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Rostami Dovom, M., Noroozzadeh, M., Mosaffa, N., Piryaei, A., Zadevakili, A., Amin Abdollahifar, M., & Ramezani Tehrani, F. (2022). Induction of a rat model of premature ovarian insufficiency using D-galactose feeding during the critical periods of development: A pilot study. International Journal of Reproductive BioMedicine (IJRM), 20(4), 319-330. https://doi.org/10.18502/ijrm.v20i4.10904
https://doi.org/10.18502/ijrm.v20i4.10904
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authors
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Marzieh Rostami Dovom
Marzieh Rostami Dovom
Reproductive Endocrinology Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Mahsa Noroozzadeh
Mahsa Noroozzadeh
Reproductive Endocrinology Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Nariman Mosaffa
Nariman Mosaffa
Department of Immunology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Abbas Piryaei
Abbas Piryaei
Urogenital Stem Cell Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Azita Zadevakili
Azita Zadevakili
Endocrine Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Mohammad Amin Abdollahifar
Mohammad Amin Abdollahifar
Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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Fahimeh Ramezani Tehrani
Fahimeh Ramezani Tehrani
Reproductive Endocrinology Research Center, Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
Published Date
- May 23, 2022
Induction of a rat model of premature ovarian insufficiency using D-galactose feeding during the critical periods of development: A pilot study
Abstract
Background: Premature ovarian insufficiency (POI) affects about 1% of women of reproductive ages (15-45 yr), with no curative treatment.
Objective: We aimed to present a rat model of POI using a D-galactose enriched diet.
Materials and Methods: In a pilot study, 4 pregnant Wistar rats were divided into 4 groups; 3 groups were fed galactose-enriched diets at days 3-15 of pregnancy (G1); on the 3rd day of pregnancy to parturition (G2), and the 3rd day of pregnancy until the end of the weaning period (G3). Also, group 4, as the control group (G0), was fed standard pellets during the study. After confirming the lack of adverse effects of dieting with galactose in terms of offsprings’ birth weight, we performed our study designed the same as the pilot study. A total of 40 pregnant Wistar rats were randomly divided into 4 groups. Ovarian histology, reproductive hormones, and immunological characteristics of the female offspring were examined in all experimental groups and compared.
Results: The pilot study revealed no significant differences in the birth weight of the offspring of the 4 study groups (p = 0.96). The ovarian index in the female offspring of those with a gal-exposed diet was significantly lower than that of the control group offspring (p < 0.01).
Conclusion: As the birth weights of the offspring of our experimental and control groups were similar, it can be concluded that the reduction of ovarian follicles after prenatal exposure to D-galactose is due to the ovotoxicity of galactose. The results of our final study will provide more information about the rat POI model induced by prenatal exposure to D-galactose.
Key words: Premature ovarian insufficiency, Animal model, D-galactose.
References
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[2] Jungari SB, Chauhan BG. Prevalence and determinants of premature menopause among Indian women: Issues and challenges ahead. Health Soc Work 2017; 42: 79– 86.
[3] Rostami Dovom M, Bidhendi-Yarandi R, Mohammad K, Farahmand M, Azizi F, Ramezani Tehrani F. Prevalence of premature ovarian insufficiency and its determinants in Iranian populations: Tehran lipid and glucose study. BMC Womens Health 2021; 21: 79.
[4] Iorga A, Cunningham ChM, Moazeni Sh, Ruffenach G, Umar S, Eghbali M. The protective role of estrogen and estrogen receptors in cardiovascular disease and the controversial use of estrogen therapy. Biol Sex Differ 2017; 8: 33.
[5] Almeida M, Laurent MR, Dubois V, Claessens F, O’Brien CA, Bouillon R, et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev 2017; 97: 135–187.
[6] Yela DA, Soares PM, Benetti-Pinto CL. Influence of sexual function on the social relations and quality of life of women with premature ovarian insufficiency. Rev Bras Ginecol Obstet 2018; 40: 66–71.
[7] Zhang T, Yan D, Yang Y, Ma A, Li L, Wang Z, et al. The comparison of animal models for premature ovarian failure established by several different source of inducers. Regul Toxicol Pharmacol 2016; 81: 223–232.
[8] Lee EH, Han SE, Park MJ, Kim HJ, Kim HG, Kim CW, et al. Establishment of effective mouse model of premature ovarian failure considering treatment duration of anticancer drugs and natural recovery time. J Menopausal Med 2018; 24: 196–203.
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[10] Frederick AB, Zinsli AM, Carlock G, Conneely K, Fridovich-Keil JL. Presentation, progression, and predictors of ovarian insufficiency in classic galactosemia. J Inherit Metab Dis 2018; 41: 785–790.
[11] Liang X, Yan Zh, Ma W, Qian Y, Zou X, Cui Y, et al. Peroxiredoxin 4 protects against ovarian ageing by ameliorating D-galactose-induced oxidative damage in mice. Cell Death Dis 2020; 11: 1053.
[12] Thakur M, Shaeib F, Khan SN, Kohan-Ghadr HR, Jeelani R, Aldhaheri SR, et al. Galactose and its metabolites deteriorate metaphase II mouse oocyte quality and subsequent embryo development by disrupting the spindle structure. Sci Rep 2017; 7: 231.
[13] Flechtner I, Viaud M, Kariyawasam D, Perrissin-Fabert M, Bidet M, Bachelot A, et al. Puberty and fertility in classic galactosemia. Endocr Connect 2021; 10: 240–247.
[14] Yan Z, Dai Y, Fu H, Zheng Y, Bao D, Yin Y, et al. Curcumin exerts a protective effect against premature ovarian failure in mice. J Mol Endocrinol 2018; 60: 261– 271.
[15] Rostami Dovom M, Noroozzadeh M, Mosaffa N, Zadeh- Vakili A, Piryaei A, Ramezani Tehrani F. Induced premature ovarian insufficiency by using D galactose and its effects on reproductive profiles in small laboratory animals: A systematic review. J Ovarian Res 2019; 12: 96.
[16] Swartz WJ, Mattison DR. Galactose inhibition of ovulation in mice. Fertil Steril 1988; 49: 522–526.
[17] Wang Sh, Sun M, Yu L, Wang Y, Yao Y, Wang D. Niacin inhibits apoptosis and rescues premature ovarian failure. Cell Physiol Biochem 2018; 50: 2060–2070.
[18] Myers M, Britt KL, Wreford NGM, Ebling FJP, Kerr JB. Methods for quantifying follicular numbers within the mouse ovary. Reproduction 2004; 127: 569–580.
[19] Altunkaynak BZ, Altunkaynak E, Unal D, Unal B. A novel application for the cavalieri principle: A stereological and methodological study. Eurasian J Med 2009; 41: 99–101.
[20] Ajayi AF, Akhigbe RE. Staging of the estrous cycle and induction of estrus in experimental rodents: An update. Fertil Res Pract 2020; 6: 5.
[21] Wang JJ, Yu XW, Wu RY, Sun XF, Cheng SF, Ge W, et al. Starvation during pregnancy impairs fetal oogenesis and folliculogenesis in offspring in the mouse. Cell Death Dis 2018; 9: 452.
[22] Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 2010; 5: e15558.
[23] Dorostghoal M, Moazedi AA, Moattari M. Long-term developmental effects of lactational exposure to lead acetate on ovary in offspring Wistar rats. Int J Fertil Steril 2011; 5: 39–46.
[24] Thakur M, Feldman G, Puscheck EE. Primary ovarian insufficiency in classic galactosemia: Current understanding and future research opportunities. J Assist Reprod Genet 2018; 35: 3–16.
[25] Banerjee S, Chakraborty P, Saha P, Bandyopadhyay SA, Kabir SN. Ovotoxic effects of galactose involve attenuation of follicle-stimulating hormone bioactivity and up-regulation of granulosa cell p53 expression. PLoS One 2012; 7: e30709.
[26] Sozen B, Ozekinci M, Erman M, Gunduz T, Demir N, Akouri R. Dehydroepiandrosterone supplementation attenuates ovarian ageing in a galactose-induced primary ovarian insufficiency rat model. J Assist Reprod Genet 2019; 36: 2181–2189.
[27] Misselwitz B, Butter M, Verbeke K, Fox MR. Update on lactose malabsorption and intolerance: Pathogenesis, diagnosis and clinical management. Gut 2019; 68: 2080–2091.
[28] Lai K, Elsas LJ, Wierenga KJ. Galactose toxicity in animals. IUBMB Life 2009; 61: 1063–1074.
[29] Bandyopadhyay S, Chakrabarti J, Banerjee S, Pal AK, Goswami SK, Chakravarty BN, et al. Galactose toxicity in the rat as a model for premature ovarian failure: an experimental approach readdressed. Hum Reprod 2003; 18: 2031–2038.
[30] Pan B, Li J. The art of oocyte meiotic arrest regulation. Reprod Biol Endocrinol 2019; 17: 8.
[31] Tingen C, Kim A, Woodruff TK. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009; 15: 795–803.
[32] Chou ChH, Chen MJ. The effect of steroid hormones on ovarian follicle development. Vitam Horm 2018; 107: 155– 175.
[33] Liu G, Shi F, Blas-Machado U, Yu R, Davis VL, Foster WG, et al. Dietary galactose inhibits GDF-9 mediated follicular development in the rat ovary. Reprod Toxicol 2006; 21: 26–33.
[34] Andersen MD, Alstrup AKO, Duvald C, Mikkelsen EFR, Vendelbo MH, Ovesen PG, et al. Animal models of fetal medicine and obstetrics. In: Bartholomew I, editor. Experimental animal models of human diseases- An effective therapeutic strategy [Internet]. London: IntechOpen; 2018 [cited 2022 Mar 16]. Available from: https://www.intechopen.com/chapters/60219 doi: 10.5772/intechopen.74038.
[2] Jungari SB, Chauhan BG. Prevalence and determinants of premature menopause among Indian women: Issues and challenges ahead. Health Soc Work 2017; 42: 79– 86.
[3] Rostami Dovom M, Bidhendi-Yarandi R, Mohammad K, Farahmand M, Azizi F, Ramezani Tehrani F. Prevalence of premature ovarian insufficiency and its determinants in Iranian populations: Tehran lipid and glucose study. BMC Womens Health 2021; 21: 79.
[4] Iorga A, Cunningham ChM, Moazeni Sh, Ruffenach G, Umar S, Eghbali M. The protective role of estrogen and estrogen receptors in cardiovascular disease and the controversial use of estrogen therapy. Biol Sex Differ 2017; 8: 33.
[5] Almeida M, Laurent MR, Dubois V, Claessens F, O’Brien CA, Bouillon R, et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev 2017; 97: 135–187.
[6] Yela DA, Soares PM, Benetti-Pinto CL. Influence of sexual function on the social relations and quality of life of women with premature ovarian insufficiency. Rev Bras Ginecol Obstet 2018; 40: 66–71.
[7] Zhang T, Yan D, Yang Y, Ma A, Li L, Wang Z, et al. The comparison of animal models for premature ovarian failure established by several different source of inducers. Regul Toxicol Pharmacol 2016; 81: 223–232.
[8] Lee EH, Han SE, Park MJ, Kim HJ, Kim HG, Kim CW, et al. Establishment of effective mouse model of premature ovarian failure considering treatment duration of anticancer drugs and natural recovery time. J Menopausal Med 2018; 24: 196–203.
[9] Nie X, Dai Y, Zheng Y, Bao D, Chen Q, Yin Y, et al. Establishment of a mouse model of premature ovarian failure using consecutive superovulation. Cell Physiol Biochem 2018; 51: 2341–2358.
[10] Frederick AB, Zinsli AM, Carlock G, Conneely K, Fridovich-Keil JL. Presentation, progression, and predictors of ovarian insufficiency in classic galactosemia. J Inherit Metab Dis 2018; 41: 785–790.
[11] Liang X, Yan Zh, Ma W, Qian Y, Zou X, Cui Y, et al. Peroxiredoxin 4 protects against ovarian ageing by ameliorating D-galactose-induced oxidative damage in mice. Cell Death Dis 2020; 11: 1053.
[12] Thakur M, Shaeib F, Khan SN, Kohan-Ghadr HR, Jeelani R, Aldhaheri SR, et al. Galactose and its metabolites deteriorate metaphase II mouse oocyte quality and subsequent embryo development by disrupting the spindle structure. Sci Rep 2017; 7: 231.
[13] Flechtner I, Viaud M, Kariyawasam D, Perrissin-Fabert M, Bidet M, Bachelot A, et al. Puberty and fertility in classic galactosemia. Endocr Connect 2021; 10: 240–247.
[14] Yan Z, Dai Y, Fu H, Zheng Y, Bao D, Yin Y, et al. Curcumin exerts a protective effect against premature ovarian failure in mice. J Mol Endocrinol 2018; 60: 261– 271.
[15] Rostami Dovom M, Noroozzadeh M, Mosaffa N, Zadeh- Vakili A, Piryaei A, Ramezani Tehrani F. Induced premature ovarian insufficiency by using D galactose and its effects on reproductive profiles in small laboratory animals: A systematic review. J Ovarian Res 2019; 12: 96.
[16] Swartz WJ, Mattison DR. Galactose inhibition of ovulation in mice. Fertil Steril 1988; 49: 522–526.
[17] Wang Sh, Sun M, Yu L, Wang Y, Yao Y, Wang D. Niacin inhibits apoptosis and rescues premature ovarian failure. Cell Physiol Biochem 2018; 50: 2060–2070.
[18] Myers M, Britt KL, Wreford NGM, Ebling FJP, Kerr JB. Methods for quantifying follicular numbers within the mouse ovary. Reproduction 2004; 127: 569–580.
[19] Altunkaynak BZ, Altunkaynak E, Unal D, Unal B. A novel application for the cavalieri principle: A stereological and methodological study. Eurasian J Med 2009; 41: 99–101.
[20] Ajayi AF, Akhigbe RE. Staging of the estrous cycle and induction of estrus in experimental rodents: An update. Fertil Res Pract 2020; 6: 5.
[21] Wang JJ, Yu XW, Wu RY, Sun XF, Cheng SF, Ge W, et al. Starvation during pregnancy impairs fetal oogenesis and folliculogenesis in offspring in the mouse. Cell Death Dis 2018; 9: 452.
[22] Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 2010; 5: e15558.
[23] Dorostghoal M, Moazedi AA, Moattari M. Long-term developmental effects of lactational exposure to lead acetate on ovary in offspring Wistar rats. Int J Fertil Steril 2011; 5: 39–46.
[24] Thakur M, Feldman G, Puscheck EE. Primary ovarian insufficiency in classic galactosemia: Current understanding and future research opportunities. J Assist Reprod Genet 2018; 35: 3–16.
[25] Banerjee S, Chakraborty P, Saha P, Bandyopadhyay SA, Kabir SN. Ovotoxic effects of galactose involve attenuation of follicle-stimulating hormone bioactivity and up-regulation of granulosa cell p53 expression. PLoS One 2012; 7: e30709.
[26] Sozen B, Ozekinci M, Erman M, Gunduz T, Demir N, Akouri R. Dehydroepiandrosterone supplementation attenuates ovarian ageing in a galactose-induced primary ovarian insufficiency rat model. J Assist Reprod Genet 2019; 36: 2181–2189.
[27] Misselwitz B, Butter M, Verbeke K, Fox MR. Update on lactose malabsorption and intolerance: Pathogenesis, diagnosis and clinical management. Gut 2019; 68: 2080–2091.
[28] Lai K, Elsas LJ, Wierenga KJ. Galactose toxicity in animals. IUBMB Life 2009; 61: 1063–1074.
[29] Bandyopadhyay S, Chakrabarti J, Banerjee S, Pal AK, Goswami SK, Chakravarty BN, et al. Galactose toxicity in the rat as a model for premature ovarian failure: an experimental approach readdressed. Hum Reprod 2003; 18: 2031–2038.
[30] Pan B, Li J. The art of oocyte meiotic arrest regulation. Reprod Biol Endocrinol 2019; 17: 8.
[31] Tingen C, Kim A, Woodruff TK. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009; 15: 795–803.
[32] Chou ChH, Chen MJ. The effect of steroid hormones on ovarian follicle development. Vitam Horm 2018; 107: 155– 175.
[33] Liu G, Shi F, Blas-Machado U, Yu R, Davis VL, Foster WG, et al. Dietary galactose inhibits GDF-9 mediated follicular development in the rat ovary. Reprod Toxicol 2006; 21: 26–33.
[34] Andersen MD, Alstrup AKO, Duvald C, Mikkelsen EFR, Vendelbo MH, Ovesen PG, et al. Animal models of fetal medicine and obstetrics. In: Bartholomew I, editor. Experimental animal models of human diseases- An effective therapeutic strategy [Internet]. London: IntechOpen; 2018 [cited 2022 Mar 16]. Available from: https://www.intechopen.com/chapters/60219 doi: 10.5772/intechopen.74038.