Quantitative Histomorphometry of Pre-ovulatory Follicles and Uterine Glands of Ongole-grade Heifer in Response to the Low Doses of PMSG Administration
Abstract
Injection of female mammalian animals with gonadotropin prior to mating using superovulation dose increases estradiol 17beta (E2) synthesis and secretion and improves the growth and development of the uterus to support prenatal growth with the side effect of increasing litter size. This experiment was designed to study the effects of low doses of PMSG injection in heifers on the growth of granulose cells (GC) of pre-ovulatory follicles, E2 synthesis, and uterine glands growth and development. Nine Ongole-grade heifers were divided into three groups of doses of PMSG injection, i.e., 0 IU/kg BW, 0.5 IU/kg BW, and 1.0 IU/kg BW. The injection of pregnant mare serum gonadotropin (PMSG) was conducted at the early stage of the second follicle wave. Blood samples were collected at estrus (day 0) to measure plasma E2 concentrations. The ovary and uterus were collected for histological observation after slaughtering the animal. The results showed that non-superovulation doses of PMSG injections at the second follicle wave significantly increased the growth of GC that eventually produced a significantly higher plasma E2 concentration by 39.47% and 113.57%, in heifers receiving 0.5 IU/kg BW and 1.0 IU/kg BW (p<0.05), respectively. The increase in E2 synthesis and secretion significantly stimulated the growth and development of uterine glands (p<0.05), which was reflected in the improved measures of uterine glands. In conclusion, injections of heifers with low doses of PMSG at the second follicle wave could increase the growth of GC to produce a higher secretion of E2 that eventually improves the growth and development of uterine glands in the endometrium without the risk of multiple calving.
References
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Fowden A. L. & A. J. Forhead. 2015. Glucocorticoids as regulatory signals during intrauterine development. Exp. Physiol. 100:1477-87. https://doi.org/10.1113/EP085212
Fowden A. L, O. A. Valenzuela, O. R. Vaughan, J. K. Jellyman, & A. J. Forhead. 2016. Glucocorticoid programming of intrauterine development. Domest. Anim. Endocrinol. 56:S121-32. https://doi.org/10.1016/j.domaniend.2016.02.014
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Gonella-Diaza, A. M., F. S. Mesquita, K. R. da Silva, J. C. de Carvalho Balieiro, N. P. dos Santos, G. Pugliesi, S. R. de Fransisco, & M. Binelli. 2017. Sex steroid modulate morphological and functional features of the bovine oviduct. Cell. Tissue Res. 370:319-333. https://doi.org/10.1007/s00441-017-2666-0
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Habibizad, J., M. Towhidi, & F. Samadian. 2020. Determining the optimal dose of eCG to improve the reproductive performance of Lake-Ghashghaei ewes in the breeding season. Journal Animal Environment 12:33-40.
Jitjumnong, J., P. Sudwan, R. Maktrirat, P. Yama, W. Pirokad, U. Warittha, & T. Moonmanee. 2019. Additional growth of dominant follicle during synchronized ovulatory cycle affects ovulatory follicle size, corpus luteum parameters, and progesterone level in northern Thai Native Cattle. Science & Technology Asia 24:83-93.
Murphy, B. D. 2012. Equine chorionic gonadotropin: An enigmatic but essential tool. Anim. Reprod. 9:223-230.
Nugroho, P., K. G. Wiryawan, D. A. Astuti, & W. Manalu. 2021. Stimulation of follicle growth and development during estrus in Ettawa Grade does fed a flushing supplement of different polyunsaturated fatty acids. Vet. World. 14:11–22. https://doi.org/10.14202/vetworld.2021.11-22
Núñez-Olivera, R., F. Cuadro, D. Bosolasco, V. de Brun, J. de la Mata, C. Brochado, A. Meikle, G. A. Bó, & A. Menchaca. 2020. Effect of equine chorionic gonadotropin (eCG) administration and proestrus length on ovarian response, uterine functionality and pregnancy rate in beef heifers inseminated at a fixed-time. Theriogenology 151:16-27. https://doi.org/10.1016/j.theriogenology.2020.03.031
Perry, G. A., R. A. Cushman, B. I. Perry, A. K. Schiefelbein, E. J. Northrop, J. J. Rich, & S. D. Perkins. 2021. Role of preovulatory concentrations of E2 on timing of conception and regulation of the uterine environment in beef cattle. Syst. Biol. Reprod. Med. 66:12-25. https://doi.org/10.1080/19396368.2019.1695979
Pulley, S. L., L. D. Wallace, H. L. Jr. Mellison, & J. S. Stevenson. 2013. Ovarian characteristics, serum concentration of progesterone and estradiol, and fertility in lactating dairy cows in response to equine chorionic gonadotropin. Theriogenology 79:127-134. https://doi.org/10.1016/j.theriogenology.2012.09.017
Putro, K. B., Amrozi, A. Winarto, A. Boediono, & W. Manalu. 2020. Pre-ovulatory follicle of crossed ongole heifer stimulated by using low dose of PMSG. Acta Vet. Indones. 8:1-7. https://doi.org/10.29244/avi.8.3.1-7
Regan, S. L. P., P. G. Knight, J. L. Yovich, Y. Leung, F. Arfuso, & A. Dharmarajan. 2018. Granulosa cell apoptosis in the ovarian follicle – a changing view. Front. Endocrinol. 9:1-10. https://doi.org/10.3389/fendo.2018.00061
Reynolds, L. P., P. P. Borowicz, J. S. Caton, M. S. Crouse, C. R. Dahlen, & A. K. Ward. 2019. Developmental programming of fetal growth and development. Vet. Clin. North Am. Food Anim. Pract. 35:229-247. https://doi.org/10.1016/j.cvfa.2019.02.006
Sakaguchi, K., Y. Yanagawa, K. Yoshioka, T. Suda, S. Katagiri, & M. Nagano. 2019. Relationships between the antral follicle count, steroidogenesis, and secretion of follicle-stimulating hormone and anti-Müllerian hormone during follicular growth in cattle. Reprod. Biol. Endocrinol. 17:1-13. https://doi.org/10.1186/s12958-019-0534-3
Sangha, G. K., H. Kaur, & K. S. Khera. 2012. Morphological changes in cultured GC from different sized follicles of goat ovary. Indian Journal Animal Reproduction 33: 1-5.
Santos, P. H., R. A. Satrapa, P. K. Fontes, F. F. Franchi, E. M. Razza, F. Mani, M. F. G. Nogueira, C. M. Barros, & A. C. S. Castilho. 2018. Effect of superstimulation on the expression of microRNAs and genes involved in steroidogenesis and ovulation in Nelore cows. Theriogenology 110:192-200. https://doi.org/10.1016/j.theriogenology.2017.12.045
Singh, J. & G. P. Adams. 2000. Histomorphometry of dominant and subordinate bovine ovarian follicle. Anat. Record. 258:58-70. https://doi.org/10.1002/(SICI)1097-0185(20000101)258:1<58::AID-AR7>3.0.CO;2-P
Sferuzzi-Perri, A. N., O. R. Vaughan, A. J. Forhead, & A. L. Fowden. 2013. Hormonal and nutritional drivers of intrauterine growth. Curr. Opin. Clin. Nutr. Metab. Care. 16:298-309. https://doi.org/10.1097/MCO.0b013e32835e3643
Spencer, T. E. 2014. Biological roles of uterine glands in pregnancy. Semin. Reprod. Med. 32:346-357. https://doi.org/10.1055/s-0034-1376354
Strauss, J. F., B. Modi, & J. M. McAllister. 2014. Defects in Ovarian Steroid Hormone Biosynthesis. In Cellular Endocrinology in Health and Disease. [Chapter 18]. Academic Press: Massachusetts. https://doi.org/10.1016/B978-0-12-408134-5.00018-4
Sugiura, T., S. Akiyoshi, F. Inoue, Y. Yanagawa, M. Moriyoshi, M. Tajima, & S. Katagiri. 2018. Relationship between bovine endometrial thickness and plasma progesterone and E2 concentrations in natural and induced estrus. J. Reprod. Dev. 64:135-143. https://doi.org/10.1262/jrd.2017-139
Wildman, E. E., G. M. Jones, P. E. Wagner, R. L. Boman, H. F. Jr. Troutt, & T. N. Lesch. 1982. A dairy cow body condition scoring system and its relationship to selected production characteristics. J. Dairy. Sci. 65:495-501. https://doi.org/10.3168/jds.S0022-0302(82)82223-6
Wang, C. K., R. S. Robinson, A. P. F. Flint, & G. E. Mann. 2007. Quantitative analysis of changes in endometrial gland morphology during bovine oestrus cycle and their association with progesterone levels. Reproduction 134:365-371. https://doi.org/10.1530/REP-06-0133
Zeng, Y., E. O. Adegoke, X. Wang, X. Lin, H. Wang, C. Wang, & G. Zhang. 2017. Expression of β-defensins in bovine oviduct and uterus during follicular and luteal phase. Comp. Clin. Path. 26:749-756. https://doi.org/10.1007/s00580-017-2442-2
Adams, G. P., R. Jaiswal, J. Singh, & P. Malhi. 2008. Progress in understanding ovarian follicular dynamic in cattle. Theriogenology. 69:72-80. https://doi.org/10.1016/j.theriogenology.2007.09.026
Alvarez, R. H., F. L. Natal, M. T. Ribela, B. E. de Almeida, J. E. de Oliveira, & P. Bartolini. 2016. Physical-chemical and biological characterization of different preparations of equine chorionic gonadotropin. J. Vet. Sci. 17:459–465. https://doi.org/10.4142/jvs.2016.17.4.459
Andriyanto, Amrozi, M. Rahminiwati, A. Boediono, & W. Manalu. 2015. Correlation of stimulated dominant follicle by PMSG injection with estrous response in kacang Goat. Jurnal Kedokteran Hewan 9:20-23. https://doi.org/10.21157/j.ked.hewan.v9i1.2779
Andriyanto, Amrozi, M. Rahminiwati, A. Boediono, & W. Manalu. 2017. Optimum dose and time of PMSG injections in Kacang goats to increase endogenous secretion of estradiol and progesterone without superovulation response. Small. Rumin. Res. 149:147-153. https://doi.org/10.1016/j.smallrumres.2017.02.005
Andriyanto & W. Manalu. 2012. Improvement of small holder farms sheep productivity through the application of pregnant mare serum gonadotrophin. Jurnal Veteriner : Jurnal Kedokteran Hewan Indonesia 13:235-241. https://ojs.unud.ac.id/index.php/jvet/article/view/6010. [May 12, 2022].
Arif, R., Andriyanto, A. Boediono, A. Winarto, F. Satrija, & W. Manalu. 2018a. Sonometri fetus kambing kacang usia 7 minggu hasil superovulasi menggunakan hormon PMSG. ARSHI Veterinary Letter 2:13-14. https://doi.org/10.29244/avl.2.1.13-14
Arif, R., F. Satrija, A. Winarto, A. Boediono, & W. Manalu. 2018b. Production of lambs’ resilience to Hemonchus contortus. Small. Rumin. Res. 167:110-116. https://doi.org/10.1016/j.smallrumres.2018.08.016
Benbia, S., M. Yahia, I. R. Letron, & O. Benounne. 2017. Endometrial cells morphology depending on estrous cycle and histologic layers in cows: morphometric study. Glob. Vet. 18:68-73.
Braun, T., J. R. Challis, J. P. Newnham, & D. M. Sloboda. 2013. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr. Rev. 34:885-916. https://doi.org/10.1210/er.2013-1012
Bunma, T., C. Kanjanaruch, N. Kogram, S. Uriyapongson, V. Khanthusaeng, & C. Navanukraw. 2021. Effects of FSH treatment and withdrawal during proestrus on uterine proliferation and steroid hormone receptor expression in beef heifers. Anim. Sci. J. 92:e13621. https://doi.org/10.1111/asj.13621
Chwalisz, M. & R. Fűrbass. 2014. Evaluation of coding-independent functions of the transcribed bovine aromatase pseudogene CYP19P1. BMC. Res. Notes. 7:1-5. https://doi.org/10.1186/1756-0500-7-378
de Lima, M. A., F. Morotti, B. M. Bayeux, R. G. de Rezende, R. C. Botigelli, T. H. C. De Bem, P. K. Fontes, M. F. G. Nogueira, F. V. Meirelles, P. S. Baruselli, J. C. De Silveira, F. Perecin, & M. M. Seneda. 2020. Ovarian follicular dynamics, progesterone concentrations, pregnancy rates and transcriptional patterns in Bos indicus females with a high or low antral follicle count. Sci. Rep. 10:1-13. https://doi.org/10.1038/s41598-020-76601-5
Forhead, A. J. & A. L. Fowden. 2014. Thyroid hormones in fetal growth and prepartum maturation. J. Endocrinol. 221:R87-R103. https://doi.org/10.1530/JOE-14-0025
Fowden, A. L. & A. J. Forhead. 2004. Endocrine mechanism of intrauterine programming. Reproduction. 127:515-526. https://doi.org/10.1530/rep.1.00033
Fowden, A. L., A. J. Forhead, P. M. Coan, & G. J. Burton. 2008. The placenta and intrauterine programming. J. Neuroendocrinol. 20:439-450. https://doi.org/10.1111/j.1365-2826.2008.01663.x
Fowden, A. L. & A. J. Forhead. 2009. Endocrine regulation of feto-placental growth. Horm. Res. 72:257–265. https://doi.org/10.1159/000245927
Fowden A. L. & A. J. Forhead. 2015. Glucocorticoids as regulatory signals during intrauterine development. Exp. Physiol. 100:1477-87. https://doi.org/10.1113/EP085212
Fowden A. L, O. A. Valenzuela, O. R. Vaughan, J. K. Jellyman, & A. J. Forhead. 2016. Glucocorticoid programming of intrauterine development. Domest. Anim. Endocrinol. 56:S121-32. https://doi.org/10.1016/j.domaniend.2016.02.014
Fu, S. B., H. L. Zhang, H. Riaz, S. Ahmad, X. M. Wang, X. Li, G. H. Hua, X. R. Liu, A. Z. Guo, & L. G. Yang. 2013. Effects of different doses of PMSG on reproductive performance in Chinese Holstein dairy cows. Pak. Vet. J. 33:209-212.
Gonella-Diaza, A. M., F. S. Mesquita, K. R. da Silva, J. C. de Carvalho Balieiro, N. P. dos Santos, G. Pugliesi, S. R. de Fransisco, & M. Binelli. 2017. Sex steroid modulate morphological and functional features of the bovine oviduct. Cell. Tissue Res. 370:319-333. https://doi.org/10.1007/s00441-017-2666-0
Guillemin, N., I. Dufort, & M. A. Sirard. 2015. A genetical genomics methodology to identify genetic markers of a bovine fertility phenotype based on CYP19A1 gene expression. Gene Expression to Genetical Genomics 8:9-18. https://doi.org/10.4137/GGG.S24691
Habibizad, J., M. Towhidi, & F. Samadian. 2020. Determining the optimal dose of eCG to improve the reproductive performance of Lake-Ghashghaei ewes in the breeding season. Journal Animal Environment 12:33-40.
Jitjumnong, J., P. Sudwan, R. Maktrirat, P. Yama, W. Pirokad, U. Warittha, & T. Moonmanee. 2019. Additional growth of dominant follicle during synchronized ovulatory cycle affects ovulatory follicle size, corpus luteum parameters, and progesterone level in northern Thai Native Cattle. Science & Technology Asia 24:83-93.
Murphy, B. D. 2012. Equine chorionic gonadotropin: An enigmatic but essential tool. Anim. Reprod. 9:223-230.
Nugroho, P., K. G. Wiryawan, D. A. Astuti, & W. Manalu. 2021. Stimulation of follicle growth and development during estrus in Ettawa Grade does fed a flushing supplement of different polyunsaturated fatty acids. Vet. World. 14:11–22. https://doi.org/10.14202/vetworld.2021.11-22
Núñez-Olivera, R., F. Cuadro, D. Bosolasco, V. de Brun, J. de la Mata, C. Brochado, A. Meikle, G. A. Bó, & A. Menchaca. 2020. Effect of equine chorionic gonadotropin (eCG) administration and proestrus length on ovarian response, uterine functionality and pregnancy rate in beef heifers inseminated at a fixed-time. Theriogenology 151:16-27. https://doi.org/10.1016/j.theriogenology.2020.03.031
Perry, G. A., R. A. Cushman, B. I. Perry, A. K. Schiefelbein, E. J. Northrop, J. J. Rich, & S. D. Perkins. 2021. Role of preovulatory concentrations of E2 on timing of conception and regulation of the uterine environment in beef cattle. Syst. Biol. Reprod. Med. 66:12-25. https://doi.org/10.1080/19396368.2019.1695979
Pulley, S. L., L. D. Wallace, H. L. Jr. Mellison, & J. S. Stevenson. 2013. Ovarian characteristics, serum concentration of progesterone and estradiol, and fertility in lactating dairy cows in response to equine chorionic gonadotropin. Theriogenology 79:127-134. https://doi.org/10.1016/j.theriogenology.2012.09.017
Putro, K. B., Amrozi, A. Winarto, A. Boediono, & W. Manalu. 2020. Pre-ovulatory follicle of crossed ongole heifer stimulated by using low dose of PMSG. Acta Vet. Indones. 8:1-7. https://doi.org/10.29244/avi.8.3.1-7
Regan, S. L. P., P. G. Knight, J. L. Yovich, Y. Leung, F. Arfuso, & A. Dharmarajan. 2018. Granulosa cell apoptosis in the ovarian follicle – a changing view. Front. Endocrinol. 9:1-10. https://doi.org/10.3389/fendo.2018.00061
Reynolds, L. P., P. P. Borowicz, J. S. Caton, M. S. Crouse, C. R. Dahlen, & A. K. Ward. 2019. Developmental programming of fetal growth and development. Vet. Clin. North Am. Food Anim. Pract. 35:229-247. https://doi.org/10.1016/j.cvfa.2019.02.006
Sakaguchi, K., Y. Yanagawa, K. Yoshioka, T. Suda, S. Katagiri, & M. Nagano. 2019. Relationships between the antral follicle count, steroidogenesis, and secretion of follicle-stimulating hormone and anti-Müllerian hormone during follicular growth in cattle. Reprod. Biol. Endocrinol. 17:1-13. https://doi.org/10.1186/s12958-019-0534-3
Sangha, G. K., H. Kaur, & K. S. Khera. 2012. Morphological changes in cultured GC from different sized follicles of goat ovary. Indian Journal Animal Reproduction 33: 1-5.
Santos, P. H., R. A. Satrapa, P. K. Fontes, F. F. Franchi, E. M. Razza, F. Mani, M. F. G. Nogueira, C. M. Barros, & A. C. S. Castilho. 2018. Effect of superstimulation on the expression of microRNAs and genes involved in steroidogenesis and ovulation in Nelore cows. Theriogenology 110:192-200. https://doi.org/10.1016/j.theriogenology.2017.12.045
Singh, J. & G. P. Adams. 2000. Histomorphometry of dominant and subordinate bovine ovarian follicle. Anat. Record. 258:58-70. https://doi.org/10.1002/(SICI)1097-0185(20000101)258:1<58::AID-AR7>3.0.CO;2-P
Sferuzzi-Perri, A. N., O. R. Vaughan, A. J. Forhead, & A. L. Fowden. 2013. Hormonal and nutritional drivers of intrauterine growth. Curr. Opin. Clin. Nutr. Metab. Care. 16:298-309. https://doi.org/10.1097/MCO.0b013e32835e3643
Spencer, T. E. 2014. Biological roles of uterine glands in pregnancy. Semin. Reprod. Med. 32:346-357. https://doi.org/10.1055/s-0034-1376354
Strauss, J. F., B. Modi, & J. M. McAllister. 2014. Defects in Ovarian Steroid Hormone Biosynthesis. In Cellular Endocrinology in Health and Disease. [Chapter 18]. Academic Press: Massachusetts. https://doi.org/10.1016/B978-0-12-408134-5.00018-4
Sugiura, T., S. Akiyoshi, F. Inoue, Y. Yanagawa, M. Moriyoshi, M. Tajima, & S. Katagiri. 2018. Relationship between bovine endometrial thickness and plasma progesterone and E2 concentrations in natural and induced estrus. J. Reprod. Dev. 64:135-143. https://doi.org/10.1262/jrd.2017-139
Wildman, E. E., G. M. Jones, P. E. Wagner, R. L. Boman, H. F. Jr. Troutt, & T. N. Lesch. 1982. A dairy cow body condition scoring system and its relationship to selected production characteristics. J. Dairy. Sci. 65:495-501. https://doi.org/10.3168/jds.S0022-0302(82)82223-6
Wang, C. K., R. S. Robinson, A. P. F. Flint, & G. E. Mann. 2007. Quantitative analysis of changes in endometrial gland morphology during bovine oestrus cycle and their association with progesterone levels. Reproduction 134:365-371. https://doi.org/10.1530/REP-06-0133
Zeng, Y., E. O. Adegoke, X. Wang, X. Lin, H. Wang, C. Wang, & G. Zhang. 2017. Expression of β-defensins in bovine oviduct and uterus during follicular and luteal phase. Comp. Clin. Path. 26:749-756. https://doi.org/10.1007/s00580-017-2442-2
Authors
PutroK. B., WinartoA., Amrozi, BoedionoA., & ManaluW. (2023). Quantitative Histomorphometry of Pre-ovulatory Follicles and Uterine Glands of Ongole-grade Heifer in Response to the Low Doses of PMSG Administration. Tropical Animal Science Journal, 46(1), 1-12. https://doi.org/10.5398/tasj.2023.46.1.1
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