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Arginase Activity in Solid Mouse Tumor Transplants and a Comparison with Ascites Tumors and Normal Tissues*

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Arginase Activity in Solid Mouse Tumor Transplants and a Comparison with Ascites Tumors and Normal Tissues* The Histological Distribution of Arginase Activity in Solid Mouse Tumor Transplants and a Comparison with Ascites Tumors and Normal Tissues* HARRY MALMOREN AND BENGT SYLVI~.N (The Cancer l~search Division of Radiumheramet, Karolinska Instituter, Radiurahemmet, Stockholm 60, Sweden) The first arginase assays on tumor tissues led tein synthesis has been discussed by Kochakian to the suggestion that such material in general et al. (10, 11), by Smith and Richterich (16) contains a greater arginase activity than do nor- and, with reference to the gluconeogenesis of the mal tissues (e.g., 8). The postulated increase in mammary gland, by Folley (4). arginine metabolism--together with the increased However, all arginase data on tumors so far glycolytic reaction--was even believed to repre- represent average figures on extracts from very sent basic characteristics of malignant growths large populations of tumor cells including cells in general (1~). These and other controversial with greatly different growth capacities and cyto- results (19) regarding the arginase activity of chemical characteristics. When it is considered tumors have been reviewed (17). By means of (el. ~) that solid tumors axe mainly built up of improved technics and comparable normal control a nongrowing cell type (B) and necrotic tissue, tissues, Greenstein, Jenrette, Mider, and White while the rapidly growing and multiplying typical (8, 9), in their macrochemical assays on liver and tumor cells (A type) represent only a small part manarnary tumors and also on lymphomas, found of the whole tumor mass, it will be understood that that the arginase levels in tumors were variable; more refined methods for the sampling and study in transplanted hepatomas as well as in embryonic of the particular cellular characteristics are needed. liver the values were markedly lower than in If the scale of sampling and assay were diminished normal adult livers, whereas the levels of spon- from a fresh weight of about 1,000 rag. (about taneous mammary tumors in mice were consider- gS0 mg. of protein content) to approximately ably higher and, in the case of lymphomas, slightly 0.01 rag. of total protein content per sample, higher than those in the comparable normal con- the enzymic data obtained could possibly be cor- trol tissue. Other tumors, e.g., a mouse melanoma, related with the cytological types and numbers a mouse Sarcoma 180, and the Jensen rat sarcoma of tumor cells per sample. This has recently been yielded high arginase levels similar to those of attempted in the study of the regional distribution the hepatomas and lymphomas. These results of the total dipeptidase and catheptic activity serve as a basis for the present concept of the in unicentric solid mouse tumor transplants (18). arginase activity of tumor tissue (6, 7). Subse- In this paper similar data will be reported on quently, few new results on the arginase activity the quantitative histological distribution of ar- of different tumor types have been reported. The ginase activity in a few representative tumor high activity levels in spontaneous C3H mouse types. Correlations with the regional cell types mammary adenocarcinomas and mammary glands and cell numbers per sample will be attempted. during lactation as compared with those in preg- nancy were recently studied on a fresh-weight A limited amount of data from some normal mouse basis (16). The arginase activity figures were cor- and rat tissues has been added for comparison. related with the tissue concentrations of RNA, The reason why an amidase like arginase was cho- DNA, and total nitrogen content. The possible sen for study was that this enzyme could be relationship between arginase activity and pro- assumed to play some essential role during cellular * This investigation was supported by grants from the growth and protein metabolism and, further, that Jubilee Fund of King Gustaf V, the Swedish Cancer Society, a suitable micromethod for assay was available. and the Jane Coffin Childs Memorial Fund for Medical Re- In addition, the previous conflicting findings and search, all of which is gratefully acknowledged. ideas as outlined above suggest that differences Received for publication December 28, 1958. in arginase activity occur between different tumor 5~5 Downloaded from cancerres.aacrjournals.org on September 24, 2021. © 1959 American Association for Cancer Research. 5~6 Cancer Research Vol. 19, June, 1959 cell generations; this would explain the variations All transplants were actively growing without in the previous macroscale figures. histological or clinical signs of regression (cf.18). The present micromethod, as well as the com- For comparison, a series of ascites tumors has mon macrochemical procedures, provides chemical been studied, comprising the hyperdiploid Ehrlich- data referring to the in situ characteristics, viz., Landschtitz and tetraploid Ehrlich strains. no distinctions are made between contributions Normal control material.--H om o gen a tes of larg- derived from the tumor cells per se and the er samples and serial sections of punched-out inherent stromal and interstitial fluid compart- cylinders were studied from normal mouse muscle, ments. This point will be further discussed below. subcutaneous connective tissue, and liver of the Furthermore, the term arginase activity refers same strains. Data on whole blood, plasma, eryth- to the total activity obtained with the present rocytes, and leukocytes, separated according extraction method. The actual total amounts of to the technic of Bucldey et al. (1) were also added. enzyme cannot, as usual, be evaluated. These latter materials are of importance for the evaluation of the enzymic activities residing in MATERIALS AND METHODS the stromal compartments of tumors. The diffi- General procedure.--The main steps in the sam- culty of getting a pure fibroblast material has pling of fresh tumor material and normal mouse further prompted some assays on the Earle strain tissues intended for serial sectioning were as fol- L fibroblasts grown in in vitro suspensions. lows: Unicentric intramuscular tumor transplants Extraction method.--Serial sections intended for enzymic were used. From a block of fresh tumor tissue, assay were lysed and extracted for 1 hour at room temperature excised from the living animal under narcosis in 5 or 7 gl. of 0.05 per cent aqueous sodium deoxyeholate solu- tion containing 25 per cent glycerol (18). The extent of tumor and rapidly frozen in isopentane chilled by liquid cell cytolysis was estimated microscopically at about 80 per air, small cylinders were punched out and then cent. All cell debris was left with the extracts in the small ex- stored in isopentane chilled by solid carbon dioxide. traction vessels during the subsequent incubation with the Precautions were taken so that the punched out substrate. Fresh normal tissues and isolated blood cells were tumor cylinder included a good deal of the sur- homogenized for about 20 minutes with continuous cooling in small motor-driven homogenizers in a similar solution of rounding normal connective tissue and muscle, sodium deoxycholate, and the homogenates were then ex- the peripheral growing tumor zone, and some tracted for another hour without further stirring. of the more or less necrotic tumor center. The The relative efficiency of various hypotonic extraction length of such punched-out cylinders was in gen- media was previously tested (18). With reference to arginase it was found that about 50 per cent more activity per total pro- eral about 6 mm., and the diameter of the punch tein content was extracted from serial sections of mouse liver was 8 mm. The cylinder was then frozen on to lysed in deoxycholate solution than was obtained following the the microtome head with a drop of water and usual homogenization of larger liver samples in deoxycholate subjected to serial sectioning in a cryostat at solution (Table 3). The use of a lytic agent in the extraction about - 15 ~ C. The serial sections were each about fluid seems of advantage only when mechanical homogeniza- tion of tissue sections cannot be accomplished. 10-1~/~ thick, 3 mm. in diameter, and contained Arginase assay.--The arginase assay, according to a micro- on an average a total amount of protein of about adaption of Greenberg's method (5), is based upon the de- 8-1~ gg. The average volume of these samples termination of urea liberated during the enzymic reaction was about 0.08 ~1. catalyzed by Mn ++ ions. The urea is precipitated with xan- thydrol, and the dixanthyl urea (DXU) is determined colori- Successive serial sections were then used al- metrically at 430 m/~. ternately for histology and cell counting, deter- A volume of 5 gl. of the enzyme (tissue extract) was first mination of the amount of protein mass, and preineubated for about 3 hours at 40~ C. with 5 gl. of 0.05 M peptidase and arginase assays. Sections for his- MnSO, containing 0.05 Mmaleate at ptI 7. Then 5 gl. of 0.85 M tology were dried, while still frozen, on glass arginine solution at pH 9.5 was added. The final pit was 9.4. After 10 minutes' incubation at 40~ C. the reaction was stopped slides in air or in a desiccator. Sections used for by addition of 20 gl. of 87 per cent acetic acid. The urea was chemical analyses were transferred, while still fro- precipitated by addition of 3 gl. of a 5 per cent xanthydrol zen, to precooled small glass tubes and thawed solution, and the mixture was left in the refrigerator overnight. when the extraction medium was added. DXU was washed once with a saturated DXU solution in These procedures have recently been described methanol, and twice with a saturated DXU solution in methanol-water (3:1). After being dried in vacuo the DXU was in detail, and the technical errors have been dissolved in 200 gl. 50 per cent sulfuric acid.
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