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Medical Hypotheses L Medicn/H\Pnthmr.~(L994)42

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Medical Hypotheses L Medicn/H\Pnthmr.~(L994)42 Medical Hypotheses L Medicn/H\pnthmr.~(l994)42. 237-242 D LongmanGroup Lul1994 Nervonic Acid and Demyelinating Disease J. R. SARGENT’. K. COUPLAND? and R. WILSONt ‘Department of Biological and Molecular Sciences, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, UK, tCroda Universal Ltd, Hull, HU6 7PH, UK, *Cardiovascular Unit, Hugh Robson Building, University of Edinburgh, George Square, Edinburgh, EH8 9XF; UK. Abstract - Demyelination in adrenoleukodystrophy (ALD) is associated with an accumulation of very long chain saturated fatty acids such as 26:0 stemming from a genetic defect in the peroxisomal beta oxidation system responsible for the chain shortening of these fatty acids. Long chain monoenoic acids such as erucic acid, 22:1(n-9), can normalise elevated serum levels of 26:0 in ALD by depressing their biosynthesis from shorter chain saturated fatty acids. Sphingolipids from post mortem ALD brain have decreased levels of nervonic acid, 24:l (n-9), and increased levels of stearic acid, 18:0. Increased levels of 26:0 are accompanied by decreased nervonic acid biosynthesis in skin fibroblasts from ALD patients. Sphingolipids from post mortem MS brain have the same decreased 24:1(n-9) and increased 18:0 seen in post mortem ALD brain. The 24:1(n-9) content of sphingomyelin is depressed in erythrocytes from multiple sclerosis (MS) patients. Defects in the microsomal biosynthesis of very long chain fatty acids including 24:l (n-9) in ‘jumpy’ and ‘quaking’ mice are accompanied by impaired myelination. An impairment in the provision of nervonic acid in demyelinating diseases is indicated, suggesting that dietary therapy with oils rich in very long chain monenoic acid fatty acids may be beneficial in such conditions. Introduction tal fatty acids as very long chain saturated and es- pecially very long chain monounsaturated moieties Myelination of nerves in human brain starts at a ges- exemplified by lignoceric acid, 24:0, and nervonic tational age of approximately 32 weeks, increases acid, 24:1(n-9) respectively. Moreover, the level of rapidly until and beyond birth, and is largely com- nervonic acid in human brain sphingolipids increases plete in the first 2 or 3 years of life (l-3). The ra- markedly from birth to reach a maximum at about pidity of myelination is illustrated by the myelinat- 4 years after which it remains almost constant (6). ing oligodendrocyte in the rat producing more than Given such a large demand for relatively specialised three times its weight of myelin per day (4). Myelin fatty acids over a relatively short and critical pe- is unusual among biological membranes in that it con- riod of neural development, an impaired provision tains more than 70% of its dry weight as lipid which of these fatty acids early in life could have serious is rich in sphingolipids, i.e. cerebrosides, sulphatides consequences for neural performance, whether in the and sphingomyelin which comprise circa 23%, 4% short or longer terms. The present article presents ev- and 8% of total myelin lipid respectively (5). These idence for an association between demyelination and sphingolipids contain a high proportion of their to- a substantially decreased content of nervonic acid in Date received 7 October 1993 Date accepted 5 November 1993 237 238 MEDICALHYPOTHESES myelin sphingolipids in two demyelinating diseases, Recent research in our own laboratory (11) has in- adrenoleukodystropy and multiple sclerosis. Reasons dicated that the biosynthesis of nervonic acid 24:l underlying such a decrease are considered and a sim- (n-9) is depressed in skin fibroblasts from ALD pa- ple dietary therapy aimed to correct the putatively tients. Nervonic acid normally accounts for some 40% impaired provision of nervonic acid in demyelinating of the total fatty acids in sphingolipids from the brains conditions is proposed. of normal subjects (8). However, in ALD brains the nervonic acid content of sphingomyelin is decreased to less than 30% while the stearic acid 18:O content Adrenoleukodystrophy is increased from 19-2.5%, and essentially the same situation holds for cerebrosides and sulphatides (8). Recent years have seen an increased understanding These findings have led us to postulate (8) that, as of genetic disorders of lipid metabolism specifically 22: 1(n-9) [or 20: 1(n-9) or 18: 1(n-9)1 competitively associated with peroxisomes. The X-linked chromo- inhibits the biosynthesis of 26:0 in ALD, so the 26:0 somal condition adrenoleukodystrophy (ALD) is one accumulating in ALD may inhibit the biosynthesis of such disorder apparently caused by a defect in the 24: 1 and thereby ultimately cause demyelination. ligase that couples coenzyme A with very long chain The foregoing results point firmly to competitive saturated fatty acids such as 26:0, thereby reducing interactions in the biosynthesis of very long chain the oxidation of very long chain saturated acyl CoA saturated and monounsaturated fatty acids. A very derivatives by perixosomes and causing the accumu- limited build up of very long chain saturated fatty lation of these fatty acids in body lipids, Thus, the acids such as 26:0 appears to inhibit the biosynthesis serum lipids of patients with ALD have circa 1.0% of 24: l(n-9) from its 18: l(n-9) or 22: l(n-9) precur- of their fatty acids as 26:0 compared with circa 0.3- sor, presumably due to the extremely hydrophobic na- 0.4% in normal subjects (7). More important, neural ture of 26:0. Conversely, increasing the concentration tissues including the brains of ALD patients accumu- of very long chain monoenes such as 22: l(n-9) in- late 26:0 in their lipids, particularly in their sphin- hibits the biosynthesis of 26:0 from its 18:O precursor golipids. Thus, sphingomyelin, cerebrosides and sul- and simultaneously enhances the biosynthesis of 24: 1 phatides from post mortem brains of ALD patients all (n-9) as evidenced by the increased levels of 24:l(n- have some 3% of their fatty acids as 26:0 compared to 9) in serum lipids of ALD patients fed the blend 1% in normal subjects (8). Cholesteryl esters are the of glyceryl trioleate and glyceryl trierucate (7). In- final repository of excess 26:0 in ALD and in plaque creased levels of 24:l(n-9) in erythrocyte sphin- tissue from ALD brain these esters have more than gomyelin also occur in normal subjects fed borage oil 12% of their fatty acids as 26:0 (8). The accumulation rich in 22:l(n-9) (12). of very long chain fatty acids in ALD neural tissues is accompanied by destruction of myelin both centrally Multiple sclerosis and peripherally, thus causing severe neural symp- toms in young boys and ultimately death at an early Multiple sclerosis (MS) has a much higher incidence age, usually 1 or 2 years after the onset of symptoms. than ALD and, despite many years of intensive re- Fibroblasts cultured from skin biopsies of ALD search, there is still no effective therapy for this patients produce lipids with elevated levels of 26:0 severely debilitating demyelinating condition which compared to normal fibroblasts. Addition of oleic acid follows a relapsing and remitting clinical progression in 18: l(n-9) to the culture medium substantially de- in the majority of patients. Moreover, the aetiology creases the levels and 26:0 in the cultured ALD cells of MS remains unknown although its pathogenesis is (9) and erucic acid 22: l(n-9) is even more effec- generally believed to involve an autoimmune reaction tive (10). Findings such as these are consistent with to a component of myelin. A current plausible hypo- monounsaturated fatty acids inhibiting the biosynthe- thesis is that the disease may result from an autoim- sis of 26:0 with increasing efficiency in the order mune response triggered by an environmental factor, 18: 1 ~20: 1 ~22: 1. They form the rational for a dietary possibly a non-specific viral infection, in a genetically therapy of ALD, currently under clinical trial, with a susceptible individual (13). However, given the in- blend of glyceryltrioleate and glyceryltrierucate. This creased understanding of the causes and pathology of oil blend normalises the elevated levels of 26:0 in ALD, it is worthwhile reconsidering the role of lipids serum lipids of ALD patients (7) raising promise that, in the aetiology of MS. if administered sufficiently early to ALD patients, it Gerstl and his colleagues (14) originally noted may delay the appearance and/or decrease the sever- from a very limited number of samples that sph- ity of the severe neural symptoms expressed in the ingolipids in post mortem brain from MS patients condition. had reduced levels of 24: 1(n-9) accompanied by in- NERVONIC ACID AND DEMYELINATING DISEASE 239 creased levels of 1810, These authors suggested that sphingolipids. This points to a generalised defect in a defect in the biosynthesis of nervonic acid in MS nervonic acid biosynthesis in MS patients and sup- leads to breakdown of myelin which triggers the ports the contention that the decreased nervonic acid onset of the autoimmune response (14). In view content in brain sphingolipids in MS may contribute of these findings and our own findings with ALD to demyelination rather than being a consequence we have recently analysed the sphingolipids in post of it. Recent evidence indicates that levels of 24:l mortem brains from 9 MS patients and 9 normal (n-9) in erythrocyte sphingomyelin in premature in- control individuals. The results (Table) clearly estab- fants may reflect levels of 24:1(n-9) in brain sphin- lish that in sphingomyelin, sulphatides and cerebro- gomyelin and thus brain maturity (16). sides there is a marked decrease in 24: l(n-9) which That an impaired biosynthesis of 24:l(n-9) can be is almost exactly balanced by an increase in 18:O associated with dysmyelination is indisputable since + 16:O in MS individuals as compared to controls.
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