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Red-Cell and Plasma Lipids in Acanthocytosis

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Red-Cell and Plasma Lipids in Acanthocytosis RED-CELL AND PLASMA LIPIDS IN ACANTHOCYTOSIS Peter Ways, … , Claude F. Reed, Donald J. Hanahan J Clin Invest. 1963;42(8):1248-1260. https://doi.org/10.1172/JCI104810. Research Article Find the latest version: https://jci.me/104810/pdf Journal of Clinical Investigation Vol. 42, No. 8, 1963 RED-CELL AND PLASMA LIPIDS IN ACANTHOCYTOSIS * By PETER WAYS,t CLAUDE F. REED, AND DONALD J. HANAHAN WITH THE TECHNICAL ASSISTANCE OF DOLORES DONG, SUSAN PALMER, MARION MURPHY, AND GERALDINE ROBERTS (From the Departments of Biochemistry and Medicine, University of Washington, Seattle, Wash., and the Department of Medicine, University of Rochester School of Medicine and Dentistry, Rochester, N. Y.) (Submitted for publication January 18, 1963; accepted April 11, 1963) The rare syndrome of acanthocytosis was first tological, and gastrointestinal) are all secondary described in 1950 by Bassen and Kornzweig (1) to the absence of low-density lipoprotein (6, 7). and two years later by Singer, Fisher, and Perl- This is still conjectural, however, and the bio- stein (2). The principal manifestations reported chemical defect responsible for the disease has not were steatorrhea, "atypical" retinitis pigmentosa, been elucidated. progressive neurological deficits, and "thorny" The clinical and chemical abnormalities of acan- red cells. The most complete case reports to date thocytosis suggested that it might be an ideal syn- are those of Meir, Schwartz, and Boshes (3) and drome in which to seek abnormalities in red-cell Rey (4), who well review the clinical aspects. lipids. Values previously reported for total red- The erythrocytes of affected individuals have char- cell lipids in one case (3) and for red-cell choles- acteristic, spikelike excrescences, a normal or de- terol and total phospholipid (6) in another were creased life-span, probably normal osmotic fragil- probably normal (normal values were not given), ity, normal acid fragility, increased susceptibility but the possibilities of qualitative changes were to mechanical trauma, and an increased rate of not investigated. In the present study, red-cell destruction in lysolecithin hemolysis tests (2-5). and plasma lipids from three patients with the Recently, it has been demonstrated electropho- disorder were examined, and abnormalities in both retically, immunologically, and by ultracentrifu- the distribution of phospholipids and in the con- gation that beta or low-density lipoproteins are tent of esterified linoleic acid have been found. absent or very low in acanthocytosis (4, 6, 7), thus Part of these studies have been previously re- explaining the low levels of plasma total lipid, ported in preliminary form (10), and subsequently cholesterol, and phospholipid noted earlier (3, 8, Phillips (11) has reported partially confirmatory 9). Striking vacuolization of the intestinal ab- studies on red-cell and plasma lipids in acantho- sorptive cell has also been described, and histo- cytosis. chemical techniques have shown lipid in these vacuoles (4, 6, 7). METHODS On the basis of these findings, it has been sug- Patient 1 was a preadolescent male,1 not previously gested that acanthocytosis is primarily a disease of reported, with well-documented acanthocytosis (see Ap- pendix). Patient 22 was reported in abstract form by lipid or lipoprotein metabolism and that the prin- Mabry, DiGeorge, and Auerbach (7, 12). Patient 3 3 cipal clinical manifestations (neurological, hema- was reported by Mier and associates (3). Table I lists the principal manifestations of acanthocytosis found in * This study was assisted by grants from the American each of these patients. Heart Association, supported by the Washington State Blood was drawn into acid citrate dextrose,4 refrig- Heart Association; by grants from the Life Insurance erated at 40 C, and transported as directly as possible to Medical Research Fund, the Multiple Sclerosis Society, and the U. S. Public Health Service (H-7326); and by 1 Under the care of Dr. Charles U. Lowe, Buffalo, N. Y. contract DA-49-007-MD-632 with the Research and De- 2 Original material kindly furnished by Dr. Arthur velopment Division, Office of the Surgeon General, De- McElfresh of St. Christopher's Hospital, Philadelphia, Pa. partment of the Army. 3 Blood obtained through the kindness of Dr. M. Mier, t Established Investigator, American Heart Association. Chicago, Ill. This study was begun during tenure of U. S. Public 4 Formula A. National Institutes of Health, Bethesda, Health Service postdoctoral research fellowship HF 9957. Md. 1248 1249 RED-CELL AND PLASMA LIPIDS ACANTHOCYTOSIS C:0.0 0 CO~~~~~~~U00 C4 o .410o ~ CoCO . C CU 4, S 0~~~~C 02 '..CC.2 0 4 0 tic o.>o.2 - C6 7 24 ..- 0 @2 20~ ~ ~ ~ ~ ~~~~6 c 0~ ~ ~~~~~~4 41 co00v0 CO) coco.' ~ 02 A v~2.<C 04 04~~22 Cl)~~ ~ ~ ~ ~ C) Oa 4i~~~~~~~~~~~~~~~~~~ C4 0 24>2042.- ~~~4.i ~ ~ ~ ~ ~ ~ ~ ~ 4 .6 co ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~~ Cd>.4) 4iU ~ 4 CU - 2. 0 R m- S c co 1 0 0 to .- 02 co... 4,>~~~~~~~~~~~~~~~~~~~~~~~~~~4 C 4.2l.O 0 0 cd%0 4 0 4i~~ ~ ~ ~ ~ ~ *4-) *~~~~~~~~~~ 1l 1250 PETER WAYS, CLAUDE F. REED, AND DONALD J. HANAHAN one of our laboratories. The longest interval between nol and 0.04 ml of concentrated sulfuric acid, and then the time of blood collection and red-cell extraction (or refluxing 4 hours at 60° to 70° C. The methyl esters in one instance, freezing) was 15 hours. We have dem- were extracted with petroleum ether, washed with water onstrated that there is no significant change in red-cell four times, dried over anhydrous sodium sulfate, and then total lipids, lipid phosphorus, phospholipid distribution, or dissolved in redistilled hexane. Gas-liquid chromatogra- fatty acid composition during storage at 40 C in acid phy -of the methyl esters was performed on either a citrate dextrose for this length of time. Plasma and red Barber-Colman model 15 or a Pye-Argon gas chromato- cells were separated by centrifugation at 40 C, and the graph with ethylene glycol succinate as stationary phase cells washed three times and resuspended in cold 0.9% at column temperatures of 1650 to 1720 C and gas inlet NaCl to a hematocrit of approximately 50. After mixing, pressures of 12 to 20 pounds per square inch. Methyl samples were pipetted for red-cell counts, lipid extrac- esters of myristic, palmitic, stearic, oleic, and linoleic acids tions, and hematocrit. The extraction and subsequent pure by thin-layer and gas-liquid chromatography were analysis of total lipid, cholesterol, and phospholipids in used to standardize the instrument, and the molar per- the Rochester laboratory have been described (13). In centages for these five compounds are correct to ± 2%o. the Seattle laboratory, red cells from Patient 1 were In calculating methyl arachidonate and longer-chain similarly extracted. In Patient 3, however, after the re- methyl esters for which standards were not available, the extraction with chloroform, nonlipid impurities were re- molar percentage of each ester was assumed to be propor- moved by dissolving the lipid in chloroform:methanol:0.1 tional to its peak area when the Pye-Argon equipment M KCl 8:4:3 (final relative volumes). After shaking, was used, and proportional to peak area divided by molec- cooling to 4° C, and rewarming to 250 C, clean separa- ular weight with the Barber-Colman instrument (flame de- tion occurred, and the chloroform layer was recovered. tector. Red-cell ghosts were prepared in 20-milliosmolar All extractions were performed in duplicate. pIhosphate buffer at pH 7.4 by the method of Dodge, In Seattle, lipids were fractioned on silicic acid col- MIitchell, and Hanahan (16), and red-cell counts were umns (2 g silicic acid and 1 g of Johns-Manville Hi- done on a Coulter electronic counter. Fatty acid esters Flow Super Cell per 1 mg lipid phosphorus). Neutral were quantitated by dissolving the lipid in chloroform and lipids were removed with chloroform. The first phospho- measuring infrared absorption at 5.75,u in 1-mm NaCl lipid peak, eluted with chloroform: methanol (C: M), 9: 1 cells with a Perkin-Elmer model 21 infrared spectro- (vol: vol), comprised 1 to 2%o of the total lipid phos- photometer. Calculations were made from the optical phorus. Although not fully characterized, it has the mo- density of appropriate standards. This method has been bility on paper chromatograms of phosphatidic acid or shown to be linear between 2 and 22 ,uEq fatty acid ester "polyglycerol phosphatide" (14). The next peak, eluted per ml for triolein, dimyristoyl lecithin, and cholesterol with C: M, 5: 1, or 6: 1, contained primarily phospha- palmitate. Plasmalogens (17), ultracentrifugation of tidyl ethanolamine with some phosphatidyl serine.5 The plasma lipoproteins (18), lipid phosphorus, nitrogen, third peak, eluted with the first four to five column vol- total solids, and cholesterol (15) were done by established umes of C: M or ethyl acetate: methanol, 5: 4, was pre- procedures. dominantly phosphatidyl serine by paper chromatography, Certain of the total lipid analyses and phospholipid par- but also contained phosphatidyl inositol and other com- titions were performed in both laboratories on different pounds as yet unidentified. Continuing the same solvent, samples of the same blood. When such data have been a large fraction was then eluted, the first two-thirds of it averaged, this is indicated in the tables. chromatographically pure lecithin. Subsequently, a mix- ture of lecithin and sphingomyelin appeared, the solvents RESULTS were changed to C: M, 1: 9, and the final peak, approxi- mately 90% sphingomyelin and 10% lecithin, emerged. Red-cell and plasma lipid studies in patients with Each peak containing more than one phospholipid was re- acanthocytosis chromatographed on paper by the method of Reed, Swisher, Total lipids and phospholipid distribution. Pre- Marinetti, and Eden (13), and lipid phosphorus was eluted quantitatively. These data, in addition to molar vious publications have characterized and quanti- nitrogen: phosphorus and molar fatty acid ester: phos- tated the major lipid classes in human red cells (13, phorus ratios, were used to arrive at the final phospho- 15, 19-21).
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