Metabolic homeostasis: Oxidative phosphorylation and the metabolic requirements of higher plants and animals

Journal of Applied Physiology

Volumn 125, Issue 4, 2018, Pages 1183-1192

  Wilson, David F ^a   Matschinsky, Franz M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

AMP; energy metabolism; metabolic homeostasis; metabolic regulation; oxidative phosphorylation; oxygen

Indexed keywords

EID: 85056118949     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00352.2018     Document Type: Article

References (72)

1. Baumgärtl H, Zimelka W, Lübbers DW. Evaluation of PO2 profiles to describe the oxygen pressure field within the tissue. Comp Biochem Physiol A Mol Integr Physiol 132: 75-85, 2002. doi:10.1016/S1095-6433(01)00532-3.
2. Beenakkers AMT, Van Der Horst DJ, Van Marrewijk WJA. Insect flight muscle metabolism. Insect Biochem 14: 243-260, 1984. doi:10.1016/0020-1790(84)90057-X.
3. Beis I, Newsholme EA. The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem J 152: 23-32, 1975. doi:10.1042/bj1520023.
4. Buth DG, Murphy RW, Miyamoto MM, Lieb CS. Creatine kinases of amphibians and reptiles: Evolutionary and systematic aspects of gene expression. Copeia 1985: 279-284, 1985. doi:10.2307/1444837.
5. Bylund AC, Bjurö T, Cederblad G, Holm J, Lundholm K, Sjöstroöm M, Angquist KA, Scherstén T. Physical training in man. Skeletal muscle metabolism in relation to muscle morphology and running ability. Eur J Appl Physiol Occup Physiol 36: 151-169, 1977. doi:10.1007/BF00421747.
6. Chance B, Bonner WD. Kinetics of cytochrome oxidation in skunk cabbage mitochondria. Plant Physiol 40: 1198-1204, 1965. doi:10.1104/pp.40.6.1198.
7. Keeling PJ, Koonin EV (ed.). The Origin and Evolution of Eukaryotes. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2014.
8. Constable SH, Favier RJ, McLane JA, Fell RD, Chen M, Holloszy JO. Energy metabolism in contracting rat skeletal muscle: Adaptation to exercise training. Am J Physiol 253: C316-C322, 1987. doi:10.1152/ajpcell.1987.253.2.C316.
9. Dawson MJ, Gadian DG, Wilkie DR. Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol 299: 465-484, 1980. doi:10.1113/jphysiol.1980. sp013137.
10. Erecińska M, Davis JS, Wilson DF. Regulation of respiration in paracoccus denitrificans: The dependence on redox state of cytochrome c and [ATP]/[ADP][Pi]. Arch Biochem Biophys 197: 463-469, 1979. doi:10.1016/0003-9861(79)90268-6.
11. Erecińska M, Wilson DF, Nishiki K. Homeostatic regulation of cellular energy metabolism: Experimental characterization in vivo and fit to a model. Am J Physiol 234: C82-C89, 1978. doi:10.1152/ajpcell.1978.234. 3.C82.
12. Frederich M, Balschi JA. The relationship between AMP-activated protein kinase activity and AMP concentration in the isolated perfused rat heart. J Biol Chem 277: 1928-1932, 2002. doi:10.1074/jbc.M107128200.
13. Graham TE, Saltin B. Estimation of the mitochondrial redox state in human skeletal muscle during exercise. J Appl Physiol (1985) 66: 561-566, 1989. doi:10.1152/jappl.1989.66.2.561.
14. Gray MW. Mitochondrial evolution. Cold Spring Harb Perspect Biol 4: A011403, 2012. doi:10.1101/cshperspect.a011403.
15. Green HJ. Mechanisms of muscle fatigue in intense exercise. J Sports Sci 15: 247-256, 1997. doi:10.1080/026404197367254.
16. Griffin KL, Anderson OR, Tissue DT, Turnbull MH, Whitehead D. Variations in dark respiration and mitochondrial numbers within needles of Pinus radiata grown in ambient or elevated CO2 partial pressure. Tree Physiol 24: 347-353, 2004. doi:10.1093/treephys/24.3.347.
17. Hardie DG. AMP-activated protein kinase: An energy sensor that regulates all aspects of cell function. Genes Dev 25: 1895-1908, 2011. doi:10.1101/gad.17420111.
18. Hardie DG, Ross FA, Hawley SA. AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13: 251-262, 2012. doi:10.1038/nrm3311.
19. Haseler LJ, Hogan MC, Richardson RS. Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol (1985) 86: 2013-2018, 1999. doi:10.1152/jappl.1999.86. 6.2013.
20. Hassinen IE, Hiltunen K. Respiratory control in isolated perfused rat heart. Role of the equilibrium relations between the mitochondrial electron carriers and the adenylate system. Biochim Biophys Acta 408: 319-330, 1975. doi:10.1016/0005-2728(75)90133-4.
21. Hoppeler H, Lindstedt SL, Claassen H, Taylor CR, Mathieu O, Weibel ER. Scaling mitochondrial volume in heart to body mass. Respir Physiol 55: 131-137, 1984. doi:10.1016/0034-5687(84)90018-5.
22. Holloszy JO. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242: 2278-2282, 1967.
23. Ikuma H, Bonner WD. Properties of higher plant mitochondria. I. Isolation and some characteristics of tightly-coupled mitochondria from dark-grown mung bean hypocotyls. Plant Physiol 42: 67-75, 1967. doi: 10.1104/pp.42.1.67.
24. Keilin D. On cytochrome, a respiratory pigment, common to animals, yeast, and higher plants. Proc R Soc Lond B 98: 312-339, 1925. doi:10.1098/rspb.1925.0039.
25. Kleczkowski LA, Randall DD. Maize leaf adenylate kinase: Purification and partial characterization. Plant Physiol 81: 1110-1114, 1986. doi:10.1104/pp.81.4.1110.
26. Lance C, Bonner WD Jr. The respiratory chain components of higher plant mitochondria. Plant Physiol 43: 756-766, 1968. doi:10.1104/pp.43. 5.756.
27. Lawson JWR, Veech RL. Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254: 6528-6537, 1979.
28. Lin S-C, Hardie DG. AMPK: Sensing glucose as well as cellular energy status. Cell Metab 27: 299-313, 2018. doi:10.1016/j.cmet.2017.10.009.
29. MacIntosh BR, Holash RJ, Renaud J-M. Skeletal muscle fatigue-regulation of excitation-contraction coupling to avoid metabolic catastrophe. J Cell Sci 125: 2105-2114, 2012. doi:10.1242/jcs.093674.
30. MacLennan DH, Holland PC. Calcium transport in sarcoplasmic reticulum. Annu Rev Biophys Bioeng 4: 377-404, 1975. doi:10.1146/annurev. bb.04.060175.002113.
31. Margulis L. Origin of Eukaryotic Cells. New Haven, CT: Yale University Press, 1970.
32. Margulis L, Sagan D. Origins of Sex. Three Billion Years of Genetic Recombination. New Haven, CT: Yale University Press, 1986, p. 69-71.
33. Markland FS, Wadkins CL. Adenosine triphosphate-adenosine 5'-monophosphate phosphotransferase of bovine liver mitochondria. II. General kinetic and structural properties. J Biol Chem 241: 4136-4145, 1966.
34. Mathieu O, Krauer R, Hoppeler H, Gehr P, Lindstedt SL, Alexander RM, Taylor CR, Weibel ER. Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass. Respir Physiol 44: 113-128, 1981. doi:10.1016/0034-5687(81) 90079-7.
35. McAllister RM, Terjung RL. Training-induced muscle adaptations: Increased performance and oxygen consumption. J Appl Physiol (1985) 70: 1569-1574, 1991. doi:10.1152/jappl.1991.70.4.1569.
36. McCann DJ, Molé PA, Caton JR. Phosphocreatine kinetics in humans during exercise and recovery. Med Sci Sports Exerc 27: 378-389, 1995. doi:10.1249/00005768-199503000-00014.
37. McCreary CR, Chilibeck PD, Marsh GD, Paterson DH, Cunningham DA, Thompson RT. Kinetics of pulmonary oxygen uptake and muscle phosphates during moderate-intensity calf exercise. J Appl Physiol (1985) 81: 1331-1338, 1996. doi:10.1152/jappl.1996.81.3.1331.
38. Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13: 1016-1023, 2012. doi:10.1038/ncb2329.
39. Nielsen OB, de Paoli FV. Regulation of Na+-K+ homeostasis and excitability in contracting muscles: Implications for fatigue. Appl Physiol Nutr Metab 32: 974-984, 2007. doi:10.1139/H07-099.
40. Nishiki K, Erecińska M, Wilson DF. Energy relationships between cytosolic metabolism and mitochondrial respiration in rat heart. Am J Physiol Cell Physiol 3: C73-C81, 1978. doi:10.1152/ajpcell.1978.234.3. C73.
41. Nishiki K, Erecinska M, Wilson DF, Cooper S. Evaluation of mitochondrial oxidative phosphorylation in hearts from euthyroid, hypothyroid, and hyperthyroid rats. Am J Physiol Cell Physiol 4: C212-C219, 1978. doi:10.1152/ajpcell.1978.235.5.C212.
42. Peiffer WE, Ingle RT, Ferguson-Miller S. Structurally unique plant cytochrome c oxidase isolated from wheat germ, a rich source of plant mitochondrial enzymes. Biochemistry 29: 8696-8701, 1990. doi:10.1021/bi00489a027.
43. Poole AM, Gribaldo S. Eukaryotic origins: How and when was the mitochondrion acquired? Cold Spring Harb Perspect Biol 6: A015990, 2014. doi:10.1101/cshperspect.a015990.
44. Richardson RS, Wary C, Wray DW, Hoff J, Rossiter HB, Layec G, Carlier PG. MRS evidence of adequate O2 supply in human skeletal muscle at the onset of exercise. Med Sci Sports Exerc 47: 2299-2307, 2015. doi:10.1249/MSS.0000000000000675.
45. Rossiter HB, Ward SA, Kowalchuk JM, Howe FA, Griffiths JR, Whipp BJ. Dynamic asymmetry of phosphocreatine concentration and O2 uptake between the on- and off-transients of moderate- and high-intensity exercise in humans. J Physiol 541: 991-1002, 2002. doi:10.1113/jphysiol. 2001.012910.
46. Rumsey WL, Wilson DF. Tissue capacity for mitochondrial oxidative phosphorylation and its adaptation to stress. Compr Physiol 1, Suppl 14: 1095-1113, 2011. doi:10.1002/cphy.cp040247.
47. Sacktor B, Hurlbut EC. Regulation of metabolism in working muscle in vivo. II. Concentrations of adenine nucleotides, arginine phosphate, and inorganic phosphate in insect flight muscle during flight. J Biol Chem 241: 632-634, 1966.
48. Sahlin K. Muscle fatigue and lactic acid accumulation. Acta Physiol Scand Suppl 556: 83-91, 1986.
49. Storey BT. The respiratory chain of plant mitochondria: XI. Electron transport from succinate to endogenous pyridine nucleotide in mung bean mitochondria. Plant Physiol 48: 694-701, 1971. doi:10.1104/pp.48.6.694.
50. Suarez RK. Energy metabolism during insect flight: Biochemical design and physiological performance. Physiol Biochem Zool 73: 765-771, 2000. doi:10.1086/318112.
51. Suarez RK, Lighton JRB, Brown GS, Mathieu-Costello O. Mitochondrial respiration in hummingbird flight muscles. Proc Natl Acad Sci USA 88: 4870-4873, 1991. doi:10.1073/pnas.88.11.4870.
52. Suarez RK, Staples JF, Lighton JRB, Mathieu-Costello O. Mitochondrial function in flying honeybees (Apis mellifera): Respiratory chain enzymes and electron flow from complex III to oxygen. J Exp Biol 203: 905-911, 2000.
53. Suarez RK, Welch KC Jr. Sugar metabolism in hummingbirds and nectar bats. Nutrients 9: E743, 2017. doi:10.3390/nu9070743.
54. Teague WE Jr, Dobson GP. Thermodynamics of the arginine kinase reaction. J Biol Chem 274: 22459-22463, 1999. doi:10.1074/jbc.274.32. 22459.
55. Towler MC, Hardie DG. AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res 100: 328-341, 2007. doi:10.1161/01.RES.0000256090.42690.05.
56. Veech RL, Lawson JW, Cornell NW, Krebs HA. Cytosolic phosphorylation potential. J Biol Chem 254: 6538-6547, 1979.
57. Weibel ER, Hoppeler H. Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J Exp Biol 208: 1635-1644, 2005. doi:10.1242/jeb.01548.
58. Wilson DF. Regulation of cellular metabolism: Programming and maintaining metabolic homeostasis. J Appl Physiol (1985) 115: 1583-1588, 2013. doi:10.1152/japplphysiol.00894.2013.
59. Wilson DF. Regulation of metabolism: The rest-to-work transition in skeletal muscle. Am J Physiol Endocrinol Metab 309: E793-E801, 2015a. doi:10.1152/ajpendo.00355.2015.
60. Wilson DF. Programming and regulation of metabolic homeostasis. Am J Physiol Endocrinol Metab 308: E506-E517, 2015b. doi:10.1152/ajpendo. 00544.2014.
61. Wilson DF. Regulation of metabolism: The work-to-rest transition in skeletal muscle. Am J Physiol Endocrinol Metab 310: E633-E642, 2016. doi:10.1152/ajpendo.00512.2015.
62. Wilson DF. Oxidative phosphorylation: Regulation and role in cellular and tissue metabolism. J Physiol 595: 7023-7038, 2017a. doi:10.1113/JP273839.
63. Wilson DF. Oxidative phosphorylation: Unique regulatory mechanism and role in metabolic homeostasis. J Appl Physiol (1985) 122: 611-619, 2017b. doi:10.1152/japplphysiol.00715.2016.
64. Wilson DF, Harrison DK, Vinogradov SA. Oxygen, pH, and mitochondrial oxidative phosphorylation. J Appl Physiol (1985) 113: 1838-1845, 2012. doi:10.1152/japplphysiol.01160.2012.
65. Wilson DF, Harrison DK, Vinogradov A. Mitochondrial cytochrome c oxidase and control of energy metabolism: Measurements in suspensions of isolated mitochondria. J Appl Physiol (1985) 117: 1424-1430, 2014. doi:10.1152/japplphysiol.00736.2014.
66. Wilson DF, Lee WMF, Makonnen S, Finikova O, Apreleva S, Vinogradov SA. Oxygen pressures in the interstitial space and their relationship to those in the blood plasma in resting skeletal muscle. J Appl Physiol (1985) 101: 1648-1656, 2006. doi:10.1152/japplphysiol.00394.2006.
67. Wilson DF, Mokashi A, Chugh D, Vinogradov S, Osanai S, Lahiri S. The primary oxygen sensor of the cat carotid body is cytochrome a3 of the mitochondrial respiratory chain. FEBS Lett 351: 370-374, 1994. doi:10.1016/0014-5793(94)00887-6.
68. Wilson DF, Owen CS, Erecińska M. Quantitative dependence of mitochondrial oxidative phosphorylation on oxygen concentration: A mathematical model. Arch Biochem Biophys 195: 494-504, 1979. doi:10.1016/0003-9861(79)90376-X.
69. Wilson DF, Owen CS, Holian A. Control of mitochondrial respiration: A quantitative evaluation of the roles of cytochrome c and oxygen. Arch Biochem Biophys 182: 749-762, 1977. doi:10.1016/0003-9861(77) 90557-4.
70. Wilson DF, Vinogradov SA. Mitochondrial cytochrome c oxidase: Mechanism of action and role in regulating oxidative phosphorylation. J Appl Physiol (1985) 117: 1431-1439, 2014. doi:10.1152/japplphysiol.00737. 2014.
71. Wilson DF, Vinogradov SA. Mitochondrial cytochrome c oxidase: Mechanism of action and role in regulating oxidative phosphorylation: Reply to Pannala, Beard, and Dash. J Appl Physiol (1985) 119: 158, 2015. doi:10.1152/japplphysiol.00349.2015.
72. Wyatt CN, Mustard KJ, Pearson SA, Dallas ML, Atkinson L, Kumar P, Peers C, Hardie DG, Evans AM. AMP-activated protein kinase mediates carotid body excitation by hypoxia. J Biol Chem 282: 8092-8098, 2007. doi:10.1074/jbc.M608742200.