Antifungal Activity of Ring Poly-Chlorinated Pyrimidines:
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1 Antifungal Activity of Ring Polyhlorinated Pyrimidines: tructure Activity Relationships ABTRAT GERHON, HERMAN (Pfister hemical Works, Inc., Ridgefield, N.J.) AND RAULO PARMEGIANI. Antifungal activity of ring polychlorinated pyrimidines: structure activity relationships. Appl. Microbiol. 11: A total of 48 ring chlorinated pyrimidines was screened against strains of five fungi by the discplate method, in liquid culture, and for activity of the vapors of the compounds. orrelations of the results obtained by the three methods were made, and structure to activity relationships were discussed. The outstanding members of this series were found to be 2,4,5trichloropyrimidine, 4,5,6 trichloropyrimidine, and 2chloromethyl4, 5, 6trichloropyrimidine, in this screening system. In the course of screening pyrimidine analogues for antimicrobial activity, it was found, most consistently, that the ring chlorinated derivatives showed good antifungal properties. A search of the literature revealed no reports of such activity to date, although some members of this series were known for more than 70 years. A total of 48 ring chlorinated pyrimidines were prepared and studied. tructurally, they are as follows: N R1 R4 N R3 R2 The substituents on the ring were combinations of the following: R, = H, H3, 2H5, n3h7, i3h7, n17h35, lh2, 6H5, or l; R2 = R4 = H, H3, 2H5, n3h7, i3h7, n17h36, BrH2, OOH3, 6HW, or l; R3 = H, H3, 2H5, n3h7, i3h7, BrH2, 6H5, or l. Table 1 contains a list of the compounds studied. MATERIAL AND METHOD The organisms employed in our screening system included five bacteria (Escherichia coli, Pseudomonas aeruginosa, Leuconostoc mesenteroides P60, taphylococcus aureus, and treptococcus faecalis) and five fungi (Aspergillus niger, Trichophyton mentagrophytes, Aspergillus oryzae, Myrothecium verrucaria, and Trichoderma viride). HERMAN GERHON AND RAULO PARMEGIANI Pfister hemical Works, Inc., Ridgefield, New Jersey Received for publication 18 July 1962 All of the compounds studied were synthesized by standard methods found in the literature (Gershon, Dittmer, and Braun, 1961; Gershon, 1962; Gershon, Braun, and cala, J. Med. hem., in press), and the chemistry of the compounds that were not previously known will be reported elsewhere. Platedisc method. For the antibacterial testing, the following media were employed: E. coli and P. aeruginosa, nutrient agar (Difco);. aureus, nutrient agar enriched with 10 % beef serum;. faecalis and L. mesenteroides P60, Eugonagar (BBL). The fungal media employed were as follows: A. niger, T. viride, M. verrucaria, and A. oryzae, abouraud Dextrose Agar (Difco); and T. mentagrophytes, abouraud Dextrose Agar enriched with 10 % beef serum. The antimicrobial tests were conducted as previously described (Gershon and Parmegiani, 1962). In essence, they depended upon impregnating sterile 6mm filterpaper discs with 103, 102, and 10,ug of compound per dise for bacteria and 12mm discs with 104, 103, and 102 mg of compound per disc for fungi. The discs were placed on the appropriate inoculated agarcontaining media in petri dishes. Incubation was carried out for 18 hr at 37 for bacteria, and for 5 days at 28 to 30 for fungi. The number of zones of inhibition obtained was recorded. The antifungal index is defined as the sum total of the zones of inhibition, which is similar to Albert's (1960) concept of bacteriostatic index; the antifungal spectrum index is defined as the total number of zones of inhibition multiplied by the number of organisms inhibited within the defined system. A discussion of these constants was reported earlier by Gershon and Parmegiani (1962). Vapor method. Antifungal studies on the vapors of the ring chlorinated pyrimidines were carried out on three organisms: A. niger, T. viride, and A. oryzae. The medium employed was abouraud Dextrose Agar (Difco), and the tests were conducted in the following manner. A spore suspension (1 ml) of the respective organism, containing 6 X 106 spores in 0.9 % saline, was added to 99 ml of medium at 45. Each inoculated medium (3 to 5 ml) was poured into each of three chambers in sterile quadriplate petri dishes. To the fourth chamber were added 2 to 5 mg of solid compound, or 1 drop of liquid compound impregnated in a 12mm sterile filterpaper disc. The dishes were incubated at 28 to 30 for 5 days. A 5mm2 portion of agar was cut from all portions of medium which showed no ap 78
2 VOL ANTIFUNGAL POLYHLORINATED PYRIMIDINE 79 TABLE 1. Antifungal activity of ring chlorinated pyrimidines on discs after 5 days on abouraud Dextrose Agar at 28 a om b No. of zones of inhibition in five fungic Antifungal Antifungal pound Pyrimidine T.M.d A.O. MV. TV. indexe spectrum no. A.N. T.. M T.'index' 1 2chloro ,4dichloro ,5dichloro ,5dichloro ,6dichloro ,4,5trichloro ,4,6trichloro ,5,6trichloro ,4,5,6tetrachloro ,6dichloro2methyl ,6dichloro2ethyl ,6dichloro2propyl ,6dichloro2isopropyl ,4dichloro6methyl ,4dichloro6ethyl ,4dichloro6propyl ,4dichloro6isopropyl ,4dichloro6heptadecyl ,4dichloro6carbomethoxy ,4dichloro6phenyl ,4dichloro5methyl methyl4,5,6trichloro ethyl4,5,6trichloro propyl4,5,6trichloro isopropyl4,5,6trichloro heptadecyl4,5,6trichloro phenyl4,5,6trichloro methyl2,4,5trichloro ethyl2,4,5trichloro propyl2,4,5trichloro isopropyl2,4,5trichloro heptadecyl2,4,5trichloro carbomethoxy2,4,5trichloro phenyl2,4,5trichloro methyl2,4,6trichloro ethyl2,4,6trichloro propyl2,4,6trichloro isopropyl2,4,6trichloro phenyl2,4,6trichloro chloromethyl4,5,6trichloro bromomethyl2,4,5trichloro bromomethyl2,4,6trichloro chloro4,6dimethyl ,4dichloro5,6dimethyl ,6dichloro2,5dimethyl chloromethyl4,6dichloro5methy l bromomethyl4,6dichloro2methyl bromomethyl2chloromethyl4,6dichloro a terile 12mm filterpaper discs were prepared to contain 104, 103, and 102,g of compound per disc; 3 = zones of inhibition at all levels, 2 = zones of inhibition at the two highest levels, 1 = a zone of inhibition at the highest level only. ball of the compounds were prepared by standard methods found in the literature. ca.n., Aspergillus niger; T.M., Trichophyton mentagrophytes; A.O., Aspergillus oryzae; M.V., Myrothecium verrucaria; T.V., Trichoderma viride. d Medium enriched with 10% beef serum. Antifungal index, sum of zones of inhibition (Albert, 1960). f Antifungal spectrum index, total number of zones of inhibition multiplied by the number of organisms inhibited (Gershon and Parmegiani, 1962).
3 80 GERHON AND PARMEGIANI APPL. MIROBIOL. parent fungal growth, and was subcultured in 10 ml of abouraud Liquid Medium (Difco). The subculture was incubated at 28 to 30 for 2 weeks. If no fungal growth appeared on subculture, the compound was considered sporicidal; on the other hand, if there was fungal growth on subculture, the compound was considered sporistatic. Liquid culture method. All of the compounds were screened against A. niger (Gershon and Parmegiani, 1963). To 98 ml of sterile abouraud Liquid Medium (Difco), enriched with 0.05%o yeast extract (Difco), was added 1 ml of dimethyl sulfoxide, containing levels of compound to yield 100, 10, and a ppm on dilution to 100 ml. Inoculum (1 nil) was added, containing 6 X 106 spores in 0.9 % saline. The flasks were shaken at 250 oscillations/min on a shaker with a 1in. eccentric rotary motion at 28 to 30. Readings were taken at 3 and 6 days; after 6 days, all flasks showing no apparent growth were further tested for cidal and static effects on the spore inoculum. Medium (1 ml) that showed no growth was added to 15 ml of sterile abouraud Liquid Medium and kept at 28 to 30 for 2 weeks. If the next lower level of compound was also inhibitory, it was then necessary to dilute the test sample of medium below the concentration of compound at the next lower level. REULT All of the ring chlorinated pyrimidines appeared to have negligible antibacterial activity against the strains of the five bacteria in this system of organisms. Table 1 summarizes the antifungal data on the ring chlorinated pyrimidines by the discplate method. Based on the definition of antifungal spectrum index, it is obvious that an index value of 49 or greater can be achieved only when all five organisms are inhibited. ince the purpose of this study was to locate agents of the broadest activity, an inspection of the antifungal spectrum indices revealed that 14 compounds of 48 fulfilled this criterion. These compounds are numbered 6, 8, 9, 19, 28, 33, 34, 35, 36, 40, 41, 42, 47, and 48. Table 2 summarizes the results obtained by exposing the spores of three fungi in a growth medium to the vapors of the 48 ring chlorinated pyrimidines. For comparison, some known antifungal agents (8quinolinol, 5chloro8 quinolinol, 5iodo8quinolinol, mercurous chloride, mercuric chloride, mercury, and phenylmercuric acetate) were tested in the same system. Again, to detect the compounds of greatest overall activity, sporicidal action against all three fungi was used as the criterion. The data in Table 2 show that 15 compounds (2, 4, 6, 7, 8, 9, 14, 15, 21, 22, 23, 28, 29, 35, and 40) were sporicidal as vapors against all three fungi, whereas none of the comparison compounds were sporicidal and only 8quinolinol was sporistatic against T. viride. Table 3 summarizes the results in shake flasks obtained on the 48 pyrimidines against A. niger. By the criterion of the sporicidal effect, seven compounds (6,7, 8,9, 40, 41, and 42) appeared to be superior at a level of 100 ppm. Of these seven compounds, 6, 8, and 40 were also sporistatic at 10 ppm, 8 and 40 were still sporistatic at 5 ppm, and 8quinolinol was sporistatic at 100 and 10 ppm. TABLE 2. Effect of vapors of ring chlorinated pyrimidines on fungal spores incorporated in abouraud Dextrose Agar at 28 after 5 daysa ompound no. Pyrimidineb pores from A s per Tricho A spergillus derma gills niger viride oryzae 1 2chloro ,4dichloro ,5dichloro ,5dichloro ,6dichloro ,4,5trichloro ,4,6trichloro ,5,6trichloro ,4,5,6tetrachloro ,6dichloro2methyl ,6dichloro2ethyl ,6dichloro2propyl ,6dichloro2isopropyl ,4dichloro6methyl ,4dichloro6ethyl ,4dichloro6propyl ,4dichloro6isopropyl ,4dichloro6heptadecyl. 19 2,4dichloro6carbomethoxy ,4dichloro6phenyl ,4dichloro5methyl methyl4,5,6trichloro. 23 2ethyl4,5,6trichloro propyl34,5,6trichloro isopropyl4,5,6trichloro heptadecyl4,5,6trichloro phenyl4,5,6trichloro methyl2,4,5trichloro ethyl2,4,5trichloro propyl2,4,5trichloro isopropyl2,4,5trichloro heptadecyl2,4,5trichloro carbomethoxy2,4,5trichloro phenyl2,4,5trichloro methyl2,4,6trichloro ethyl2,4,6trichloro propyl2,4,6trichloro isopropyl2,4,6trichloro phenyl2,4,6trichloro chloromethvl4,5,6trichloro bromomethyl2,4,5trichloro bromomethyl2,4,6trichloro chloro4,6dimethyl ± 44 2,4dichloro5,6dimethyl ,6dichloro2,5dimethyl chloromethyl4,6dichloro5 methyl bromomethyl4,6dichloro2 methyl bromomethyl2chloromethyl 4,6dichloro quinolinol chloro8quinolinol iodo8quinolinol mercurous chloride mercuric chloride mercury phenylmercuric acetate a One ml of inoculm (1 ml containing 6 X 106 spores of the respective organism in 0.9% Nal) was added to 100 ml of medium at 45. The inoculated media were added to each of three chambers of quadriplate petri dishes, and into the fourth chamber was placed the test compound (2 to 5 mg of solid, or 1 drop of liquid, impregnated in a sterile 12mm filterpaper disc). I All compounds were prepared by standard methods found in the literature. c ymbols: = no inhibition; = sporicidal; = sporistatic; a number = approximate %70 of area showing no growth.
4 VOL. 1 1)1963 ANTIFUNGAL POLYHLORINATED PYRIMIDINE 81 TABLE 3. Effect of ring chlorinated pyrimidines on Aspergillus niger in liquid culture in shake flasks at 28 a oncn of compound (ppm) No. Pyrimidineb 10 Days 3c chloro ,4dichloro ,5dichloro ,5dichloro ,6dichloro ,4,5trichloro ,4,6trichloro ,5,6trichloro ,4,5,6tetrachloro ,6dichloro2methyl ,6dichloro2ethyl ,6dichloro2propyl ,6dichloro2isopropyl ,4dichloro6methyl ,4dichloro6ethyl , 4dichloro6propyl ,4dichloro6isopropyl , 4dichloro6heptadecyl , 4dichloro6carbomethoxy ,4dichloro6phenyl ,4dichloro5methyl methyl4,5,6trichloro ethyl4,5,6trichloro propyl4,5,6trichloro isopropyl4,5,6trichloro heptadecyl4,5, 6trichloro phenyl4,5,6trichloro methyl2,4,5trichloro ethyl2,4,5trichloro propyl2,4,5trichloro isopropyl2,4,5trichloro heptadecyl2,4,5trichloro carboxymethyl2,4,5trichloro phenyl2,4,5trichloro methyl2, 4,6trichloro ethyl2,4,6trichloro propyl2,4,6trichloro isopropyl2,4,6trichloro phenyl2,4,6trichloro chloromethyl4, 5,6trichloro bromomethyl2,4,5trichloro bromomethyl2,4,6trichloro chloro4,6dimethyl ,4dichloro5,6dimethyl ,6dichloro2,5dimethyl chloromethyl4,6dichloro5methyl bromomethyl4,6dichloro2methyl bromomethyl2chloromethyl4,6dichloro quinolinol... d cs ato 98 ml of sterile abouraud Liquid Medium, enriched with 0.05% yeast extract, was added 1 ml of dimethyl sulfoxide, containing levels of compound to yield 100, 10, and 5 ppm on dilution to 100 ml. Inoculum (1 ml) was added which contained 6 X 106 spores in 0.9% Nal. The flasks were shaken at 250 oscillations/min on a shaker with a 1in. eccentric rotary motion at 28. b All compounds were prepared by standard methods found in the literature. c Flasks were inspected after 3 and 6 days to record whether there was growth or no apparent growth. d ymbols: = growth, = no apparent growth, = fungistatic, and = fungicidal. Fungistatic and fungicidal tests were performed by incubating 1 ml of test medium which showed no growth in 15 ml of abouraud Liquid Medium at 28 to 30 for 14 days. If the next lower test level of compound was also inhibitory, it was necessary to dilute the test sample of medium below the concentration of compound at the next lower level.
5 82 DIscuION GERHON AND PARMEGIANI In this study, by the criterion of antifungal spectrum index, it was found that, of the 14 most active compounds, 11 contained at least three chlorine atoms on the pyrimidine ring. To explain the activity of the three dichloropyrimidines, the contribution of the side chain should be taken into account. If the structures of compounds 42, 47, and 48 are compared, it will be found that all possess in common a 5bromomethyl group. Furthermore, it can be seen that 5bromomethyl2, 4, 6trichloropyrimidine (compound 42) is more active than 5methyl2, 4, 6trichloropyrimidine (compound 35). Thus, it can be stated that a bromomethyl group in the 5 position enhances antifungal activity, and, consequently, 47 and 48 are sufficiently activated to meet the criterion. The activity of compound 19 may be explained only by assum TABLE 4. utmnnary of antifungal data on 23 of the mioire active ring chlorinated pyrimidines of 43, by three screening methods creening method No. Pyrimidine D oisca Vaporb Liquid culturec 2 2,4dichloro / ,5dichloro... 1 / ,4,5trichloro /100, /10 7 2,4,6trichloro / ,5,6trichloro /100, /5 9 2,4,5,6tetrachloro / ,4dichloro6methyl ,4dichloro6ethyl ,4dichloro6 carbomethoxy P 21 2,4dichloro5methyl ,5,6trichloro2methyl / ,5,6trichloro2ethyl / ,4,5trichloro6methyl / , 4,5trichloro6ethyl / ,4,5trichloro6 carbomethoxy P 34 2,4,5trichloro6phenyl. 75 P / ,4,6trichloro5methyl. 55 / ,4,6trichloro6ethyl.. 50 / ,5,6trichloro2 chloromethyl.60 /100, /5 41 2,4,5trichloro6 bromomethyl / ,4,6trichloro5 bromomethyl.65 P / ,6dichloro5bromomethyl 2methyl.55 P / , 6dichloro5bromomethyl 2chloromethyl.50 P /100, /10 anumbers represent the antifungal spectrum index; see Table 1. b = sporicidal, = sporistatic (against three fungi: Aspergillus niger, Trichoderma viride, and Aspergillus oryzae), P = activity poor, and 23 = cidal against two of three organisms; see Table 2. c = static, = cidal, number = at ppm, and = no inhibition at 100 ppm; see Table 3. APPL. MIROBIOL., ing that the carbomethoxy group makes a contribution. In addition, it can also be seen that addition of a side chain to the ring generally reduces the antifungal activity, and the reduction in activity is proportional to the size of the side chain. An exception is 6phenyl2, 4, 5trichloropyrimidine. In the antifungal vapor study, the 15 pyrimidines that showed sporicidal activity seem to be the lowest molecular weight compounds, and are thus generally the most volatile. For, without sufficient volatility, the fungal spores would not be exposed to a lethal concentration of agent in a short enough time to cause inhibition of germination. Another generalization that can be made is that, since 10 of the 15 pyrimidines contained three or more chlorine atoms on the ring and only five compounds were dichlorinated, a pyrimidine which possesses three or more ring chlorines is more likely to be fungicidal as a vapor than one that possesses two ring chlorines. It should also be noted that, in the homologous series of compounds, the addition of one methylene group to the side chain can make the difference between a fungicidal or fungistatic effect. In the 2,4dichloro series up to the 6ethyl analogue, the compounds are sporicidal. The propyl and higher analogues are not cidal. The same holds for the 4,5,6trichloropyrimidine series, as well as for the 2,4,.5 trichloropyrimidines. In the case of the 2,4,6trichloro pyrimidines, the sporicidal effect ends with the 5methyl homologue. The shakeflask study against A. niger was undertaken to attempt to determine in a more quantitative manner the order of magnitude of concentration, with respect to activity. In addition to this, such a method, with its highly favorable growth conditions and its hydrolytic conditions with respect to the screening compound, presents a very severe test of the efficacy of the agent under study. For the most part, where there was inhibition by the platedisc method, there was also inhibition in liquid culture. The cidal effect was observed in liquid culture only where the ring trichlorinated pyrimidines were employed. In the cases of compounds 10, 15, 16, 17, 19, 21, 33, 44, and 45, the liquid culture data did not correlate with the disc results. All of these compounds have in common the fact that they possess only two chlorine atoms on the pyrimidine ring, except 33, which is a trichloropyrimidine. It is well known that 2,4 and 4,6dichloropyrimidines are relatively unstable toward hydrolysis, especially if there is an electronattracting group on the ring such as an alkyl or carboxyl group. In the case of 2,4 and 4,6dichloropyrimidines, compounds 2 and 5, it seems that the rates of hydrolysis were sufficiently slow to permit enough compound to remain intact during the test period to prevent germination of the spore inoculum. It should also be remembered that this class of compounds is comparatively insoluble in water, and when impregnated in a filterpaper disc there is not complete contact between the water of the agarcontaining medium and the compound, which also allows
6 VOL. 11, ANTIFUNIGAL POLYHLORINATED PYRIMIDINE 83 for a diminished hydrolytic rate. A final consideration should be kept in mind; that is, these chlorinated pyrimidines possess two modes of transport: as vapors and as dissolved molecules in the culture medium. It is conceivable that, should a compact portion of ring chlorinated pyrimidine, such as is found in an impregnated disc, be exposed to water, the surface molecules would be hydrolyzed, and thus form a protective coating around the main body of compound. This protective coat could then retard further hydrolysis, but still allow the compound to diffuse as a vapor. In the case of compound 33, the chlorine atoms in positions 2 and 4 are made so labile by the carbomethoxy group that the compound will hydrolyze in water, at room temperature, to methyl 5chloroorotate. In view of these physicochemical considerations, the liquid culture and agar data can be completely correlated. Table 4 contains a summary of the 23 compounds which fulfilled at least one of the criteria established for the discplate method, vapor method, and liquid culture method. These data indicate that compounds 6 (2,4,5 trichloropyrimidine), 8 (4,5, 6trichloropyrimidine), 9 (2,4,5, 6tetrachloropyrimidine), and 40 (2chloromethyl 4,5,6trichloropyrimidine) show outstanding activity by all three screening methods. LITERATUTRE ITED ALBERT, A elective toxicity, 2nd ed. Methuen & o., Ltd., London. GERHON, H Pyrimidines. II. hlorinated pyrimidines derived from orotic acid. J. Org. hem. 27: GERHON, H., AND R. PARMEGIANI Antimicrobial activity of 8quinolinols, salicylic acids, hydroxynaphthoic acids, and salts of selected quinolinols with selected hydroxyacids. Appl. Microbiol. 10: GERHON, H., K. DITTMER, AND R. BRAUN Pyrimidines. I. ome halogenated monomethylpyrimidines. J. Org. hem. 26:1874. GERHON, H., AND R. PARMEGIANI Antimicrobial activity of 8quinolinol, its salts with salicylic acid and 3hydroxy2 naphthoic acid, and the respective copper (Il) chelates in liquid culture. Appl. Microbiol. 11:6265. Downloaded from on January 11, 2019 by guest
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