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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1985 Oct;82(20):7071–7075. doi: 10.1073/pnas.82.20.7071

Membrane lipid changes in laminectomized and traumatized cat spinal cord.

P Demediuk, R D Saunders, D K Anderson, E D Means, L A Horrocks
PMCID: PMC391312  PMID: 3863139

Abstract

Free fatty acid (FFA), diacylglycerol (acyl2Gro), icosanoid, phospholipid, and cholesterol levels were measured in samples of cat spinal cord (L2) that were frozen in situ with vertebrae intact, at various times after laminectomy, and at various times after laminectomy with compression trauma to the spinal cord. Tissue samples either were grossly dissected into gray and white portions prior to FFA and acyl2Gro analysis or were used whole for the other lipid types. Gray matter total FFA and acyl2Gro values were abnormally high in samples frozen with vertebrae intact and in those frozen 10 min after laminectomy. This indicates that the surgical procedures resulted in some perturbation of spinal cord lipid metabolism. If the experimental animals were allowed to recover for 90 min after laminectomy, the gray matter FFA and acyl2Gro levels were greatly reduced. Compression of the spinal cord with a 170-g weight for 1, 3, or 5 min (following 90 min of recovery after laminectomy) caused significant elevations of total FFA, acyl2Gro, icosanoids, and phosphatidic acid and significant decreases in ethanolamine plasmalogens and cholesterol. Among the total FFA, arachidonic acid was found to have the largest relative increase. Comparisons of gray and white matter demonstrate that, in general, changes in white matter FFA and acyl2Gro were similar to those seen in gray matter. However, the increases in white matter levels of FFA and acyl2Gro were delayed, occurring after the elevations in gray matter. For some FFA (e.g., arachidonate), the rise in white matter occurred as gray matter levels were decreasing. This suggests that the initial alteration in spinal cord lipid metabolism after trauma was in gray matter but, with time, spread radially into white matter.

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Selected References

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  1. Agardh C. D., Chapman A. G., Nilsson B., Siesjö B. K. Endogenous substrates utilized by rat brain in severe insulin-induced hypoglycemia. J Neurochem. 1981 Feb;36(2):490–500. doi: 10.1111/j.1471-4159.1981.tb01619.x. [DOI] [PubMed] [Google Scholar]
  2. Agardh C. D., Chapman A. G., Nilsson B., Siesjö B. K. Endogenous substrates utilized by rat brain in severe insulin-induced hypoglycemia. J Neurochem. 1981 Feb;36(2):490–500. doi: 10.1111/j.1471-4159.1981.tb01619.x. [DOI] [PubMed] [Google Scholar]
  3. Ahmed K., Thomas B. S. The effects of long chain fatty acids on sodium plus potassium ion-stimulated adenosine triphosphatase of rat brain. J Biol Chem. 1971 Jan 10;246(1):103–109. [PubMed] [Google Scholar]
  4. Allan D., Thomas P., Michell R. H. Rapid transbilayer diffusion of 1,2-diacylglycerol and its relevance to control of membrane curvature. Nature. 1978 Nov 16;276(5685):289–290. doi: 10.1038/276289a0. [DOI] [PubMed] [Google Scholar]
  5. Allan D., Thomas P., Michell R. H. Rapid transbilayer diffusion of 1,2-diacylglycerol and its relevance to control of membrane curvature. Nature. 1978 Nov 16;276(5685):289–290. doi: 10.1038/276289a0. [DOI] [PubMed] [Google Scholar]
  6. Anderson D. K., Nicolosi G. R., Means E. D., Hartley L. E. Effects of laminectomy on spinal cord blood flow. J Neurosurg. 1978 Feb;48(2):232–238. doi: 10.3171/jns.1978.48.2.0232. [DOI] [PubMed] [Google Scholar]
  7. Anderson D. K., Prockop L. D., Means E. D., Hartley L. E. Cerebrospinal fluid lactate and electrolyte levels following experimental spinal cord injury. J Neurosurg. 1976 Jun;44(6):715–722. doi: 10.3171/jns.1976.44.6.0715. [DOI] [PubMed] [Google Scholar]
  8. BOWMAN R. E., WOLF R. C. A rapid and specific ultramicro method for total serum cholesterol. Clin Chem. 1962 May-Jun;8:302–309. [PubMed] [Google Scholar]
  9. Banschbach M. W., Geison R. L. Post-mortem increase in rat cerebral hemisphere diglyceride pool size. J Neurochem. 1974 Oct;23(4):875–877. doi: 10.1111/j.1471-4159.1974.tb04418.x. [DOI] [PubMed] [Google Scholar]
  10. Bazan N. G., Jr Free fatty acid production in cerebral white and grey matter of the squirrel monkey. Lipids. 1971 Mar;6(3):211–212. doi: 10.1007/BF02533041. [DOI] [PubMed] [Google Scholar]
  11. Bazan N. G., Jr, de Bazan H. E., Kennedy W. G., Joel C. D. Regional distribution and rate of production of free fatty acids in rat brain. J Neurochem. 1971 Aug;18(8):1387–1393. doi: 10.1111/j.1471-4159.1971.tb00003.x. [DOI] [PubMed] [Google Scholar]
  12. Blok M. C., Van Deenen L. L., De Gier J. The effect of cholesterol incorporation on the temperature dependence of water permeation through liposomal membranes prepared from phosphatidylcholines. Biochim Biophys Acta. 1977 Feb 4;464(3):509–518. doi: 10.1016/0005-2736(77)90026-8. [DOI] [PubMed] [Google Scholar]
  13. Chan P. H., Fishman R. A., Caronna J., Schmidley J. W., Prioleau G., Lee J. Induction of brain edema following intracerebral injection of arachidonic acid. Ann Neurol. 1983 Jun;13(6):625–632. doi: 10.1002/ana.410130608. [DOI] [PubMed] [Google Scholar]
  14. Chan P. H., Fishman R. A. Transient formation of superoxide radicals in polyunsaturated fatty acid-induced brain swelling. J Neurochem. 1980 Oct;35(4):1004–1007. doi: 10.1111/j.1471-4159.1980.tb07100.x. [DOI] [PubMed] [Google Scholar]
  15. Chan P. H., Kerlan R., Fishman R. A. Reductions of gamma-aminobutyric acid and glutamate uptake and (Na+ + K+)-ATPase activity in brain slices and synaptosomes by arachidonic acid. J Neurochem. 1983 Feb;40(2):309–316. doi: 10.1111/j.1471-4159.1983.tb11284.x. [DOI] [PubMed] [Google Scholar]
  16. Chan P. H., Kerlan R., Fishman R. A. Reductions of gamma-aminobutyric acid and glutamate uptake and (Na+ + K+)-ATPase activity in brain slices and synaptosomes by arachidonic acid. J Neurochem. 1983 Feb;40(2):309–316. doi: 10.1111/j.1471-4159.1983.tb11284.x. [DOI] [PubMed] [Google Scholar]
  17. Clendenon N. R., Allen N., Gordon W. A., Bingham W. G., Jr Inhibition of Na+-K+-activated ATPase activity following experimental spinal cord trauma. J Neurosurg. 1978 Oct;49(4):563–568. doi: 10.3171/jns.1978.49.4.0563. [DOI] [PubMed] [Google Scholar]
  18. Dawson R. M., Hemington N. L., Irvine R. F. Diacylglycerol potentiates phospholipase attack upon phospholipid bilayers: possible connection with cell stimulation. Biochem Biophys Res Commun. 1983 Nov 30;117(1):196–201. doi: 10.1016/0006-291x(83)91560-7. [DOI] [PubMed] [Google Scholar]
  19. De Medio G. E., Goracci G., Horrocks L. A., Lazarewicz J. W., Mazzari S., Porcellati G., Strosznajder J., Trovarelli G. The effect of transient ischemia on fatty acid and lipid metabolism in the gerbil brain. Ital J Biochem. 1980 Nov-Dec;29(6):412–432. [PubMed] [Google Scholar]
  20. Demediuk P., Cowan D. L., Moscatelli E. A. Effects of plasmenylethanolamine on the dynamic properties of the hydrocarbon region of mixed phosphatidylcholine-phosphatidylethanolamine aqueous dispersions. A spin label study. Biochim Biophys Acta. 1983 May 5;730(2):263–270. doi: 10.1016/0005-2736(83)90342-5. [DOI] [PubMed] [Google Scholar]
  21. Demopoulos H. B., Flamm E. S., Pietronigro D. D., Seligman M. L. The free radical pathology and the microcirculation in the major central nervous system disorders. Acta Physiol Scand Suppl. 1980;492:91–119. [PubMed] [Google Scholar]
  22. Dorman R. V., Dabrowiecki Z., Horrocks L. A. Effects of CDPcholine and CDPethanolamine on the alterations in rat brain lipid metabolism induced by global ischemia. J Neurochem. 1983 Jan;40(1):276–279. doi: 10.1111/j.1471-4159.1983.tb12682.x. [DOI] [PubMed] [Google Scholar]
  23. Ellis E. F., Wright K. F., Wei E. P., Kontos H. A. Cyclooxygenase products of arachidonic acid metabolism in cat cerebral cortex after experimental concussive brain injury. J Neurochem. 1981 Oct;37(4):892–896. doi: 10.1111/j.1471-4159.1981.tb04476.x. [DOI] [PubMed] [Google Scholar]
  24. Fertel R., Yetiv J. Z., Coleman M. A., Schwarz R. D., Greenwald J. E., Bianchine J. R. Formation of antibodies to prostaglandins in the yolk of chicken eggs. Biochem Biophys Res Commun. 1981 Oct 15;102(3):1028–1033. doi: 10.1016/0006-291x(81)91641-7. [DOI] [PubMed] [Google Scholar]
  25. Gardiner M., Nilsson B., Rehncrona S., Siesjö B. K. Free fatty acids in the rat brain in moderate and severe hypoxia. J Neurochem. 1981 Apr;36(4):1500–1505. doi: 10.1111/j.1471-4159.1981.tb00592.x. [DOI] [PubMed] [Google Scholar]
  26. Gaudet R. J., Levine L. Transient cerebral ischemia and brain prostaglandins. Biochem Biophys Res Commun. 1979 Feb 14;86(3):893–901. doi: 10.1016/0006-291x(79)91796-0. [DOI] [PubMed] [Google Scholar]
  27. Gaudet R. J., Levine L. Transient cerebral ischemia and brain prostaglandins. Biochem Biophys Res Commun. 1979 Feb 14;86(3):893–901. doi: 10.1016/0006-291x(79)91796-0. [DOI] [PubMed] [Google Scholar]
  28. Goodman J. H., Bingham W. G., Jr, Hunt W. E. Ultrastructural blood-brain barrier alterations and edema formation in acute spinal cord trauma. J Neurosurg. 1976 Apr;44(4):418–424. doi: 10.3171/jns.1976.44.4.0418. [DOI] [PubMed] [Google Scholar]
  29. Griffiths I. R. Spinal cord blood flow after acute experimental cord injury in dogs. J Neurol Sci. 1976 Feb;27(2):247–259. doi: 10.1016/0022-510x(76)90065-4. [DOI] [PubMed] [Google Scholar]
  30. Griffiths I. R. Ultrastructural changes in spinal gray matter microvasculature after impact injury. Adv Neurol. 1978;20:415–422. [PubMed] [Google Scholar]
  31. Hall E. D., Braughler J. M. Effects of intravenous methylprednisolone on spinal cord lipid peroxidation and Na+ + K+)-ATPase activity. Dose-response analysis during 1st hour after contusion injury in the cat. J Neurosurg. 1982 Aug;57(2):247–253. doi: 10.3171/jns.1982.57.2.0247. [DOI] [PubMed] [Google Scholar]
  32. Hall E. D., Braughler J. M. Effects of intravenous methylprednisolone on spinal cord lipid peroxidation and Na+ + K+)-ATPase activity. Dose-response analysis during 1st hour after contusion injury in the cat. J Neurosurg. 1982 Aug;57(2):247–253. doi: 10.3171/jns.1982.57.2.0247. [DOI] [PubMed] [Google Scholar]
  33. Hara A., Radin N. S. Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem. 1978 Oct 1;90(1):420–426. doi: 10.1016/0003-2697(78)90046-5. [DOI] [PubMed] [Google Scholar]
  34. Hill D. J., Dawidowicz E. A., Andrews M. L., Karnovsky M. J. Modulation of microsomal glucose-6-phosphate translocase activity by free fatty acids: implications for lipid domain structure in microsomal membranes. J Cell Physiol. 1983 Apr;115(1):1–8. doi: 10.1002/jcp.1041150102. [DOI] [PubMed] [Google Scholar]
  35. Jonsson H. T., Jr, Daniell H. B. Altered levels of PGF in cat spinal cord tissue following traumatic injury. Prostaglandins. 1976 Jan;11(1):51–61. doi: 10.1016/0090-6980(76)90172-6. [DOI] [PubMed] [Google Scholar]
  36. Karnovsky M. J., Kleinfeld A. M., Hoover R. L., Klausner R. D. The concept of lipid domains in membranes. J Cell Biol. 1982 Jul;94(1):1–6. doi: 10.1083/jcb.94.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Keough K. M., MacDonald G., Thompson W. A possible relation between phosphoinositides and the diglyceride pool in rat brain. Biochim Biophys Acta. 1972 Jul 7;270(3):337–347. doi: 10.1016/0005-2760(72)90198-1. [DOI] [PubMed] [Google Scholar]
  38. Kimes A. S., Sweeney D., London E. D., Rapoport S. I. Palmitate incorporation into different brain regions in the awake rat. Brain Res. 1983 Sep 12;274(2):291–301. doi: 10.1016/0006-8993(83)90707-2. [DOI] [PubMed] [Google Scholar]
  39. Klausner R. D., Kleinfeld A. M., Hoover R. L., Karnovsky M. J. Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. J Biol Chem. 1980 Feb 25;255(4):1286–1295. [PubMed] [Google Scholar]
  40. Kontos H. A., Wei E. P., Povlishock J. T., Dietrich W. D., Magiera C. J., Ellis E. F. Cerebral arteriolar damage by arachidonic acid and prostaglandin G2. Science. 1980 Sep 12;209(4462):1242–1245. doi: 10.1126/science.7403881. [DOI] [PubMed] [Google Scholar]
  41. Lucy J. A. The fusion of biological membranes. Nature. 1970 Aug 22;227(5260):815–817. doi: 10.1038/227815a0. [DOI] [PubMed] [Google Scholar]
  42. Ohki K., Sekiya T., Yamauchi T., Nozawa Y. Effect of phosphatidylinositol replacement by diacylglycerol on various physical properties of artificial membranes with respect to the role of phosphatidylinositol response. Biochim Biophys Acta. 1982 Dec 22;693(2):341–350. doi: 10.1016/0005-2736(82)90441-2. [DOI] [PubMed] [Google Scholar]
  43. Osterholm J. L. The pathophysiological response to spinal cord injury. The current status of related research. J Neurosurg. 1974 Jan;40(1):5–33. [PubMed] [Google Scholar]
  44. Pappius H. M., Wolfe L. S. Functional disturbances in brain following injury: search for underlying mechanisms. Neurochem Res. 1983 Jan;8(1):63–72. doi: 10.1007/BF00965654. [DOI] [PubMed] [Google Scholar]
  45. Rhoads D. E., Kaplan M. A., Peterson N. A., Raghupathy E. Effects of free fatty acids on synaptosomal amino acid uptake systems. J Neurochem. 1982 May;38(5):1255–1260. doi: 10.1111/j.1471-4159.1982.tb07898.x. [DOI] [PubMed] [Google Scholar]
  46. Rodriguez de Turco E. B., Morelli de Liberti S., Bazan N. G. Stimulation of free fatty acid and diacylglycerol accumulation in cerebrum and cerebellum during bicuculline-induced status epilepticus. Effect of pretreatment with alpha-methyl-p-tyrosine and p-chlorophenylalamine. J Neurochem. 1983 Jan;40(1):252–259. doi: 10.1111/j.1471-4159.1983.tb12679.x. [DOI] [PubMed] [Google Scholar]
  47. Sandler A. N., Tator C. H. Review of the effect of spinal cord trama on the vessels and blood flow in the spinal cord. J Neurosurg. 1976 Dec;45(6):638–646. doi: 10.3171/jns.1976.45.6.0638. [DOI] [PubMed] [Google Scholar]
  48. Saunders R. D., Horrocks L. A. Simultaneous extraction and preparation for high-performance liquid chromatography of prostaglandins and phospholipids. Anal Biochem. 1984 Nov 15;143(1):71–75. doi: 10.1016/0003-2697(84)90559-1. [DOI] [PubMed] [Google Scholar]
  49. Sheetz M. P., Singer S. J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4457–4461. doi: 10.1073/pnas.71.11.4457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Shohami E., Rosenthal J., Lavy S. The effect of incomplete cerebral ischemia on prostaglandin levels in rat brain. Stroke. 1982 Jul-Aug;13(4):494–499. doi: 10.1161/01.str.13.4.494. [DOI] [PubMed] [Google Scholar]
  51. Stokes B. T., Fox P., Hollinden G. Extracellular calcium activity in the injured spinal cord. Exp Neurol. 1983 Jun;80(3):561–572. doi: 10.1016/0014-4886(83)90307-2. [DOI] [PubMed] [Google Scholar]
  52. Sun G. Y. Metabolism of arachidonate and stearate injected simultaneously into the mouse brain. Lipids. 1977 Aug;12(8):661–665. doi: 10.1007/BF02533761. [DOI] [PubMed] [Google Scholar]
  53. Swann A. C. Free fatty acids and (Na+,K+)-ATPase: effects on cation regulation, enzyme conformation, and interactions with ethanol. Arch Biochem Biophys. 1984 Sep;233(2):354–361. doi: 10.1016/0003-9861(84)90456-9. [DOI] [PubMed] [Google Scholar]
  54. Vaughan D. J., Keough K. M. Changes in phase transitions of phosphatidylethanolamine- and phosphatidylcholine-water dispersions induced by small modifications in the headgroup and backbone regions. FEBS Lett. 1974 Oct 1;47(1):158–161. doi: 10.1016/0014-5793(74)80449-7. [DOI] [PubMed] [Google Scholar]
  55. Wakai S., Aritake K., Asano T., Takakura K. Selective destruction of the outer leaflet of the capillary endothelial membrane after intracerebral injection of arachidonic acid in the rat. Acta Neuropathol. 1982;58(4):303–306. doi: 10.1007/BF00688614. [DOI] [PubMed] [Google Scholar]
  56. Wolfe L. S. Eicosanoids: prostaglandins, thromboxanes, leukotrienes, and other derivatives of carbon-20 unsaturated fatty acids. J Neurochem. 1982 Jan;38(1):1–14. doi: 10.1111/j.1471-4159.1982.tb10847.x. [DOI] [PubMed] [Google Scholar]
  57. Yorio T., Torres S., Tarapoom N. Alteration in membrane permeability by diacylglycerol and phosphatidylcholine containing arachidonic acid. Lipids. 1983 Jan;18(1):96–99. doi: 10.1007/BF02534698. [DOI] [PubMed] [Google Scholar]
  58. Yoshida S., Abe K., Busto R., Watson B. D., Kogure K., Ginsberg M. D. Influence of transient ischemia on lipid-soluble antioxidants, free fatty acids and energy metabolites in rat brain. Brain Res. 1982 Aug 12;245(2):307–316. doi: 10.1016/0006-8993(82)90813-7. [DOI] [PubMed] [Google Scholar]
  59. Yoshida S., Inoh S., Asano T., Sano K., Shimasaki H., Ueta N. Brain free fatty acids, edema, and mortality in gerbils subjected to transient, bilateral ischemia, and effect of barbiturate anesthesia. J Neurochem. 1983 May;40(5):1278–1286. doi: 10.1111/j.1471-4159.1983.tb13567.x. [DOI] [PubMed] [Google Scholar]
  60. Young W., Yen V., Blight A. Extracellular calcium ionic activity in experimental spinal cord contusion. Brain Res. 1982 Dec 16;253(1-2):105–113. doi: 10.1016/0006-8993(82)90677-1. [DOI] [PubMed] [Google Scholar]
  61. de la Torre J. C. Spinal cord injury. Review of basic and applied research. Spine (Phila Pa 1976) 1981 Jul-Aug;6(4):315–335. [PubMed] [Google Scholar]

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