Molecular mechanisms underlying the development of endothermy in birds (Gallus gallus): A new role of PGC-1α?

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 6, 2007, Pages

  Walter, Isabel ^a   Seebacher, Frank ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cytochrome c oxidase; Hypothermic; Metabolism; Oxidative capacity; Peroxisome proliferator activated receptor

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CHICKEN; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE EXPRESSION; LIVER DEVELOPMENT; LIVER METABOLISM; METABOLISM; MUSCLE DEVELOPMENT; NONHUMAN; PECTORAL MUSCLE; PRIORITY JOURNAL; PROTEIN FUNCTION; SKELETAL MUSCLE; THERMOREGULATION; TRANSCRIPTION REGULATION;

ANIMALS; BASAL METABOLISM; BODY TEMPERATURE REGULATION; CHICK EMBRYO; CHICKENS; PPAR GAMMA;

EID: 36849094046     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00505.2007     Document Type: Article

References (65)

1. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu PH, Rybkin II, Shelton JM, Manieri M, Cinti S, Schoen FJ, Bassel-Duby R, Rosenzweig A, Ingwall JS, Spiegelman BM. Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle. Cell Metab 1: 259-271, 2005.
2. Aulie A, Grav HJ. Effect of cold acclimation on the oxidative capacity of skeletal muscles and liver in young bantam chicks. Comp Biochem Physiol A 62: 335-338, 1979.
3. Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H, Moreteau B, Vergilino R, David JR. Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18: 700-706, 2004.
4. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen MAY, Kelly DP, Holloszy JO. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16: 1879-1886, 2002.
5. Bennett AF, Hicks JW, Cullum AJ. An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution 54: 1768-1773, 2000.
6. Bennett AF, Ruben JA. Endothermy and activity in vertebrates. Science 206: 649-654, 1979.
7. Black JL, Burggren WW. Acclimation to hypothermic incubation in developing chicken embryos (Gallus domesticus): I. Developmental effects and chronic and acute metabolic adjustments. J Exp Biol 207: 1543-1552, 2004.
8. Boulant JA. Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clin Infect Dis 31, Suppl 5: S157-S161, 2000.
9. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37: 755-767, 2004.
10. Choi IH, Ricklefs RE, Shea RE. Skeletal-muscle growth, enzyme-activities, and the development of thermogenesis - a comparison between altricial and precocial birds. Physiol Zool 66: 455-473, 1993.
11. Decuypere E. Incubation-temperature in relation to postnatal performance in chickens. Archiv Fur Experimentelle Veterinarmedizin 38: 439-449, 1984.
12. Desvergne B, Michalik L, Wahli W. Be fit or be sick: peroxisome proliferator-activated receptors are down the road. Mol Endocrinol 18: 1321-1332, 2004.
13. Dickson AJ. Gluconeogenesis in chick-embryo isolated hepatocytes. Int J Biochem 15: 861-865, 1983.
14. DiMicco JA, Zaretsky DV. The dorsomedial hypothalamus: a new player in thermoregulation. Am J Physiol Regul Integr Comp Physiol 292: R47-R63, 2007.
15. Finck BN, Kelly DP. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116: 615-622, 2006.
16. Freake HC, Oppenheimer JH. Thermogenesis and thyroid-function. Annu Rev Nutr 15: 263-291, 1995.
17. Greenbaum D, Colangelo C, Williams K, Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4: 2003.
18. Hayes JP, Garland T. The evolution of endothermy-testing the aerobic capacity model. Evolution 49: 836-847, 1995.
19. Hellon RF, Taylor DCM. An analysis of a thermal afferent pathway in the rat. J Physiol 326: 319-328, 1982.
20. Herzig S, Long FX, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183, 2001.
21. Hirabayashi M, Ijiri D, Kamei Y, Tajima A, Kanai Y. Transformation of skeletal muscle from fast-to slow-twitch during acquisition of cold tolerance in the chick. Endocrinology 146: 399-405, 2005.
22. Hoffmann AA, Parsons PA. Selection for increased desiccation resistance in drosophila-melanogaster-additive genetic-control and correlated responses for other stresses. Genetics 122: 837-845, 1989.
23. Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209: 2265-2275, 2006.
24. Houten SM, Auwerx J. PGC1α: turbocharging mitochondria. Cell 119: 5-7, 2004.
25. Hulbert AJ, Else PL. Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62: 207-235, 2000.
26. Kim Hi, Ahn Yh. Role of peroxisome proliferator-activated receptor-γ in the glucose-sensing apparatus of liver and β-cells. Diabetes 53: S60-S65, 2004.
27. Kim HI Cha JY, Kim SY, Kim JW, Roh KJ, Seong JK, Lee NT, Choi KY, Kim KS, Ahn YH. Peroxisomal proliferator-activated receptor-γ upregulates glucokinase gene expression in β-cells. Diabetes 51: 676-685, 2002.
28. Kim HI, Kim JW, Kim SH, Cha JY, Kim KS, Ahn YH. Identification and functional characterization of the peroxisomal proliferator response element in rat GLUT2 promoter. Diabetes 49: 1517-1524, 2000.
29. Knutti D, Kralli A. PGC-1, a versatile coactivator. Trends Endocrinol Metab 12: 360-365, 2001.
30. Laurberg P, Andersen S, Karmisholt J. Cold adaptation and thyroid hormone metabolism. Horm Metab Res 37: 545-549, 2005.
31. Leveille GA. Glycogen metabolism in meal-fed rats and chicks and time sequence of lipogenic and enzymatic adaptive changes. J Nutr 90: 449-460, 1966.
32. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1: 361-370, 2005.
33. Lin J, Wu H, Tarr PT, Zhang CY, Wu ZD, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibers. Nature 418: 797-801, 2002.
34. Mandard S, Muller M, Kersten S. Peroxisome proliferator-activated receptorα target genes. Cell Mol Life Sci 61: 393-416, 2004.
35. McKechnie AE, Chetty K, Lovegrove BG. Phenotypic flexibility in the basal metabolic rate of laughing doves: responses to short-term thermal acclimation. J Exp Biol 210: 97-106, 2007.
36. McKechnie AE, Lovegrove BG. Avian facultative hypothermic responses: a review. Condor 104: 705-724, 2002.
37. McNabb FMA. Avian thyroid development and adaptive plasticity. Gen Comp Endocrinol 147: 93-101, 2006.
38. Mortola JP. Metabolic response to cooling temperatures in chicken embryos and hatchlings after cold incubation. Comp Biochem Physiol A 145: 441-448, 2006.
39. Moyes CD. Controlling muscle mitochondrial content. J Exp Biol 206: 4385-4391, 2003.
40. Noble RC, Cocchi M. Lipid metabolism and the neonatal chicken. Prog Lipid Res 29: 107-140, 1990.
41. O'Hea EK, Leveille GA. Lipogenesis in isolated adipose tissue of the domestic chick (Gallus domesticus). Comp Biochem Physiol A 26: 111-120, 1968.
42. Patapoutian A, Peier AM, Story GM, Viswanath V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4: 529-539, 2003.
43. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR (Abstract). Nucleic Acids Res 29: e45, 2001.
44. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool [REST(C)] for group-wise comparison and statistical analysis of relative expression results in real-time PCR (Abstract). Nucleic Acids Res 30: e36, 2002.
45. Prinzinger R, Schmidt M, Dietz V. Embryogeny of oxygen consumption in 13 altricial and precocial birds. Respir Physiol 100: 283-287, 1995.
46. Puigserver P, Rhee J, Lin J, Wu Z, Yoon JC, Zhang CY, Krauss S, Mootha VK, Lowell BB, Spiegelman BM. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARγ coactivator-1. Mol Cell 8: 971-982, 2001.
47. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1γ): Transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90, 2003.
48. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839, 1998.
49. Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14, 2002.
50. Schreihofer AM, Ito S, Sved AF. Brain stem control of arterial pressure in chronic arterial baroreceptor-denervated rats. Am J Physiol Regul Integr Comp Physiol 289: R1746-R1755, 2005.
51. Seebacher F, Guderley H, Elsey RM, Trosclair PL III. Seasonal acclimatization of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J Exp Biol 206: 1193-1200, 2003.
52. Seebacher F, Murray SA. Transient receptor potential ion channels control thermoregulatory behaviour in reptiles (Abstract). PLoS ONE 2: e281, 2007.
53. Seebacher F, Schwartz TS, Thompson MB. Transition from ectothermy to endothermy: the development of metabolic capacity in a bird (Gallus gallus). Proc Royal Soc B-Biolog Sci 273: 565-570, 2006.
54. Speake BK, Noble RC, McCartney RJ. Tissue-specific changes in lipid composition and lipoprotein lipase activity during the development of the chick embryo. Biochim Biophys Acta 1165: 263-270, 1993.
55. St-Pierre J, Charest PM, Guderley H. Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatization of rainbow trout Oncorhynchus mykiss. J Exp Biol 201: 2961-2970, 1998.
56. Tzschentke B, Nichelmann M. Development of avian thermoregulatory system during the early postnatal period: development of the thermoregulatory set-point. Ornis Fennica 76: 189-198, 1999.
57. Ueda M, Watanabe K, Sato K, Akiba Y, Toyomizu M. Possible role for avPGC-1α in the control of expression of fiber type, along with avUCP and avANT mRNAs in the skeletal muscles of cold-exposed chickens. FEBS Lett 579: 11-17, 2005.
58. Van der Geyten S, Sanders JP, Kaptein E, Darras VM, Kuhn ER, Leonard JL, Visser TJ. Expression of chicken hepatic type I and type III iodothyronine deiodinases during embryonic development. Endocrinology 138: 5144-5152, 1997.
59. Vleck CM, Vleck D. Energetics of avian embryonic-development. Am Zool 26: A87-A87, 1986.
60. Walczak R, Tontonoz P. PPARadigms and PPARadoxes: expanding roles for PPARγ in the control of lipid metabolism. J Lipid Res 43: 177-186, 2002.
61. Wallace JC, Newsholm. Ea. A Comparison of properties of fructose 1,6-diphosphatase and activities of other key enzymes of carbohydrate metabolism in livers of embryonic and adult rat sheep and domestic fowl. Biochem J 104: 378-384, 1967.
62. Wechselberger M, Wright CL, Bishop GA, Boulant JA. Ionic channels and conductance-based models for hypothalamic neuronal thermosensitivity. Am J Physiol Regul Integr Comp Physiol 291: R518-R529, 2006.
63. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.
64. Yamazaki F, Sone R. Modulation of arterial baroreflex control of heart rate by skin cooling and heating in humans. J Appl Physiol 88: 393-400, 2000.
65. Yoon JC, Puigserver P, Chen GX, Donovan J, Wu ZD, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413: 131-138, 2001.