Abstract
Secondary neurochemical events contribute to progressive tissue damage and subsequent neurological deficit after traumatic spinal-cord injury (SCI). Among proposed injury factors are alterations of phospholipids and certain cations. To clarify the relationship of membrane lipid changes (phospholipids, cholesterol, and arachidonic acid) to changes in tissue content of water and selected ions (sodium, potassium, and magnesium) after SCI, these variables were examined in spinal-cord segments from anesthetized ventilated rabbits subjected to laminectomy or to moderate (40 g-cm) or severe (150 g-cm) impact trauma at the lumbar (L2) segment. Trauma caused significant increases in tissue sodium, water, and arachidonic acid content, and significant decreases in phospholipids, cholesterol, potassium, and magnesium content. Alterations in magnesium were significantly related to injury severity. In contrast, changes in spinal-cord water content occurred to a similar degree in the two injury groups, as did tissue sodium and potassium content. Decreases in phospholipids were strongly correlated with decreases in tissue magnesium content, whereas changes in sodium and potassium were less well-correlated. Because magnesium ions play a critical role with regard to cellular bioenergetic state, calcium flux, amino acid receptor function, and eicosanoid production, reductions in tissue magnesium after injury may be important in the progression of secondary tissue damage.
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References
Aikawa, J. K. (1981)Magnesium: Its Biological Significance pp. 21–29 CRC, Boca Raton, FL.
Allen A. R. (1914) Remarks on the histopathological changes in the spinal cord due to impact: An experimental study.J. Nerv. Ment. Dis. 41, 141–147.
Allen K. G., Fellows M. E., Tornheim P. A., and Wagner K. R. (1984) A new procedure to analyze free fatty acids. Application to 20-mg brain tissue samples.J. Chromatogr. 309, 33–42.
Alvarez-Lefmans F. J., Giraldez F., and Gamino S. M. (1987) Intracellular free magnesium in excitable cells: Its measurement and biologic significance.Can. J. Physiol. Pharmacol. 65, 915–925.
Anderson D. K., Means E. D., Waters T. R., and Spears C. J. (1980) Spinal cord energy metabolism following compression trauma to the feline spinal cord.J. Neurosurg. 53, 375–380.
Bowman R. E. and Wolf R. C. (1962) A rapid ultramicro method for total serum cholesterol.Clin. Chem. 8, 302–309.
Bradford M. (1976) A rapid and sensitive method for the quantitation, of microgram quantities of protein utilizing the principle of dye binding.Anal. Biochem. 72, 248–254.
Chang K. J., Hazum E., Killian A., and Cautrecasas P. (1981) Interactions of ligands with morphine and enkephalin receptors are differentially affected by guanine nucleotide.Mol. Pharmacol. 20, 1–7.
Choi D. W. Ionic dependence of glutamate neurotoxicity.J. Neurosci. 7, 369–379, (1987).
Chutkow J. G. (1972) Distribution of magnesium and calcium in brains of normal and magnesium-deficient rats.Mayo Clin. Proc. 47, 647–653.
Corkey B. E., Dusnzynski J., Rich T. L., Matschinsky B., and Williamson, J. R. (1986) Regulation of free magnesium in rat hepatocytes and isolated mitochondria.J. Biol. Chem. 261, 2567–2574.
Demediuk P., Saunders R. D., Anderson D. K., Means E. D., and Horrocks L. A. (1985a) Membrane lipid changes in laminectomized and traumatized cat spinal cord.Proc. Natl. Acad. Sci. USA 82, 7017–7057.
Demediuk P., Saunders R. D., Clendenon N. R., Means E. D., Anderson D. K., and Horrocks L. A. (1985b) Changes in lipid metabolism in traumatized spinal cord.Prog. Brain Res. 63, 1–16.
Dugan L. L., Demediuk P., Pendley C. E., and Horrocks L. A. (1986) Separation of phospholipids by high performance liquid chomatography: All major classes, including ethanolamine and choline plasmalogens, and most minor classes, including lysophosphatidylethanolamine.J. Chromatogr. 378, 317–327.
Ebel H. and Guenther T. (1980) Magnesium metabolism: A Review.J. Clin. Chem. Clin. Biochem. 18, 257–270.
Faden A. I., Chan P. H., and Longar S (1987) Alterations in lipid metabolism, Na+, K+-ATPase activity, and tissue water content of spinal cord following experimental traumatic injury.J. Neurochem. 48, 1809–1816.
Faden A. I., Lemke M., Simon R. P., and Noble L. J. (1988)N-Methyl-d-aspartate antagonist MK801 improves outcome following traumatic spinal cord injury in rats: behavioral, anatomic, and neurochemical studies.J. Neurotrauma 5, 27–37.
Faden A. I., Molineaux C. J., Rosenberger J. G., Jacobs T. P., and Cox B. M. (1985) Endogenous opioid immunoreactivity in rat spinal cord following traumatic injury.Ann. Neurol. 17, 386–390.
Garfinkel L. and Garfinkel D. (1985) Magnesium regulation of the glycolytic pathway and the enzymes involved.Magnesium 4, 60–72.
Gibson B. L. and Reif-Lehrer L. (1985) Magnesium reducesN-methyl-d-aspartate neurotoxicity in embryonic chick neural retina in vitro.Neurosci. Lett. 57, 13–18.
Hara A. and Radin N. S. (1978) Lipid extraction of tissues with low toxicity solvent.Anal. Biochem. 90, 420–426.
Haynes D. H. (1974) 1-Anilino-8-naphthalensulfonate: A fluorescent indicator of ion binding and electrostatic potential on the membrane surface.J. Membr. Biol. 17, 341–366.
Horrocks L. A. and Sun G. Y. (1972) Ethanolamine, plasmalogens.Reseach Methods in Neurochemistry, vol. 1, Marks N. and Rodnight R., eds. pp. 223–231, Plenum, New York.
Hsu C. Y., Halushka P. V., Hogan E. L., Banik N. L., Lee W. A., and Perot P. L. (1985) Alteration of thromboxane and prostacyclin levels in experimental spinal cord injury.Neurology 35, 1003–1009.
Jones M. and Keenan R. W. (1982) A biochemical investigation of spinal cord after contusive injury.Exp. Neurol. 78, 67–82.
Jones M., Keenan R. W., and Horowitz P. (1982) Use of 6-p-toluidine 2-naphthalensulfonic acid to quantitate lipids after thin-layer chromatography.J. Chromatogr. 237, 522–524.
Kwo S., Young W., and DeCrescito V. (1989) Spinal cord sodium, potassium, calcium, and water concentration changes in rats after graded contusion injury.J. Neurotrauma 6, 13–24.
Lawson J. W. and Veech R. L. (1979) Effects of pH and free magnesium on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions.J. Biol. Chem. 254, 6528–6537.
Lemke M. and Faden A. I. (1990) Edema development and ion changes in rat spinal cord after impact trauma: Injury dose-response studies.J. Neurotrauma.
Lemke M., Demediuk P., McIntosh T. K., Vink R., and Faden A. I. (1987) Alterations in tissue Mg++, Na+ and spinal cord edema following impact trauma in rats.Biochem. Biophys. Res. Commun. 147, 1170–1175.
Lewin M. G., Hansebout R. H., and Pappius H. M. (1974) Chemical characteristics of traumatic spinal cord edema in cats.J. Neurosurg. 40, 65–75.
McIntosh T. K., Faden A. I., Yamakami I., and Vink R. (1988) Magnesium deficiency exacerbates and pretreatment improves outcome following traumatic brain injury in rats:31P magnetic resonance study.J. Neurotrauma 5, 17–31.
Means E. D., Anderson D. K., Nicolosi G., and Gaudsmit J. (1978) Microvascular perfusion in experimental spinal cord injury.Surg. Neurol. 9, 353–360.
Nemecek S., Petr R., Suba P., Rozsival V., and Melka O. (1977) Longitudinal extension of oodema in experimental spinal cord injury—evidence for two types of post-traumatic oedema.Acta Neurochir. 37, 7–16.
Nigam S., Averdunk R., and Guenther T. (1986) Alteration of prostanoid metabolism in rats with magnesium deficiency.Prostaglandins Leukotrienes Med.23, 1–10.
Nowak L., Bregestovski P., Ascher P., Herbt A., and Prochiantz A. (1984) Magnesium gates glutamate-activated channels in mouse neurones.Nature 307, 462–465.
Rothman S. M. (1983) synaptic activity mediates death of hypoxic neurons.Science 220, 536, 537.
Rouser G., Siakotos V., and Fleischer S. (1969) Quantitative analysis of phospholipids by thin layer chromatography and phosphorus analysis of spots.Lipids 1, 85, 86.
Rubin H. (1976) Magnesium deprivation reproduces the coordinate effects of serum removal or cortisol addition on transport and metabolism in chick embryo fibroblasts.J. Cell. Physiol. 89, 613–626.
Sandler A. N. and Tator C. H. (1976) Review of the effect of spinal cord trauma on the vessels and blood flow in the spinal cord.J. Neurosurg. 45, 638–646.
Saunders R. D. and Horrocks L. A. (1984) Simultaneous extraction of and preparation for HPLC of prostaglandins and phospholipids.Anal. Biochem. 143, 71–75.
Segler-Stahl K., Demediuk P., Catillo R., Watts C., and Moscatelli E. A. (1985) Phospholipids of normal and experimentally injured spinal cord of the miniature pig.Neurochem. Res. 10, 563–569.
Stokes B. T., Fox P., and Hollinden G. (1983) Extracellular calcium activity in the injured spinal cord.Exp. Neurol. 80, 561–572.
Veloso D., Guynn R. W., Oskarrson M., and Veech R. L. (1973) The concentration of free and bound magnesium in rat tissues. Relative constancy of free magnesium concentration.J. Biol. Chem. 248, 4811–4819.
Vink R., McIntosh T. K., Demediuk P., Weiner M. W., and Faden A. I. (1988) Decline in intracellular free Mg2+ is associated with irreversible tissue injury after brain trauma.J. Biol. Chem. 263, 757–761.
Vink R., Noble L. J., Knoblach S. M., Bendall M. R., and Faden, A. I. (1989a) Metabolic changes in rabbit spinal cord after trauma: Magnetic resonance spectroscopy studies.Ann. Neurol. 25, 26–31.
Vink R., Yum S. W., Lemke M., Demediuk P., and Faden A. I. (1989b) Traumatic spinal cord injury in rabbits decreases intracellular free magnesium concentration as measured by31P MRS.Brain Res. 490, 144–147.
Walker J. G., Yates R. R., O’Neil J. J., and Yashon D. (1977) Canine spinal cord energy state after experimental trauma. J. Neurochem.29, 929–932.
Yashon D., Bingham W. G., Faddoul E. M., and Hunt W. E. (1973) Edema of the spinal cord following experimental impact trauma.J. Neurosurg. 38, 693–697.
Young W. and Koreh I. (1986) Potassium and calcium changes in injured spinal cord.Brain. Res. 365, 42–53.
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Lemke, M., Yum, S.W. & Faden, A.I. Lipid alterations correlate with tissue magnesium decrease following impact trauma in rabbit spinal cord. Molecular and Chemical Neuropathology 12, 147–165 (1990). https://doi.org/10.1007/BF03159941
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DOI: https://doi.org/10.1007/BF03159941