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Journal of comparative physiology

, Volume 153, Issue 2, pp 159–166 | Cite as

Phosphorus nuclear magnetic resonance studies of energy metabolism in molluscan tissues

Effect of anoxia and ischemia on the intracellular pH and high energy phosphates in the ventricle of the whelk,Busycon contrarium
  • W. Ross Ellington
Article

Summary

Isolated ventricles of the whelkBusycon contrarium were perfused in 15 mm (internal diameter) nuclear magnetic resonance tubes at 22–24°C. Phosphorus nuclear magnetic resonance (31P-NMR) spectra were generated at 60.7071 MHz using a multi nuclei FT spectrometer. Methodologies were developed to utilize31P-NMR spectra to assess intracellular pH (pHi) and the relative levels of high energy phosphates in experimental preparations. Ventricles perfused under normoxic conditions for 6 h showed no changes in the levels of arginine phosphate and ATP. There was a slight decrease in pHi (0.08 unit). Anoxia and anoxia+ischemia resulted in a number of metabolic changes. There was a linear decay in arginine phosphate with half times of decay of 4.9 and 5.6 h, respectively. Inorganic phosphate levels rose 3–5 fold in both experimental groups. In contrast, no statistically significant changes in the adenylates were observed. 6 h of anoxia and anoxia+ischemia produced significant reductions in pHi. During anoxia, the pHi fell from 7.11 to 6.87, and during anoxia+ischemia the pHi fell from 7.14 to 6.79. Rates of accumulation of succinate and alanine under these conditions were quite low. The apparent low rates of glycolysis were probably related to minimal activities of phosphofructokinase due to reduced pHi and the lack of large alterations in the adenylates. The general response of the ventricle of the whelkB. contrarium to reduced oxygen tensions is a reduction in energy demands leading to low rates of anaerobic energy metabolism and resultant alterations in pHi and levels of high energy phosphates.

Keywords

Ischemia Nuclear Magnetic Resonance Succinate Inorganic Phosphate Level Normoxic Condition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Achs MJ, Garfinkel D (1982) Computer simulation of energy metabolism in acidotic ischemia. Am J Physiol 242:R533-R544Google Scholar
  2. Baginski RM, Pierce SK (1978) A comparison of amino acid accumulation during high salinity adaptation with anaerobic energy metabolism in the ribbed muscleModiolus demissus demissus. J Exp Zool 203:419–428Google Scholar
  3. Barrow KD, Jamieson DD, Norton RS (1980)31P nuclear magnetic resonance studies of energy metabolism in tissue from the marine invertebrateTapes watingi. Eur J Biochem 103:289–297Google Scholar
  4. Bicher HI, Ohki S (1972) Intracellular pH electrode experiments on the giant squid axon. Biochim Biophys Acta 255:900–904Google Scholar
  5. Boron WF, Roos A (1976) Comparison of microelectrode, DMO and methylamine methods for measuring intracellular pH. Am J Physiol 231:799–809Google Scholar
  6. Cobbe SM, Poole-Wilson PA (1980) Tissue acidosis in myocardial hypoxia. J Mol Cell Cardiol 12:761–770Google Scholar
  7. Collicutt JM, Hochachka PW (1977) The anaerobic oyster heart: Coupling of glucose and aspartate fermentation. J Comp Physiol 115:147–157Google Scholar
  8. Dawson MJ, Gadian DG, Wilkie DR (1977) Contraction and recovery of living muscles studied by31P nuclear magnetic resonance. J Physiol 267:703–735Google Scholar
  9. Ebberink RHM (1982) Control of adductor muscle phosphofructokinase activity in the sea musselMytilus edulis during anaerobiosis. Mol Physiol 2:345–355Google Scholar
  10. Ebberink RHM, Zurburg W, Zandee DI (1979) The energy demand of the posterior adductor muscle ofMytilus edulis in catch during air exposure. Mar Biol Lett 1:23–31Google Scholar
  11. Ellington WR (1981) Energy metabolism during hypoxia in the isolated, perfused ventricle of the whelk,Busycon contrarium Conrad. J Comp Physiol 142:457–464Google Scholar
  12. Ellington WR (1982) Metabolic responses of the sea anemoneBunodosoma cavernata to declining oxygen tensions and anoxia. Physiol Zool 55:240–249Google Scholar
  13. Gäde G (1980) The energy metabolism of the foot muscle of the jumping cockle,Cardium tuberculatum: sustained anoxia versus muscular activity. J Comp Physiol 137:177–182Google Scholar
  14. Gäde G, Ellington WR (1983) Energy metabolism in molluscan hearts. (A review). Comp Biochem Physiol (in press)Google Scholar
  15. Gevers W (1977) Generation of protons by metabolic processes in heart cells. J Mol Cell Cardiol 9:867–874Google Scholar
  16. Gillies RJ (1981) Intracellular pH and growth in eukaryotic cells. In: Cameron IL, Pool TB (ed) The transformed cell. Academic Press, New York, p 347Google Scholar
  17. Jacobus WE, Taylor GJ, Hollis RP, Nunnally RL (1977) Phosphorus nuclear magnetic resonance of perfused working rat hearts. Nature 265:756–758Google Scholar
  18. Jarmakani JM, Nagatomo T, Nakazawa M, Langer GA (1978) Effect of hypoxia on myocardial high-energy phosphates in the neonatal mammalian heart. Am J Physiol 235:H475–481Google Scholar
  19. Kostyuk PG, Sorokina ZA, Kholodova YD (1969) Measurement of activity of hydrogen, potassium and sodium ions in striated muscle fibers and nerve cells. In: Lavallee M, Schanne OF, Hebert NV (eds) Glass microelectrodes. Wiley, New York, pp 322–348Google Scholar
  20. Mangum CP, Polites G (1980) Oxygen uptake and transport in the prosobranch molluscBusycon canaliculatum I. Gas exchange and the response to hypoxia. Biol Bull 158:77–90Google Scholar
  21. Neely JR, Morgan HE (1974) Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annu Rev Physiol 36:413–459Google Scholar
  22. Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61:296–434Google Scholar
  23. Thomas RC (1974) Intracellular pH of snail neurones with a new pH-sensitive glass microelectrode. J Physiol 238:159–180Google Scholar
  24. Trivedi B, Danforth WH (1966) Effect of pH on the kinetics of frog muscle phosphofructokinase. J Biol Chem 241:4110–4114Google Scholar
  25. Wijsman TCM (1975) pH fluctuations inMytilus edulis L. in relation to shell movements under aerobic and anaerobic conditions. Proc 9th Eur Mar Biol Symp, pp 139–149Google Scholar
  26. Williamson JR (1974) Succinate. In: Bergmeyer HV (ed) Methods of enzymatic analysis, vol 3. Academic Press, New York, pp 1616–1621Google Scholar
  27. Zwaan A de (1977) Anaerobic energy metabolism in bivalve molluscs. Oceanogr Mar Biol Annu Rev 15:103–187Google Scholar
  28. Zwaan A de, Bont AMT de, Zurburg W, Bayne BL, Livingstone DR (1983) On the role of strombine formation in the energy metabolism of adductor muscle of a sessile bivalve. J Comp Physiol 149:557–563Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • W. Ross Ellington
    • 1
  1. 1.Department of Biological ScienceFlorida State UniversityTallahasseeUSA

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