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Energy Consumption by Phospholipid Metabolism in Mammalian Brain

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Abstract

Until recently, brain phospholipid metabolism was thought to consume only 2% of the ATP consumed by the mammalian brain as a whole. In this paper, however, we calculate that 1.4% of total brain ATP consumption is consumed for the de novo synthesis of ether phospholipids and that another 5% is allocated to the phosphatidylinositide cycle. When added to previous estimates that fatty acid recycling within brain phospholipids and maintenance of membrane lipid asymmetries of acidic phospholipids consume, respectively, 5% and 8% of net brain ATP consumption, it appears that phospholipid metabolism can consume up to 20% of net brain ATP consumption. This new estimate is consistent with recent evidence that phospholipids actively participate in brain signaling and membrane remodeling, among other processes.

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REFERENCES

  1. Vierbuchen, M., Gunawan, J., and Debuch, H. 1979. Studies on the hydrolysis of 1–alkyl-sn-glycero-3–phosphoethanolamine in subcellular fractions of rat brain. Hoppe-Zeyler' Z. Physiol. Chem. 360:1091–1097.

    Google Scholar 

  2. Porcellati, G., Goracci, G., and Arienti, G. 1983. Lipid turnover. Pages 277–294, in Lajtha, A. (ed.), Handbook of neurochemistry, vol. 5. Plenum, New York.

    Google Scholar 

  3. Clarke, D. D. and Sokoloff, L. 1994. Circulation and energy metabolism of the brain. Pages 645–680, in Siegel, G. J., Agranoff, B. W., Albers, R. W., and Molinoff, M. D. (eds.), Basic neurochemistry: Molecular, cellular, and medical aspects. Raven Press, New York.

  4. Ansell, G. B. 1973. Phospholipids in the nervous system. Pages 377–422, in Ansell, G. B., Hawthorne, J. N., and Dawson, R. M. C. (eds.), Form and function of phospholipids. Elsevier, New York.

    Google Scholar 

  5. Miller, S. L., Benjamins, J. A., and Morell, P. 1977. Metabolism of glycerophospholipids of myelin and microsomes in rat brain. J. Biol. Chem. 252:4025–4037.

    Google Scholar 

  6. Dawson, R. M. C. 1985. Enzymic pathways of phospholipid metabolism in the nervous system. Pages 45–78, in Eichberg, J. (ed.), Phospholipids in nervous tissues. John Wiley and Sons, New York.

    Google Scholar 

  7. Fisher, S. K. and Agranoff, B. W. 1985. The biochemical basis and functional significance of enhanced phosphatidate and phosphoinositide turnover. Pages 241–295, in Eichberg, J. (ed.), Phospholipids in nervous tissues. John Wiley and Sons, New York.

    Google Scholar 

  8. Horrocks, L. 1985. Metabolism and function of fatty acids in brain. Pages 173–199, in Eichberg, J. (ed.), Phospholipids in nervous tissues. John Wiley and Sons, New York.

  9. Bazán, N. G. 1990. Supply of n-3 polyunsaturated fatty acids and their significance in the central nervous system. Pages 1–24, in Wurtman, R. J. and Wurtman, J. J. (eds.), Nutrition and the brain, vol. 8. Raven Press, New York.

    Google Scholar 

  10. Glaser, P. E. and Gross, R. W. 1994. Plasmenylethanolamine facilitates rapid membrane fusions: A stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion. Biochemistry 33:5805–5812.

    Google Scholar 

  11. Purdon A. D. and Rapoport, S. I. 1998. Energy requirements for two aspects of phospholipid metabolism in mammalian brain. Biochem. J. 335:313–318.

    Google Scholar 

  12. Zachowski, A. and Gaudry-Talarmain, Y. M. 1990. Phospholipid transverse diffusion in synaptosomes: Evidence for the involvement of the aminophospholipid translocase. J. Neurochem. 55:1352–1356.

    Google Scholar 

  13. Williamson, P. and Schlegel, R. A. 1994. Back and forth: The regulation and function of transbilayer phospholipid movement in eukaryotic cells. Mol. Membr. Biol. 11:199–216.

    Google Scholar 

  14. Blank, M. L., Cress, E. A., Robinson, M., and Snyder, F. 1985. Metabolism of unique diarachidonoyl and linoleoylarachidonoyl species of ethanolamine and choline phosphoglycerides in rat testes. Biochim. Biophys. Acta 833:366–371.

    Google Scholar 

  15. Fisher, S. K., Heacock, A. M., and Agranoff, B. W. 1992. Inositol lipids and signal transduction in the nervous system: An update. J Neurochem 58:18–38.

    Google Scholar 

  16. Izumi, T. and Shimizu, T. 1995. Platelet-activating factor receptor: Gene expression and signal transduction. Biochim. Biophys. Acta 1259:317–333.

    Google Scholar 

  17. Cooper, J. R., Bloom, F. E., and Roth, R. H. 1996. The biochemical basis of neuropharmacology, 7th ed., Oxford University Press, Oxford.

  18. Shetty, H. U., Smith, Q. R., Washizaki, K., Rapoport, S. I., and Purdon, A. D. 1996. Identification of two molecular species of rat brain phosphatidylcholine that rapidly incorporate and turn over arachidonic acid in vivo. J. Neurochem. 67:1702–1710.

    Google Scholar 

  19. Kuwae, T., Schmid, P. C., and Schmid, H. H. 1997. Alterations of fatty acyl turnover in macrophage glycerolipids induced by stimulation. Evidence for enhanced recycling of arachidonic acid. Biochim. Biophys. Acta 1344:74–86.

    Google Scholar 

  20. Zoeller, R. A., Lake, A. C., Nagan, N., Gaposchkin, D. P., Legner, M. A., and Lieberthal, W. 1999. Plasmalogens as endogenous antioxidants: Somatic cell mutants reveal the importance of the vinyl ether. Biochem. J. 338:769–776.

    Google Scholar 

  21. Chikhale, E. G., Balbo, A., Galdzicki, Z., Rapoport, S. I., and Shetty, H. U. 2001. Measurement of myo-inositol turnover in phosphatidylinositol: Description of a model and mass spectrometric method for cultured cortical neurons. Biochemistry 40:11114–11120.

    Google Scholar 

  22. Rosenberger, T. A., Oki, J., Purdon, A. D., Rapoport, S. I., and Murphy, E. J. 2002. Rapid synthesis and turnover of brain microsomal ether phospholipids in the adult rat. J. Lipid Res. 43:59–68.

    Google Scholar 

  23. Rana, R. S. and Hokin, L. E. 1990. Role of phosphoinositides in transmembrane signaling. Physiol. Rev. 70:115–64.

    Google Scholar 

  24. Hokin, L. E. and Dixon, J. F. 1993. The phosphoinositide signaling system. I. Historical background. II. Effects of lithium on the accumulation of second messenger inositol 1,4,5–trisphosphate in brain cortex slices. Prog. Brain Res. 98:309–315.

    Google Scholar 

  25. Agranoff, B. W. and Fisher, S. K. 1994. Phosphoinositides. Pages 417–448 in Siegel, G. J., Agranoff, B. W., Albers, R. W., and Molinoff, P. B. (eds.), Basic neurochemistry, 5th ed. Raven Press, New York.

    Google Scholar 

  26. Hajra, A. K. 1995. Glycerolipid biosynthesis in peroxisomes (microbodies). Prog. Lipid Res. 34:343–364.

    Google Scholar 

  27. Verhoeven, A. J., Tysnes, O. B., Aarbakke, G. M., Cook, C. A., and Holmsen, H. 1987. Turnover of the phosphomonoester groups of polyphosphoinositol lipids in unstimulated human platelets. Eur. J. Biochem. 166:3–9.

    Google Scholar 

  28. Bell, R. M. and Coleman, R. A. 1980. Enzymes of glycerolipid synthesis in eukaryotes. Annu. Rev. Biochem. 49:459–487.

    Google Scholar 

  29. Pollock, R. J., Hajra, A. K., and Agranoff, B. W. 1976. Incorporation of D-[3–3H, U-14C] glucose into glycerolipid via acyl dihydroxyacetone phosphate untransformed and viral-transformed BHK-21–c13 fibroblasts. J. Biol. Chem. 251:5149–5154.

    Google Scholar 

  30. Lee, T. C. 1998. Biosynthesis and possible biological functions of plasmalogens. Biochim. Biophys. Acta 1394:129–145.

    Google Scholar 

  31. Ford, D. A. and Gross, R. W. 1994. The discordant rates of sn-1 aliphatic chain and polar head group incorporation into plasmalogen molecular species demonstrate the fundamental importance of polar head group remodeling in plamalogen metabolism in rabbit myocardium. Biochemistry 33:1216–1222.

    Google Scholar 

  32. Hinkle, P. C., Kumar, M. A., Resetar, A., and Harris, D. L. 1991. Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry 30:3576–3582.

    Google Scholar 

  33. Rolfe, D. F. S. and Brown, G. C. 1997. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77:731–747.

    Google Scholar 

  34. Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O., and Shinohara, M. 1977. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:897–916.

    Google Scholar 

  35. Dobson, G. P. and Headrick, J. P. 1995. Bioenergetic scaling: Metabolic design and body-size constraints in mammals. Proc. Natl. Acad. Sci. USA 92:7317–7321.

    Google Scholar 

  36. Paltauf, F. 1994. Ether lipids in biomembranes. Chem. Phys. Lipids 74:101–139.

    Google Scholar 

  37. Snyder, F. 1996. Ether-linked lipids and their bioactive species: Occurrence, chemistry, metabolism, regulation, and function. Pages 183–210 in Vance, D. E. and Vance, J. E. (eds.), Biochemistry of lipids, lipoproteins, and membranes. Elsevier, New York.

    Google Scholar 

  38. Pediconi, M. F. and Barrantes, F. J. 1990. Brain asymmetry in phospholipid polar head group metabolism: Parallel in vivo and in vitro studies. Neurochem. Res. 15:25–32.

    Google Scholar 

  39. Tong, W. and Sun, G. Y. 1996. Effects of ethanol on phosphorylation of lipids in rat synaptic plasma membranes. Alcohol Clin. Exp. Res. 20:1335–1339.

    Google Scholar 

  40. Soukup, J. F., Friedel, R. O., and Shanberg, S. M. 1978. Microwave irradiation fixation for studies of polyphosphoinositide metabolism in brain. J. Neurochem. 30:635–637.

    Google Scholar 

  41. Nishihara, M. and Keenan, R. W. 1985. Inositol phospholipid levels of rat forebrain obtained by freeze-blowing method. Biochim. Biophys. Acta 835:415–418.

    Google Scholar 

  42. Reddy, T. S. and Bazan, N. G. 1987. Arachidonic acid, stearic acid, and diacylglycerol accumulation correlates with the loss of phosphatidylinositol 4,5–bisphosphate in cerebrum 2 seconds after electroconvulsive shock: Complete reversion of changes 5 minutes after stimulation. J. Neurosci. Res. 18:449–455.

    Google Scholar 

  43. Masuzawa, Y., Sugiura, T., Ishima, Y., and Waku, K. 1984. Turnover rates of the molecular species of ethanolamine plasmalogen of rat brain. J. Neurochem. 42:961–968.

    Google Scholar 

  44. Tabata, H., Bell, J. M., Miller, J. C., and Rapoport, S. I. 1986. Incorporation of plasma palmitate into the brain of the rat during development. Dev. Brain Res. 29:1–8.

    Google Scholar 

  45. Tysnes, O. B., Verhoeven, A. J., and Holmsen, H. 1988. Rates of production and consumption of phosphatidic acid upon thrombin stimulation of human platelets. Eur. J. Biochem. 174: 75–79.

    Google Scholar 

  46. Brusa, R., Eva, C., Oberto, A., Peila, R., Ricci Galamero, S., and Genazzani, E. 1992. Down regulation of muscarinic receptor subtypes messenger RNAs in rat primary culture of corticostriatal neurons. Pharmacol. Res. 25 (Suppl 1):121–122.

    Google Scholar 

  47. Hertz, L. and Peng, L. 1992. Energy metabolism at the cellular level of the CNS. Can J. Physiol. Pharmacol. 70 (Suppl):S145–S157.

    Google Scholar 

  48. Murphy, T. H., Wright, D. D., and Baraban, J. M. 1992. Phosphoinositide turnover associated with synaptic transmission. J. Neurochem. 59:2336–2339.

    Google Scholar 

  49. Rowlands, D. K., Kao, C., and Wise, H. 2001. Regulation of prostacyclin and prostaglandin E(2) mediated responses in adult rat dorsal root ganglion cells in vitro. Br. J. Pharmacol. 133:13–22.

    Google Scholar 

  50. Gammon, C. M., Allen, A. C., and Morell, P. 1989. Bradykinin stimulates phosphoinositide hydrolysis and mobilization of arachidonic acid in dorsal root ganglion neurons. J. Neurochem. 53:95–101.

    Google Scholar 

  51. del Rio, E., Bevilacqua, J. A., Marsh, S. J., Halley, P., and Caulfield, M. P. 1999. Muscarinic M1 receptors activate phosphoinositide turnover and Ca2+ mobilization in rat sympathetic neurones, but this signaling pathway does not mediate M-current inhibition. J. Physiol. 520 (Pt 1):101–111.

    Google Scholar 

  52. Washizaki, K., Smith, Q. R., Rapoport, S. I., and Purdon, A. D. 1994. Brain arachidonic acid incorporation and precursor pool specific activity during intravenous infusion of unesterified [3H]arachidonate in the anesthetized rat. J. Neurochem. 63: 727–736.

    Google Scholar 

  53. Grange, E., Deutsch, J., Smith, Q. R., Chang, M., Rapoport, S. I., and Purdon, A. D. 1995. Specific activity of brain palmitoyl-CoA pool provides rates of incorporation of palmitate in brain phospholipids in awake rats. J. Neurochem. 65:2290–2298.

    Google Scholar 

  54. Pestonjamasp, V. K. and Burstein, S. H. 1998. Anandamide synthesis is induced by arachidonate mobilizing agonists in cells of the immune system. Biochim. Biophys. Acta 1394:249–260.

    Google Scholar 

  55. DeMar, J. C. J., Wensel, T. G., and Anderson, R. E. 1996. Biosynthesis of the unsaturated 14–carbon fatty acids found on the N termini of photoreceptor-specific proteins. J. Biol. Chem. 271:5007–5016.

    Google Scholar 

  56. Lehninger, A. L., Nelson, D. L., and Cox, M. M. 1993. Principles of biochemistry, 2nd ed. Worth Press, New York, p. 1090.

    Google Scholar 

  57. Cunnane, S. C., Belza, K., Anderson, M. J., and Ryan, M. A. 1998. Substantial carbon recycling from linoleate into products of de novo lipogenesis occurs in rat liver even under conditions of extreme dietary deficiency. J. Lipid Res. 39:2271–2276.

    Google Scholar 

  58. Rapoport, S. I. 2001. In vivo fatty acid incorporation into brain phospholipids in relation to plasma availability, signal transduction and membrane remodeling. J. Mol. Neurosci. 16:243–261.

    Google Scholar 

  59. Bazan, N. G., Aveldano de Caldironi, M. I., and Rodriguez de Turco, E. B. 1981. Rapid release of free arachidonic acid in the central nervous system due to stimulation. Prog. Lipid Res. 20:523–529.

    Google Scholar 

  60. Rabin, O., Chang, M. C. J., Grange, E., Bell, J. M., Rapoport, S. I., Deutsch, J., and Purdon, A. D. 1998. Selective acceleration of arachidonic acid reincorporation into brain membrane phospholipid following transient ischemia in awake gerbil. J. Neurochem. 70:324–334.

    Google Scholar 

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Authors and Affiliations

  1. Brain Physiology and Metabolism Section, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, 20892

    A. D. Purdon, T. A. Rosenberger, H. U. Shetty & S. I. Rapoport

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  1. A. D. Purdon
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Purdon, A.D., Rosenberger, T.A., Shetty, H.U. et al. Energy Consumption by Phospholipid Metabolism in Mammalian Brain. Neurochem Res 27, 1641–1647 (2002). https://doi.org/10.1023/A:1021635027211

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