Neurochemical Research

, Volume 9, Issue 6, pp 785–801 | Cite as

P-31 nuclear magnetic resonance analysis of brain: Normoxic and anoxic brain slices

  • Maynard M. Cohen
  • Jay W. Pettegrew
  • Stephen J. Kopp
  • Nancy Minshew
  • Thomas Glonek
Original Articles
Accepted:

Abstract

Perchloric acid extracts were prepared from liquid-N2-frozen gerbil and guinea pig brain slices studied under one of three conditions: O2-incubated, N2-incubated or O2-incubated recovery following N2 incubation. Mole percentages of the various phosphatic components contained in the extracts were determined by phosphorus-31 nuclear magnetic resonance spectroscopy. The brain slice extract spectrum revealed a previously unreported group of brain phosphodiesters at −0.73 δ relative to 85% orthophosphoric acid Although the phosphatic profiles from O2-incubated slices fromgerbils and guinea pigs revealed only minor species variations, which differed quantitatively rather than qualitatively, species-specific differences were made readily apparent and amplified by incubating brain slices under oxygen-deficient conditions. Despite these differences which were most prevalent during the recovery phase, the overall metabolic changes described herein in response to N2-incubation were in accord with the results obtained by other analytical techniques. Inorganic orthophosphate (2.63 δ) was increased, while nucleoside (principally, adenosine) triphosphate (α-, −10.92 δ, β-, −21.45 δ, and γ-, −5.80 δ) and phosphocreatine (−3.12 δ) levels were decreased in response to N2 incubation. In addition, inosine monophosphate (3.78 δ) was increased and the levels of a partially characterized acid-labile phosphate (0.85 δ, guinea pig) were decreased upon N2 incubation. Phosphoglyceride metabolism also appeared to be altered by oxygen deprivation (gerbil). These latter findings provide additional information concerning the metabolic responses of cerebral tissue to oxygen deficient conditions.

Keywords

Nuclear Magnetic Resonance Brain Slice Nuclear Magnetic Resonance Spectroscopy Nuclear Magnetic Resonance Analysis Inosine Monophosphate 
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.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ackerman, J. H., Grove, T. H., Wong, G. G., Gadian, D. G., andRadda G. K. 1980. Mapping of metabolites in whole animals by 31-P NMR using surface coils. Nature 283:167–170.PubMedGoogle Scholar
  2. 2.
    Akesson, B., Fehling, C., Jagerstad, M., andStenram, U. 1982. Effect of experimenta folate deficiency on lipid metabolism in liver and brain. Br. J. Nutr. 47:505–522.PubMedGoogle Scholar
  3. 3.
    Bárány, M., andGlonek, T. 1982. Phosphorus-31 nuclear magnetic resonance of contractile systems, Pages 624–676,in Frederiksen, D. L., Cunningham, L. W., (eds.) Methods of Enzymology. Structural and Contractile Proteins, Vol. 85: Part B. Academic Press, New York.Google Scholar
  4. 4.
    Burt, C. T., Glonek, T., andBárány, M. 1976. Phosphorus-31 nuclear magnetic resonance detection of unexpected phosphodiesters in muscle. Biochemistry 15:4850–4853.PubMedGoogle Scholar
  5. 5.
    Chance, B., Nakase, Y., Bond, M., Leigh Jr., J. S., andMcDonald, G. 1978. Detection of31P nuclear magnetic resonance signals in brain by in vivo and freeze trapped assays. Proc. Natl. Acad. Sci. USA 75:4925–4929.PubMedGoogle Scholar
  6. 6.
    Cady, E. B., Dawson, M. J., Hope, P. L., Tofts, P. S., Costello, A. M. L., Delpy, D. T., Reynolds, E. O. R., andWilkie, D. R. 1983. Non-invasive investigation of cerebral metabolism in newborn infants by phosphorus nuclear magnetic resonance spectroscopy. Lancet i:1059–1062.Google Scholar
  7. 7.
    Cohen, M. M., andHeald, P. J. 1960. Effects of phenobarbital on phosphate metabolism of cerebral cortex in vitro. J. Pharmacol. Exp. Ther. 129:361–367.PubMedGoogle Scholar
  8. 8.
    Cohen, M. M. 1962. Effect of anoxia on the chemistry and morphology of cerebral cortex slices in vitro. J. Neurochem. 9:337–344.PubMedGoogle Scholar
  9. 9.
    Cohen, M. M. andLin, S. 1962. Acid soluble phosphates in the developing rabbit brain. J. Neurochem. 9:345–352.PubMedGoogle Scholar
  10. 10.
    Cohen, M. M., Bluhm, R., Glonek, T., Kopp, S., Patel-Mandlik, K., andPettegrew, J. 1982. In vitro models of stroke. Pages 1–12,in Stefanovich, V. (eds.), Advances in Biosciences, Vol. 43. Stroke: Animal Models, Pergamon Press, Oxford.Google Scholar
  11. 11.
    Costello, A. J. R., Glonek, T., Slodki, M. E., andSeymour, F. R. 1975. Phosphorus-31 nuclear magnetic resonance spectroscopy of extracellular, yeast O-phosphonohexoglycans. Carbohydrate Res. 42:23–37.Google Scholar
  12. 12.
    Cox, D. W. G., Morris, P. G., Feeney, J., andBachelard, H. S. 1983.31P-N.M.R. studies on cerebral energy metabolism under conditions of hypoglycaemia and hypoxia in vitro. Biochem J. 212:365–370.PubMedGoogle Scholar
  13. 13.
    Duffy, T. E., Howse, D. C., andPlum, F. 1975. Cerebral energy metabolism during experimental status epilepticus. J. Neurochem. 24:925–934.PubMedGoogle Scholar
  14. 14.
    Glonek, T., andMarotta, S. F. 1978.31P magnetic resonance of intact endocrine tissue: adrenal glands of dogs. Horm. Metab. Res. 10:420–424.PubMedGoogle Scholar
  15. 15.
    Glonek, T., Kopp, S. J. Kot, E., Pettegrew, J. W., Harrison, W. H., andCohen, M. 1982. P-31 nuclear magnetic resonance analysis of brain. The perchloric acid extract spectrum. J. Neurochem. 39:1210–1219.PubMedGoogle Scholar
  16. 16.
    Greiner, J. V., Kopp, S. J., Sanders, D. R., andGlonek, T. 1981. Organophosphates of the crystalline lens: A nuclear magnetic resonance spectroscopic study. Invest. Ophthalmol. Vis. Sci. 21:700–713.PubMedGoogle Scholar
  17. 17.
    Henderson, T. O., Glonek, T., andMyers, T. C. 1974. Phosphorus-31 nuclear magnetic resonance spectroscopy of phospholipids. Biochemistry 13:623–628. (Note that the scale is reversed in this paper.)PubMedGoogle Scholar
  18. 18.
    Hollis, D. P., Nunnaly, R. L., Jacobus, W. E., andTaylor, G. J., IV 1977. Detection of regional ischemia in perfused beating hearts by phosphorus nuclear magnetic resonance. Biochem. Biophys. Res. Commun. 75:1086–1091.PubMedGoogle Scholar
  19. 19.
    Hoult, D. R., Busby, S. J. W., Gadian, D. G., Radda, G. K. Richards, R. E., andSeeley, P. J. 1974. Observation of tissue metabolites using31P nuclear magnetic resonance. Nature 252:285–287.PubMedGoogle Scholar
  20. 20.
    Howse, D. C., andDuffy, T. E. 1975. Control of the redox state of the pyridine nucleotides in the rat cerebral cortex. Effect of electroshock-induced seizures. J. Neurochem. 24:935–940.PubMedGoogle Scholar
  21. 21.
    Kauffman, F. L., Brown, J. G., Passonneau, J. V., andLowry, O. H. 1969. Effects of change in brain metabolism on levels of pentose phosphate pathway intermediates. J. Biol. Chem. 244:3647–3653.PubMedGoogle Scholar
  22. 22.
    Kopp, S. J., Glonek, T., andGreiner, J. V. 1982. Interspecies variations in mammalian lens metabolites as detected by phosphorus-31 nuclear magnetic resonance. Science 215:1622–1625.PubMedGoogle Scholar
  23. 23.
    McIlwain H. 1951. Metabolic response in vitro to electrical stimulation of sections of mammalian brain. Biochem. J. 49:382–393.Google Scholar
  24. 24.
    Navon, G., Navon, R., Shulman, R. G., andYamane, T. 1978. Phosphate metabolites in lymphoid, Friend erythroleukemia and HeLa cells observed by high resolution31P nuclear magnetic resonance. Proc. Natl. Acad. Sci USA 75:891–895.PubMedGoogle Scholar
  25. 25.
    Nishikawa, H., Fujii, T., Yamada, S., Yoshizaki, K., andWatari, H. 1980.31P Nuclear magnetic resonance study on perfused brain slices of guinea pig. J. Biochem. 87:663–666.PubMedGoogle Scholar
  26. 26.
    Norwood, W. I., Ingwall, J. S., Norwood, C. R., andFossel, E. T. 1983. Developmental changes of creatine kinase metabolism in rat brain. Am. J. Physiol. 244:C205-C210.PubMedGoogle Scholar
  27. 27.
    Ogawa, S., Rottenberg, H., Brown, T. R., Shulman, R. G., Castillo, C. L., andGlynn, P. 1978. High resolution31P nuclear magnetic resonance study of rat liver mitochondria. Proc. Natl. Acad. Sci. USA 75:1796–1800.PubMedGoogle Scholar
  28. 28.
    Pettegrew, J. W., Glonek, T., Baskin, F., andRosenberg, R. N. 1979. Phosphorus-31 NMR of neuroblastoma clonal lines. Effects of cell confluency state and dibutyryl cyclic AMP. Neurochem. Res. 4:795–802.PubMedGoogle Scholar
  29. 29.
    Pettegrew, J. W., Kopp, S. J. Minshew, N. Feliksik, J. M., Dadok, J., Glonek, T., andCohen, M. M. 1984. Chemical characterization of a prominent phosphomonoester resonance in mammalian brain:31P and1H NMR analyses at 4.7 and 14.1 Tesla. J. Neurochem. submitted.Google Scholar
  30. 30.
    Rimm, A. A., Hartz, A. J., Kalbfleisch, J. H., Anderson, A. J., andHoffman, R. G. 1980. Basic biostatistics in medicine and epidemiology (Appleton-Century-Crofts of Prentice Hall, Inc., New York).Google Scholar
  31. 31.
    Rosner M. R., Khorana, H. G., andSatterthwait, A. C. 1979. The structure of lipopolysaccharide from a heptose-less mutant ofEscherichia coli K-12. J. Biol. Chem. 254:5918–5925.Google Scholar
  32. 32.
    Ross, B. D., Radda, G. K., Gadian, D. G., Rochker, G., Esiri, M., andFalconer-Smith, J. 1981. Examination of a case of suspected McArdle's syndrome by31P nuclear magnetic resonance. New Engl. J. Med. 304:1338–1342.PubMedGoogle Scholar
  33. 33.
    Sundler, R. 1975. Ethanolaminephosphate cytidylyltransferase. Purification and characterization of the enzyme from rat liver. J. Biol. Chem. 250:8585–8590.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1984

Authors and Affiliations

  • Maynard M. Cohen
    • 1
  • Jay W. Pettegrew
    • 2
  • Stephen J. Kopp
    • 3
    • 4
  • Nancy Minshew
    • 2
  • Thomas Glonek
    • 3
    • 4
  1. 1.Department of Neurological ScienceRush-Presbyterian St. Lukes Medical CenterChicago
  2. 2.Laboratory of Neurophysics Department of Neurology and PediatricsUniversity of Texas Health Science Center at DallasDallas
  3. 3.Department of PhysiologyChicago College of Osteopathic MedicineChicagoUSA
  4. 4.Nuclear Magnetic Resonance LaboratoryChicago College of Osteopathic MedicineChicagoUSA

Personalised recommendations