SYNTHESIS OF N-SUBSTITUTED GLUCOSAMINES AND THEIR EFFECT ON HEXOKINASE*
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1 SYNTHESIS OF N-SUBSTITUTED GLUCOSAMINES AND THEIR EFFECT ON HEXOKINASE* BY FRANK MALEY AND HENRY A. LARDY (From the Department of Biochemistry and the Institute for Enzyme Research, University of Wisconsin, Madison, Wisconsin) (Received for publication, October 25, 1954) The enzyme hexokinase prepares carbohydrates for degradation by both the glycolytic and the direct oxidat,ive pat.hways. For this reason, hormonal control of this enzyme in animals (1, 2) exerts a profound influence on their carbohydrate metabolism. Because synthetic inhibitors of hexokinase have proved useful in kinetic st.udies (3), in identifying different hexokinases (4), and in elucidating the mechanism by which glyceraldehyde inhibits glycolysis (5), we have undertaken the synt,hesis of a new series of inhibitors of hexokinase in the hope that kinetic studies with these compounds might aid in elucidating the mode of action of the naturally occurring inhibitory or regulatory agents (6, 7). Harpur and Quastel (8) found that glucosamine is phosphorylat,ed by brain hexokinase and suggested that it might possess antit.umor act,ivit,y because of its ability to deplete the adenosine triphosphate (ATP) supply (9). Since glucosamine competitively inhibits glucose phosphorylation (S), it seemed that the antitumor activity preliminarily reported (9) might have resulted from a decreased supply of utilizable carbohydrate rather than from a decreased supply of ATP. Better inhibit,ors of hexokinase were therefore sought and have been found in the form of N-substituted derivatives of glucosamine. As shown by Harpur and Quastel (8), N- acetylglucosamine is a competitive inhibitor of brain hexokinase, but, unlike free glucosamine, this derivative is not phosphorylated. Most of the compounds prepared here have been shown t,o behave in a manner analogous to N-acet,ylglucosamine, except for N-anisylideneglucosamine, which was found to be a non-competitive inhibitor of brain hexokinase. Of the compounds tested, none inhibited sarcoma 180 in mice. Synthesis of Glucosamine Derivatives Two alternative routes are available for the synthesis of N-acyl derivatives of glucosamine. The most direct method is the reaction of an acyl * This investigation was supported in part by a research grant (A-531) from the National Institute of Arthritis and Metabolic Diseases of t.he National Institutes of Health, Public Health Service, by a grant-in-aid from the American Cancer Society upon recommendation of the Committee on Growth of the National Research Council, and by a grant from the University Research Committee. 765
2 766 iv-substituted GLUCOSAMINE~ chloride with free glucosamine in an alkaline medium (10). This method proved successful for the synthesis of most of the compounds described in this paper, but it was found essential to purify the commercial glucosamine by the procedures of Breuer (11) and Westphal and Holzmann (12). A second procedure for the synthesis of N-acyl derivatives of glucosamine is that of Bergmann and Zervas (13), who synthesized benzoylglucosamine from the tetra-o-acetyl derivative of glucosamine. Their method locates the aroyl group specifically, but suffers the disadvantage of a small yield (30 per cent) in the removal of the 0-acetyl groups with NaOH. Other deacetylation methods which might improve the yield were therefore sought. The catalytic barium methoxide method was found to give yields of 40 to 55 per cent. When this method was used, the anhydrous methanolic solution of the compound and barium methoxide was kept in the refrigerator for 24 hours, although deacetylation apparently proceeded as rapidly as the acetylated derivative was brought into solution. If desired, the barium may be removed with the aid of the cation exchange resin, IR-100-H (Rohm and Haas). This is usually not necessary, since the small quantity of barium present is removed in the process of purification by recrystallization. Deacetylation with ammoniated methanol (prepared by passing anhydrous ammonia into anhydrous methanol) was found to be even more satisfactory. By this procedure the yields of deacetylated product averaged between 50 and 60 per cent. The preferred method for obtaining the aminobenzoylglucosamine derivatives was that of hydrogenating the deacetylated nitro derivatives in hot ethanol with PtOz as the catalyst. Larger quantities of the acetylated nitro compounds could bc handled at one time because of their greater solubility in ethanol, but it was found that, upon deacetylation of the resultant aminobenzoyl compounds, highly colored products were obtained. Only typical preparations by each of the two procedures and a typical reduction of a nitrobenzoyl derivative to the corresponding amino derivative will be described in detail. The other compounds were prepared in the same manner with only minor modifications in the solvent composition for recrystallizing. The analytical data, melting points, and rotations for the new compounds reported here are described in Table I. Absolute ethanol and methanol were prepared by the procedure of Lund and Bjerrum (14). The acid chlorides used were Eastman, white label grade, and melted with 1-2 of the literature values. Tetra-hcetyl-N-(p-nitrobenzoyl)-D-ghcosamine-A solution of 14.5 gm. of tetra-o-acetyl-n-glucosamine in 100 ml. of dry pyridine (distilled from BaO) was chilled to 0 and 8.1 gm. of p-nitrobenzoyl chloride were added. The solution was kept at 0 for 2 hours before pouring into 1 liter of rapidly
3 * Bromine, theory per cent; found, t Decomposition. $ The water of crystallization could be removed by drying at W in vacua, but some decomposition of the anhydrous compounds resulted, as was evidenced by discoloration; figures in parentheses. $ This compound begins to darken at 220 and gradually decomposes as the temperature increases. 11 Becomes dark at 178 and gradually decomposes as the temperature increases. [al, N-(m-Bromobenzoyl)glucosamine N-(Phenylacetyl)glucosamine N-(Phenylpropionyl)glucosamine N-(p-Nitrobenzoyl)tetraacetylglucosamine N-(p-Nitrobenzoyl)glucosamine N-(m-Nitrobenzoyl)tetraacetylglucosamine 2 N-(m-Nitrobenzoyl)glucosamine N-(3,5-Dinitrobenzoyl)tetraacetylglucosamine N-(3,5-Dinitrobenzoyl)glucosamine N-(p-Aminobenzoyl)tetraacetylglucosamine N-(p-Aminobenzoyl)glucosamine N-(m-Aminobenzoyl)tetraacetylglucosamine N-(m-Aminobenzoyl)glucosamine N-(3,5-Diaminobenzoyl)tetraacetylglucosamine Compound Mol. wt (337.2): (391.3): TABLE I N-Substituted Glucosamine Derivatives Per, cent c Per cent H Per cent N I I! 1 - M.p. Found ~~ -I-l-l-l- from by guest on December 7, ) 46.4 (5.04) 5.16 (8.31: : ) 40.3 (4.37) 4.57 (10.7) C. degrees ~222t t 41.1 f 1.0, C 1.06, Hz %218t f 0.4, C 5.68, CHCl, t 53.7 f 1.3, C 1.03, Hz f 1.0, C 2.68, CHClt t 48.3 f 1.3, C 0.476, Hz OOt 45.5 f 1.3, C 1.10, Hz !207t 9.22 $ t f 1.2, C 1.20, Hz ~184t
4 768 N-SUBSTITUTED a~ucosm~ms stirred ice water. The product solidified; it was collected by filtration, washed with water and cold ethanol, and dried; yield, 17 gm. The analytically pure compound was obtained as long, white, thread-like crystals by repeated crystallization from absolute ethanol. N-(p-NitrobenzoyZ)-n-glucosamine-(a) The tetra-o-acetyl-n-(p-nitrobenzoyl)glucosamine (2 gm.) was dissolved in ammoniated absolute methanol (50 ml.) and allowed to stand at room temperature overnight. The resultant red solution was concentrated iti vucuo until crystals began to appear, and was then placed in the refrigerator for several hours before filtering; yield, 0.8 gm. Recrystallization was accomplished from 95 per cent ethanol. (b) Deacetylation by the catalytic barium methoxide procedure was accomplished by dissolving 5.4 gm. of tetra-o-acetyl-n-(pnitrobenzoyl)glucosamine in 50 ml. of absolute methanol. 1 ml. of 2.5 N barium methoxide was then added and the solution kept in the refrigerator for 24 hours. The product was isolated from the yellow solution as described in (a) above; yield, 1.9 gm. Direct Synthesis of N-(p-Nitrobenzoyl)-D-glucosamine-A solution of 5 gm. of glucosamine in 25 ml. of water was immersed in an ice bath and stirred vigorously while 5.4 gm. of p-nitrobenzoyl chloride were added in small portions. During the reaction, a total of 25 ml. of 1 N h aoh was slowly added so as to keep the ph of the solution between 8 and 9. The temperature of the reaction mixture was kept below 5 at all times, and stirring was continued for 2 hours after the final addition. The mixture was then neutralized with HCl and, while st,ill cold, the product was collected by filtration. It was purified by two recrystallizations from 95 per cent ethanol; yield, 3.0 gm. N-(p-Aminobenzoyl)-D-glucosamine-A solution of 0.53 gm. of N-(p-nitrobenzoyl)glucosamine in about 50 ml. of hot 80 per cent ethanol was shaken with 0.05 gm. of PtOt in an atmosphere of Hz. The initial rate of hydrogen consumption was very rapid. When the theoretical amount of Hz for reduction of the nitro group had been consumed (5 to 15 minutes were required), the catalyst was filtered off. Crystals began to appear as the solution cooled. After the mixture had been kept at -5 to complete crystallizat,ion, the product was collected by filtration and dried in vacua. A small additional quantity (12 mg.) was recovered by concentrating the filtrate in vacua and crystallizing again at -5O. Yield, gm.; the compound darkened when heated to 220, but did not melt below 300. Inhibition of Hexokinase by Glucosamine Derivatives The synthetic derivatives of glucosamine were tested as inhibitors of both brain and yeast hexokinase. An aqueous extract of beef brain ace- 1 In some of the preparations (e.g., the phenylacetyl and phenylpropionyl derivatives) better yields were obtained when 1 N Na&03 was used to maintain the ph.
5 F. MALEY AND H. A. LARDY 769 tone powder (6) was dialyzed and lyophilized as described elsewhere (15). When this lyophilized preparation was dissolved in redistilled water and centrifuged at 100,000 X g for 30 minutes, from 85 to 90 per cent of the hexokinase activity remained in the clear supernatant solution. This is in marked contrast to extracts of fresh brain in which most of the enzyme is associated with particles which sediment at much lower centrifugal force (3). The manometric assay for hexokinase (16) was employed with conditions as described previously (15). Following a 10 minute equilibration period, ATP was tipped into the reaction mixture from a side arm. Manometer l/s x 1o-2 Fro. 1. Competitive inhibition of glucose phosphorylation by N- (3,5-dinitrobenzoyl)-n-glucosamine. 0, 0; X, 1.3 X KY4 M, and 0, 5 X lo- N N-(3,5-dinitrobenzoyl)glucosamine. The velocity is expressed in terms of microliters of CO2 per 30 minutes. readings were made 5 minutes later and at 10 minute intervals thereafter. With glucose as the substrate, t,he velocities were calculated from the linear portion of the rate curve. For fructose, which has a much higher K, (15, 17), the init,ial velocity was estimat,ed by extrapolating the observed values to zero time (15). Each inhibit,or was tested at two concentrations in the presence of varying concentrations (from M t,o 0.01 M) of glucose and fructose. A flask containing all components except glucose or fructose was included in each experiment. None of the glucosamine derivatives test.ed was phosphorylat.ed at a det,ectable rate. The data were plotted according to Lineweaver and Burk, and the dissociation constants of the enzyme inhibitor complexes were calculated (13). Fig. 1 depicts the inhibit.ion, by dinitrobenzoylglucosamine, of glucose phosphorylation. Since it, is difficult to
6 770 N-S~~STITUT~D ~LUCOSAMINES measure K, for glucose manometrically (15), an arbitrary value of 1 X W4 M (8, 15) waa used to calculate K; for the various competitive inhibitors with glucose as t,he substrate. The results are summarized in Table II. TABLE II Ki Values for Competitive Inhibition of Beef Brain Hexokinase by Glucosamine Derivatives Inhibitor Glucose Substrate Fructose N-(p-Nitrobenzoyl)glucosamine. N-(m-Nitrobenzoyl)glucosamine.. N-(3,5-Dinitrobenzoyl)glueosamine N-(p-Aminobenzoyl)glucosamine. N-(m-Aminobenzoyl)glucosamine.. N-Benzoylglucosamine.. N-Acetylglucosamine.. N-Phenylacetylglucosamine. 5 Y 4 x 10-S 3.3 x 10-s 1.1 x lo-6 2 x x 10-4 Y 5 x x 10-s 4 x 10-e 1.1 x 10-d 8.1 X 10-h 3.6 x 10-S 4.6 x lo- 8.6 X 10-4 FM. 2. Non-competitive inhibition of fructose phosphorylation by N-anisylideneglucosamine. 0, no inhibitor; 0, 1.7 X 10-* M N-anisylideneglucosamine. The velocity is expressed in terms of microliters of COZ per 10 minutes. The Ki values are only appr0ximat.e because of complications in the assay. The brain hexokinase preparation contains phosphohexokinase and the CO2 evolved results from phosphorylation by both enzymes. In the preparat,ions of brain hexokinase tested, phosphohexokinase activity was equal to or greater than hexokinase, although this result may be more apparent than real (3, 19). Nonetheless, hexokinase was assumed to be the rate-
7 F. MALEY AND H. A. LARDY 771 limiting enzyme in the assay. For these various reasons, no significance can be attached to the differences in Ki values for any given inhibitor with glucose and fructose, respectively, as substrates. N-Anisylideneglucosamineamine2 was found to inhibit fructose phosphorylation by brain hexokinase in a non-competitive manner with a Ki of about M (Fig. 2). The phosphorylation of glucose by yeast hexokinase was also inhibited by the glucosamine derivatives tested (Table III). Liver fructokinase was not significantly inhibited by M N-(p-nitrobenzoyl)glucosamine. TABLE III Inhibition of Yeast Hexokinase by Glucosamine Derivatives Compound tested N-(p-Nitrobenzoyl)glucosamine... N-(m-Nitrobeneoyl)glucosamine... N-(3,5-DinitrobensoyI)glucosamine.... N-(m-Aminobenzoyl)glucosamine... N-(p-Aminobenzoyl)glucosamine,... N-Benzoylglucosamine... N-Phenylacetylglucosamine... N-Acetylglucosamine.... The substrate was M glucose. -.- Concentration Y 5 x 10-a 2 x lo- 2.5 X 10-a 5 x 10-s 4 x 10-a 5 x 10-a 5 x 10-a 5 x 10-a - 1?a cent inhibition ~- E$ect of Glucosamine Derivatives on Tumor-Bearing Mice8 Several of the compounds synthesized were tested as possible inhibit,ors of tumor growth in mice. The techniques employed were similar to those of Quastel and Canter0 (9), except that white mice bearing Cracker sarcoma 180 were used. The compounds tested and the daily dose per mouse were as follows: glucosamine hydrochloride, 5 mg.; N-(p-aminoben.zoyl)- glucosamine, 7 mg.; N-benzoylglucosamine, 6.6 mg.; N-(metu-nitrobenzoyl)glucosamine, 7.5 mg.; N-acetylglucosamine, 5 mg. In another experiment N-(dinitrobenzoyl)glucosamine was injected at 650 mg. per kilo of body weight each day for 5 days only. In no case was the growth of the tumors or the percentage of tumor regressions in the treated animals significantly different from that of saline-injected control mice. * Dr. Robert Crane, Washington University, has tested this compound with the particulate brain hexokinase and obtained a Ki value of about 0.01 M with fructose as the substrate. He found dinitrobenzoylglucosamine to inhibit competitively with a Ki of 1 x 10-S M. 3 We are indebted to Dr. K. K. Chen, Dr. P. N. Harris, and Dr. J. Probst of the Lilly Research Laboratories for these assays
8 772 N-SUBSTITUTED GLUCOSAMINRS DISCUSSION The competitive nature of the inhibition of phosphorylation indicates that the substituted glucosamine compounds combine with the active enzyme site, yet none of these compounds appeared to be phosphorylated, whereas free glucosamine is. Molecular models indicate that the substituted group does not overlap the 6 position of the sugar, and, therefore, other reasons must be sought to explain their failure to become phosphorylated. One possibility is that the substituent attached to the 2- amino position interferes with the ability of hexokinase to bind ATP. It appears that the intrinsic nature of the enzyme is such that the metusubstituted nitrobenzoyl derivatives of glucosamine are more effectively bound than the para-nitrobenzoyl or benzoyl derivatives, with two nitro groups being 2 to 3 times as potent as one. The N-acyl derivatives of glucosamine are probably hydrolyzed by the various cathepsins in animal tissues, and this may be one reason for their failure to inhibit tumor growth. Other derivatives of glucosamine which are less likely to be hydrolyzed by tissue enzymes are therefore being synthesized, and their biological properties will be tested. SUMMARY The synthesis of the following N-acyl derivatives of D-glucosamine is described: m-bromobenzoyl-, phenylacetyl-, phenylpropionyl-, p-nitrobenzoyl-, m-nitrobenzoyl-, 3,5-dinitrobenzoyl-, p-aminobenzoyl-, and m- aminobenzoyl-d-glucosamine. These glucosamine derivatives are powerful competitive inhibitors of beef brain hexokinase (K; = 1W to 1W6 M) but are not phosphorylated. N-Anisylideneglucosamine was found to inhibit brain hexokinase in a noncompetitive manner with respect to fructose. BIBLIOGRAPHY 1. Cori, C. F., Harvey Lectures, 41,253 (194546). 2. Stadie, W. C., Physiol. Rev., 34, 52 (1954). 3. Sols, A., and Crane, R. K., Federation Proc., 12, 271 (1953). Crane, R. K., and Sols, A., J. Biol. Chem., ao3, 273 (1953). 4. Bueding, E., and MacKinnon, J., Federation Proc., 12, 184 (1953). 5. Lardy, H. A., Wiebelhaus, V. D., and Mann, K. M., J. Biol. Chem., 187, 325 (1950). 6. Colowick, S. P., Cori, G. T., and Slein, M. W., J. Biol. Chem., 168, 533 (1947). 7. Bornstein, J., J. Riol. Chem., 206, 513 (1953). 8. Harpur, R. P., and Quastel, J. H., Nature, 184, 693 (1949). 9. Quastel, J. H., and Cantero, A., Nature, 171, 262 (1953). 10. T,ipton, S., Thesis, University of Wisconsin (1949). 11. Breuer, R., Ber. them. Ges., 31, 2193 (1898).
9 F. MALEY AND H. A. LARDY Westphal, O., and Holzmann, H., Ber. them. Gee., 76 B, 1274 (1942). 13. Bergmann, F., and Zervas, L., Ber. them. Ges., 64 B, 975 (1931). 14. Lund, H., and Bjerrum, J., Ber. them. Gee., 64 B, 210 (1931). 15. Wiebelhaus, V. D., and Lardy, H. A., Arch. Biochem., 21, 321 (1949). 16. Colowick, S. P., and Kalckar, H. M., J. Biol. Chem., 148, 117 (1943). 17. Slein, M. W., Cori, G. T., and Cori, C. E., J. Bid. Chem., 188, 763 (1950). 18. Lineweaver, H., and Burk, D., J. Am. Chem. Sot., 66, 658 (1934). 19. Weil-Malherbe, H., and Bone, A. D., Biochem. J., 49, 339 (1951).
10 SYNTHESIS OF N-SUBSTITUTED GLUCOSAMINES AND THEIR EFFECT ON HEXOKINASE Frank Maley and Henry A. Lardy J. Biol. Chem. 1955, 214: 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 ml#ref-list-1
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