METABOLISM OF ESSENTIAL FATTY ACIDS
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1 METABOLISM OF ESSENTIAL FATTY ACIDS V. METABOLIC PATHWAY OF LINOLENIC ACID* BY GUNTHER STEINBERG, WILLIAM H. SLATON, JR., DAVID R. HOWTON, AND JAMES F. MEAD (From the Atomic Energy Project, School of Medicine, University of California, Los Angeles, California) (Received for publication, July 16, 1956) Essential fatty acid activity is generally ascribed to a group of higher polyunsaturated fatty acids, including linoleic, linolenic, and arachidonic acids (1). Recent work from this laboratory has demonstrated that fed linoleate is incorporated in its entirety into arachidonate (2). This conversion could logically take place in three steps, one involving chain lengthening and two involving dehydrogenation. It has been shown (3) that chain lengthening occurs by addition of acetate, but the position of this homologation in the three-step sequence is not yet known. One fatty acid with the required empirical formula of an intermediate in this sequence is linolenic acid, although the positions of its double bonds do not make it a logical precursor of arachidonate. Furthermore, although it has been listed with the essential fatty acids by some authors, there is general agreement that in biological activity linolenic acid differs both quantitatively and qualitatively from linoleate and arachidonate (4-6). Moreover, experiments on alkali isomerization have indicated that administration of linolenate to animals results in an increase in pentaene and hexaene (rather than tetraene) acids (7,8). In order to ascertain whether linolenate can be converted to arachidonate in the animal body and to elucidate its metabolic pathway, methyl linolenate, labeled with Cl4 in the carboxy group, -*as fed to rats. Its metabolic transformations were then followed by isolation and characterization, when possible, of its conversion products. EXPERIMENTAL Methyl lindenate-l-c14 was synthesized by Dr. Nevenzel and Dr. Howton of this laboratory by methods (to be published) similar to those used in preparing methyl linoleate-l-cl4 (9). Treatment of An&&--To each of ten rats (400 f 50 gm.) were administered about 90 mg. of a mixture of 40 per cent methyl linolenate-1-p * This paper is based on work performed under contract No. AT-94-l-gen-12 between the Atomic Energy Commission and the University of California at Los Angeles. 841
2 842 METABOLISM OF ESSENTIAL FATl!Y ACIDS (7.4 X l(r disintegrations per second per mg.) and 60 per cent corn oil (total administered activity, about 3 X lo* disintegrations per second per rat). Eight animals were killed after 4 hours, and two were utilized for 8 hour respiratory carbon dioxide studies (10) and were killed subsequently _ _ _.g l.ooo- s.900- z a.800, x y 100, d.600- z 500, ii z 400- % 0 IO Fraction (25 ml.) FIQ. 1. Reversed phase separation of fatty acids obtained by reduction of etherinsoluble polybromides. Solvents (A-70, etc.) were composed of mineral oil-saturated acetone-water mixtures containing the volume per cent acetone indicated by the number. The arrows indicate the solvent changes. Livers, kidneys, hearts, spleens, and abdominal fat of the animals killed after 4 hours and of one rat utilized after 8 hours for this study were pooled and frozen at once. Isolation of Higher Unsaturated Fatty Acids. Separation and Degradation of Arachidic A&c-The higher unsaturated fatty acids were isolated as insoluble polybromides as described previously (2, 3) ; these were de-
3 STEINBERG, SLATON, HOWTON, AND MEAD 843 brominated, the resulting unsaturated fatty acids hydrogenated, and the saturated acids thus obtained separated by reversed phase chromatography (see Fig. 1) to yield 78 mg. of arachidic acid as previously described (2). After dilution with 242 mg. of synthetic arachidic acid (Sapon Laboratories), this acid was degraded by the method of Dauben et al. (2, 11) to margaric acid, and three successive samples of benzoic acid, the carboxy carbon of which represented carbon atoms 1, 2, and 3, respectively, of the original arachidonic acid. The resulting margaric acid was counted (see below) and, after subsequent recovery from admixture with the scintillator by chromatography on silicic acid, was decarboxylated via the Schmidt reaction (3, 12). The stearic acid obtained from the reversed phase chromatographic separation and a sample of the fed mixture of linolenate-l-cl4 in corn oil (after hydrogenation and saponification) were similarly decarboxylated; both the amines and the carbon dioxide (as BaCOJ were counted. Lirwleic Acid-The ether-soluble, petroleum ether-insoluble tetrabromostearic acid was obtained from the main bromination mixture. After repeated crystallization from ethylene chloride and acetone, the crude material was esterified with diazomethane and chromatographed on alumina (13). Alkali Isomerization of Higher Polyene Mixture-The ether-insoluble polybromides obtained from additional animals fed linolenate-l-cl4 were debrominated, and 38 mg. of the resulting oil were isomerized in 21 per cent KOH-ethylene glycol for 15 minutes at 180 under nitrogen (14). RESULTS AND DISCUSSION The excretion of the carboxy carbon in urine and respiratory carbon dioxide of two of the linolenate-fed rats is presented in Table I. Rat 1 appeared very torpid during the study and slept almost continuously. These facts may explain the low activity of the respiratory COZ. The high activity of the urine in Rat 2 is not explained and has not been noted previously. The distribution of activity in the organ lipides of the rats fed linolenate is presented in Table II; it is evident that activity from linolenate is distributed in all fatty acid fractions. The activity of the saturated fatty acids derived from the ether-insoluble polybromides and of the products of their chemical degradation is shown in Table III. The distribution of the label in the different portions of the arachidic acid molecule determined by three l-carbon degradations revealed that 4 per cent of the total activity still resided in the margaric acid, representing the terminal 17 carbon atoms of the arachidic acid. Decarboxylation of
4 844 METABOLISM OF ESSENTIAL FATTY ACIDS the (31, acid disclosed that 22 per cent of its activity was present in the hexadecylamine (terminal C,,) portion. The over-all distribution of label TABLE I Excretion of Carbozy Carbon of Linolenic Acid %z Activity administered Activity of respiratory COP (cumulative urine at following post8 r cent of administered dose) and 8 hr. Einistration intervals 1 hr. 2 hrs. 3 hrs. 4 hrs. 3 hn. 6 hrs. 7 hrs. 8 hrs. Urine Total disintegmtions per sec X X * Counted as B&O* in the usual manner. TABLE II Weights* and Activitiest of tipide Fractions from Linclenate-Fed Rats I Speci6c activity (c.p.8. per mg.) of (16.0) 0.55 (15.5) 0.76 (8.5) 3.29 (0.532) (3.51) (29.0) 1.28 (12.0) 3.00 (13.0) (0.341) 1.11 (6.57) (13.0) 7.05 (10.0) 3.10 (3.0) 7.77 (7.0) (0.266) (12.60) (36.0) 6.18 (32.0) 2.98 (12.0) 9.49 (17.0) (0.914) (9.cw (23.0) 1.75 (8.0) (15.0) (0.716) (7.00) * The figures in parentheses represent the weights of the fractions in gm. t Counting performed with a Nuclear Instrument and Chemical Corporation flow counter on lipides plated directly on 1 inch aluminum planchets with lens paper (21). $ For total activity of saturated acids derived from octabromide fraction, see Table III. 5 Sacrificed after 8 hours; all others were sacrificed at 4 hours. 11 Recrystallized to constant activity. in arachidic acid is indicated below: CrfiHsa-CHn-CHr-CHs-COOH Total activity, Y For comparison with the activities of carbon 4 and carbons 5 through 20, the distribution of label in the fed linolenate in corn oil and in the stearic acid obtained from the first main peak of the reversed phase chromatogram was determined (see Table IV).
5 STEINRERCi, SLATON, HOWTON, AND MEAD 845 These results indicate that the activity beyond the originally labeled atom (C-3) is indeed real. Such activity may be explained by assuming TABLE III Isotope Concentration in Various Fractions Fraction Arachidic acid (Go), 78 mg. diluted to 242 mg. Benzoic acid, carbon atom 1 I I I 2 I 3 Margaric acid (Cl,) Barium carbonate, carbon atom 4 Hexadecylamine Stearic acid (reversed phase chromatogram) Barium carbonate (carboxy group) Heptadecylamine Linolenic-1-C acid in corn oil (fed) Barium carbonate (carboxy group) Heptadecylamine Behenic acid (CW) Tetrabromostearic acid (recrystallized) Methyl tetrabromostearate (chromatographed) icintihtion counter* C.)J. fia mmols 4, , ,860 5,472,OOO 10, _. Kicromfl countert , , * Tracerlab CE-1 liquid scintillation counter operating at 45.7 f 1.5 per cent efficiency; scintillation medium, 50 ml. of toluene (reagent) containing gm. of 2,5-diphenyloxazole and gm. of 1,4-bis-2(5-phenyloxazol)benzene (scintillation grade; Arapahoe Chemicals, Inc., Boulder, Colorado) per liter at 20. t Since barium carbonate cannot be counted in a liquid scintillation counter, a Nuclear Instrument and Chemical Corporation Micromil thin window, Q gas flow counter, model D-47, was used to count the products of the Schmidt reactions. Samples corrected for counter variation by means of a National Bureau of Standards sodium carbonate standard plated and counted as barium carbonate. TABLE IV Distribution of Label in Fed Linolenate in Corn Oil and in Stearic Acid Source of stesric acid C17H;rCooH )C? cent )CI cent loto1 ocrioiry Reversed phase chromatogram* Fed linolenate-1-c in corn oil * See Fig. 1. that several /3 oxidations of linolenate occur without affecting the double bond system and that the molecule is rebuilt by addition of labeled acetate which would be expected to result from /3 oxidation of linolenate or
6 846 METABOLISM OF ESSENTIAL FATTY ACIDS its derivatives. This interpretation seems to be strengthened by the results of the decarboxylation of the l&carbon acid separated by chromatography from the saturated fatty acids derived from the polybromo acids and containing, again, measurable activity beyond the carboxy group. The possibility that some total synthesis occurred could not be excluded, since no hexabromide derived from linolenate was isolable from the polybromide mixture. It is significant that in the arachidic acid derived from exactly similar experiments, but starting with carboxy-labeled linoleate, no activity occurred beyond carbon atom 3 (2). The GO acid degraded in this experiment is undoubtedly not derived entirely from arachidonic acid. Alkali isomerization data from other laboratories (7, 8) indicate that linolenate is converted in the animal body mainly to pentaene and hexaene acids, and similar data obtained in the TABLE V Extinction Coeficients at Characteristic Maxima of Polyunsaturated Fatty Acids after Alkali Isomerization (in dl Per Cent KOH-Glycol for lb Minutes at 180 ) Sample Wave length, mp PP Methyl araohidonate (Hormel lot No. 1) Linoleate-fed control Linolenate-l-P-fed present study (see Table V) indicate qualitatively that the linolenate-fed animals contain a somewhat larger proportion of pentaene and hexaene fatty acids. By using the equations given by Hammond and Lundberg (15), a 3.5 to 6 per cent excess pentaene over the controls may be calculated, depending on whether the pentaene is assumed to be CzO or Cn. Klenk and his coworkers characterized a number of eicosapolyenoic acids from brain and liver phosphatides (16, 17) and presented evidence for the existence of a GO pentaene acid with double bonds at positions 5,8, 11, 14, 17 and two GO tetraene acids, arachidonic (double bonds at 5, 8, 11, 14) and an acid with double bonds at 8, 11, 14, 17. Those with a double bond at position 17 are presumably derived from linolenate and, after isolation as ether-insoluble polybromides and reduction, would be expected to contribute to the arachidic acid fraction otherwise derived from arachidonic acid. The direct separation of the octa- and decabromides is precluded by their solubility characteristics. However, separation of acids of a given chain length differing only in degree of unsaturation (which is feasible (18)
7 STEINBERG, SLATON, HOWTON, AND MEAD 847 and presently under consideration) could conceivably indicate which Go polyene acid (pentaene or tetraene) contributes the major activity to the arachidic acid fraction. No distinction betyeen acids isomeric with respect to disposition of double bonds can be expected to be accomplished chromatographically, although such differences may be shown by degradation methods such as those described by Klenk and Bongard (19). Chromatography on reversed phase columns with sample polyene substrates has permitted estimation of the place where a Go pentaenoic acid would be expected to emerge from the column. However, in the absence of an authentic sample of this material, no positive confirmation could be obtained. Nevertheless, these experiments did serve to indicate that Go pentaene and tetraene would be separable, but that Cl8 triene and CZ hexaene would probably emerge between the two Go acids, thus obscuring two well defined peaks, broadening them into one continuous, undifferentiated band. An actual run with polyenes derived from the polybromides from rats fed linolenate-l-cl4 resulted in a very broad peak, which is probably a composite of three or four overlapping peaks. The eluate was divided into three fractions (leading, trailing, and central) and each was processed, hydrogenated, extracted into scintillation medium (toluene solution), and counted. The leading portion representing the area where Czo pentaene was expected to emerge contained 10 times the activity of the trailing fraction (arachidonic acid concentrate), giving presumptive evidence that most of the activity is associated with CZ~ pentaene. The activity found in the even-numbered carbon atoms of arachidic acid is surprising in view of the almost complete absence of apparent randomization of activity in the linoleate experiment (2). The question of the reality of such a randomization and how to account for it has drawn the attention of several workers (11, 20). The usual ratio of activity of oddto even-numbered carbon atoms in acids derived from carboxy-labeled acetate ranges from 1O:l to 6O:l and may be suspect, since oxidative methods used may have given rise to lower homologues by overoxidation. The methods utilized here are considered to be unambiguous in this respect. Little conversion of linolenate to linoleate seems to occur. Although the isolated tetrabromostearic acid contained some label after repeated crystallization, this activity was almost completely removed by chromatography of the methyl ester on alumina, a method known to be capable of clean separation of C18 tetra- and hexabromo esters. Thus if linolenate is converted to arachidonate, its Al6 double bond is evidently not reduced until after a chain lengthening step has occurred. However, such a conversion seems most unlikely from other evidence, since linolenate does not exhibit the same biological activity as do linoleate and arachidonate. Thomasson (4) has pointed out a difference in structure that divides the
8 848 METABOLISM OF ESSENTLkL FATTY ACIDS higher polyene acids into two distinct groups. This hypothesis, based on a water consumption assay of a number of fatty acids, reveals that those polyene acids having a double bond system in the 6 and 9 positions (counting from the terminal methyl group) have essential fatty acid activity. The presence of additional 1,4 double bonds towards the carboxy1 end of the fatty acid molecule resulted in retention or enhancement of essential fatty acid activity, while extending the 1,4 polyene system towards the methyl group caused decrease or loss of activity. The results of the present study substantiate, on a metabolic level, the differences in essential fatty acid activity of linoleate and linolenate, and suggest that the latter is converted to CA0 and Czz pentaene and hexaene acids, possibly via a CzO tetraenoic acid isomeric with arachidonic acid. Chain lengthening of linolenate to related higher polyene acids probably takes place in a manner analogous to that shown previously to function in the case of linoleate. There is also evidence that partial oxidation and resynthesis may occur. SUMMARY The polybromo fatty acids isolated from rats which had been fed methyl linolenate-l-cl4 were isolated, debrominated, and hydrogenated. Degradation by l-carbon steps of the arachidic acid separated from the resulting saturated fatty acids revealed that its unsaturated precursor had been formed from linolenate by the addition of acetate to the carboxyl end. However, linolenate carbon did not contribute appreciably to the linoleic acid isolated from these rats, and indirect evidence was obtained which indicated that linolenate is converted, not to arachidonic, but to a different polyunsaturated acid, possibly eicosapentaenoic acid. BIBLIOGRAPHY 1. Holman, R. T., in Sebrell, W. H., Jr., and Harris, R. S., The vitamins, New York, 2, 267 (1954). 2. Steinberg, G., Slaton, W. H., Jr., Howton, D. R., and Mead, J. F., J. Biol. Chem., 220, 257 (1956). 3. Mead, J. F., Steinberg, G., and Howton, D. R., J. Biol. Chem., 206, 633 (1953). 4. Thomasson, H. J., International conference on biochemical problems of lipids, Brussels, 212 (1953). 5. Hume, E. M., Nunn, L. C. A., Smedley-McLean, I., and Smith, H. H., Biochem. J., 34, 879 (1940). 6. Greenberg, S. M., Calbert, C. E., Savage, E. E., and Deuel, H. J., Jr., J. Nutr., 41,473 (1950). 7. Widmer, C., Jr., and Holman, R. T., Arch. Biochem., 26, 1 (1950). 8. Reiser, R., J. Nutr., 42, 325 (1950). 9. Howton, D. R., Davis, R. H., and Nevenzel, J. C., J. Am. Chem. Sot., 76, 4970 (1954). 10. Mead, J. F., Slaton, W. H., Jr., and Decker, A. B., J. Biol. Chem., 218,401 (1956).
9 STEINBERG, SLATON, HOWTON, AND MEAD Dauben, W. G., Hoerger, E., and Petersen, J. W., J. Am. Chem. Sot., 76, 2347 (1953). 12. Phares, E. F., Arch. Biochem. and Biophys., 33, 173 (1951). 13. Howton, D. R., Science, 121, 704 (1955). 14. Abu-Nasr, A. M., and Holman, R. T., J. Am. Oil Chem. Sot., 31, 41 (1954). 15. Hammond, E. G., and Lundberg, W. O., J. Am. Oil Chem. Sot., 30, 433 (1953). 16. Klenk, E., and Dreike, A., 2. physiol. Chem., 300, 113 (1955). 17. Klenk, E., and Lindlar, F., 2. physiol. Chem., 301, 156 (1955). 18. Crombie, W. M. L., Comber, R., and Boatman, S. G., Biochem. J., 69,309 (1955). 19. Klenk, E., and Bongard, W., 2. physiol. Chem., 290, 181 (1952). 20. Anker, H. S., J. BioZ. Chem., 194, 177 (1952). 21. Entenman, C., Lerner, S. R., Chaikoff, I. L., and Dauben, W. G., Proc. Sot. Exp. BioZ. and Med., 70, 364 (1949).
10 METABOLISM OF ESSENTIAL FATTY ACIDS: V. METABOLIC PATHWAY OF LINOLENIC ACID Gunther Steinberg, William H. Slaton, Jr., David R. Howton and James F. Mead J. Biol. Chem. 1957, 224: Access the most updated version of this article at Alerts: When this article is cited When a correction for this article is posted Click here to choose from all of JBC's alerts This article cites 0 references, 0 of which can be accessed free at tml#ref-list-1
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