Regulation of pyruvate dehydrogenase in the common killifish, Fundulus heteroclitus, during hypoxia exposure

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 3, 2008, Pages

  Richards, Jeffrey G ^a   Sardella, Brian A ^b   Schulte, Patricia M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Energy charge; Fish; Gibbs free energy; Muscle; Pyruvate dehydrogenase kinase

Indexed keywords

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; CARBOHYDRATE; CREATINE PHOSPHATE; LACTIC ACID; MITOCHONDRIAL PROTEIN; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ADENOSINE DIPHOSPHATE; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXYGEN; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL TRANSFERRING) KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ENERGY; CONTROLLED STUDY; CYPRINODONTIFORMES; CYTOPLASM; DISEASE SEVERITY; HYDROLYSIS; HYPOXIA; METABOLISM; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; SURVIVAL; ANIMAL; ANOXIA; CYTOSOL; ENERGY METABOLISM; ENZYMOLOGY; GENETICS; PATHOPHYSIOLOGY; PHYLOGENY; PHYSIOLOGY; SKELETAL MUSCLE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ANOXIA; CYTOSOL; ENERGY METABOLISM; FUNDULIDAE; ISOENZYMES; MITOCHONDRIA; MUSCLE, SKELETAL; NAD; OXYGEN; PHYLOGENY; PROTEIN-SERINE-THREONINE KINASES; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVIC ACID;

EID: 54049123250     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00192.2008     Document Type: Article

References (58)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402, 1997.
2. Bergmeyer HU. Methods of Enzymatic Analysis. New York: Academic, 1983.
3. Bishop T, Brand MD. Processes contributing to metabolic depression in hepatopancreas cells from the snail Helix aspersa J Exp Biol 203: 3603-3612, 2000.
4. Bishop T, St-Pierre J, Brand MD. Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282: R372-R382, 2002.
5. Boutilier R, Heming TA, Iwama GK. Appendix: physicochemical parameters for use in fish respiratory physiology. In: Fish Physiology, edited by Hoar WS and Randall DJ. New York: Academic, 1984, p. 403-430.
6. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 329: 191-196, 1998.
7. Bradford MM. 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, 1976.
8. +-ATPase and constant membrane potential in hepatocytes: support for channel arrest. Am J Physiol Regul Integr Comp Physiol 265: R1020-R1025, 1993.
9. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid quanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
10. Denko NC, Fontana LA, Hudson KM, Sutphin PD, Raychaudhuri S, Altman R, Giaccia AJ. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 22: 5907-5914, 2003.
11. DiMichele L, Powers DA. Physiological basis for swimming endurance differences between LDH-B genotypes of Fundulus heteroclitus. Science 216: 1014-1016, 1982.
12. Dong Z, Venkatachalam MA, Wang J, Patel Y, Saikumar P, Semenza GL, Force T, Nishiyama J. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia. Hif-1-independent mechanisms. J Biol Chem 276: 18702-18709, 2001.
13. Golding EM, Teague WE Jr., Dobson GP. Adjustment of K′ to varying pH and pMg for the creatine kinase, adenylate kinase and ATP hydrolysis equilibria permitting quantitative bioenergetic assessment. J Exp Biol 198: 1775-1782, 1995.
14. Guppy M. The biochemistry of metabolic depression: a history of perceptions. Comp Biochem Physiol B 139: 435-442, 2004.
15. Guppy M, Reeves DC, Bishop T, Withers P, Buckingham JA, Brand MD. Intrinsic metabolic depression in cells isolated from the hepatopancreas of estivating snails. FASEB J 14: 999-1004, 2000.
16. Hardewig I, Van Dijk PL, Portner HO. High-energy turnover at low temperatures: recovery from exhaustive exercise in Antarctic and temperate eelpouts. Am J Physiol Regul Integr Comp Physiol 274: R1789-R1796, 1998.
17. Hassid W, Abraham S. Chemical procedures for analysis of polysaccharides. In: Methods in Enzymology, edited by Colowick S and Kaplan N. New York: Academic, 1957.
18. Henriksson P, Mandic M, Richards J. The osmo-respiratory compromise in sculpins: impaired gas exchange is associated with freshwater tolerance. Physiol Biochem Zool 81: 310-319, 2008.
19. Hochachka PW, Buck LT, Doll CJ, Land SC. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498, 1996.
20. Holness MJ, Sugden MC. Regulation of pyruvate dehydrogenase complex activity by reversible phosphorylation. Biochem Soc Trans 31: 1143-1151, 2003.
21. + gradient in the oxygenated isolated heart: effect of changing the free energy of ATP hydrolysis. Am J Physiol Heart Circ Physiol 285: H2437-H2445, 2003.
22. Katz A, Spencer MK, Sahlin K. Failure of glutamate dehydrogenase system to predict oxygenation state of human skeletal muscle. Am J Physiol Cell Physiol 259: C26-C28, 1990.
23. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV. Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 27: 7381-7393, 2007.
24. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177-185, 2006.
25. Kramer lD, Schulte PM. Prior PCB exposure suppresses hypoxia-induced up-regulation of glycolytic enzymes in Fundulus heterclitus. Comp Biochem Physiol C 139: 23-29, 2004.
26. Laemmli UK. Cleavage of structural protein during assembly of the head bacteriophage T4. Nature 227: 680-685, 1970.
27. Larade K, Storey KB. Analysis of signal transduction pathways during anoxia exposure in a marine snail: a role for p38 MAP kinase and downstream signaling cascades. Comp Biochem Physiol B 143: 85-91, 2006.
28. Lewis JM, Costa I, Val AL, Almeida-Val VM, Gamperl AK, Driedzic WR. Responses to hypoxia and recovery: repayment of oxygen debt is not associated with compensatory protein synthesis in the Amazonian cichlid, Astronotus ocellatus. J Exp Biol 210: 1935-1943, 2007.
29. Martinez ML, Landry C, Boehm R, Manning S, Cheek AO, Rees BB. Effects of long-term hypoxia on enzymes of carbohydrate metabolism in the Gulf killifish, Fundulus grandis. J Exp Biol 209: 3851-3861, 2006.
30. Mattisson A, Johansson R, Boström S. The cellular localization of lactate dehydrogenase in skeletal muscle of eel (Anguilla anguilla). Comp Biochem Physiol B 41: 475-482, 1972.
31. Moyes CD, Buck LT, Hochachka PW. Temperature effects on pH of mitochondria isolated from carp red muscle. Am J Physiol Regul Integr Comp Physiol 254: R611-R615, 1988.
32. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metab Rev 39: 443-455, 2007.
33. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3: 187-197, 2006.
34. Powell WH, Hahn ME. Identification and functional characterization of hypoxia-inducible factor 2α from the estuarine teleost, Fundulus heteroclitus: interaction of HIF-2α with two ARNT2 splice variants. J Exp Zool 294: 17-29, 2002.
35. Pörtner H, Boutlier R, Tang Y, Toews D. The use of fluoride and nitriloacetic acid in tissue acid-base physiology. II. Intracellular pH. Respir Physiol 81: 255-275, 1991.
36. 2(s) in oxyconforming and oxyregulating animals: gas exchange, metabolic rate and the mode of energy production. In: The Vertebrate Gas Transport Cascade: Adaptations to Environment and Mode of Life, edited by Eduardo J and Bicudo PW. Boca Raton: CRC, 1993.
37. Rees BB, Bowman JA, Schulte PM. Structure and sequence conservation of a putative hypoxia response element in the lactate dehydrogenase-B gene of Fundulus. Biol Bull 200: 247-251, 2001.
38. Richards JG, Heigenhauser GJF, Wood CM. Glycogen phosphorylase and pyruvate dehydrogenase transformation in white muscle of trout during high-intensity exercise. Am J Physiol Regul Integr Comp Physiol 282: R828-R836, 2002.
39. +-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206: 4475-4486, 2003.
40. Richards JG, Wang YS, Brauner CJ, Gonzalez RJ, Patrick ML, Schulte PM, Choppari-Gomes AR, Almeida-Val VM, Val AL. Metabolic and ionoregulatory responses of the Amazonian cichlid, Astronotus ocellatus, to severe hypoxia. J Comp Physiol B 177: 361-374, 2007.
41. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425, 1987.
42. Scott GR, Richards JG, Forbush B, Isenring P, Schulte PM. Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am J Physiol Cell Physiol 287: C300-C309, 2004.
43. Semenza GL. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 405: 1-9, 2007.
44. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537, 1996.
45. Smith RW, Houlihan DF, Nilsson GE, Brechin JG. Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol Regul Integr Comp Physiol 271: R897-R904, 1996.
46. St-Pierre J, Brand MD, Boutilier RG. The effect of metabolic depression on proton leak rate in mitochondria from hibernating frogs. J Exp Biol 203: 1469-1476, 2000.
47. 2 affinity of mitochondria in hypoxic hypometabolism. Am J Physiol Regul Integr Comp Physiol 279: R1205-R1214, 2000.
48. Stierhoff KL, Targett TE, Grecay PA. Hypoxia tolerance of the mummichog: the role of access to the water surface. J Fish Biol 63: 580-592, 2003.
49. Storey KB, Storey JM. Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79: 207-233, 2004.
50. Sugden MC, Holness MJ. Mechanisms underlying regulation of the expression and activities of the mammalian pyruvate dehydrogenase kinases. Arch Physiol Biochem 112: 139-149, 2006.
51. Tamura K, Dudley J, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4. Mol Biol Evol doi: 10.1093/molbev.msm092. 2007.
52. Teague WE Jr, Golding EM, and Dobson GP. Adjustment of K′ for the creatine kinase, adenylate kinase and ATP hydrolysis equilibria to varying temperature and ionic strength. J Exp Biol 199: 509-512, 1996.
53. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680, 1994.
54. + transport and distribution after exercise in rainbow trout white muscle. Am J Physiol Regul Integr Comp Physiol 271: R1239-R1250, 1996.
55. Wang Y, Heigenhauser GJF, Wood CM. Integrated responses to exhaustive exercise and recovery in rainbow trout white muscle: acid-base, phosphogen, carbohydrate, lipid, ammonia, fluid volume and electrolyte metabolism. J Exp Biol 195: 227-258, 1994.
56. Wieser W, Krumschnabel G. Hierarchies of ATP-consuming processes: direct compared with indirect measurements, and comparative aspects. Biochem J 355: 389-395, 2001.
57. Williamson D, Lund P, Krebs H. The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J 103: 514-527, 1967.
58. Yeager DP, Ultsch GR. Physiological regulation and conformation: a BASIC program for the determination of critical points. Physiol Zool 62: 888-907, 1989.