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MICROBIAL TRANSFORMATION of ANTIBIOTICS CLINDAMYCIN RIBONUCLEOTIDES* A. D. ARGOUDELIS, J. H. COATS and S. A. MIZSAK Research

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MICROBIAL TRANSFORMATION of ANTIBIOTICS CLINDAMYCIN RIBONUCLEOTIDES* A. D. ARGOUDELIS, J. H. COATS and S. A. MIZSAK Research 474 THE JOURNAL OF ANTIBIOTICS JUNE 1977 MICROBIAL TRANSFORMATION OF ANTIBIOTICS CLINDAMYCIN RIBONUCLEOTIDES* A. D. ARGOUDELIS,J. H. COATS and S. A. MIZSAK Research Laboratories, The Upjohn Company Kalamazoo, Michigan 49001, U.S.A. (Received for publication March 22, 1977) Addition of clindamycin to whole-cell cultures of Streptomyces coelicolor MuLLER resulted in the loss of in vitro activity against organisms sensitive to clindamycin. Incubation of such culture filtrates with crude alkaline phosphatase generated a biologically active material identified as clindamycin. Fermentation broths containing inactivated clindamycin yielded clindamycin 3-ribonucleotides and clindamycin 3-phosphate the structure of which was established by physicochemical and enzymatic means. Attempts to transform clindamycin to clindamycin 3-ribonucleotides by lysates or partially purified enzyme preparations from S. coelicolor have failed. In the past few years we have been involv- Fig. 1 ed in studies related to biomodification of anti- biotics by actinomycetes. Previous papers have described the acylation of chloramphenicol by Streptomyces coelicolorl), the phosphorylation of lincomycin by Streptomyces rochei2), the trans- formation of clindamycin (1) to 1-demethylclin- damycin and clindamycin sulfoxide by Strepto- myces punipalus and Streptomyces armentosus3) and the phosphorylation of clindamycin by whole cells and lysates of Streptomyces coeli- color4). Further studies have shown that whole cells (but not cell-free extracts) of S. coelicolor transform clindamycin to a mixture of clinda- mycin 3-phosphate and clindamycin 3-ribonucle- otides. The present paper discusses the produc- tion, isolation, chemistry and biological pro- perties of these clindamycin bioconversion pro- ducts. Production and Isolation of Clindamycin 3-Ribo- nucleotides and Clindamycin 3-Phosphate In our initial paper4) describing the phos- phorylation of clindamycin by S. coelicolor we * Preliminary report of this work has been published; see A . D. ARGOUDELIS and J. H. COATS: J. Amer. Chem. Soc. 93: 534, 1971 VOL. XXX NO. 6 THE JOURNAL OF ANTIBIOTICS 475 reported that clindamycin was inactivated when added to 24-hour cultures of the organism grown in a complex medium. Clindamycin could be regenerated by treatment of the bioinactive fermentation broth with crude alkaline phosphatase. This observation led us to the isolation of clindamycin 3- phosphate. However, during the isolation studies we observed the presence of unidentified com- pounds that also yielded clindamycin when incubated with crude alkaline phosphatase. We decided therefore to study further the products of biotransformation of clindamycin by whole cell cultures of S. coelicolor. The fermentation conditions used in the present study were identical with those reported earlier). Clindamycin (50 mcg/ml) was added to whole cell cultures of S. coelicolor 24 hours after inoculation. Cultures were harvested after 48 hours of fermentation at which time clindamycin was no longer detectable. Clindamycin could be regenerated by the treatment of the bioinactive fermentation broth with either crude alkaline phosphatase or snake venom phosphodiesterase. Since clindamycin 3- phosphate was not converted to clindamycin by venom phosphodiesterase we concluded that S. coeli- color converted clindamycin not only to clindamycin 3-phosphate but, in addition, to compound(s) con- taining phosphodiester bonds. Fermentation and isolation studies were followed by in vitro assays vs. Sarcina lutea before and after treatment of the sample under evaluation with crude alkaline phosphatase. This crude enzyme preparation exhibited both phosphomono- and phosphodiesterase activities. Fractions containing the clindamycin bioconversion products did not show any bioactivity before treatment with the enzyme. Incubation of these fractions with alkaline phosphatase afforded clindamycin which was easily identified by TLC. The clindamycin bioconversion products, which for convenience would be designated as clinda- mycin 3-ribonucleotides and clindamycin 3-phosphate, were isolated from culture filtrates by adsorption on Amberlite XAD-2 followed by elution with aqueous methanol. Chromatography of the methanolic eluates on Dowex-1 (acetate) resulted in the separation of clindamycin 3-ribonucleotides (isolated from the spent) from most of clindamycin 3-phosphate (eluted from the column with 5 % aqueous acetic acid). Amberlite XAD-2 chromatography of the crude clindamycin 3-ribonucleotides followed by counter double current distribution (1-butanol-water, 1:1 v/v) yielded a mixture of bioinactive, UV- absorbing compounds which afforded clindamycin by treatment with venom phosphodiesterase. Chromatography of the mixture on DEAE-Sephadex (acetate) using tris-acetate (pH 8.0, 0.1 - 0.2 M) buffer gave eight compounds designated A, B, C, D, E, F, G and H in order of elution from the column Fig. 2. DEAE-Sephadex chromatography of clindamycin ribonucleotides 476 THE JOURNAL OF ANTIBIOTICS JUNE 1977 Table 1. Analytical data obtained on compounds A, D, E, G and H Com- Mol. Calculated Found pound formula C H N Cl P S C H N Cl P S A C27H45N5012C1PS 44.48 6.17 9.60 4.87 4.25 4.39 45.62 6.99 9.80 4.04 3.44 4.61 D C28H45N7011C1PS 44.63 6.05 13.07 4.72 4.11 4.28 44.77 6.66 12.57 4.38 3.52 4.65 E C27H44N4013CIPS 44.27 6.33 7.68 4.86 4.24 4.39 44.62 6.19 7.79 4.32 4.22 4.04 G C28H45N7012CIPS 43.71 5.85 12.74 4.61 4.03 4.16 43.69 6.34 11.62 4.15 3.81 3.63 H C18H34N208ClPS 42.85 6.79 5.55 7.02 6.15 6.35 42.91 7.04 6.34 6.74 5.29 5.56 Table 2. Characterization data Mol. weight UV [Amax (E X 10-3)]c Com- Mol. fa25b1b formula [M]D pound Calcd Founda pH 2.0 pH 7.0 pH 11.0 A C27H45N5O12C1PS 729 [a]D742 D +61° +445` 279 (9.60) 269 (6.80) 271 (6.60) D C28H45N7011CIPS 753 726 +62.9° +473° 257 (12.60) 261 (12.50) 261 (12.70) E C27H44N4013C1PS 732 764 +79.5` +578° 261 (8.20) 262 (8.40) 262 (6.50 G C28H45N7012CIPS 769 750 +69° +530` 256 (11.10) 254 (12.50) 259 (10.70) 277 (7.50) (sh) 273 (8.00) (sh) 266 (10.60) H C18H34N208C1PS 504 530 +91.3° +458° No UV absorption a Molecular weights were determined by vapor pressure osmometry in methanol. b Specific rotation was determined in water (c 1). Reported for: cytidine 5'-phosphate, pH 2.0, 280 (13,200); pH 7.0, 271 (9,100); pH 11.0, 271 (9,100). Adenosine 5'-phosphate, pH 2.0, 257 (15,000); pH 7.0, 259 (15,400); pH 11.0, 259 (15,400). Uridine 5'-phosphate, pH 2.0, 262 (10,000); pH 7.0, 262 (10,000); pH 11.0, 261 (7,800). Guanosine 5'-phosphate, pH 1.0, 256 (12,200); pH 7.0, 252 (13,700); pH 11.0, 258 (11,600). (Fig. 2). All but compound H yielded clindamycin by treatment with venom phosphodiesterase and were followed during the chromatography by UV absorption at 260 nm. Compound H showed no UV absorption, was not effected by treatment with venom phosphodiesterase but yielded clindamycin by treatment with alkaline phosphatase. Removal of THAM-acetate buffer and isolation of pure com- pounds A, B, C, D, E, F, G and H was done by chromatographies over Amberlite XAD-2. Characteriza- tion of compounds A, D, E, G and H, the main components of the mixture, is discussed in the next section. Compounds B, C and F are not completely characterized. Possible structures for these com- pounds are proposed in the later part of this paper. Characterization and Structure of Clindamycin 3-Ribonucleotides (A, D, E, G) and Clindamycin 3-Phosphate (H) Clindamycin 3-ribonucleotides (compounds A, D, E and G) and clindamycin 3-phosphate (com- pound H) were isolated as amorphous colorless materials soluble in water and lower alcohols and practically insoluble in acetone, ethyl acetate and chlorinated and saturated hydrocarbon solvents. All five compounds are amphoteric and like clindamycin, contain a basic group, pKa' ca. 7.5-7.7 (water). Analytical data obtained on compounds A, D, E, G and H (Table 1) combined with molec- ular weight determinations (vapor pressure osmometry in methanol; Table 2) indicated the molecular formulas shown in Tables 1 and 2. The IR spectra of compounds A, D, E, G and H, though different from each other, showed common features like broad absorption at 3300-3100cm-1 (-OH; -NH) and strong amide carbonyl absorption (1685 1675 cm-1, amide I; 1550 1530 cm-1, amide II). VOL. XXX NO. 6 THE JOURNAL OF ANTIBIOTICS 477 Compounds A, D, E and G showed UV Fig. 3. UV spectra of clindamycin 3-ribonucleotides. absorptions (Table 2 and Fig. 3) identi- cal to those reported for cytidine, adeno- sine, uridine and guanosine phosphate, respectively. Compound H showed no UV maxima. Compound H was identified as clindamycin-3-phosphate (2, Fig. 1) by comparison ([a]D, IR and NMR spectra) to an authentic sample4). This material afforded clindamycin by treatment with alkaline phosphatase (Table 4) but re- mained unchanged after incubation with either snake venom or spleen phosphodiesterases. The molecular formulae of com- pounds A, D, E and G (specifically the presence of one P atom per molecule), the UV spectra and the conversion of these compounds to clindamycin by treatment with crude alkaline phosphatase and Table 3 Thin-layer chromatography of clindamycin venom phosphodiesterase suggested structures 3-ribonucleotides and their degradation products for these compounds in which clindamycin is Rfa Compound linked to the phosphate group of cytidine Ab Be Cd phosphate (compound A), adenosine phosphate Clindamycin 3-(5'-cytidy- late) (A) 0.18 0.77 (compound D), uridine phosphate (compound Cytosine 0.66 0.72 0.22 Cytidine 0.81 0.69 0.14 E) and guanosine phosphate (compound G).
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