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Investigation of the Effect of Crowding Stress on Mice Oocyte Parameters and Reproductive Organs
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Farzad Rajaei1    , Fatemeh Sabbaghziarani 2 |
1- Cellular and Molecular Research Center, Research Institute for Prevention of Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran. Department of Anatomical Sciences, School of Medicine, Qazvin University of Medical Sciences, Qazvin, Iran.
2- Cellular and Molecular Research Center, Research Institute for Prevention of Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran. Department of Anatomical Sciences, School of Medicine, Qazvin University of Medical Sciences, Qazvin, Iran. , saba.ziarani95@gmail.com |
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Abstract: (1141 Views) |
Background and Aim: Stress is known to affect many reproductive variables, including gonadotropins and sex steroid levels. Stressors such as crowding can alter the normal function of the ovaries, fallopian tubes, and uterine cycles. In the this study, we investigated the effect of crowding stress on mice oocyte parameters and reproductive organs.
Materials and Methods: Mice were divided into control, low & high- density crowding stress groups, and kept under stres condition for one month. Superovulation was induced in the mice in all groups by pregnant mare serum gonadotropin (PMSG) and human chorionic gonadotropin (hCG). The mice were sacrificed 15 hours after hCG injection. Grade I and IV oocytes were stained with the terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) method after collection and evaluation. Ovarian, fallopian tubes and uterine horns tissues were evaluated after staining with hematoxylin and eosin (H&E). Data were analyzed by ANOVA. p-value ≤0.05 was considered significant.
Results: The number of grade I and the size of grades I and IV oocytes in the high-density crowding stress group were significantly decreased compared to those in the control group. The rate of DNA fragmentation of grade I and IV oocytes in the low and high- density crowding stress groups demonstrated a significant increase compared to that in the control group. The number of monolayer primary follicles and the height of the fallopian tube epithelium significantly decreased in the high- density crowding stress group compared to those in the control group (p≤0.05).
Conclusion: Crowding as an environmental stress can affect DNA fragmentation by inducing irregularities in follicular and oocyte development.
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| Keywords: Crowding stress, Oocyte, DNA fragmentation, Ovary, Fallopian tube, Uterine horn |
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Full-Text [PDF 850 kb]
(255 Downloads)
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Type of Study: Original Research |
Subject:
Biology of Reproduction
Received: 2023/07/29 | Accepted: 2023/11/15 | Published: 2024/04/16
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| References |
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[ DOI:10.1242/jeb.138826] 23. Mileva VR, Gilmour KM, Balshine S. Effects of maternal stress on egg characteristics in a cooperatively breeding fish. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2011;158(1):22-9. [ DOI:10.1016/j.cbpa.2010.08.017] [ PMID] 24. Lu J-H, Wang J-Z, Wang H-L, Sui H-S, Liu Y, Li J-J, et al. Damaging effect of cumulus denudation on rabbit oocytes. Fertil. Steril. 2010;93(5):1567-73. [ DOI:10.1016/j.fertnstert.2009.05.066] [ PMID] 25. Yuan H-J, Li Z-B, Zhao X-Y, Sun G-Y, Wang G-L, Zhao Y-Q, et al. Glucocorticoids impair oocyte competence and trigger apoptosis of ovarian cells via activating the TNF-α system. Reproduction. 2020;160(1):129-40. [ DOI:10.1530/REP-20-0025] [ PMID] 26. Sun L, Lv H, Wei W, Zhang D, Guan Y. Angiotensin-converting enzyme D/I and plasminogen activator inhibitor-1 4G/5G gene polymorphisms are associated with increased risk of spontaneous abortions in polycystic ovarian syndrome. J. Endocrinol. Invest. 2010;33:77-82. [ DOI:10.1007/BF03346557] [ PMID] 27. Peña Ó, Palumbo A, González-Fernández R, Hernández J, Naftolin F, Ávila J. Expression of angiotensin II type 1 (AT1) and angiotensin II type 2 (AT2) receptors in human granulosa-lutein (GL) cells: correlation with infertility diagnoses. Fertil. Steril. 2010;93(5):1601- [ DOI:10.1016/j.fertnstert.2009.03.092] [ PMID] 28. Kim J, You S. High Housing Density-Induced Chronic Stress Diminishes Ovarian Reserve via Granulosa Cell Apoptosis by Angiotensin II Overexpression in Mice. Int J Mol Sci. 2022;23(15):8614. [ DOI:10.3390/ijms23158614] [ PMID] [ ] 29. Chukwuebuka NB, Emeka OA, Irikefe OS, Iju WJ, Godsday O, Temitope O, et al. Stress-induced morphological changes of ovarian histology in female Wistar rats. Biomed Pharmacol J. 2020;13(4):1625-43. [ DOI:10.13005/bpj/2038] 30. Son YL, Ubuka T, Tsutsui K. Regulation of stress response on the hypothalamic-pituitary-gonadal axis via gonadotropin-inhibitory hormone. Front Neuroendocrinol. 2022;64:100953. [ DOI:10.1016/j.yfrne.2021.100953] [ PMID] 31. Díaz Pacheco M, Vargas Romero J, Rojas‐Maya S, Retana‐Márquez S. Effects of crowding and water restriction stress on creole goat reproduction in the Oaxacan Sierra Mixteca, Mexico. Reprod Domest Anim . 2018;53(6):1386-95. [ DOI:10.1111/rda.13267] [ PMID] 32. Ozawa H. Kisspeptin neurons as an integration center of reproductive regulation: Observation of reproductive function based on a new concept of reproductive regulatory nervous system. Reprod Med Biol. 2022;21(1):e12419. [ DOI:10.1002/rmb2.12419] [ ] 33. Lu W, Huang S, Liu J, Batsuren E, Li G, Wan X, et al. Effects of Group Size on Behavior, Reproduction, and mRNA Expression in Brains of Brandt's Voles. Brain Sci. 2023;13(2):311. [ DOI:10.3390/brainsci13020311] [ PMID] [ ] 34. Suvorov A. Population numbers and reproductive health. Endocrinology. 2021;162(11):bqab154. [ DOI:10.1210/endocr/bqab154] [ PMID] 35. Karin O, Raz M, Tendler A, Bar A, Korem Kohanim Y, Milo T, et al. A new model for the HPA axis explains dysregulation of stress hormones on the timescale of weeks. Mol Syst Biol . 2020;16(7):e9510. [ DOI:10.15252/msb.20209510] [ PMID] [ ] 36. Dong Y-z, Zhou F-j, Sun Y-p. Psychological stress is related to a decrease of serum anti-müllerian hormone level in infertile women. Reprod Biol. 2017;15(1):1-4. [ DOI:10.1186/s12958-017-0271-4] [ PMID] [ ] 37. Pankhurst MW. A putative role for anti-Müllerian hormone (AMH) in optimising ovarian reserve expenditure. J Endocrinol. 2017;233(1):R1-R13. [ DOI:10.1530/JOE-16-0522] [ PMID] 38. Whirledge S, Cidlowski JA. A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology. 2013;154(12):4450-68. [ DOI:10.1210/en.2013-1652] [ PMID] [ ] 39. Yu X, Li Z, Zhao X, Hua L, Liu S, He C, et al. Anti-Müllerian Hormone Inhibits FSH-Induced Cumulus Oocyte Complex In Vitro Maturation and Cumulus Expansion in Mice. Animals. 2022;12(9):1209. [ DOI:10.3390/ani12091209] 40. Sadeghi M, Chegini R, Sabbaghziarani F, Soleimani P, Ashtarimajelan M, Zafari F. Investigating the Effect of Atorvastatin on the Rate of Apoptosis in Mouse Oocytes. Cell and Tissue Journal. 2023;13(4):248-56. [ DOI:10.52547/JCT.13.4.248] 41. Shafiei A, Ehteram H, Akbari H, Kashani MM, Beigi M, Mahabadi JA, et al. The effect of chronic noise stress on serum levels of cortisol, gonadotropins, and sexual hormones at implantation time of mice. Comp Clin Path. 2017;26:779-84. [ DOI:10.1007/s00580-017-2446-y] 42. Calisir M, Yilmaz O, Kolatan HE, Sezgin AK. Effects of litter size and caging on physical and mental development in rats. Physiol. Behav. 2023;267:114200. [ DOI:10.1016/j.physbeh.2023.114200] [ PMID] 43. Love J, Zelikowsky M. Stress Varies Along the Social Density Continuum. Front. Syst. Neurosci. 2020;14. [ DOI:10.3389/fnsys.2020.582985] [ PMID] [ ] 44. Jalali M, Saki G, Sarkaki AR, Karami K, Nasri S. Effect of noise stress on count, progressive and non-progressive sperm motility, body and genital organ weights of adult male rats. J. Hum. Reprod. Sci. . 2012;5(1):48. [ DOI:10.4103/0974-1208.97801] [ ] 45. Jeong JY, Lee DH, Kang SS. Effects of chronic restraint stress on body weight, food intake, and hypothalamic gene expressions in mice. Endocrinol Metab. 2013;28(4):288-96. [ DOI:10.3803/EnM.2013.28.4.288] [ PMID] [ ] 46. Lin EJ, Sun M, Choi EY, Magee D, Stets CW, During MJ. Social overcrowding as a chronic stress model that increases adiposity in mice. Psychoneuroendocrinology. 2015;51:318-30. [ DOI:10.1016/j.psyneuen.2014.10.007] [ PMID] [ ] 47. Jiang Y, He Y, Pan X, Wang P, Yuan X, Ma B. Advances in Oocyte Maturation In Vivo and In Vitro in Mammals. Int. J. Mol. Sci.. 2023;24(10):9059. [ DOI:10.3390/ijms24109059] [ ] 48. Prasad S, Tiwari M, Pandey AN, Shrivastav TG, Chaube SK. Impact of stress on oocyte quality and reproductive outcome. J. Biomed. Sci. 2016;23:1-5. [ DOI:10.1186/s12929-016-0253-4] [ PMID] [ ] 49. Jeffrey JD, Gilmour KM. Programming of the hypothalamic-pituitary-interrenal axis by maternal social status in zebrafish (Danio rerio). J. Exp. Biol.. 2016;219(11):1734-43. [ DOI:10.1242/jeb.138826] [ PMID] 50. Mileva VR, Gilmour KM, Balshine S. Effects of maternal stress on egg characteristics in a cooperatively breeding fish. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2011;158(1):22-9. [ DOI:10.1016/j.cbpa.2010.08.017] [ PMID] 51. Lu J-H, Wang J-Z, Wang H-L, Sui H-S, Liu Y, Li J-J, et al. Damaging effect of cumulus denudation on rabbit oocytes. Fertil. Steril. 2010;93(5):1567-73. [ DOI:10.1016/j.fertnstert.2009.05.066] [ PMID] 52. Yuan H-J, Li Z-B, Zhao X-Y, Sun G-Y, Wang G-L, Zhao Y-Q, et al. Glucocorticoids impair oocyte competence and trigger apoptosis of ovarian cells via activating the TNF-α system. Reproduction. 2020;160(1):129-40. [ DOI:10.1530/REP-20-0025] 53. Sun L, Lv H, Wei W, Zhang D, Guan Y. Angiotensin-converting enzyme D/I and plasminogen activator inhibitor-1 4G/5G gene polymorphisms are associated with increased risk of spontaneous abortions in polycystic ovarian syndrome. J. Endocrinol. Invest. 2010;33:77-82. [ DOI:10.1007/BF03346557] [ PMID] 54. Peña Ó, Palumbo A, González-Fernández R, Hernández J, Naftolin F, Ávila J. Expression of angiotensin II type 1 (AT1) and angiotensin II type 2 (AT2) receptors in human granulosa-lutein (GL) cells: correlation with infertility diagnoses. Fertil. Steril. 2010;93(5):1601- [ DOI:10.1016/j.fertnstert.2009.03.092] [ PMID] 55. Kim J, You S. High Housing Density-Induced Chronic Stress Diminishes Ovarian Reserve via Granulosa Cell Apoptosis by Angiotensin II Overexpression in Mice. Int J Mol Sci. 2022;23(15):8614. [ DOI:10.3390/ijms23158614] [ PMID] 56. Chukwuebuka NB, Emeka OA, Irikefe OS, Iju WJ, Godsday O, Temitope O, et al. Stress-induced morphological changes of ovarian histology in female Wistar rats. Biomed Pharmacol J. 2020;13(4):1625-43. [ DOI:10.13005/bpj/2038] 57. Son YL, Ubuka T, Tsutsui K. Regulation of stress response on the hypothalamic-pituitary-gonadal axis via gonadotropin-inhibitory hormone. Front Neuroendocrinol. 2022;64:100953. [ DOI:10.1016/j.yfrne.2021.100953] [ PMID] 58. Díaz Pacheco M, Vargas Romero J, Rojas‐Maya S, Retana‐Márquez S. Effects of crowding and water restriction stress on creole goat reproduction in the Oaxacan Sierra Mixteca, Mexico. Reprod Domest Anim . 2018;53(6):1386-95. [ DOI:10.1111/rda.13267] [ PMID] 59. Ozawa H. Kisspeptin neurons as an integration center of reproductive regulation: Observation of reproductive function based on a new concept of reproductive regulatory nervous system. Reprod Med Biol. 2022;21(1):e12419. [ DOI:10.1002/rmb2.12419] [ PMID] [ ] 60. Lu W, Huang S, Liu J, Batsuren E, Li G, Wan X, et al. Effects of Group Size on Behavior, Reproduction, and mRNA Expression in Brains of Brandt's Voles. Brain Sci. 2023;13(2):311. [ DOI:10.3390/brainsci13020311] [ PMID] 61. Suvorov A. Population numbers and reproductive health. Endocrinology. 2021;162(11):bqab154. [ DOI:10.1210/endocr/bqab154] [ PMID] 62. Karin O, Raz M, Tendler A, Bar A, Korem Kohanim Y, Milo T, et al. A new model for the HPA axis explains dysregulation of stress hormones on the timescale of weeks. Mol Syst Biol . 2020;16(7):e9510. [ DOI:10.15252/msb.20209510] [ PMID] [ ] 63. Dong Y-z, Zhou F-j, Sun Y-p. Psychological stress is related to a decrease of serum anti-müllerian hormone level in infertile women. Reprod Biol. 2017;15(1):1-4. [ DOI:10.1186/s12958-017-0271-4] [ PMID] [ ] 64. Pankhurst MW. A putative role for anti-Müllerian hormone (AMH) in optimising ovarian reserve expenditure. J Endocrinol. 2017;233(1):R1-R13. [ DOI:10.1530/JOE-16-0522] [ PMID] 65. Whirledge S, Cidlowski JA. A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology. 2013;154(12):4450-68. [ DOI:10.1210/en.2013-1652] [ PMID] [ ] 66. Yu X, Li Z, Zhao X, Hua L, Liu S, He C, et al. Anti-Müllerian Hormone Inhibits FSH-Induced Cumulus Oocyte Complex In Vitro Maturation and Cumulus Expansion in Mice. Animals. 2022;12(9):1209. [ DOI:10.3390/ani12091209] [ PMID] [ ] 67. Sadeghi M, Chegini R, Sabbaghziarani F, Soleimani P, Ashtarimajelan M, Zafari F. Investigating the Effect of Atorvastatin on the Rate of Apoptosis in Mouse Oocytes. Cell and Tissue Journal. 2023;13(4):248-56. [ DOI:10.52547/JCT.13.4.248] 68. Shafiei A, Ehteram H, Akbari H, Kashani MM, Beigi M, Mahabadi JA, et al. The effect of chronic noise stress on serum levels of cortisol, gonadotropins, and sexual hormones at implantation time of mice. Comp Clin Path. 2017;26:779-84. [ DOI:10.1007/s00580-017-2446-y] 69. Calisir M, Yilmaz O, Kolatan HE, Sezgin AK. Effects of litter size and caging on physical and mental development in rats. Physiol. Behav. 2023;267:114200. [ DOI:10.1016/j.physbeh.2023.114200] [ PMID] 70. Love J, Zelikowsky M. Stress Varies Along the Social Density Continuum. Front. Syst. Neurosci. 2020;14. [ DOI:10.3389/fnsys.2020.582985] [ PMID] [ ] 71. Jalali M, Saki G, Sarkaki AR, Karami K, Nasri S. Effect of noise stress on count, progressive and non-progressive sperm motility, body and genital organ weights of adult male rats. J. Hum. Reprod. Sci. . 2012;5(1):48. [ DOI:10.4103/0974-1208.97801] [ PMID] [ ] 72. Jeong JY, Lee DH, Kang SS. Effects of chronic restraint stress on body weight, food intake, and hypothalamic gene expressions in mice. Endocrinol Metab. 2013;28(4):288-96. [ DOI:10.3803/EnM.2013.28.4.288] [ ] 73. Lin EJ, Sun M, Choi EY, Magee D, Stets CW, During MJ. Social overcrowding as a chronic stress model that increases adiposity in mice. Psychoneuroendocrinology. 2015;51:318-30. [ DOI:10.1016/j.psyneuen.2014.10.007] [ ] 74. Jiang Y, He Y, Pan X, Wang P, Yuan X, Ma B. Advances in Oocyte Maturation In Vivo and In Vitro in Mammals. Int. J. Mol. Sci.. 2023;24(10):9059. [ DOI:10.3390/ijms24109059] [ PMID] [ ] 75. Prasad S, Tiwari M, Pandey AN, Shrivastav TG, Chaube SK. Impact of stress on oocyte quality and reproductive outcome. J. Biomed. Sci. 2016;23:1-5. [ DOI:10.1186/s12929-016-0253-4] [ PMID] [ ] 76. Jeffrey JD, Gilmour KM. Programming of the hypothalamic-pituitary-interrenal axis by maternal social status in zebrafish (Danio rerio). J. Exp. Biol.. 2016;219(11):1734-43. [ DOI:10.1242/jeb.138826] [ PMID] 77. Mileva VR, Gilmour KM, Balshine S. Effects of maternal stress on egg characteristics in a cooperatively breeding fish. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2011;158(1):22-9. [ DOI:10.1016/j.cbpa.2010.08.017] [ PMID] 78. Lu J-H, Wang J-Z, Wang H-L, Sui H-S, Liu Y, Li J-J, et al. Damaging effect of cumulus denudation on rabbit oocytes. Fertil. Steril. 2010;93(5):1567-73. [ DOI:10.1016/j.fertnstert.2009.05.066] [ PMID] 79. Yuan H-J, Li Z-B, Zhao X-Y, Sun G-Y, Wang G-L, Zhao Y-Q, et al. Glucocorticoids impair oocyte competence and trigger apoptosis of ovarian cells via activating the TNF-α system. Reproduction. 2020;160(1):129-40. [ DOI:10.1530/REP-20-0025] 80. Sun L, Lv H, Wei W, Zhang D, Guan Y. Angiotensin-converting enzyme D/I and plasminogen activator inhibitor-1 4G/5G gene polymorphisms are associated with increased risk of spontaneous abortions in polycystic ovarian syndrome. J. Endocrinol. Invest. 2010;33:77-82. [ DOI:10.1007/BF03346557] 81. Peña Ó, Palumbo A, González-Fernández R, Hernández J, Naftolin F, Ávila J. Expression of angiotensin II type 1 (AT1) and angiotensin II type 2 (AT2) receptors in human granulosa-lutein (GL) cells: correlation with infertility diagnoses. Fertil. Steril. 2010;93(5):1601- [ DOI:10.1016/j.fertnstert.2009.03.092] [ PMID] |
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