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468.
4. Bradley, N. S., Snook, L. A., Jain, S. S., Heigenhauser, G. J. F., Bonen, A. and Spriet, L. L. (2012). Acute endurance exercise increases plasma membrane fatty acid transport proteins in rat and human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 302, E183-E189.
5. Bruce, C. R., Thrush, A. B., Mertz, V. A., Bezaire, V., Chabowski, A., Heigenhauser, G. J. F. and Dyck, D. J. (2006). Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am. J. Physiol. Endocrinol. Metab. 291, E99-E107.
6. Burgomaster, K. A., Heigenhauser, G. J. F. and Gibala, M. J. (2006). Effect of shortterm sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-Trial performance. J. Appl. Physiol. 100, 2041-2047.
7. Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobowchuk, M., MacDonald, M. J., McGee, S. L. and Gibala, M. J. (2008). Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586, 151-160.
8. Buttemer, W., Bech, C. and Chappell, M. (2010). Citrate synthase activity does not account for age-related differences in maximum aerobic performance in House Sparrows (Passer domesticus). Aust. Zool. 35, 378-382.
9. Campbell, S. E., Tandon, N. N., Woldegiorgis, G., Luiken, J. J. F. P., Glatz, J. F. C. and Bonen, A. (2004). A novel function for Fatty Acid Translocase (FAT)/CD36: involvement in long chain fatty acid transfer into the mitochondria. J. Biol. Chem. 279, 36235-36241.
10. Chabowski, A., Chatham, J. C., Tandon, N. N., Calles-Escandon, J., Glatz, J. F. C., Luiken, J. J. F. P. and Bonen, A. (2006). Fatty acid transport and FAT/CD36 are increased in red but not in white skeletal muscle of ZDF rats. Am. J. Physiol. Endocrinol. Metab. 291, E675-E682.
11. Chabowski, A., Górski, J., Luiken, J. J. F. P., Glatz, J. F. C. and Bonen, A. (2007). Evidence for concerted action of FAT/CD36 and FABPpm to increase fatty acid transport across the plasma membrane. Prostaglandins. Leukot. Essent. Fatty Acids 77, 345-353.
12. Dawson, W. R. and Marsh, R. L. (1989). Metabolic acclimatization to cold and season in birds. In Physiology of Cold Adaptation in Birds (ed. C. Bech and R. E. Reinertsen), pp. 83-94. New York: Plenum.
13. Driedzic, W. R., Crowe, H. L., Hicklin, P. W. and Sephton, D. H. (1993). Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can. J. Zool. 71, 1602-1608.
14. Fu, M.-h. H., Maher, A. C., Hamadeh, M. J., Ye, C. and Tarnopolsky, M. A. (2009). Exercise, sex, menstrual cycle phase, and 17β-estradiol influence metabolismrelated genes in human skeletal muscle. Physiol. Genomics 40, 34-47.
15. Gagnon, D. D., Rintamäki, H., Gagnon, S. S., Oksa, J., Porvari, K., Cheung, S. S., Herzig, K.-H. and Kyröläinen, H. (2014). Fuel selection during short-Term submaximal treadmill exercise in the cold is not affected by pre-exercise lowintensity shivering. Appl. Physiol. Nutr. Metab. 39, 282-291.
16. Glatz, J. F. C., Luiken, J. J. F. P. and Bonen, A. (2010). Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol. Rev. 90, 367-417.
17. Guglielmo, C. G. (2010). Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr. Comp. Biol. 50, 336-345.
18. Guglielmo, C. G., Haunerland, N. H., Hochachka, P. W. and Williams, T. D. (2002). Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am. J. Physiol. 282, R1405-R1413.
19. Haman, F., Péronnet, F., Kenny, G. P., Massicotte, D., Lavoie, C. and Weber, J.-M. (2005). Partitioning oxidative fuels during cold exposure in humans: muscle glycogen becomes dominant as shivering intensifies. J. Physiol. 566, 247-256.
20. Hamilton, J. A., Kamp, F. and Guo, W. (2002).Mechanism of cellular uptake of longchain fatty acids: do we need cellular proteins? Mol. Cell. Biochem. 239, 17-23.
21. Hammond, K. A., Chappell, M. A., Cardullo, R. A., Lin, R.-s. and Johnsen, T. S. (2000). The mechanistic basis of aerobic performance variation in red junglefowl. J. Exp. Biol. 203, 2053-2064.
22. Helge, J. W. and Kiens, B. (1997). Muscle enzyme activity in humans: role of substrate availability and training. Am. J. Physiol. 272, R1620-R1624.
23. Holloway, G. P., Bezaire, V., Heigenhauser, G. J. F., Tandon, N. N., Glatz, J. F. C., Luiken, J. J. F. P., Bonen, A. and Spriet, L. L. (2006). Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase I activity in human skeletal muscle during aerobic exercise. J. Physiol. 571, 201-210.
24. Jenni-Eiermann, S., Jenni, L., Kvist, A., Lindstrom, A., Piersma, T. and Visser, G. H. (2002). Fuel use and metabolic response to endurance exercise: A wind tunnel study of a long-distance migrant shorebird. J. Exp. Biol. 205, 2453-2460.
25. Jeppesen, J., Jordy, A. B., Sjøberg, K. A., Füllekrug, J., Stahl, A., Nybo, L. and Kiens, B. (2012). Enhanced fatty acid oxidation and FATP4 protein expression after endurance exercise training in human skeletal muscle. PLoS ONE 7, e29391.
26. Kiens, B. (2006). Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol. Rev. 86, 205-243.
27. Kiens, B., Roepstorff, C., Glatz, J. F. C., Bonen, A., Schjerling, P., Knudsen, J. and Nielsen, J. N. (2004). Lipid-binding proteins and lipoprotein lipase activity in human skeletal muscle: influence of physical activity and gender. J. Appl. Physiol. 97, 1209-1218.
28. Lee, J. K., Lee, J. S., Park, H., Cha, Y.-S., Yoon, C. S. and Kim, C. K. (2007). Effect of L-carnitine supplementation and aerobic training on FABPc content and β-HAD activity in human skeletal muscle. Eur. J. Appl. Physiol. 99, 193-199.
29. Liknes, E. T. and Swanson, D. L. (2011). Phenotypic flexibility in passerine birds: seasonal variation of aerobic enzyme activities in skeletal muscle. J. Therm. Biol. 36, 430-436.
30. Liknes, E. T., Guglielmo, C. G. and Swanson, D. L. (2014). Phenotypic flexibility in passerine birds: seasonal variation in fuel storage, mobilization and transport. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 174, 1-10.
31. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-δδC(T))method. Methods 25, 402-408.
32. Luiken, J. J. F. P., Dyck, D. J., Han, X.-X., Tandon, N. N., Arumugam, Y., Glatz, J. F. C. and Bonen, A. (2002). Insulin induces the translocation of the fatty acid transporter FAT/CD36 to the plasma membrane. Am. J. Physiol. Endocrinol. Metab. 282, E491-E495.
33. Luiken, J. J. F. P., Koonen, D. P. Y., Coumans, W. A., Pelsers, M. M. A. L., Binas, B., Bonen, A. and Glatz, J. F. C. (2003). Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-Type-FABP null mice. Lipids 38, 491-496.
34. McFarlan, J. T., Bonen, A. and Guglielmo, C. G. (2009). Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-Throated sparrows (Zonotrichia albicollis). J. Exp. Biol. 212, 2934-2940.
35. McWilliams, S. R., Guglielmo, C., Pierce, B. and Klaassen, M. (2004). Flying, fasting, and feeding in birds during migration: A nutritional and physiological ecology perspective. J. Avian Biol. 35, 377-393.
36. Mezentseva, N. V., Kumaratilake, J. S. and Newman, S. A. (2008). The brown adipocyte differentiation pathway in birds: An evolutionary road not taken. BMC Biol. 6, 17.
37. OConnor, T. P. (1995). Seasonal acclimatization of lipid mobilization and catabolism in house finches (Carpodacus mexicanus). Physiol. Zool. 68, 985-1005.
38. Odland, L. M., Howlett, R. A., Heigenhauser, G. J., Hultman, E. and Spriet, L. L. (1998). Skeletal muscle malonyl-CoA content at the onset of exercise at varying power outputs in humans. Am. J. Physiol. 274, E1080-E1085.
39. Petit, M. and Vézina, F. (2014). Phenotype manipulations confirm the role of pectoral muscles and haematocrit in avian maximal thermogenic capacity. J. Exp. Biol. 217, 824-830.
40. Piersma, T. and Dietz, M. W. (2007). Twofold seasonal variation in the supposedly constant, species-specific, ratio of upstroke to downstroke flight muscles in red knots Calidris canutus. J. Avian Biol. 38, 536-540.
41. Price, E. R., McFarlan, J. T. and Guglielmo, C. G. (2010). Preparing for migration? The effects of photoperiod and exercise on muscle oxidative enzymes, lipid transporters, and phospholipids in white-crowned sparrows. Physiol. Biochem. Zool. 83, 252-262.
42. Price, E. R., Staples, J. F., Milligan, C. L. and Guglielmo, C. G. (2011). Carnitine palmitoyl transferase activity and whole muscle oxidation rates vary with fatty acid substrate in avian flight muscles. J. Comp. Physiol. B 181, 565-573.
43. Putri, M., Syamsunarno, M. R. A. A., Iso, T., Yamaguchi, A., Hanaoka, H., Sunaga, H., Koitabashi, N., Matsui, H., Yamazaki, C., Kameo, S. et al. (2015). CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem. Biophys. Res. Commun. 457, 520-525.
44. Roepstorff, C., Helge, J.W., Vistisen, B. and Kiens, B. (2004). Studies of plasma membrane fatty acid-binding protein and other lipid-binding proteins in human skeletal muscle. Proc. Nutr. Soc. 63, 239-244.
45. Schaeffer, P. J., Hokanson, J. F., Wells, D. J. and Lindstedt, S. L. (2001). Cold exposure increases running VO2max) and cost of transport in goats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R42-R47.
46. Schenk, S. and Horowitz, J. F. (2006). Coimmunoprecipitation of FAT/CD36 and CPT I in skeletal muscle increases proportionally with fat oxidation after endurance exercise training. Am. J. Physiol. 291, E254-E260.
47. Siu, P. M., Donley, D. A., Bryner, R. W. and Alway, S. E. (2003). Citrate synthase expression and enzyme activity after endurance training in cardiac and skeletal muscles. J. Appl. Physiol. 94, 555-560.
48. Starritt, E. C., Howlett, R. A., Heigenhauser, G. J. and Spriet, L. L. (2000). Sensitivity of CPT I to malonyl-CoA in trained and untrained human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 278, E462-E468.
49. Stephens, F. B., Constantin-Teodosiu, D. and Greenhaff, P. L. (2007). New insights concerning the role of carnitine in the regulation of fuel metabolism in skeletal muscle. J. Physiol. 581, 431-444.
50. Suarez, R. K. (1998). Oxygen and the upper limits to animal design and performance. J. Exp. Biol. 201, 1065-1072.
51. Swanson, D. L. (2010). Seasonal metabolic variation in birds: functional and mechanistic correlates. In Current Ornithology, Vol. 17 (ed. C. F. Thompson), pp. 75-129. New York: Springer.
52. Swanson, D. L. and Dean, K. L. (1999). Migration-induced variation in thermogenic capacity in migratory passerines. J. Avian Biol. 30, 245-254.
53. Swanson, D. L. and King, M. O. (2013). Short-Term captivity influences maximal cold-induced metabolic rates and their repeatability in summer-Acclimatized American goldfinches Spinus tristis. Curr. Zool. 59, 439-448.
54. Swanson, D. L. and Liknes, E. T. (2006). A comparative analysis of thermogenic capacity and cold tolerance in small birds. J. Exp. Biol. 209, 466-474.
55. Swanson, D. L., Zhang, Y. and King, M. O. (2013). Individual variation in thermogenic capacity is correlated with flight muscle size but not cellular metabolic capacity in American goldfinches (Spinus tristis). Physiol. Biochem. Zool. 86, 421-431.
56. Swanson, D. L., Zhang, Y. and King, M. (2014a). Mechanistic drivers of flexibility in summit metabolic rates of small birds. PLoS ONE 9, e101577.
57. Swanson, D., Zhang, Y., Liu, J.-S., Merkord, C. L. and King, M. O. (2014b). Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J. Exp. Biol. 217, 866-875.
58. Talanian, J. L., Galloway, S. D. R., Heigenhauser, G. J. F., Bonen, A. and Spriet, L. L. (2007). Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J. Appl. Physiol. 102, 1439-1447.
59. Talanian, J. L., Holloway, G. P., Snook, L. A., Heigenhauser, G. J. F., Bonen, A. and Spriet, L. L. (2010). Exercise training increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am. J. Physiol. 299, E180-E188.
60. Tremblay, A., Simoneau, J.-A. and Bouchard, C. (1994). Impact of exercise intensity on body fatness and skeletal muscle metabolism. Metabolism 43, 814-818.
61. Tunstall, R. J., Mehan, K. A., Wadley, G. D., Collier, G. R., Bonen, A., Hargreaves, M. and Cameron-Smith, D. (2002). Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am. J. Physiol. 283, E66-E72.
62. van Loon, L. J. C., Greenhaff, P. L., Constantin-Teodosiu, D., Saris, W. H. M. and Wagenmakers, A. J. M. (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. J. Physiol. 536, 295-304.
63. Vézina, F. and Williams, T. D. (2005). Interaction between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European starlings: implications for metabolic rate and organ mass relationships. Funct. Ecol. 19, 119-128.
64. Weber, T. P. and Piersma, T. (1996). Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canutus. J. Avian Biol. 27, 215-224.
65. Yang, Y., Creer, A., Jemiolo, B. and Trappe, S. (2005). Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J. Appl. Physiol. 98, 1745-1752.
66. Zajac, D. M., Cerasale, D. J., Landman, S. and Guglielmo, C. G. (2011). Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. Gen. Comp. Endocrinol 174, 269-275.
67. Zhang, Y., King, M. O., Harmon, E. and Swanson, D. L. (2015a). Summer-Towinter phenotypic flexibility of fatty acid transport and catabolism in skeletal muscle and heart of small birds. Physiol. Biochem. Zool. 88, 535-549.
68. Zhang, Y., Eyster, K., Liu, J.-S. and Swanson, D. L. (2015b). Cross-Training in birds: cold and exercise training produce similar changes in maximal metabolic output, muscle masses and myostatin expression in house sparrows, Passer domesticus. J. Exp. Biol. 218, 2190-2200.
69. Zhang, Y., King, M. O., Harmon, E., Eyster, K. and Swanson, D. L. (2015c). Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds. J. Comp. Physiol. B 185, 797-810.