Twenty nonpregnant cycling Tsigai ewes in the breeding season were treated for synchronization of estrus using intravaginal progestagen sponges (medroxyprogesterone-acetate, MAP) followed by an intramuscular injection of 350-400 IU of pregnant mare serum gonadotrophin (PMSG). A control group of ewes was formed from 20 animals in the natural estrous cycle. Hormonal status was investigated by determination of plasma triiodothyronine (T3) and thyroxine (T4) concentrations using radioimmunoassay (RIA). Samples of jugular venous plasma were collected on the day of sponge insertion (P), the day of estrus (0. day), 7, 14 and 18 days after estrus. Plasma T3 levels in the control group of ewes were significantly lower compared to the ewes after synchronization of estrus, except the level of T3 on day 18 after estrus. Plasma T4 level was not significantly different in the treated and control ewes, except on day 18 after estrus.Ispitivanja hormonalnog statusa ovaca nakon sinhronizacije estrusa u sezoni parenja vršena su određivanjem nivoa T3 (trijodtironina) i T4 (tiroksina) u krvnoj plazmi radioimunološkom (RIA) metodom. Uzorci krvne plazme su prikupljani na dan stavljanja sunđera (P), dan estrusa (0. dan), 7, 14. i 18. dana od estrusa. Nivo T3 u krvnoj plazmi kontrolne grupe ovaca u prirodnom estrusnom ciklusu je značajno niži u odnosu na tretirane životinje, osim nivoa T3 18. dana posle estrusa. Nivo T4 nije se značajno razlikovao između tretiranih ovaca i kontrolne grupe, izuzev 18 dana ispitivanja, kada je ustanovljen značajno veći nivo kod tretiranih gravidnih ovaca

Gvozdić, Dragan

Stojić, Velibor

Acta veterinaria

English

Veterinar - Repository of the Faculty of Veterinary Medicine

Acta Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001.UDK 619:612.444:636.32/38PLASMA THYROXINE AND TRIIODOTHYRONINE LEVELS AFTER SYNCHRONIZATION OFESTRUS IN THE BREEDING SEASON IN EWES*GVOZDIC D. and *STOJIC V.Faculty of Veterinary Medicine, Belgrade, Bul. JNA 18. Yugoslavia(Received 23. November 2000)Twenty nonpregnant cycling Tsigai ewes in the breeding seasonwere treated for synchronization of estrus using intravaginalprogestagen sponges (medroxyprogesterone-acetate, MAP) followedby an intramuscular injection of 350-400 IU of pregnant mare serumgonadotrophin (PMSG). A control group of ewes was formed from 20animals in the natural estrous cycle. Hormonal status was investigatedby determination of plasma triiodothyronine (T3) and thyroxine (T4)concentrations using radioimmunoassay (RIA). Samples of jugularvenous plasma were collected on the day of sponge insertion (P), theday of estrus (0. day), 7, 14 and 18 days after estrus. Plasma T31evelsin the control group of ewes were significantly lower compared to theewes after synchronization of estrus. except the level of T3 on day 18after estrus. Plasma T4 level was not significantly different in the treatedand control ewes, except on day 18 after estrus.Key words : estrous season, ewes, progestagen, thyroxine,triiodothyronine. ,INTRODUCTIONThe thyroid gland plays an important role in the seasonality of reproductionin ewes. Many seasonally breeding birds and mammals require an intact thyroidgland for a normal end to the reproductive period (Jallageas et al., 1979; Follettet al., 1985; Weiselthier et al., 1972). The end of the breeding season in ewesseems to be the manifestation of an endogenous rhythm that is synchronized byenvironmental changes. At this time the rhythm expresses itself at theneuroendocrine level as an increased responsiveness of the hypothalamus to thenegative feedback effect of estradiol on gonadotropin secretion (Karsch et al.,1989).The thyroid gland is necessary for the transition from the breeding seasonto anestrus in the ewe, but the importance of the seasonal changes in thyroidhormone secretion in this process remains to be investigated. In seasonalbreeding sheep thyroidectomy does not alter the onset of the estrous cycle, butabolishes the transition to anestrus at the end of the breeding season (Nicholls etal., 1988). Thyroxine (T4) replacement reverses the effect of thyroidectomy ontransition to anestrus (Webster et al., 1991a), suggesting that this treatment10 Acta Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001.D. Gvozdi6 et. al. Plasma thyroxine and triiodothyronine levels after synchronization of estrus___. .:..:.in:..:.:.the breeding season in ewesprevents the seasonal shift in potency of negative feedback of estradiol onluteinizing hormone (LH). Thyroxine (T4) treatment during the breeding seasoncan advance anestrus and thus shorten the duration of the breeding season(OCallaghan et al., 1993). Secretion of T4 after the onset of reproductive activityis required for the endogenously generated change in the neuroendocrine axisthat leads to the intensified estradiol negative feedback and an end to the breedinqseason (Dahl et al., 1995). The aim of the present study was to investigate plasmathyroxine (T4) and triiodthyronine (T3) levels in ewes of the Tsigai breed aftersynchronization of estrus in the breeding season.MATERIAL AND METHODSThe hormonal status of ewes after synchronization of estrus in the breedingseason was investigated by determination of plasma T3 and T4 concentrationsusing commercial radioimmunoassay (RIA) kits (INEP-Zemun). During thebreeding season (October) estrus was synchronized by progestagen treatment(intravaginal sponges impregnated with 60 mg of MAP/14 days) followed by350-400 of PMSGjewe (20 ewes). A control group of ewes during the breedingseason (August/September) was formed with 20 cycling ewes. At the time ofestrus all ewes were naturally mated to rams of known fertility. Samples of jugularvenous plasma were collected on the day of sponge insertion (P), on the day ofestrus (0. day), 7, 14 and 18 days after estrus. Differences in plasma hormonelevels between treated and control ewes were tested using Students t-test,RESULTSPlasma T3 levels in the treated group of nonpregnant and pregnant ewesafter the synchronization of estrus and the control group of cycling ewes arepresented in Table 1.Table 1. Plasma T3 levels (X ±SD nmol/l.) in the treated group of nonpregnant andpregnant eNes after synchronization of estrus and in the control group of cycling f:.-wesTime of treated control treated control statisticallyinvestigation (I) (II) (III) (IV) significant(days) (nonpreg.) (nonpreg.) (preg.) (preg.) differencenumber of 9 13 11 7eNesP. 2.37 :±D.58 - 3.02 :±D.67 - 1:111*O. 3.69 ±1.13 2.68 :±D.53 3.95 ±1.30 2.36 :±DA7 1:1I*,III:IV**7. 3.85 :±D.55 2.64 :±DA6 4.13±1.03 2.66 :±D.62 1:11**, 1I1:IV**14. 4.18 :±D.97 2.81 :±D.55 4.19+1.39 2.92 :±D.31 1:11**, III:IV*18. 2.86 :±D.60 2.37:±D.57 2.69 :±D.55 3.24 :±D.36 II:IV**, 1I1:IV*legend: * - p<0.05; ** - p<0.01; P. - day of sponge insertion in the treated eNesActa Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001. 11D. Gvozdi6 et. al, Plasma thyroxine and triiodothyronine levels after synchronization of estrusin the breeding season in ew:....e:.;:s'---- _The plasma T3 levels presented in Table 1.show that there are no differencesbetween pregnant and nonpregnant treated ewes, except on the day of spongeinsertion (3.02 ± 0.6"7 : 2.37 ± 0.58 nmol/L, p<O.05). In the control group of ewesthere were also no statistically significant differences between pregnant andnonpregnant ewes except on day 18. after estrus (3.02 ± 0.67 : 2.37 ± 0.58nmol/L, p<0.05). Data presented in Table 1. also show that plasma levels OfT3 inthe treated ewes are significantly higher on days 0, 7, and 14.Plasma T4 levels in the treated group of nonpregnant and pregnant ewesafter the synchronization of estrus, and in the control group of cycling ewes arepresented in Table 2.Table 2. Plasma T4 levels (X ±SD nrnol/l.) in the treated group of nonpregnant and pregnantONes after synchronization of estrus and in the control group of cycling ONes.Time or treated control treated control statisticallylnvestiqatlon (I) (II) (III) (IV) significant(days) (nonpreg.) (nonpreg.) (preg.) (preg.) dITferencenumber of 9 13 11 7ONesP. 69.58 :!£.62 - 74.83 :t19.94 - -O. 86.93 ±19.28 75.91 :t10.04 88.57 :t15.71 84.79 :!:B.30 -7. 101.3J :t12.54 91.5±12.32 103.54 :t10.02 104.28 :t5.03 II:IV*14. 104.94 ±13.01 100.49±82 101.68:t10A6 100.96 :t10.37 -18. 89.26 :!:B. 15 87.9 :t15.79 103.94 :t10.69 90.71 :!:B.27 1:111**,III:IV*I~Jend : * - p<0.05; ** - p<O.01; P. 0 day of sponge insertion in treated ONesThe results presented in Table 2. show that there were no significantdifferences in plasma T4 levels between the treated and control group of ewes,except for the T4 level on day 18, when it was significantly higher in the treatedpregnant ewes compared to groups I and IV. Those results could be explainedby a reversion of the possible inhibitory effect of progestagen treatment on thyroidhormone secretion in ewes during the anoestrous season (Gvozdi6 et et., 1997).Exact places where this effect is mediated are still to be identified. There were nosignificant differences between plasma levels of the thyroid hormones in pregnantand nonpregnant animals in both groups of ewes. Only the mean plasma T4 levelon day 18 in the treated pregnant ewes was higher compared to the controlpregnant ewes (1 03.94±1 0.69: 90.71 ±8.27 nmol/L, p.05).DISCUSSIONThe exact mechanism of the involvement of the thyroid gland in theregulation of the seasonality of reproduction in ewes remains to be clarified, butthe investigation of Webster et al., (1991 a) revealed an annual cycle of serum T412 Acta Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001.D. Gvozdi6 et. al. Plasma thyroxine and triiodothyronine levels after synchronization of estrusin the breeding season in eweslevels in ewes. Values of serum T4 (X±SEM) reached a peak in winter (latebreeding season) and a nadir in summer (late anestrus). During the low stage ofthe cycle the level of T4 in the serum of the control group of ewes was 39 ± 1.6ng/mL (50.19 ± 2.06 nrnol/l.), and the maximum level during the high stage was52 ± 2.2 ng/mL (66.92 ± 2.83 nmol/L). OCallaghan et al., (1993) found even lowervalues for serum thyroxine in rams during the breeding season (33.4 ± 4 ng/mL:42.47 ± 5.12 nmol/t), Bekeova et al. (1994) also observed lower serum T3 andT4 levels in control ewes during the postpartum period, but the experiment wasconducted during the anestrous season. Our results show that the values ofplasma T4 in Tsigai ewes after synchronization of estrus during the breedingseason are comparable to the control group, while plasma Ts levels are higher onmost days of investigation (Table 1).The end of the breeding season in the ewe results from the expression ofan endogenous rhythm that is synchronized by the annual photoperiodic cycle(Karsch et al., 1989). This seasonal change in reproduction in ewes is based onthe sensitivity of the hypothalamo-hypophyseal axis to negative feedback ofestradiol (Legan et al., 1977). Secretion ofT4 after the onset of reproductive activityis required for the endogenously generated change in neuroendocrine axis thatleads to an intensified negative feedback and an end of the breeding season(Webster et et., 1991a). Thyroidectomy prevented this endogenously driventransition to anestrus and allowed estrous cyclicity to continue all year-round(Nicholls et et., 1988). On the other hand, supplementary thyroxine during thebreeding season can advance anestrus and thus shorten the duration of thebreeding season (OCallaghan et el., 1993). One possible explanation of our resultscould be based on the hypothesis that progestagen treatment during the breedingseason can have a stimulatory effect on thyroid hormone secretion, or at least itno longer has an inhibitory effect on thyroid gland function (Gvozdi6 et al., 1997).It is necessary to point out that the levels of T3 in the jugular venous plasmain the control group of ewes of Tsigai breed were lower at most investigated timescompared to the nonpregnant and pregnant synchronized ewes.The proposed inhibitory effect of progestagen treatment on thyroid hormonesecretion is possibly connected to the central inhibitory influence of GABA on TSHsecretion, but further investigation is necessary to determine the significance ofthe registered phenomenon, as well as the exact sites of its realisation.It is interesting to speculate that progestagen treatment may have aninhibitory effect on the thyroid hormone secretion during the subsequent estrouscycle. If we start from this speculation, another question is the exact site of theprogestagen effect on thyroid hormone secretion? Possible places were theinfluence of progestagen could be mediated are the hypothalamus or the pituitarygland. In monkeys and rats progesterone probably acts in the mediobasalhypothalamus and somewhere in the brain to block LH secretion, while thestimulatory effects of progesterone on the LH surge may well occur at thehypophyseal level in both species (Goodman and Knobil, 1981). The investigationof Webster et al., (1991b) failed to connect high frequency pulses of GnRH andLH in thyroidectomized ewes with changes in total number, distribution and lightmicroscopic morphology of GnRH neurons in the hypothalamus and preopticarea. The investigation of the role of central neurotransmiters in the regulation ofthyrotropin (TSH) secretion revealed that the central dopaminergic system has aninhibitory influence on TSH secretion in humans and rats (Krulich, 1982). Vijayanand McCann (1978) reported that intraventricular administration ofActa Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001. 13D. Gvozdi6 et. al. Plasma thyroxine and triiodothyronine levels after synchronization of estrusin the breeding season in ewesgama-aminobutyric (GABA) lowered basal TSH levels possibly via activation ofthe dopaminergic system because the effect could be abolished by pretreatmentof the rats with a dopamine receptor blocker. y-Aminobutyric acid is generallyrecognized as the major inhibitory neurotransmitter in the mature mammalianbrain. The investigation of Han et al., (1995) established that a progesteronemetabolite in rat hippocampal neurons potentiated GABA-mediated chloridecurrents, but Hales et et., (1994) found that GABA has excitatory actions onGnRH-secreting imortalized hypothalamic neurons. Our present work as well asthe previous one (Gvozdic, et al., 1997) suggest that the proposed inhibitory effectof progestagen tretment on thyroid hormone secretion may be connected to thecentral inhibitory influence of GABA on thyroid stimulating hormone.REFERENCES1. Dahl GE, Evans NP, Thrun LA, Karsch FJ, 1995, Thyroxine is permisive to seasonal transitions inreproductive neuroendocrine activity in the ewe, Bioi Reprod, 52(3), 690-962. Follett BK, Nicholls TJ 1985, Influences of thyroidectomy and thyroxine replacement onphoperiodically controled reproduction in quail, J Endocrinol, 107, 211-223. Gvoziiic 0, Stoji6 V 1997, Plasma thyroxine and triiodthyronine levels after induction andsynchronization of estrus in the anoestrus season in ewes, Acta Veterinaria, 5-6, 271-76.4. Goodmann RL, Knobil E 1981, The sites of action of ovarian steroids in the regulation of LH secretion,Neuroendocrinol, 32, 57-63.5. Hetes GT, Sanderson MJ, Charles AC 1994. GABA has excitatory actions on GnRH-secretingimortalized hypothalamic (GT1-7) neurons. Neuroendocrinol, 59, 297-308.6. Hen MC, Hu YF, Zorumski CF, Covey OF 1995, Neurosteroid analogues.3. The synthesis andelectrophysiological evaluation of benz(e)indene congeners of neuroactive steroids having the5 beta configuration, J Med Chem, 38, 22, 4548-56.7. Jallageas M, Assenmacher I 1979, Further evidence for reciprocal interactions between the theannual sexual and thyroid cycles in male Peking ducks, Gen Comp Endocrinol, 37: 44-51.8. Karsch FJ, Robinson JE, Woodfill CJI, Brown MB '1989, Circannual cycles of luteinizing hormoneand prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: evidencefor an endogenous reproductive rhythm, Bioi Reprod, 41, 1034-46.9. Krulich L 1982, Neurotransmiter control of thyrotropin secretion. Neuroendocrinol. 35, 139-47.10. Legan SJ, Karsch FJ, and Foster DL 1977, The endocrine control of seasonal reproductive functionin the ewe: a marked change in response to the negative feeback action of estradiol onluteinizing hormone secretion, Endocrinol, 101. 818-24.11. Nicholls TJ, Goldsmith AR, Dawson A 1988, Photorefractoriness in birds and comparison withmammals, Physiol Rev, 68, 133-76.12. OCallaghan 0, Wendling A, Karsch FJ, Roche JF 1993, Effect of exogenous thyroxine on timing ofseasonal reproductive transmision in ewes, Bioi Reprod, 49,2, 311-15.13. Vijayan E, McCann SM 1978, Effects of intraventricular injection of y-aminobutyric acid (GABA) onplasma growth hormone and thyrotropin in conscious ovariectomized rats, Endocrinol, 103,1888-93.14. Webster RJ, Moenter SM, Woodfill CJI, Karsch FJ 1991a, Role of the thyroid gland in seasonalreproduction. II. Thyroxine allows a season-specific suppression of gonadotropin secretion insheep, Endocrinol, 129, 176-183.15. Webster JR, Moenter SM, Barrell CJ, L.ehmanMN, Karsch FJ 1991b, Role of the thyroid gland inseasonal reproduction. III. Thyreoidectomy blocks seasonal suppression ofgonadotrophin-releasing hormone secretion in sheep, Endocrino/, 129,3, 1635-43.16. Weiselthier M, Van Tienhoven A 1972, The effect of thyroidectomy on testicular size and onphoto refractory period in the starling (StUf/JUS vulgaris L.), J Exp Zool, 179,331-38.14 Acta Veterinaria (Beograd), Vol. 51. No.1, 9-14, 2001.D. Gvozdi6 et. al. Plasma thyroxine and triiodothyronine levels after synchronization of estrusin the breeding season in ewesKONCENTRACIJA TIROKSINA I TRIJODTIRONINA U KRVNOJ PLAZMI OVACA POSLESINHRONIZACIJE ESTRUSA U SEZONI PARENJAGVOZDIC D i STOJIC VSADRZAJIspitivanja hormonalnog statusa ovaca nakon sinhronizacije estrusa usezoni parenja vrsena su odredivanjem nivoa T3 (trijodtironina) i T4 (tiroksina) ukrvnoj plazmi radiolmunoloskorn (RIA) metodom. Uzorci krvne plazme suprikupljani na dan stavljanja sundera (P), dan estrusa (0. dan), 7,14. i 18. danaod estrusa. Nivo T3 U krvnoj plazmi kontrolne grupe ovaca u prirodnom estrusnomciklusu je znacajno nizi u odnosu na tretirane zivottn]e, osim nivoa T3 18. danaposle estrusa. Nivo T4 nije se znacajno razlikovao izmedu tretiranih ovaca ikontrolne grupe, izuzev 18 dana ispitivanja, kadaje ustanovljen znacajno veci nivokod tretiranih gravidnih ovaca.

Koncentracija tiroksina i trijodtironina u krvnoj plazmi ovaca posle sinhronizacije estrusa u sezoni parenja

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Koncentracija tiroksina i trijodtironina u krvnoj plazmi ovaca posle sinhronizacije estrusa u sezoni parenja

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