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Polypodium Vulgare Biochem. J. (1980) 190, 537-544 537 Printed in Great Britain Mechanism offormation of the A/B cis ring junction of ecdysteroids in Polypodium vulgare Timothy G. DAVIES, William J. S. LOCKLEY, Richard BOID, Huw H. REES and Trevor W. GOODWIN Department ofBiochemistry, University ofLiverpool, P.O. Box 147, Liverpool L69 3BX, U.K. (Received 14 February 1980) 1. The fates of the 3 a-, 4 a- and 4fl-hydrogen atoms of cholesterol during formation of the A/B cis ring junction of ecdysteroids was investigated by administration of [4-14C, 3a-3H]-, [4-14C, 4a-3H1- and [4-14C, 4,B-3H]cholesterol species to the fern, Polypodium vulgare, and isolation of the 20-hydroxyecdysone formed in each case. 2. The 3H was retained in the ecdysteroid formed from each substrate. 3. Location of the 3H in the 20-hydroxyecdysone indicated that migration of 3H from the 3a- and 4pi-positions to C-4 and C-5, respectively, had occurred, whereas the 4a-3H atom was retained at C-4. 4. A possible mechanism for the formation of the A/B cis ring junction of ecdysteroids in P. vulgare is presented. Most species of insect larvae investigated contain Sakurai, 1974), thus suggesting that as in insects, the 20-hydroxyecdysone (I) as the major moulting A/B cis ring junction is introduced early in the hormone (ecdysteroid), which is frequently accom- ecdysteroid biosynthetic pathway. It has been panied by smaller amounts of ecdysone (II) assumed frequently that this A/B cis ring junction is (Thompson et al., 1973; Gilbert et al., 1977). formed by mere equilibration of a 6-oxo-5a-H 20-Hydroxyecdysone is also the most widely occur- steroid. However, numerous plausible pathways ring of the numerous compounds possessing insect- could account for the transformation of a Al moulting-hormone activity that have been isolated structure to give the 5,/ stereochemistry in ecdy- from plants (Horn, 1971). Cholesterol can serve as a steroids (Rees, 1971). An analogous change during precursor of the C2, ecdysteroids in both insects and steroid hormone and bile acid formation in verte- plants (Rees, 1971). It is known that at least some brates involves the intermediacy of a 3-oxo-A4 modification of the nucleus precedes side chain steroid (Samuels & Eik-Nes, 1968). Similarly, during hydroxylation. the formation of cardenolides from cholesterol in the In plants, 2/1,3/1,14 a-trihydroxy-5,B-cholest-7-en- plant Digitalis lanata, introduction of 5, stereo- 6-one is incorporated into ecdysteroids (Tomita & chemistry involves oxidation at C-3 as an obli- OH (I) R1=H,R2=OH (V) R = /1-OH, (a-H (II) R1= H, R2= H (VI) R = 0 (III) R'= Ac, R2= OH (IV) RI = A¢, R2= H Vol. 190 0306-3283/80/090537-08$01.50/1 (A 1980 The Biochemical Society 538 T. G. Davies, W. J. S. Lockley, R. Boid, H. H. Rees and T. W. Goodwin gatory step (Caspi & Hornby, 1968). Although was eluted from the gel with dry redistilled diethyl [4-14C]cholest-4-en-3-one is not incorporated sig- ether. nificantly into 20-hydroxyecdysone in Podocarpus T.l.c. separation of ecdysteroids and their deri- elatus seedlings (Sauer et al., 1968), the possibility vatives was carried out on silica gel (0.5mm thick remains that a 3-oxo-A4 grouping could be involved Kieselgel GF254; E. Merck A.G., Darmstadt, Ger- at a later stage in the pathway, e.g. after insertion of many) developed as specified in the text. Com- the A7 bond or some ofthe hydroxyl groups. pounds were detected under u.v. light and eluted The present paper reports investigations on the thoroughly from the gel with chloroform/methanol mechanism of formation of the A/B cis ring junction (l:1,v/v). of ecdysteroids in the fern, Polypodium vulgare. [4-'4C,3a-3H1-, [4-'4C,4a-3H1- and [4-14C,46- Analytical methods 3Hlcholesterol species were incorporated, in turn, 'H.n.m.r. spectra were determined for solutions of into 20-hydroxyecdysone in this plant. Examination ecdysteroid derivatives in (2H)chloroform at 220 or of the fate of the two C-4 hydrogen atoms of 1OOMHz on Varian HR-220 and HA 100 instru- cholesterol would show whether either of these ments, respectively, by the Physico-Chemical hydrogen atoms is removed during ecdysteroid Measurements Unit, Harwell, Berks., U.K. or at biosynthesis, irrespective of the stage at which 60MHz on a Perkin-Elmer R12 instrument. Mass removal occurs. Similarly, investigation of the fate of spectra were determined on A.E.I. M.S.902 and the 3H in [3a-3Hjcholesterol should reveal whether M.S. 12 mass spectrometers. oxidation at C-3 occurs during formation of ecdy- steroids. Part of this work has been reported Radiochemical methods previously in preliminary form (Lockley et al., Radioactivity was measured on an Intertechnique 1975). The development of improved chemical three-channel scintillation spectrometer, model methods has now allowed more complete location of ABAC SL30. Samples were dissolved in lOml of a the tritium in the labelled 20-hydroxyecdysone. dioxan-based scintillation solution containing 15 g of 5-(biphenyl-4-yl)-2-(4-t-butylphenyl)- 1-oxa-3,4- Experimental diazole (butyl-PBD)/litre and lOOg of naphthalene/ litre. 3H and '4C radioactivities are quoted after Nomenclature corrections for background, counting efficiency and Trivial names are often used. Systematic names quenching had been applied. are as follows: ecdysone, (22R)-2f,3f,14,22,25- pentahydroxy-511-cholest-7-en-6-one; 20-hydroxy- Administration oflabelled cholesterol ecdysone, (22R)-2f,3f3,14,20,22,25-hexahydroxy- [4-14C]Cholesterol was mixed with the appro- 5,-cholest-7-en-6-one. priate [3H]cholesterol sample and purified by t.l.c. on silica gel. A portion of the purified cholesterol was Chemicals removed, diluted with carrier non-radioactive choles- [4-'4C]Cholesterol (54Ci/mol) and NaB3H4 were terol and recrystallized to constant specific radio- purchased from The Radiochemical Centre, Amer- activity from chloroform/methanol to establish the sham, Bucks., U.K. [4 a-3Hl- and [41J-3Hlcholes- 3H/14C radioactivity ratio for the substrate. The terol samples were prepared by the method of remaining cholesterol was then dissolved by soni- Lockley et al. (1978) and contained 96 and 91%, cation in ethanol (2 ml) containing 0.05% Tween 80. respectively, of the 3H in the expected positions. Fronds of Polypodium vulgare sub-sp. inter- [3 a-3HlCholesterol was prepared by Dr. I. F. Cook jectum (obtained from Ness Botanical Gardens, by reduction of cholest-5-en-3-one with NaB3H4 and Cheshire, U.K.) were cut back to the rhizome, and purified by t.l.c. Samples of ecdysone and 20- were left until viable fronds (8-10cm long) had hydroxyecdysone were generously given by Dr. G. appeared. The solutions of labelled cholesterol were B. Russell, D.S.I.R., Palmerston North, New Zea- applied to the leaves by using a glass capillary tube, land. Berberine sulphate was purchased from Sigma. twice weekly over a 4-week period. Approx. eight to twelve growing fronds were used per experiment. Thin-layer chromatography The entire plants were extracted 2 weeks after the Sterols were separated by t.l.c. on (i) silica gel final administration of substrate. (0.5mm thick Kieselgel G; E. Merck A.G., Darm- stadt, Germany) developed in chloroform and (ii) on Extraction ofplant material 10% (w/w) AgNO3-impregnated silica gel (0.5 mm The extraction of the plants treated with [4-14C, thick Kieselgel H) developed in chloroform/ethanol 4a-3H1jcholesterol (13.5 uCi of 14C; 28.3 ,uCi of 3H) (97:3, v/v). After t.l.c., the sterol was detected under is given as a typical procedure. The rhizomes and u.v. light (360nm) by spraying with 0.05% ber- roots were washed free of soil and the whole plants berine sulphate in methanol/acetone (1: 1, v/v), and (180g) were cut into small pieces before maceration 1980 Biosynthesis of ecdysteroids 539 in ethanol (1 litre). The slurry was then refluxed for (approx. 4 mg) was added to turn the solution 6 h, cooled, and filtered through glass wool. The solid green (Galbraith & Horn, 1969). The mixture was residue was then re-extracted as above and the two left for 30min at room temperature and was then ethanol extracts were combined and evaporated to poured into butan-l-ol (50ml), which was washed dryness under vacuum. successively with saturated NaHCO3 solution and The dried extract (15 g; 4.37 x 106 d.p.m. of 14C) water. The butanol layer was then evaporated to was then partitioned between n-hexane (300ml) and dryness under vacuum, azeotroping with benzene/ methanol/water (7: 3, v/v) (300 ml). Each phase was ethanol. The 20,22-acetonide-20-hydroxyecdysone then re-partitioned against the complementary sol- 2-acetate (V; 4.53mg; 4.93 x 103d.p.m. of 14C) was vent and the combined hexane extracts and the isolated by t.l.c. on silica gel with chloroform/ combined methanol/water extracts were evaporated methanol (19: 1, v/v) for development and was to dryness under vacuum. The residue (7.85 g; recrystallized from chloroform/diethyl ether: m/e 5.44 x 105 d.p.m. of 14C) from the methanol/water 562 (M+, very weak), 544 (M+-H2O), 526 fraction was then partitioned between butan- 1 -ol (M+-2H2O), 510, 487 (M+-acetate-CH3), 469 (200ml) and water (200ml) and each phase was (M+-acetate-H2O-CH3), 451 (M+-ace- re-extracted with the complementary solvent. The tate-2H20-CH3), 446, 405 (M+-side chain), combined butan-l-ol extracts (1.59g; 1.01 x 105 395, 387 (405-H20), 345 (387-acetate), 327 d.p.m.
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