Lipid composition of the normal human brain: gray matter, white matter, and myelin

Lipids of nervous tissue: composition and metabolism.

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Metabolism and Physiological Significance of Lipids

Quantitative densitometric thin-layer chromatography of lipids using copper acetate reagent.

IN an earlier report (AUTILIO, NORTON and TERRY, 1964) we described a method for isolating purified bovine brain myelin. The two myelin fractions which were obtained were called light and heavy, according to their relative positions after centrifugation in a sucrose density gradient. Preliminary data on the lipid composition of the light myelin fractions have already been reported (NORTON and AUTILIO, 1965). The detailed analysis of both fractions is presented here.

The lipid composition of purified bovine brain myelin

ELECTRON microscopic studies have shown that the myelin sheath is composed of a compact ordered arrangement of unit membranes (FINEAN, 1957 ; ROBERTSON, 1959, 1964). Myelin therefore provides a particularly suitable model for the investigation of the molecular organisation of biological membranes. However, until quite recently it was not possible to isolate myelin from nervous tissue and reliable information about its chemical composition was not available. Improved methods for the separation of subcellular structures have now been applied to neural tissue and a number of laboratories have described techniques for the isolation of myelin in a form suitable for direct analysis (WHITTAKER, 1959; PATTERSON and FINEAN, 1961 ; AUGUST, DAVISON and WILLIAMS, 1961 ; LAATSCH, KIES, GORDON and ALVORD, 1962; DAVISON and GREGSON, 1962; HULCHER, 1963). Some reports of the lipid composition of myelin from individual species have already appeared (PATTERSON and FINEAN, 1961 ; NUSSBAUM, BIETH and MANDEL, 1963; AUTILIO, NORTON and TERRY, 1964; EICHBERG, WHITTAKER and DAWSON, 1964; SEMINARIO, HREN and GOMEZ, 1964; CUZNER, DAVISON and GREGSON, 1965). Although it has been suggested that all membranes may have a common ‘unit membrane’ structure (ROBERTSON, 1964) both electron microscopic and biochemical evidence indicate that the various membranes found in the cell are not necessarily similar in all properties (STOECKENIUS, 1964). Earlier work from this laboratory has indicated that mammalian myelin may represent a unique class of membrane for it has a characteristically slow rate of turnover with little associated enzyme activity (ADAMS, DAVISON and GREGSON, 1963). In addition indirect evidence led to the idea that the lipid composition of myelin also differs from that of other membranes (ROSSITER, 1962; ADAMS and DAVISON, 1965; GREGSON 1965). The purpose of the present work has been to investigate this possibility more thoroughly by comparing the chemical composition of myelin with that of another cell membrane fraction from the same tissue. Myelin and microsomal fractions have been prepared therefore from the brains of a number of mammalian and more primitive vertebrates ; samples have been examined by electron microscopy and submitted to chemical analysis. The results of these and earlier observations will be discussed with particular reference to the possible molecular organisation of membranes. EXPERIMENTAL Materiais. The following animals were used in the present work: white Wistar rats, rabbits, the feral pigeon, common frog (Rana temporaria) and dogfish (Scyllium cuniculu). These animals were killed, exsanguinated and the brain removed. Ox brain, collected in ice from the slaughter house, and human frontal cerebral cortex obtained at autopsy, were brought to the laboratory and white matter removed. Human brains were obtained from patients who had died from non-neurological causes.

The chemical composition of vertebrate myelin and microsomes

The brain differs from other organs in that dynamic metabolism of total lipids is restricted in the former in comparison to the rest of the body. Previous investigators (Davison & Dobbing, 1960a, b; Davison, Morgan, Wajda & Payling Wright, 1959) have shown, by introduction of radioactive precursors into developing anini’als, that part of the brain lipids remained metabolically stable during growth and subsequently in the adult animal. It was further suggested that this metabolic stability was associated with the myelin sheath and possibly other anatomical structures in the brain. Evidence in support of this concept has recently been reviewed (Davison, 1964).

Chemical and metabolic studies of rat myelin of the central nervous system.

— The surface properties of isolated rat brain myelin have been investigated by the method of particle microelectrophoresis. The mobility has been measured as a function of ionic strength and composition of the buffer, the results suggesting the presence of areas of non-ionogenic material. Antisera against ganglioside and myelin produce a fall in mobility whereas antiproteolipid apoprotein produces a slight increase but antibasic protein and anticerebroside sera had no effect on mobility. Of the lipases studied only phospholipase D produced a clear increase in mobility. From this preliminary study some indications of the asymmetric disposition of components in the myelin sheath may be derived. The ganglioside appears to be wholly located at intraperiod line interface, along with some fraction of the galactocerebroside and phosphatidylcholine. There appears to be few amino groups, but SH groups are present.

The surface properties of isolated rat brain myelin: a microelectrophoretic study.

—New data are presented and published data reviewed to show that the protein content of rat brain myelin must be close to 21 per cent. Ultraviolet absorption measurements in the 220 nm region, however, indicate an apparent protein content of 44·3 per cent which, after solubilization with lysophosphatidylcholine falls to 35·8 per cent. It is shown that this latter proportion can be accounted for in terms of u.v. absorption by myelin protein and lipids, contributions being made by sphingolipids, phospholipids and cholesterol. It is concluded that in the environment of the intact myelin structure, u.v. absorption due to some of the chromophores is enhanced and that this effect is relaxed by lysophosphatidylcholine solubilization. Supportive evidence is given from measurements in the 280 nm region.

Ultraviolet absorption characteristics of myelin from the central nervous system.

EARLIER work on the lipid and protein metabolism of grey and white matter of brain suggested that the myelin sheath may be in a metabolically dynamic state (SCHEINBERG and KOREY, 1962). Quantitative cytochemical studies of Ammon’s horn in the rabbit (LOWRY et af., 1954) first suggested that myelin may itself be enzyinically active. This view was based on finding more enzyme activity and more acid soluble phosphorus derivatives in the myelinated layer than would then be expected from the content of axons and neuroglia. More recently, it has been claimed that a wide range of oxidative and hydrolytic enzymes are present i n the myelin sheath of the peripheral nerve and in its neurokeratiri network (WOLFGRAM and ROSE, 1960; TEWARI and BOURNE, 1960a, b and c): some enzyme activity has also been reported in CNS myelin (TEWAIU and BOURNE, 1962n and h). TEWARI and BOURNE regard the tieurokeratin network as the locus of metabolic activity within the myelin sheath. If these histological and histochemical observations on neurokeratin and myelin enzymes can be substantiated, the myelin sheath would appear to be potentially metabolically active and could be regarded as a functional part of the cytoplasm of its formative cell-oligodendrocyte or Schwann cell~-and therefore, susceptible to injury by metabolic derangements. However, evidence has been accumulated from isotope studies to show that myelin lipids (DAVISON et al., 1959 a and 6; DAVISON and D o B B I N c ; , 1960) and proteins

Enzyme inactivity of myelin: histochemical and biochemical evidence.

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