Bulletin of the Japanese Society of Scientific Fisheries Vol. 34, No. 7,
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1 Bulletin of the Japanese Society of Scientific Fisheries Vol. 34, No. 7, Studies on the Discoloration of Red Fishes- X Enzyme Involved in the Discoloration of Carotenoid Pigments in Fish Skin Tissues* Nobuo TSUKUDA** and Keishi AMANO** (Received February 23, 1968) It was assumed in the previous paper1) that the discoloration could be caused by the action of a certain tissue enzyme in the skins of the red fishes. The nature and activity of this newly observed factor of color fading are regarded important when one considers practical measures to prevent discoloration. But, in the previous work, the occurrence of enzyme activity was only demonstrated in fresh skin homogenates and that was not sufficient for discussion on the nature or specificity of the enzyme. The present report deals with the enzyme activity of aqueous extract of dried skin preparation from which lipid fraction has been completely removed, in addition to the effect of the freshness of fish on the activity. The results obtained so far may indicate that the enzyme in question should be a kind of lipoxidase occurring in the skin tissues. Experiments and Results Freshness of raw fish and the discoloration activity of its skin tissues on astaxan thin. The effect of freshness of fish on the discoloration activity of skin homogenates was examined by a storage test of gurnard. Gurnards, Chelidonichthys kumu, (Hobo in Japanese), sampled at Choshi Fish Market in Chiba Prefecture, June 20, 1967, were brought in the laboratory packed with ice in an insulated container. These fish showed a good freshness; in fact, they had been held in iced sea water for ten to fifteen hours before landing and two hours' train trip to the laboratory. The discoloration activity on astaxanthin was tested for the composite sample of skin homogenates prepared from each four individuals of fish taken up from the stock held in a refrigerator at 5 to 7 Ž every other day. The method of activity examina tion is outlined as follows: a 5ml of the skin homogenate, 5ml of M/50 phosphate buffer (ph 6.88) and 0.5ml of acetone solution of astaxanthin were consecutively placed in a glass-stoppered tube and three drops of a mixture of toluene and chloro form were added as antiseptics. The whole solution was made homogeneous by shaking and kept at a temperature of 10 }3 Ž under darkness. The activity was estimated by measuring the decrease in astaxanthin concentration using a spectro * Contribution from the Tokai Reg. Fish. Res. Lab., No. B. 488.
2 634 photometer at wavelength of 475mƒÊ after incubation of two and four days at 10 } 3 Ž. And, the homogenates heat-treated at 100 Ž for ten minutes were employed as control runs. A trimethylamine determination was also conducted on the muscle portion of the samples as an objective index of freshness according to Dyer's method.2) The activity of skin homogenates has been well retained until the third day of storage, when the fish remained in good condition of freshness as seen in Table 1. The activity, however, evidently attenuated with the progress of spoilage. Table 1. Freshness of gurnard and discoloration activity of its skin homogenate on carotenoid pigment (astaxanthin). Days of storage Discoloring rate Discoloring rate TMA mg % Organoleptic 5o-7 C after of astaxanthin 2 days % after of astaxanthin 4 days in muscle observation o Sea fresh Weakly fresh g discolored fishy, slightly i discolored Strongly fishy, Putrid Discoloration activity of dehydrated and defatted skin tissues. Materials and preparation of defatted Rockfish, Sebastes thompsoni, (Usumebaru in Japanese), in rigor mortis, were purchased from Tokyo Central Fish Wholesale Market and their skin portions were collected and dried under vacuum at room temperature. Then, the skins were cut into small pieces and half of these cuts were defatted five times with ten-fold quantity of acetone, followed by repeated treatments with ten-fold quantity of petroleum ether. The water content of raw skins of the samples was 65.8% and oil content was 1.38% on the average. And, the two series of dried skin preparations, of which one had been defatted, were stored at low temperature (0 Ž) under vacuum until they were used. Preparation of aqueous extracts of the skins (crude enzyme The vacuum-dried rockfish skins and vacuum-dried and defatted ones were added to ten fold quantity of M/50 phosphate buffer (ph 6.88) respectively and macerated with sea sand in an iced bath and homogenized in a blendor for one minute. After holding overnight, the supernatant on centrifugation was subjected to the examination. One ml of this solution contained 6.4mg of dry matter except the amount of phosphate and 0.65mg of nitrogen. The homogenates were also prepared from the raw skins of the rockfish by the method described in the foregoing paragraph. Tunaxanthin Tunaxanthin portion was collected by the column chromatographic separation of the unsaponifiables prepared from crude carotenoids extracted from the skins of gurnard, rockfish, and grouper, Coryphaena hippurus
3 635 Linnaeus, (Shiira in Japanese). Tunaxanthin thus obtained showed an extinction coefficient of 1,380 at 440mƒÊ in petroleum ether (b.p Ž) and this was equivalent to 61% of pure tunaxanthin, E1 1cm value of which is 2,250.3) The preparatien was stored at -20 Ž and diluted to an E1 1cm value of about 20 with acetone when the activity test was conducted. Procedure of the A 3ml part of the tissue extract was added to 7ml of M/50 phosphate buffer (ph 6.88) and then 0.5ml of tunaxanthin diluted with acetone was mixed and made homogeneous, and the whole suspensions were incubated in darkness at temperatures ranging from 10 to 15 Ž. Tunaxanthin concentration was determined during the course of storage by a spectrophotometric measurement at 440mƒÊ after the pigment was transferred from the suspension to a mixed solvent of ethanol and ether (1 F2). Fig. 1. Decrease in concentration of tunaxan thin by extracts from dehydrated and defatted rockfish skins. 1. Heat-treated raw skin extracts 2. Defatted skin extracts 3. Dehydrated skin extracts 4. Raw skin extracts Fig. 2. Effect of methyl linoleate on decrease of tunaxanthin concentration by extracts from defatted rockfish skins. 1. Control (buffer solution+methyl lino leate) 2. Control (heat-treated raw skin ex tracts) 3. Defatted skin extracts+methyl lino leate Occurrence of the activity in the dried In Fig. 1 is shown the rate or discoloration of tunaxanthin in three different preparations: raw, dried and dried and defatted skin tissues of rockfish. A similarly rapid rate of discoloration was evident in both raw and simply dried tissues, while very retarded rate was observed in either lipidfree samples or raw one which has been heat-treated at 100 Ž for ten minutes.
4 636 These findings may indicate that the removal of lipid from the skins essentially inhibits the activity. The effect of methyl linoleate on the action of lipid-free skin The examination results seen in Fig, 1 may suggest a significant role of lipid in the process of discoloration. Therefore, methyl linoleate, an unsaturated fatty acid susceptible to auto-oxidation, was examined of its effect on a possible enhancement Fig. 4. Decrease in concentration of Ĉ-caro Fig. 3. Effect of methyl palmitate, methyl linoleate, and methyl ester of highly unsaturated fatty acids on decrease of astaxanthin concentration by extracts from defatted rockfish skins. 1. Control (buffer solution+h. U. F. A) 2, Defatted skin extracts+m. P. 3. Extracts only 4. Defatted skin extracts+m. L. 5. Defatted skin extracts+h. U. F. A. (H. U. F. A.: highly unsaturated fatty acids, M. P.: methyl palmitate, M. L.: methyl linoleate). tene, tunaxanthin, and astaxanthin by extracts of defatted rockfish skins with added methyl ester of highly unsaturated fatty acids. 1. Control (buffer solution+tx.) 2. Control (Ĉ-c., heat-treated) 3. Ĉ-c.+m. L. 4. Ĉ-c.+h. U. F. A. 5. Ax.+H. U. F. A. 6. Tx.+H. U. F, A. (Ĉ-c: a-carotene, M. L.: methyl lino leate, H.U.F. A.: highly unsaturated fatty acids, Ax.: astaxanthin, Tx.: tunaxanthin). of the enzyme action. A 0.5ml of 2% methyl linoleate solution in acetone (10mg of methyl linoleate) was added to the mixture containing tunaxanthin and the extract of lipid-free skin tissues in the same proportion as described above, where a heat treated sample of raw skin homogenate, as a control, was also tested in the presence of methyl linoleate and the buffer.
5 637 Fig. 2 reveals that an addition of methyl linoleate makes a remarkable enhance ment of the discoloratian reaction, though methyl linoleate alone shows none of the promoting actions. The effect of different fatty Another rockfish, Sebastescus marmoratus, (Kasago in Japanese), was used in this experiment. A dry matter content of lipid free skin extract, excluding the amount of phosphate, was 5.8mg, nitrogen was 0.56mg per ml, and iron content was 1.12ƒÊg per ml, respectively. Three varieties of fatty acid esters examined were methyl palmitate refined by re-distillation; methyl linoleate (Tokyo Kasei Kogyo Co.); and a mixture of methyl esters of highly unsaturated fatty acids from squid liver oil. The last sample was prepared by the methylation of the squid liver oil and refined by urea-methanol method. A 0.5ml of each 2% methyl ester in acetone was added to a mixture of astaxanthin and M/50 phosphate buffer (ph 6.88) in the proportion mentioned above. In Fig. 3 are indicated the changes in the concentration of astaxanthin during the incubation period. It is quite evident from Fig. 3 that methyl linoleate and particu larly methyl esters of highly unsaturated fatty acids from squid liver oil show a marked effect on the discoloration of astaxanthin. However, methyl palmitate dem onstrates virtually none of the promoting effects on the discoloration. Possibly the degree of unsaturation of the fatty acids may play an important part in the reaction. The susceptibility of three carotenoid pigments to the action of lipid-free skin extract in the presence of methyl esters of highly unsaturated fatty The extract prepared in the same way from Sebastescus marmoratus was employed to test its activity on three different carotenoid pigments in the presence of mixed methyl esters of highly unsaturated fatty acids from squid liver oil. The purity of carotenoid preparations were: ƒà-carotene 98% (Merck); tunaxanthin E1%1cm 1,380 (61%); astaxanthin E1%1cm 750 (63% as di-palmitic acid esters of astaxanthin). Discoloration occurred most rapidly in the run of tunaxanthin followed by astaxanthin which appeared to discolor even faster than ƒà-carotene as seen in Fig. 4. But, more detailed study should be carried out on this subject using the pigments in pure preparation. Discussion It was suggested in the previous paper1) that the discoloration of carotenoid pigments in the skins of some marine red fishes would be caused by a certain enzyme in the tissues. Inactivation of the discoloring action by heat treatment or addition of KCN was the evidences to support the conclusion. In regard to the absence of activity in the dried and defatted skin tissues, the authors presume that the activity observed in the homogenates of raw skins in the previous paper as well as in the extracts of vacuum-dried skins in the present report should owe to the naturally existing lipids in the quantities which enable the enzyme to act. So, it is quite certain that the enzyme needs lipids for causing carotenoids dis
6 638 coloration. And, this finding led the authors to examine the effect of unsaturated fatty acids, In the presence of a very small quantity of unsaturated fatty acid, the dehydrated and lipid-free skin tissues of some red fish exhibited a pronounced dis coloration activity on astaxanthin, tunaxanthin, and Ĉ-carotene. This fact may indicate that the enzyme in these skin tissues could be lipoxidase, which is known of its action on unsaturated fatty acids forming corresponding hydroperoxides which subsequently induce discoloration of carotenoids. Another possible carotenoid discoloration can be non-enzymatic process by the auto-oxidation of unsaturated fatty acids under catalytic action of heme compounds. BOYD and ADAMS4), WATTS5), TAPPEL6-8) YOUNATHAN and WATTS9), and BISHOV10) are rather skeptical about the existence of lipoxidase in animal tissues which contain heme compounds. And, BOYD and ADAMS4) stated that catalytic oxidation of linoleate emulsions by heme compounds was inhibited by KCN. However, there have been some publications suggesting the occurrence of lipoxidase in the animal tissues which contains heme compounds. For example, KHAN11) has reported that it is contained in the dark muscle of herring, and SHIMIZU and FUKUHARA12,13) observed the action in liver of mackerel, while ONO and NAGAYAMA14-16) described existence of lipoxidase in the livers of mackerel, and sea bass, and also in the liver and dark muscle of frigate mackerel In the present examination, iron content in the aqueous extract of defatted skins was below a level of 1 Đg per ml and this amount is regarded far lower than 72 Đg per ml of the extract of mackerel liver tested by ONO and NAGAYAMA.16) And, corresponding heme compound containing this quantity of iron is considered not sufficient to put forth the auto-oxidative reaction of the unsaturated fatty acids. Summary 1. Discoloration action of red fish skin homogenates becomes inactive due to degradation of freshness of these fishes. For example, gurnard, Cheliddonichthys kumu, showed a remarkable decrease in the discoloring action of the skins with the progress of deterioration and no more activity was observed in spoiled tissues. 2. Although the defatted skins of some red fish showed no activity, an addition of a small quantity of methyl ester of unsaturated fatty acid like methyl linoleate restored almost completely of their activity. By this finding, in addition to the fact of heat inactivation, the authors conclude that lipoxidase occurs in the skin tissues of red fishes which may participate discoloration of carotenoid pigments together with physical and chemical discoloration. References 1) N. TSUKUDA and K. AMANO: This Bull., 33, (1967). 2) W. J. DYER: J. Biol. Res. Bd. Canada, 6, (1945).
7 6393) S. HIRAO: Unpublished data. 4) D. H. J. BOYD and G. A. ADAMS: Can. J. Biochem. and Physiol., 33, (1955). 5) B. M. WATTS and Da-H. PENG: J. Biol. Chem., 170, (1947). 6) A. L. TAPPEL: Food Res., 17, (1952). 7) A. L. TAPPEL: ibid., 18, (1953). 8) A. L. TAPPEL: Arch. Biochem., 44, (1953). 9) M. T. YOUNATHAN and B. M. WATTS: Food Res., 24, (1959). 10) S. J. BISHOV, A. S. HENICK and R. B. KOCH: ibid., 25, (1960). 11) M. M. R. KHAN: J. Fish. Res. Bd. Canada., 9, (1952). 12) C. SHIMIZU and T. FUKUHARA: This Bull., 23, (1957). 13) C. SHIMIZU and T. FUKUHARA: ibid., 23, (1957). 14) T. ONE and F. NAGAYAMA: ibid., 23, (1957). 15) T. ONO and F. NAGAYAMA: ibid., 23, (1957). 16) F. NAGAYAMA and T. ONO: ibid., 24, (1959).
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