1-(2,4-Dichlorobenzyl)-1 H-lndazole-3-Carboxylic Acid (DICA), an Exfoliative Antispermatogenic Agent in the Rat
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1 Archives of Andrology Journl of Reproductive Systems ISSN: (Print) (Online) Journl homepge: 1-(2,4-Dichlorobenzyl)-1 H-lndzole-3-Crboxylic Acid (DICA), n Exfolitive Antispermtogenic Agent in the Rt T. J. Lobl To cite this rticle: T. J. Lobl (1979) 1-(2,4-Dichlorobenzyl)-1 H-lndzole-3-Crboxylic Acid (DICA), n Exfolitive Antispermtogenic Agent in the Rt, Archives of Andrology, 2:4, , DOI: / To link to this rticle: Published online: 09 Jul Submit your rticle to this journl Article views: 7 View relted rticles Citing rticles: 13 View citing rticles Full Terms & Conditions of ccess nd use cn be found t
2 1 -(2,4-Dichlorobenzyl)-1 H-lndzole-3-Crboxylic Acid (DICA), n Exfolitive Antispermtogenic Agent in the Rt T. J. LOBL The orl dministrtion of 50 mg DICNkg t nine weekly or four monthly intervls produced prtilly reversible infertility in mle rts s judged by the results of seril mting nd testiculr histology. Orl 500 mg DICNkg doses dministered t the sme intervls produced permnent sterility. Single orl doses of 50 or 500 mg DICMkg elevted men FSH concentrtions on dys 2, 3, nd 7 but did not ffect LH or testosterone. Men plsm concentrtion peked t 74 pghl 4 hr fter 50 mg/kg dose of uniformly tritited DICA; 24 hr lter, it hd declined rpidly to 5.5 &ml. The drug did not hve strong ffinity for ny tissue studied including the testis. DICA-induced exfolition of immture germ cells ws first observed 4 hr fter dministrtion nd led to significntly reduced testis weights by dy 2. Neither single doses of mg DICNkg nor five dily doses of mg DICMkg reduced seminl vesicle, ventrl prostte, or body weights of mle rts. Chronic weekly DICA dministrtion did reduce men seminl vesicle weight. These studies hve shown tht DICA is n effective, prtilly reversible ntifertility gent tht directly ffects the rt testis. Key Words: Sertoli cells; Mle fertility; Antispermtogenic chemicl; Mle contrception. INTRODUCTION The numerous heterocyclic ntifertility compounds found over the yers hve not been developed becuse of toxic side effects [l]. One of the most potent compounds in new clss of ntispermtogenic gents [3], 1-(2,4-dichlorobenzyl)-lH-indzole- 3-crboxylic cid (DICA, AF 1890; Fig. 1) is remrkbly nontoxic (orl LD,, > 2 g/kg body weight) nd free of serious side effects in the rt. This study describes its biologicl nd hormonl ctivities. MATERIALS AND METHODS Mture, mle Upjohn Sprgue-Dwley rts (5/group) received single subcutneous or orl doses of mg DICA/kg body weight, mg DICA/kg dily for 5 dys, or vehicle (0.25% methylcellulose). The nimls were utopsied on dy 10 nd their bodies, testes, seminl vesicles, nd ventrl prosttes were weighed. The testes nd one epididymidis from ech rt were fixed in Bouin s solution for histologicl exmintion. The other epididymidis ws minced in pool of sline nd exuded spermtozo were exmined microscopiclly (wet mount) for gross bnormlities. Received Jnury 30, From Fertility Reserch, Upjohn Compny, Klmzoo, Michign. Presented in prt t the First Pn Americn Congress of Andrology, Crcs, Venezuel, Mrch 13-16, Address reprint requests to: T. J. Lobl, Fertility Reserch, Upjohn Compny, Klmzoo, Michign Elsevier North Hollnd Inc., 1979, ARCHIVES OF ANDROLOGY, 2, (1979) I I$
3 354 T. J. Lob1 C02H / CI FIGURE 1. I-( 2,4-Dichlorobenzyl)-lH-indzole-3-crboxylic cid (DICA, AF 1890). In longitudinl study mle rts were given single orl dose of vehicle (IOigroup), 50 mg DICAIkg (5igroup). or 500 mg DICNkg (Sigroup). They were guillotined 0, 1.25, 2.5, 4, 8, 17, nd 168 hr lter. The blood ser were ssyed for LH, FSH, nd testosterone (T) 171. One testis from ech niml ws fixed in Bouin's solution for histologicl exmintion. Two fertility studies were conducted with proven fertile mles given weekly or monthly doses of DICA. The mle rts (IOigroup) given weekly doses received vehicle, 50 mgikg, or 500 mgikg once week for 9 consecutive weeks. Members of ech group were utopsied on dys 65 nd 245. The mle rts ( I2igroup) given monthly doses received vehicle, 50 mgikg or 500 mgikg once month for 4 consecutive months. Members of ech group were utopsied on dys 126 nd 277. The body, testis. seminl vesicle. nd ventrl prostte weights were determined. The nimls from both studies were mted serilly throughout the study. The femles were utopsied on dys of pregnncy nd the implnts were counted. One testis nd epididymis from ech rt ws preserved in Bouin's solution. The other epididymis ws minced in pool of sline, nd the spermtozo exuded were exmined microscopiclly in wet mount. Spermtozo from selected nimls were fixed in 2% gluterldehyde, wshed in buffer (phosphte, ph 7), suspended in gr. embedded in Epon. nd sectioned for nlysis by electron microscopy. Uniformly tritited DICA ws prepred by New Englnd Nucler Corportion using :'H,SO, exchnge procedure nd purified by silic gel chromtogrphy (HCCI,/MeOH/HCO,H, 95:5: 1); it ws identicl to nonrdioctive DICA by thin-lyer chromtogrphy nd ultrviolet spectrophotometry. Its nonexchngeble tritium content ws 1000 Ciimole. Fifty mgikg rdioctive DICA (20 pciil2.5 mg nonrdioctive DICA. cocrystllized) ws dministered to 28 mture mle rts (4igroup). The rts were utopsied , I. 2, 4, 8, nd 24 hr lter nd the testes, ventrl prostte, seminl vesicles, epididymides, kidneys, liver, drenl glnd, hert, lung, pituitry, brin. nd thigh muscle were weighed nd homogenized in wter (Brinkmn PI0 polytron). Blood drwn from the bdominl ort ws nlyzed s serum nd plsm. Aliquots (0.5 ml) of the homogentes were combusted in Pckrd Tri Crb Oxidizer. The tritium ws cptured in Monophse 40 (Pckrd). The smple dpm were individully corrected for quench with specilly prepred clibrtion curve. For direct :'H20 nlysis, frozen liquots in specil devices with in-line. individul dry ice trps to ctch the voltile portion of ech smple were ttched to lyophilizer. The wter in Diotol (Burdick & Jckson) ws counted in Pckrd scintilltion counter. RESULTS Subcutneous dministrtion of DICA ws not s effective s orl dministrtion in cusing reduced testiculr weights (Fie. 2). The reduced subcutneous potency did
4 Antifertility Effects of DICA in Mle Rts 355 not result from reduced drug vilbility (dministered s suspension) since there ws no injection site lump formtion. The minimum dose to reduce testis weight ws the sme with multiple, once dy orl doses nd single orl dose. There ws no effect on body, seminl vesicle, nd ventrl prostte weights. The testiculr weight reduction ws cused by reduced cellulrity in the germinl epithelium. In the longitudinl experiment the erliest significnt testis weight reduction occurred t 48 hr (Tble 1). Histologiclly, however, the erliest drug effects were observed 2-4 hr posttretment s n opening of spces in the tight rry of spermtids nd spermtocytes (Fig. 3A). By 8 hr exfolited cells were evident in the lumin of mny tubules (Fig. 3B) nd in the rete testis (Fig. 3C). At 24 hr there were mny prominent cler vcuoles djcent to nuclei in the epithelium (Fig. 3D). By dy 7 posttretment the germinl epithelium ws depleted nd the seminiferous tubules contined mny multinucleted gint cells (Fig. 4A). The exfolited immture germ cells were swept into the epididymis. The drug did not hve n effect on spermtozo since treted nimls were fertile for 2-3 wk posttretment. Serum FSH concentrtions were elevted on dys 2, 3, nd 7 following DICA tretment (Fig. 5). The 500 mg/kg dose of DICA cused in ddition trnsient elevtion of FSH t 4 nd 8 hr posttretment. This elevtion t 4-8 hr coincided with pek plsm nd testiculr drug concentr z 90 0 u Y 0 Y 80 c1 I- 2 Y C v) I- I Y 9 v) Y I e -4 Single orl dose Single subcutneous dose 5 orl doses I I DOSE (mg/kg) FIGURE 2. Reduction in men testiculr weights s percentge of body weight s result of single dose or consecutive dily doses of DICA nd the method of dministrtion (five rts per group). The sterisks indicte significnt difference from control: *p < 0.05, **p < 0.01.
5 356 T. J. Lob1 TABLE 1 Testiculr Weight Following Single Orl Dose of 50 or 500 mg DICNkg Body Weight DICA DOSE NO. OF TIME POST- MEAN (tse) TESTIS WT. AS (MG/KC) RATS TREATMENT PERCENTAGE OF BODY WT. x 10 Vehicle hr Vehicle hi so Vehicle hi S Vehicle 10 1 wk so S f t e f ? 0.42" b f " 7.94? 't f 1.1Y 5.31? 0.16" " Significntly different ( p < 0.01) from the corresponding control vlue. Significntly different ( p < 0.05) from the corresponding control vlue. tions (Fig. 6). The elevtion of FSH on dy 2 coincided with the time the testis hd become significntly reduced in weight nd the seminiferous epithelium first showed gint multinucleted cells. Concentrtions of LH nd T were unchnged. The rpid bsorption of drug prlleled the cute histologiclly observble events (Fig. 6). One-hlf hour fter n orl dose of 50 mglkg rdioctive DICA ws dministered significnt numbers of dpm were found in the plsm. Men plsm drug concentrtion peked t 74 puglml t 4 hr nd declined to 5.5 puglml t 24 hr (7.5% of pek vlue). Drug bsorption in the testis ws similr to tht in the plsm. Testiculr concentrtions peked t 8 hr posttretment nd fell rpidly to 12% of pek vlues by 24 hr. Chronic weekly or monthly therpy with DICA reduced the fertility of mle rts given 50 or 500 mg/kg (Fig. 7). All of the nimls given 50 or 500 mg/kg t weekly intervls becme infertile. Fertility ws regined in 2 of the 5 low-dose nimls live t the end of the study nd none of the high-dose nimls. Among the rts given 50 or 500 mg/kg t monthly intervls, 10 of the 12 low-dose nd ll of the high-dose nimls becme infertile; only 5 of the 8 low-dose nimls live t the end of the study nd none of the high-dose regined fertility. The two low-dose nimls tht hd not become infertile were given one nd two dditionl monthly 100 mg/kg doses, respectively, but they never becme infertile. The testes of the sterile nimls scrificed t the end of the experiment showed the sme weight reduction reltive to controls s those of the nimls killed t the end of the dosing period (Tbles 2 nd 3). The testiculr weight of nimls tht regined fertility still remined significntly reduced, but there ws prtil recovery of testiculr weight due to lrge number of spermtogenic tubules in the fertile testes (Fig. 4B). Other nimls still showed gint multinucleted cells in some tubules 6 mo fter the lst dose (Fig. 4C). The sterile nimls lmost invribly showed only shrunken spermtogenic seminiferous tubules contining minly Sertoli cells. The bsement membrne ws thickened nd contined mny prominent peritubulr cells (Fig. 4D). Some
6 Antifertility Effects of DlCA in Mle Rts 357 FIGURE 3. A. Seminiferous tubule 4 hr fter n orl dose of 50 mg DICA/kg. The usully closely positioned germ cells hve begun to move prt, opening prominent spces in the epithelium. Exfolition of some immture germinl cells hs lredy begun. B. Seminiferous tubule 8 hr fter n orl dose of 50 mg DICAlkg showing exfolited cells in the lumen. C. Rete testis 8 hr fter n orl dose of SO mg DICA/kg showing some immture germ cells. D. Seminiferous epithelil cells 17 hr fter n orl dose of 500 mg DICA/kg showing mny prominent cytoplsmic vcuoles with enclosed nuclei. The epithelil cells re disorgnized nd depleted nd the lumin re filled with cellulr mteril.
7 358 T. J. Lob1 FIGIlRE 4. A. One week fter single orl dose of 53 mg DICAIkg the germinl epithelium contins mny multinucleted cells nd is reduced in cellulrity. B. Six months fter the lst of 4 monthly orl doses of 50 mg DICAikg the testis of rt with returned fertility shows numerous spermtogenic tubules. C. Even 6 mo fter DICA tretment (s in Fig. 4C) some seminiferous tubules still produce bnorml nd multinucleted cells. D. Seminiferous tubules fter 9 Heekly orl doses of 500 mg DICNkg show Sertoli cell only tubules, mny lumin contining bsophillic clcium deposits, nd thickened wlls. No niml given 500 mglkg recovered fertility.
8 Antifertility Effects of DICA in Mle Rts 359 tubules were prtilly occluded with bsophillic substnce (Fig. 4D) tht ws positive for clcium when stined with von Koss s stin. Two treted, sterile nimls showed spermtozo in the vginl lvge in five nd six mtings over 4 mo without producing single pregnncy. Following necropsy, the epididyml spermtozo were exmined by light nd electron microscopy. No gross morphologicl bnormlities were seen. The ultrstructure of the rt sperm tils were norml, unlike spermtozo from monkeys treted with DICA [9]. Prominent hlo cells or epididyml epithelil vcuoles were lso noted in DICA-treted rts. The epididyml lumin contined pink morphous mteril mixed with sperm nd debris. No strong ffinity for rdioctive drug ws shown by the testis or ny tissue studied. The dpdg reflected more the vsculrity of the orgn thn tissue ffinity. There ws no evidence tht metbolism of tritited DICA produced 3H,0 since combustion of wet nd dry blood plsm differed less thn 6% nd there ws 0 cpm in the lyophilized wter from plsm. DISCUSSION High doses of DICA irreversibly sterilize the mle rt nd lower doses provide prtilly reversible inhibition of fertility. The drug ppers to be non-tissue-specific, f 50 mg/kg (N=5) $ 500 mg/kg (N=5) Control (95% Confidence Limits) (N=10) W%F--- TIME IN HOURS FIGURE 5. Men (?SE) plsm concentrtion of FSH following single orl doses of DICA, expressed s nnogrms per milliliter of NIH reference preprtion RP1. The sterisks indicte significnt difference from control: *p < 0.05, **p < 0.01, ***p <
9 360 T. J. Lob \ - DPM/ml plsm v) n U ra 0 I I- - z n E TIME IN HOURS AFTER DOSING FIGURE 6. Men (rse) bsorption of tritited DICA into the blood plsm nd testes of rts fter single orl dose of 50 mgikg, four rts per group. The ordinte is expressed in thousnds of dpm. exfoliting, ntispermtogenic gent. Other exfoliting compounds hve been described in the literture [6, 101. The minimum effective contrceptive dose ppers to be t lest 50 mgikg given monthly or less thn 50 mgikg given weekly. This finding confirms the dt of Coulston et l., who reported tht 50 mg/kg/dy for 5 dys resulted in reduced testiculr weights in rts [4]. The minimum orl ntispermtogenic dose (MED) of DICA hs been reported to be mg/kg [3, 111 with testiculr drug concentrtion of 4 pgig tissue t the MED [2]. The serum nd testiculr bsorption profile ws similr to tht seen by Ctnese et ]. [2] but peked lter. This ws prtilly due to Ixge vritions in bsorption rte from rt to rt tht skewed the men
10 Antifertility Effects of DICA in Mle Rts r A WEEK OF STUDY \ \ \ I WEEK OF STUDY FIGURE 7. Men litter size (per number of dms in group) of dms following mting with DICAtreted sires versus week of the study. A. dministered monthly for 4 mo. DICA dministered weekly for 9 wk. B. DICA vlues to longer times. Further comprison is complicted by differences in methods of mesurement, dosge, nd smple preprtion, however, the generl profile is similr. DICA did not concentrte in reproductive tissue nd disppered rpidly from ll tissues; since sterility persisted long fter DICA dministrtion hd cesed, its ntifertility effects do not depend on the continuing presence of the drug itself. The lck of cute hormonl chnges nd the rpid exfolition of germinl cells suggest drug effects tht specificlly lter the Sertoli-germ cell ttchment, the Sertoli cell spermition mechnism or other relted events. These dt, together with the reports of ltertions in ndrogen-binding protein (ABP) concentrtions in DICA-treted nimls
11 362 T. J. Lob1 TABLE 2 Effects of Weekly Orl Doses of DICA on the Body, Testis, Seminl Vesicle, nd Ventrl Prostte of Mture Rts (Men 2 SE1 Orgn Wt. s Percentge of Body Wt. DICA DOSE DAY OF EXPT. TESTES SEM. VES. v. PROST. GROUP ( MGIKG) AT NECROPSY (WT. X 10) (WT. X 10') (WT. X 10') Control Vehicle t t Low dose t 0.77" 6.23? 0.32b t 0.90 High dose " 6.18? 0.12b 15.84? 0.62 Control Vehicle t ? 0.98 Low dose _c 0.51" 5.55 t ? 1.05 Fertile' t 0.44b Sterile" " High dose t 0.28" 6.08 t t 0.85 Two nimls in the high-dose group died during the study. There were five rts per group nd ech group received nine doses. (' Significntly different (p < 0.001) from the corresponding control vlue. ') Significntly different (p < 0.05) from the corresponding control vlue. ' Two rts. Three rts. [SJ, support further the suggestion tht DICA cts on the Sertoli cell. Similr conclusions were drwn by DeMrtino et l. [5] following light nd electron microscopy study of AF 1312/TS, structurlly similr compound, in rts. Although this study did not show depression in T concentrtions, nother study [S] did show cute depressions following single 50, 250, or 500 mg/kg orl dose of TABLE 3 Effects of Monthly Orl Doses of DICA on the Body, Testis, Seminl Vesicle, nd Ventrl Prostte of Mture Rts (Men t SE) ORGAN WT. AS PERCENTAGE OF BODY WT. DICA DOSE DAY OF EXPT. TESTES SEM. VES. v. PROST. GROUP" (MG/KG) AT NECROPSY (WT. X 10) (WT. X lo') (WT. X 10') Control (4) Lou dose (3) High dose (4) Control (7) Low dose (8) Fertile (5) Sterile (3) High dose (7) Vehicle Vehicle t t t b 6.65 t t t 0.39? _c _t t c 0.56' t O.6Od t 0.20" ' One niml ech from the low- nd high-dose groups died during the study. Dt is missing for one control niml. Ech group received four doses. Number of nimls per group is in prentheses. '' Significntly different (p < 0.01) from the corresponding control vlue. Significntly different (p < 0.001) from the corresponding control vlue. " Significntly different (p < 0.05) from the corresponding control vlue.
12 Antifertility Effects of DICA in Mle Rts 363 DICA. Concurrent dministrtion of testosterone propionte (500 pg/rt/dy for 10 dys) following single 50 mg/kg orl dose of DICA did not inhibit its ntispermtogenic effects. This suggests tht the ntispermtogenic ctivity of DICA is not secondry to ndrogen suppression. The serum T concentrtion inconsistencies seem to reflect niml vribility nd my not be biologiclly importnt. No effect on libido ws observed insofr s successful mtings occurred throughout the study. The mechnism of ction of this drug is still uncler. The drug does not hve posttesticulr ctivity, since femles were fertile s long s spermtozo were observed in the vginl lvge. DICA is ctive on the Sertoli cell becuse it induces exfolition nd chnges in ndrogen-binding protein concentrtions. There is no evidence of direct DICA toxicity on germ cells but some nimls become sterile. The possible explntions for this result include the following: () the Sertoli cell tight junction my be dmged nd thereby enble the spermtogoni to escpe the bsl comprtment; (b) the drugtreted Sertoli cell my not be ble to support the development of germ cells; nd (c) since Sertoli cells do not hve n ctive dult renewl mechnism, seriously drugdmged cells cnnot support spermtogenesis. Additionl studies re needed to define the mechnism of drug ction. Acknowledgments: We thnk D. W. Frnk for determining the cute LDSo in rts, B. Silvestrini of the F. Angelini Reserch Institute, Rome, for the smple of DICA nd for experimentl informtion, A. F. Prlow;the NIH, nd the NIAMDD for gift of the rt LH nd FSH rdioimmunossy kits, H. D. Hfs for gift of ntitestosterone ntiser [7], J. Mthews for the TEM studies of epididyml sperm. nd S. E. Porteus for some technicl ssistnce. REFERENCES 1. Bennett JB (1974): Chemicl Contrception. New York: Columbi University Press, pp Ctnese B, Cioli V, DeMrtino C, et l (1978): A comprtive study of serum nd testiculr concentrtions of AF1312/TS (or 1-[(4-chlorophen yl)methyl]- 1H-indzole-3-crboxylic cid) nd diclondzolic cid (or 1-[(2,4-dichlorophenyl)- methyl]- 1H-indzole-3-crboxylic cid) in rts. Phrmcol Res Commun 10: Corsi G, Plzzo G, Germni C, et l (1976): I-Hlobenzyl-lH-indzole-3-crboxylic cids. A new clss of ntispermtogenic gents. J Med Chem 19: Coulston F, Doughterty WJ, LeFevre R, et l (1975): Reversible inhibition of spermtogenesis in rts nd monkeys with new clss of indzolcrboxylic cids. Exp Mol Pthol 23: DeMrtino C, Stefnini M, Agrestini A, et l (1975): Antispermtogenic ctivity of l-p-chlorobenzyl- 1H-indzol-3-crboxylic cid (AF13 12fTS) in rts 111. A light nd electron microscopic study fter single orl doses. Exp Mol Pthol 23: Ericsson RJ (1975): Chemosterilnts. In Scirr JJ, Mrklnd C, Speidel JJ (eds): Control of Mle Fertility. Hgerstown, Md: Hrper & Row, pp Kiser TD, Milve RA, Hfs HD, et l (1978): Comprison of testosterone nd ndrostenedione secretion in bulls given prostglndin F, or luteinizing hormone. J Anim Sci 46: Lob1 TJ, Gunslus GL, Musto N, et l (1979): Modultion of testiculr, epididyml, nd serum ndrogen binding protein (ABP) levels by three heterocyclic exfoliting ntispermtogenic gents. Proc. fourth Annul Meeting, Amer. SOC. Andrology, Houston, TX, USA, Mrch 13-16, Lob1 TJ, Mthews J (1978): Effect of I-(2,4- dichlorobenzyl)-indzole-3-crboxylic cid on sperm tils in rhesus monkeys. J Reprod Fertil 52: Lob1 TJ, Porteus SE (1977): Antispermtogenic effects of 5-minoindzole in rts. J Reprod Fertil 50: Silvestrini B, DeMrtino C, Cioli V, et l(l977): Antispermtogenic ctivity of diclondzolic cid in rts. Pper presented t the Conference on Recent Progress in Andrology, L'Aquil, Itly, April (Proceedings in press)
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