[GANN, 59, ; October, 1968] CHANGES IN ALDOLASE ISOZYME PATTERNS OF HUMAN CANCEROUS TISSUES
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1 [GANN, 59, ; October, 1968] UDC CHANGES IN ALDOLASE ISOZYME PATTERNS OF HUMAN CANCEROUS TISSUES Kiyoshi TSUNEMATSU, Shin-ichi YOKOTA, and Tadao SHIRAISHI (Third Department of Internal Medicine, Hokkaido University Medical School*) Synopsis The presence of two types of aldolase isozyme, aldolase-a (muscle type) and aldolase-b (liver type), was demonstrated in various human tissues as in other mammals. The skeletal muscle contained primarily aldolase-a, while the liver contained primarily aldolase-b. The other tissues, including red cells, possessed mixtures of aldolase-a and -B in proportions characteristic to each tissue. Cancerous tissue of liver was found to produce aldolase-a, which was not usually found in the liver, as well as aldolase-b. Gastric cancer contained higher concentration of aldolase-a than normal gastric mucosa. This was also the case in the cancer of liver and colon, irrespective of absolute activity of FDP-aldolase in the tissues. INTRODUCTION It is well known that at least two distinct types of aldolase isozyme, aldolase-a and aldolase-b, are present in mammalian aldolase.1-7) These patterns of isozyme could be characterized by their abilities to split fructose 1,6-diphosphate (FDP) and fructose 1-phosphate (FMP), The ratio of enzymatic activity for FDP to that for FMP (FDP/ FMP) of these isozymes is about 60 in aldolase-a and about 1 in aldolase-b in the same concentration of the substrate.1,6) Other observations indicate that aldolase-a and -B have different amino acid compositions and immunochemical properties.1,5,10) It was reported that in rabbits and rats the skeletal muscle contained primarily aldolase- A and the liver contained aldolase-b, while other tissues such as kidney possessed a mixture of these two aldolases.1) Furthermore, Penhoet et al.3) recently isolated a new aldolase isozyme, isozyme-c, from rabbit brain. Schapira et al.9) and Sugimura et al.13) showed that FDP/FMP in rat hepatoma and ascites hepatoma was elevated to more than one, getting near the value of skeletal muscle. These findings appear to give a clue to know the relation between carcinogenesis and gene function, and in addition could be applied to clinical diagnosis of cancer, for the changes in enzyme patterns of cancerous tissues should be reflected on serum enzyme activities. The present study was designed to compare the isozyme patterns of various cancerous tissues with those of normal tissues in human. MATERIALS AND METHODS Extraction of Enzymes The tissue specimens were cut into pieces and disrupted immediately after removal by means of Potter-Elvehjem type homogenizer with distilled water. The homogenizer was kept cool in an ice bath during homogenization.
2 K. TSUNEMATSU, ET AL. Thereafter, freezing and thawing were repeated twice and then homogenized speci- The supernatant extract was used for the estimation of aldolase activity. All the tissues other than stomach were obtained from the patients who died of cerebral apoplexia or myocardial infarction within 6hrs. after death. Gastric tissue were obtained at surgical operation of gastric cancer and ulcer. Normal gastric tissues were separated into two parts, mucosa and muscle layer, and assayed separately for enzyme activity. Red cells were taken from the vein, washed several times with physiological saline, hemolyzed with distilled water, centrifuged, and the supernatant was used for the assay of red cell enzyme. Analytical Methods Aldolase was assayed by the method of Sibley and Lehninger,12) as modified by Schapira.8) One unit of the enzyme is equivalent to the cleavage of one packed erythrocytes. FDP. and FMP were obtained from the Sigma Chemical Corporation (St Louis, Mo.) as a barium salt and converted into sodium salt before use. RESULTS Table I. Aldolase Activities and FDP/FMP of Various Human Tissues and Erythrocytes * Each value is the mean of five samples. Table I shows FDP- and FMP-aldolase activities and FDP/FMP of seven kinds of normal tissues and red cells. FDP-aldolase activity was highest in the brain, followed by heart, liver, kidney, spleen, lung, and skeletal muscle. In case of FMP-aldolase activity, the liver showed the highest and the kidney followed it, but other tissues revealed extremely low values. FDP/FMP was maximal (54.0) in the skeletal muscle and minimal (1.0) in the liver. In other tissues, including red cells, FDP/FMP lies between these two values. Results from 10 normal gastric tissues are given in Table II. FDP- and FMP-aldolase activities were higher in mucosa than in muscle layer, whereas FDP/FMP was higher In case of ten cancerous gastric tissues (Table III), FDP-aldolase activity was higher than in normal gastric mucosa, while FMP-aldolase activity was lower. Consequently
3 CHANGES IN ALDOLASE ISOZYME PATTERNS Table II. Aldolase Activities and FDP/FMP of Mucosa and Muscle Layer of the Stomach Table III. Aldolase Activities and FDP/FMP of Stomach Cancer Tissues Table IV. Aldolase Activities and FDP/FMP of Various Cancerous Tissues value of muscle layer. Table IV summarizes the results obtained from two cases of hepatic cancer, two cases of lung cancer, and one case of colon cancer. Although the number of cases is small, some characteristic features can be seen. In hepatic cancer, both FDP- and FMP-
4 K. TSUNEMATSU, ET AL. aldolase activities, especially FMP-aldolase activity, were lower than those of normal liver. Lung cancer exhibited higher value in FDP-aldolase but lower in FMP-aldolase than those in normal lung. On the contrary, FDP/FMP was uniformly and extremely high in cancers of liver, lung, and colon, compared with the ratio of each corresponding normal tissue. DISCUSSION The present study demonstrated that human skeletal muscle had a maximal FDP/ FMP, 54.0, and liver had a minimal, 1.0, among the organs examined. These results are in fair agreement with those obtained in rabbits by Blostein et al.,1) suggesting that in humans aldolase-a is contained primarily in the skeletal muscle and aldolase-b primarily in the liver. However, Penhoet et al.3) recently reported that rabbit skeletal muscle contained only aldolase-a, while liver contained small amount of aldolase-a and hybrid form of aldolase-a and aldolase-b as well as aldolase-b, separating aldolase isozyme by electrophoresis with cellulose acetate. Tissues other than skeletal muscle and liver appear to contain mixtures of aldolase-a and aldolase-b in proportions characteristic to each tissue, since FDP/FMP values are between those of skeletal mucle and liver. This has been confirmed with phosphocellulose column chromatography of rabbit renal enzyme.1) It is, therefore, of great interest to study the changes in aldolase isozyme patterns characteristic to each tissue in the process of carcinogenesis. The present study clearly demonstrated that FDP/FMP ratios measured in two malignant tissues of liver (3.6 and 11.3) were greater than in normal hepatic tissue, probably reflecting the production of aldolase-a, which was not found in the normal liver. This was also the case in lung cancer; FDP/FMP in cancerous tissue showed an extremely high value as compared with that in normal tissue. FDP/FMP varied between 28.0 mucosa from which cancer originated and lying rather near those of gastric muscle layer. Other workers have also reported similar shifts as ours in aldolase isozyme patterns, that is, towards the muscle type, in hepatoma and ascites hepatoma of rats.9,13) As to the absolute activity of FDP-aldolase in normal and malignant tissues, results do not agree completely according to the researchers and to the kinds of cancer.2,11,13) However, it could be concluded that such similarity in aldolase isozyme patterns to muscle type is commonly observed for cancerous tissue irrespective of its kind. (Received May 11, 1968)
5 CHANGES IN ALDOLASE ISOZYME PATTERNS REFERENCES 1) Blostein, R. E., et al., J. Biol. Chem., 238, 3280 (1963). 2) Dale, R. A., Clin. Chim. Acta, 11, 547 (1965). 3) Penhoet, E., et al., Proc. Natl. Acad. Sci. U.S., 56, 1275 (1966). 4) Rutter, W. J., et al., J. Biol. Chem., 236, 3193 (1961). 5) Idem, Acta Chem. Scand., 17, (Suppl.) 226 (1963). 6) Idem, Advan. Enzyme Regulation, 1, 39 (1963). 7) Rutter, W. J., Federation Proc., 23, 1248 (1964). 8) Schapira, F., Rev. Franc. Etudes Clin. Biol., 5, 500 (1960). 9) Schapira, F., et al., Nature, 200, 995 (1963). 10) Shimizu, H., et al., Biochem. Biophys. Acta, 133, 195 (1967). 11) Shonk, C. E., et al., Cancer Res., 25, 206 (1965). 12) Sibley, J. A., et al., J. Biol. Chem., 177, 859 (1949). 13) Sugimura, T., et al., GANN Monograph, 1, 143 (1966). 59(5)
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