ANTIFERTILITY ACTIVITY OF VARIOUS STEROIDS IN THE FEMALE RAT. synthetic steroids lacking a 3, or a 17 oxygen function showed a
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1 ANTIFERTILITY ACTIVITY OF VARIOUS STEROIDS IN THE FEMALE RAT FRED A. KINCL and RALPH I. DORFMAN Institutes of Clinical Medicine and Hormone Biology, Syntex Research Center, Palo Alto, California {Received th January ) Summary. Antifertility of fifty-three steroids was studied in the adult, mated female rat. The steroids were given daily for days beginning on the day of pro-oestrus. On Day of the test implantation sites were counted. In most cases the antifertility was correlated with oestrogenic. Several tetrahydropyranyl ethers derived from oestradiol and synthetic steroids lacking a, or a 1 oxygen function showed a separation on these two parameters; this may indicate a relatively effective antifertility agent with low oestrogenicity. INTRODUCTION A bioassay procedure based on the fact that ovulating hormone in the rat is released between. and 4. p.m. (Everett, Sawyer c Markee, ) has been developed to detect compounds which interfere with a succession of reproductive processes from ovulation to implantation. This paper reports the relative potencies of various phenolic and neutral steroids when studied in this assay and administered subcutaneously and/or orally. MATERIALS AND METHODS of the adult white albino of the Holzman strain was The oestrous cycle followed by vaginal cytology. The first dose of the test compound was given during the morning of pro-oestrus. At 4. p.m. on the same day, the females were caged with fertile males for days in succession. Treatment was either by subcutaneous injection or by gavage for a total of days. The total dose of steroid was contained in - ml of an aqueous solution of sodium chloride (-%), polysorbate (-4%), carboxymethylcellulose (-%) and benzyl alcohol (-%). The daily dose was contained in - ml of vehicle. Fertilization was confirmed by the presence of sperm in vaginal smears taken on the 1st or nd day. At autopsy, 4 hr after the last treatment, the uterine horns were examined and the number of implantation sites recorded. Oestradiol-1ß served as the reference standard for studies of phenolic and the steroids and their derivatives administered by subcutaneous injection relative potencies of these compounds, administered by gavage, are listed in terms of mestranol (-methoxy-1a-ethynyloestra-l,,(1)-trien-1ß-oi). 1 - Ethynyl-a-androst--en-1ß-ol served as the corresponding reference standard for the neutral steroids administered either by subcutaneous injection or by
2 1 Fred A. Kind and Ralph I. Dorf man gavage. Results are based on the mean number of implantation sites calculated by graphic estimate. For the reference standards the percentage of pregnancies in any given group is also included. Table 1 reference phenolic steroid standards for antifertility assays by subcutaneous and oral administration to Route of administration dose Pregnant (%) implantation sites Mean Range 11 to 1 Subcutaneous injection Oestradiol-1p to 1 to 11 to 4 to 11 to 1 to to 1 Oto 1 Oto 1 Oto Oral Mestranol to 1 Oto Oto Oto 1 Oto Oto Oto Table anttfertility of 1oc-ethynyl-oc-androst--en-1ß-ol by subcutaneous and oral administration to Route of administration Total dose Pregnant (%) implantation sites Mean Range Subcutaneous to 4 to 11 Oto Oto Oto Oto Oral to 4 to 11 Oto 1 Oto RESULTS Antifertility of the standard reference compounds administered sub cutaneously and/or by gavage are given in Tables 1 and. Oestradiol-1ß was studied at a daily dose of - to 1 pg. A daily dose of - Mg did not influence
3 Antifertility of steroids 1 fertilization and pregnancy, but an increase to - ug resulted, in six females, in a modest decrease in fertility from % to %, and a mean often implanta tion sites. At the daily dose of - ug, fertility decreased to % of the pregnancy rate and a mean of four implantation sites. At the daily dose of -4 Mg, pregnancy was completely inhibited and implantation sites could not be found. On a weight basis mestranol was a less effective antifertility agent than oestradiol-1ß by injection. The average number of implantation sites and frequency of fertility decreased at daily doses between and Mg, and ata daily dose of 4 Mg pregnancy was completely inhibited in the three animals studied (Table 1). 1oc-Ethynyl-oc-androst--en-1ß-ol demonstrated a significant antifertility effect at the daily dose level of Mg, given subcutaneously, as indicated by the fact that only two of the six became pregnant and the mean number of implantation sites decreased to one (Table ). When this compound was given orally, Mg/day was needed to inhibit fertility. At the daily dose of Mg, inhibition was not observed in either of the two parameters (i.e. percentage of pregnant ; mean number of implantation sites). Tripling the daily dose to the same indices. Mg resulted in complete inhibition, judged by Our findings accord with the results reported by Guéritée & Savini () who found that the acetate inhibits luteinization in female at a daily dose of mg/kg. Antifertility of phenolic steroids by subcutaneous injection is given in Table, and by oral route in Table 4. The following information has been included : the daily dose range studied in Mg, the total number of used, relative antifertility, and relative oestrogenic determined in immature mice by the method of Rubin, Dorfman, Black & Dorfman (1). Fifteen steroids, all less active than oestradiol-1 ß, were given by subcutaneous injection. Three of these were roughly one-tenth as active as oestradiol-1ß. Mestranol was found to have 1% of the antifertility and 1% of the oestrogenic of oestradiol. A closely related compound, -methoxy-1 ß-cyanethoxyoestra-l,,(1)-trien, showed % of the antifertility and % of the oestrogenic. A three-fold separation between antifertility and oestrogenic was found for 1a-ethynyloestra-l(1),-diene-ß,1ß-diol, which had % of the antifertility but only % of the oestrogenic of oestradiol-1 ß. Although this compound is not a phenolic steroid, it has been included in this group since it may readily aromatize. The corresponding 1-ketone derivative and 1-deoxyoestradiol (oestra-l,,(1)-trien--ol) were only moderately active, having 1% and % of the of oestradiol-1 ß. Three steroids had between - and *1% of the antifertility of oestradiol-1ß. These include -methoxy-1a-fluoroestra-l,,(1)-trien (-%); oestra-1,,(1)- trien-1-one (-%); and -methoxy-,1-methylenoestra-l,-dien-1-one ( 1%). The antifertility of the remaining six weakly active steroids could be defined with much less certainty since in several cases the compounds were tested only at one dose level and on only three /dose. These compounds include l-methyl--acetoxyoestra-l,,(1),-tetraen-1-one, -methyl oestra diol, oestradiol -methyl-1-methylformyl bis ether, 4-allyl oestradiol,,4-diallyloestradiol and -hydroxypregna-l,,(1)-trien--one.
4 1 Fred A. Kind and Ralph I. Dorfman Table antifertility of phenolic steroids (and derivatives) in a subcutaneous injection assay Oestradiol-1ß Mestranol -Methoxy-1ß-cyanethoxy oestra-l,,(l)-trien 1ct-Ethynyloestra-1 ( 1),-diene-ß, 1ß-diol -Acetoxy-f, Ç-dichlorooestral,,(1)-trien-1-one Oestra-l,,(1)-trien-1ß-ol p-hydroxyoestra-1 ( 1), -dien-1- one -Methoxy-1ot-fluorooestra-1,,(1)- triene Oestra-1,,(1) -trien-1-one -Methoxy-, 1-methyleneoestra-l,-dien-1-one 1 -Methy1--acetoxyoestra-1,,(1), -tetraen-1-one -Methyl oestradiol -Methoxy-1ß-methoxyformy 1- oestra- l,,(1)-triene 4-Allyloestradiol-1ß,4-Diallyloestradiol-1ß -Hydroxy- 1-norpregnal,,(1)-trien--one dose range (Ug) 1 to 1 to -1 to to 1 to 1 to to to to to to Relative antifertility < <- < - Oestrogenic (immature mouse uterus) Table 4 antifertility of phenolic steroids (and derivatives) in an oral assay dose range Relative antifertility Oestrogenic (immature mouse uterus) Mestranol -Methoxy-1ß-cyanefhoxyoestral,,(1)-triene Oestradiol-1ß-tetrahydropyranyl Oestradiol-1ß ether Oestradiol-, 1ß bis-tetrahydropyranyl ether 1<x-Ethynyloestradiol-, 1-bis tetrahydropyranyl ether 1oc-Ethynyloestra-1,,-(1) -trien- 1p-ol 1ß- ( '-hydroxy) -ethoxyoestral,,(1)-trien- methoxy Oestra-l,,(1)-trien--ol ß-Hydroxyoestra-1 (1)--dien- 1-one Oestra-l,,(1)-trien-1-one - to 1 to 1 to 1 to 4 1 to to to to to to
5 Antifertility of steroids 1 Oral often steroids defined in terms of mestranol is given in Table 4. The most active steroid was -methoxy-1ß-cyanethoxyoestra-l,,(1)-triene. This compound had only % of the oestrogenic of mestranol but was six times more active in the antifertility test: this gave a separation between antifertility and oestrogenic of over sixty-fold. Two steroids, oestradiol -tetrahydropyranyl ether (%) and oestradiol-1ß (%) were more active than mestranol. Oestradiol, 1-bis tetrahydropyranyl ether was as active as the standard and ethynyl oestradiol,1-bis tetrahydropyranyl ether was somewhat less active. These four compounds showed marked separation between antifertility and oestrogenic. -Deoxyethynyl oestradiol (1cc-ethynyloestra-1,, (1) -trien-1 ß-ol) was ten times more active as an antifertility agent Table antifertility of neutral steroids in a subcutaneous injection assay 1a-Ethynyl-cc-androst--en- 1ß-ol -Methyl-1ß-propionoxy-aandrostan--one 1ß-Hydroxy-A-homoandrosta- 1 (1),,4a-trien-4-one -Hydroxymethyl-oc-androst- -en-1ß-ol Testosterone -Hydroxymethyl-1cc-methyl- oc-androst--en-1ß-ol ot, 1cc-Dimethyl-1ß-hydroxy- a-androstan--one -Ghloro--dehydro-1-nor progesterone 1-Norprogesterone ß-Hydroxy-1-norpregn-4-en- -one -Carboxy-a-androst--en-1ß-ol dose range 1 to 1 to 4 to 1 to to to to to to to Relative antifertility 1 1 <4 than oestrogen; -deoxyoestrone (oestra-l,,(1)-trien-1-one) had a ratio of fifty, and 1-deoxyoestrone (oestra-l,,(1)--ol) a ratio of seventy-five. Relative antifertility of neutral steroids expressed in terms of 1aethynyl-a-androst--en-1ß-ol is listed in Table (subcutaneous injection) and Table (oral assays). As an antifertility agent, this neutral steroid was itself considerably less active than oestradiol-1ß by injection (-1%), or mestranol given orally (%). Ten steroids were studied by the subcutaneous route. Two, a-methyl-1ß-propionoxy-a-androstan--one and 1ß-hydroxy- A-homoandrosta-l(1),,4a-trien-4-one were respectively three times and equally as potent as the standard. The remaining eight compounds were less active. These included three -deoxy C1 steroids, -hydroxymethyl-aandrost--en-1ß-ol (%), the corresponding 1a-mefhyl derivative (%) and -carboxy-a-androst--en-1ß-ol (<4). Testosterone assayed at %; a,1a-dimethyl-1ß-hydroxy-a-androstan--one at %, and three pregnan
6 11 Fred A. Kind and Ralph I. Dorfman derivatives at 1 to 1% (-chloro--dehydro-1-norprogesterone at 1%, 1-norprogesterone at %; and ß-hydroxy-1-norprogesterone at 1%). By the oral test, a,a-difluoromethylene-1a-methyl-a-androstan-1ß-ol Table antifertility of neutral steroids in an oral assay 1a-Efhynyl-ot-androst--en-1ß-ol a,a-difluoromethylene-1 a- methyl-a-androstan-1ß-ol 1 Norprogesterone -Formyl-1a-ethynyl-a-androst- -en-1ß-ol -Hydroxymethyl-1a-methyl- a-androst--en-1ß-ol -Carboxy-1a-methyl-aandrost--en-1ß-ol dose range to 4 to Relative antifertility 4 < < < Table compounds which did not inhibit fertility in adult mated (subcutaneous administration) Norethindrone* Chlormadinone acetate* Progesterone a-dihydro-1-norprogesterone 1a-Hydroxy-1-norprogesterone ß, 1ß-Diacetoxypregn--en--one ß-Hydroxy-1a-acetoxypregn--en- -one ß-Hydroxypregn-4-en--one ß-Pregnan-,11,-trione ß-Pregnan-ß,ß-diol ß-Acetoxy-ß-pregnan--one a-hydroxy-ß-pregnan--one a-acetoxy-ß-pregnan--one a-hydroxy-ß-pregn-1-en--one ß, llß, C-Trihydroxy-ß-pregnan-, diacetate a, 1 lß,a-trihydroxy-ß-pregnan-, diacetate 1a-Cyano-ß-hydroxy-a-pregnan-- one a-fluoro-1a-methylpregna-1,4-diene-,-dione Total used * Administered orally. dose studied (Range in mg) - to -4 to 1 to 1-1 to 1-1 to 1 1 to 1 - to was 4% as active as the standard. The other steroids listed in Table were not highly active. Table lists various steroids which were inactive in the antifertility test, together with the daily doses and the total numbers of used. Except for two
7 Antifertility of steroids 111 steroids, norethindrone (1a-ethynyl-1ß-hydroxyoestr-4-en--one) and chlor madinone acetate (-chloro-1a-acetoxypregna-4,-diene-,-dione) which were given by gavage, all the other compounds were injected. These include progesterone (which was not active at a dose of mg/day) and two derivatives of 1-norprogesterone ( -dihydro-l -norprogesterone and 1a-hydroxy-1- norprogesterone, both inactive at a dose of 1 mg/day). The remaining pounds com represent a variety of C1 steroids, many of which are possible pro gesterone metabolites. The relation between the subcutaneous and oral of phenolic steroids is illustrated in Table. Oestradiol-1ß was about six times more active by Table relative antifertility of various phenolic steroids by subcutaneous injection and by gavage Sub cutaneous injection A Gavage Ratio A Oestra-1,,(1)-trien-ß-ol Oestra-l,,( 1)-trien-l -one -Methoxy-1ß-cyanoethoxyoestral,,(1)-trien Oestradiol-1ß (Mestranol =.) Table relative antifertility of various neutral steroids by subcutaneous injection and by gavage Sub cutaneous injection A Gavage Ratio A -Hydroxymethyl-1a-methyl- a-androst--en-1ß- < < 1 Norprogesterone -1 injection than orally, but the other three steroids which were studied by both routes were all more active orally. The oral/subcutaneous ratio was - for -methoxy-1ß-cyanoethoxyoestra-l,,(1)-trien, 1 for -deoxyoestrone and 1 - for -deoxyoestradiol. Two neutral steroids, -hydroxymethyl-1a-methyl-a-androst--en-1ß-ol and 1-norprogesterone were both more active by injection than by gavage (Table ). DISCUSSION Including the three steroids which were used as primary standards, oestradiol- 1ß, mestranol and 1a-ethynyl-1ß-hydroxy-a-androst--en-1ß-ol, fifty steroids were studied for antifertility in the adult mated rat by injection
8 1 Fred A. Kind and Ralph I. Dorfman and/or oral routes. The first dose of the test compounds was on given the morning of pro-oestrus several hours before the beginning of the chain of events which leads to ovulation. It could be expected, therefore, that this method might interfere in the overall effect of fertility, including ovulation. Detailed study with two compounds, oestradiol-1ß and -methoxy-cyanethoxyoestra- 1,, (1)-trien showed, however, that transport of the zygote is involved. The results of this study will be published separately. It appears that this assay measured mainly the influence of steroids on ovum development and/or transport in the oviduct, or on nidation. Additional evidence that mechanisms other than ovulation inhibition may be involved is provided by our findings that there was no apparent correlation between the in this test and several other parameters of biological, i.e. the uterotrophic, anti-ovulatory measured in the adult oestrous rabbit (Kind & Dorfman, 1), anti-oestrogenic (Dorfman, Kind c Ringold, 11; Dorfman & Kind, 1), and inhibition Table 1 minimum effective daily doses (in mg) of subcutaneously injected steroids needed to produce significant biological effect s Oestradiol-1ß Mestranol Progesterone 1-Norprogesterone Norethindrone Chlormadinone acetate - > >4 > Oestrogenic Antifertility Antiovulatory Antioestrogenic 1 1 Parabiotic rat 1 1* 4* > * Administered orally. of gonadotrophin assayed in the parabiotic rat (Kind & Dorfman, ; Kind, Birch & Dorfman, ). This is more apparent from Table 1 which lists the minimum daily doses needed to produce a significant inhibitory effect. The amounts of ring A phenolic steroids, oestradiol-1ß and of mestranol needed for antifertility effect in the rat or the parabiotic rat were a hundred times less than those needed for anti-ovulatory effect in the rabbit. Compounds with progestational, namely progesterone, 1-norprogesterone, nor ethindrone and chlormadinone acetate were, on the other hand, considerably more active in the anti-ovulation test on the rabbit and only weakly active, if active at all in the antifertility test on the intact and parabiotic rat. Although it may not be permissible to compare different species and under varying conditions, these data indicate that in the present antifertility test on the rat, other factors besides inhibition of ovulation are involved. A clear dissociation of oestrogenicity, as measured by the uterotrophic assay and the present antifertility test, was observed for the tetrahydropyranyl ethers. This was true for the,1-di substituted ether of oestradiol-1ß where the separation factor (ratio of relative antifertility to oestrogenic ) was thirty-three, the three substituted ether of oestradiol-1( had a separation
9 Antifertility of steroids 11 factor of eight and finally that for 1a-ethynyl oestradiol-,1-bis tetrahydro pyranyl ether was -. This may indicate a relatively effective antifertility of these ethers with relatively low oestrogenicity. ACKNOWLEDGMENTS These assays were performed at the Endocrine Laboratories, Madison, Wisconsin, under the supervision of Dr Elva G. Shipley. REFERENCES Dorfman, R. I. & Kincl, F. A. (1) anti-estrogens. s, 1, 1. Dorfman, R. I., Kincl, F. A. & Ringold, H. J. (11) Anti-estrogen assay of neutral steroids adminis tered by gavage. Endocrinology,, 4. Everett, J. W., Sawyer, C. H. & Markee, J. E. () Neurogenic timing factor in control of the ovulatory discharge ofluteinizing hormone in the cyclic rat. Endocrinology, 44, 4. GuÉRiTÉE,. & Savini, E. C. () Involution gonadique réversible, chez le rat des deux sexes, pro duite par voie buccale, par un steroide dépourvu d'actions hormonales et anabolisantes: l'acétate de 1a-éthinyl -androstène 1ß-oI. Ann. Endocr. (Paris),, 44. Kincl, F.., Birch, A. J. & Dorfman, R. I. () Pituitary gonadotropic inhibitory of var ious steroids in ovariectomized-intact female in parabiosis. Proc. Soc. exp. Biol., N.T. 11, 4. Kincl, F. A. & Dorfman, R. I. (1) Anti-ovulatory of steroids in the adult oestrous rabbit. Acta endocr. (Kbh.), 4, Suppl.. Kincl, F. A. & Dorfman, R. I. () Pituitary gonadotrophin inhibitory action of neutral steroids. Acta endocr. (Kbh.), 4,. Rubin, B. L., Dorfman, A. S., Black, L. & Dorfman, R. I. (1) Bioassay of estrogens using the mouse uterine response. Endocrinology, 4, 4.
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