Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Chronic stress effects and their reversibility on the Fallopian tubes and uterus in rats

S. Divyashree A and H. N. Yajurvedi A B
+ Author Affiliations
- Author Affiliations

A Department of Zoology, University of Mysore, Manasagangotri, Mysuru-570006, India.

B Corresponding author. Email: hnyajurvedi@rediffmail.com

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17082
Submitted: 4 March 2017  Accepted: 23 June 2017   Published online: 26 July 2017

Abstract

The durational effects of chronic stress on the Fallopian tubes and uterus were studied by exposing rats to stressors in the form of restraint (1 h) and forced swimming (15 min) daily for 4, 8 or 12 weeks. One group of stressed rats from each time period was then maintained without exposure to stressors for a further 4 weeks to assess their ability to recover from stress. All time periods of stress exposure resulted in decreased weight of the body and Fallopian tubes; however, the relative weight of the uterus and serum concentrations of oestradiol and insulin increased significantly. The antioxidant potential was decreased with increased malondialdehyde concentrations in the Fallopian tubes following all durations of exposure and after 4 and 8 weeks of stress exposure in the uterus. Interestingly, rats stressed for 12 weeks showed an increase in serum testosterone concentration and antioxidant enzyme activities with a decrease in malondialdehyde concentration in the uterus. The antioxidant enzyme activities and malondialdehyde concentration in the Fallopian tubes of all recovery group rats were similar to stressed rats. However, in the uterus these parameters were similar to controls in recovery group rats after 4 weeks or 8 weeks of exposure, but after 12 weeks of stress exposure these parameters did not return to control levels following the recovery period. These results reveal, for the first time, that chronic stress elicits an irreversible decrease in antioxidant defence in the Fallopian tubes irrespective of exposure duration, whereas the uterus develops reversible oxidative stress under short-term exposure but increased antioxidant potential with endometrial proliferation following long-term exposure.

Additional keywords: antioxidant enzymes, endometrium, malondialdehyde, restraint, testosterone.


References

Aebi, H. (1984). Catalase in vitro methods. Methods Enzymol. 105, 121–126.
Catalase in vitro methods.CrossRef | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=aa97186b48704db9f8cb7817f01bba77CAS | open url image1

Agarwal, A., Gupta, S., and Sharma, R. K. (2005). Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 3, 28.
Role of oxidative stress in female reproduction.CrossRef | open url image1

Ahlbom, E., Prins, G. S., and Ceccatelli, S. (2001). Testosterone protects cerebellar granule cells from oxidative stress-induced cell death through a receptor mediated mechanism. Brain Res. 892, 255–262.
Testosterone protects cerebellar granule cells from oxidative stress-induced cell death through a receptor mediated mechanism.CrossRef | 1:CAS:528:DC%2BD3MXhtFSmtL0%3D&md5=b8457f30b70ee0fe69fe87ba96d8d20eCAS | open url image1

Allahbadia, G. N., and Merchant, R. (2011). Polycystic ovary syndrome and impact on health. Middle East Fertil. Soc. J. 16, 19–37.
Polycystic ovary syndrome and impact on health.CrossRef | open url image1

Alvarez, S. M., Biaggio, V. S., Ciminari, M. E., Piguillem, S. N., Guinazu, A. B. P., Correas, S. M. E., Chaca, M. V. P., and Gomez, N. N. (2015). Androgen deprivation and cytoprotective parameters in rat lung. Int. J. Res. Stud. Biosci. 3, 150–163. open url image1

Benzie, I. F., and Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal. Biochem. 239, 70–76.
The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay.CrossRef | 1:CAS:528:DyaK28XksFCmt7Y%3D&md5=330f229599e8f95753d826bc86af9a52CAS | open url image1

Bhat, M. S., and Yajurvedi, H. N. (2011). Stress induced alterations in pre-pubertal ovarian follicular development in rat. J. Stress Physiol. Biochem. 7, 51–68. open url image1

Chatterjee, A., and Chatterjee, R. (2009). How stress affects female reproduction: an overview. Biomed. Res. 20, 79–83.
| 1:CAS:528:DC%2BC3cXnvFWgu7g%3D&md5=093fe7b8a95629df21d8addbf388cf4fCAS | open url image1

Cooper, R. L., Goldman, J. M., and Vandenbergh, J. G. (1993). Monitoring of the estrous cycle in the laboratory rodent by vaginal lavage. In ‘Methods in Toxicology: Female Reproductive Toxicology’. (Eds J. J. Heindel and R. E. Chapin.) pp. 45–56. (Academic Press: San Diego.)

Daley, C. A., Macfarlane, M. S., Sakurai, H., and Adams, T. E. (1999). Effect of stress-like concentrations of cortisol on follicular development and the preovulatory surge of luteinizing hormone in sheep. J. Reprod. Fertil. 117, 11–16.
Effect of stress-like concentrations of cortisol on follicular development and the preovulatory surge of luteinizing hormone in sheep.CrossRef | 1:CAS:528:DyaK1MXmtlaltrk%3D&md5=fdb890edfe9b665157533fdbdabe88e2CAS | open url image1

Dechanet, C., Anahory, T., Mathieu Daude, J. C., Quantin, X., Reyftmann, L., Hamamah, S., Hedon, B., and Dechaud, H. (2011). Effects of cigarette smoking on reproduction. Hum. Reprod. Update 17, 76–95.
Effects of cigarette smoking on reproduction.CrossRef | 1:CAS:528:DC%2BC3cXhsF2rsbrM&md5=1154e4321a91dfd3096ddede1e4d3fedCAS | open url image1

Devaki, M., Nirupama, R., and Yajurvedi, H. N. (2013). Chronic stress-induced oxidative damage and hyperlipidemia are accompanied by atherosclerotic development in rats. Stress 16, 233–243.
Chronic stress-induced oxidative damage and hyperlipidemia are accompanied by atherosclerotic development in rats.CrossRef | 1:CAS:528:DC%2BC3sXit1Wntrk%3D&md5=82f7ca4161c9eccc954fe82aba0bd43eCAS | open url image1

Diamanti-Kandarakis, E., Bourguignon, J. P., Giudice, L. C., Hauser, R., Prins, G. S., Soto, A. M., Zoeller, R. T., and Gore, A. C. (2009). Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr. Rev. 30, 293–342.
Endocrine-disrupting chemicals: an endocrine society scientific statement.CrossRef | 1:CAS:528:DC%2BD1MXosVejt74%3D&md5=b035e0f12a347eccff21b5ed446472e4CAS | open url image1

Divyashree, S., and Yajurvedi, H. N. (2016). Long-term chronic stress exposure induces PCO phenotype in rat. Reproduction 152, 765–774.
Long-term chronic stress exposure induces PCO phenotype in rat.CrossRef | 1:CAS:528:DC%2BC2sXktlajsbw%3D&md5=a7fd38596357b7205e24c4d2802c810dCAS | open url image1

Dorfman, M., Arancibia, S., Fiedler, J. L., and Lara, H. E. (2003). Chronic intermittent cold stress activates ovarian sympathetic nerves and modifies ovarian follicular development in the rat. Biol. Reprod. 68, 2038–2043.
Chronic intermittent cold stress activates ovarian sympathetic nerves and modifies ovarian follicular development in the rat.CrossRef | 1:CAS:528:DC%2BD3sXks1Ggs7Y%3D&md5=e95c06b7bfcd90d8cff1e86aea02d1a9CAS | open url image1

Eroschenko, V. P. (1982). Surface changes in oviduct, uterus and vaginal cell of neonatal mice after estradiol-17 beta and insecticide chlordecone (Kepone) treatment: a scanning electron microscopic study. Biol. Reprod. 26, 707–720.
Surface changes in oviduct, uterus and vaginal cell of neonatal mice after estradiol-17 beta and insecticide chlordecone (Kepone) treatment: a scanning electron microscopic study.CrossRef | 1:CAS:528:DyaL38XktVWqsrk%3D&md5=d45f9bdade294b3bbc560d59efde5839CAS | open url image1

Fontella, F. U., Siqueira, I. R., Vasconcellos, A. P., Tabajara, A. S., Netto, C. A., and Dalmaz, C. (2005). Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem. Res. 30, 105–111.
Repeated restraint stress induces oxidative damage in rat hippocampus.CrossRef | 1:CAS:528:DC%2BD2MXotV2gug%3D%3D&md5=d33b72bbc48d7abc2cbf4915d9d8277aCAS | open url image1

García-Díaz, E. C., Gómez-Quiroz, L. E., Arenas-Ríos, E., Aragón-Martínez, A., Ibarra-Arias, J. A., and del Socorro I. Retana-Marquez, M. (2015). Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat. Syst. Biol. Reprod. Med. 61, 150–160.
Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat.CrossRef | open url image1

Grissom, N., Kerr, W., and Bhatnagar, S. (2008). Struggling behavior during restraint is regulated by stress experience. Behav. Brain Res. 191, 219–226.
Struggling behavior during restraint is regulated by stress experience.CrossRef | open url image1

Gudipudi, S., Puranik, D. S., Alla, R., Ajjarapu, U., and Kistammagari, T. R. (2015). Role of Euphorbia thymifolia L. ethanolic root extract in treating female reproductive dysfunction in rats. Int. J. Pharmacol. Research. 5, 75–79. open url image1

Gupta, S., Sekhon, L., Aziz, N., and Agarwal, A. (2008). The impact of oxidative stress on female reproduction and ART: evidence-based review. In ‘Infertility and Assisted Reproduction’. (Eds A. Makrigiannakis, B. Rizk, J.G. Velasco and H. Sallam.) pp. 178–86. (Cambridge UP: New York.)

Gupta, S., Ghulmiyyah, J., Sharma, R., Halabi, J., and Agarwal, A. (2014). Power of proteomics in linking oxidative stress and female infertility. Biomed. Res. Int. 2014, 916212.
Power of proteomics in linking oxidative stress and female infertility.CrossRef | open url image1

Habig, W. H., Babst, M. J., and Jakoby, W. J. (1974). Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139.
| 1:CAS:528:DyaE2MXltlahtg%3D%3D&md5=66678bac8ee1341ff7616433ce48041cCAS | open url image1

Jansen, R. P. (1984). Endocrine response in the fallopian tube. Endocr. Rev. 5, 525–551.
Endocrine response in the fallopian tube.CrossRef | 1:CAS:528:DyaL2MXhslOnsA%3D%3D&md5=7867559445e87ca211a274d82fda22b1CAS | open url image1

Jeong, J. Y., Lee, D. H., and Kang, S. S. (2013). Effects of chronic restraint stress on body weight, food intake, and hypothalamic gene expressions in mice. Endocrinol. Metab. (Seoul) 28, 288–296.
Effects of chronic restraint stress on body weight, food intake, and hypothalamic gene expressions in mice.CrossRef | open url image1

Koricanac, G., Milosavljevic, T., Stojiljkovic, M., Zakula, Z., Ribarac-Stepic, N., and Isenovic, E. R. (2008). Insulin signaling in the liver and uterus of ovariectomized rats treated with estradiol. J. Steroid Biochem. Mol. Biol. 108, 109–116.
Insulin signaling in the liver and uterus of ovariectomized rats treated with estradiol.CrossRef | 1:CAS:528:DC%2BD1cXhsFynsbg%3D&md5=c48865aff7128ca25d93d892cd362922CAS | open url image1

Lian, H.-Y., Gao, Y., Jiao, G.-Z., Sun, M.-J., Wu, X.-F., Wang, T.-Y., Li, H., and Ten, J.-H. (2013). Antioxidant supplementation overcomes the deleterious effects of maternal restraint stress-induced oxidative stress on mouse oocytes. Reproduction 146, 559–568.
Antioxidant supplementation overcomes the deleterious effects of maternal restraint stress-induced oxidative stress on mouse oocytes.CrossRef | 1:CAS:528:DC%2BC3sXhvFynt73L&md5=dd0d41d9e2dffd4bbb720fd745ff7948CAS | open url image1

Liu, J., Wang, X., Shigenaga, M. K., Yeo, H. C., Mori, A., and Ames, B. N. (1996). Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J. 10, 1532–1538.
| 1:CAS:528:DyaK28XntFWku78%3D&md5=c17b04187ff89d351531c987aaceb215CAS | open url image1

Liu, G., Dong, Y., Wang, Z., Cao, J., and Chen, Y. (2014). Restraint stress alters immune parameters and induces oxidative stress in mouse uterus during embryo implantation. Stress 17, 494–503.
Restraint stress alters immune parameters and induces oxidative stress in mouse uterus during embryo implantation.CrossRef | 1:CAS:528:DC%2BC2cXhvFCitLbL&md5=f1090226f8db14d96eaa6d08b0294d79CAS | open url image1

Marklund, S., and Marklund, G. (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for SOD. Eur. J. Biochem. 47, 469–474.
Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for SOD.CrossRef | 1:CAS:528:DyaE2MXhtlGm&md5=445c70c5987cd6c91ed31c15a47ba0e2CAS | open url image1

Nirupama, M., and Yajurvedi, H. N. (2013). Durational effects of chronic stress on the testicular damage and its reversibility in albino rat. Euro. J. Exp. Bio. 3, 229–239.
| 1:CAS:528:DC%2BC2cXntVGjtrw%3D&md5=db153e410e1c20038df8fee8b2752cf6CAS | open url image1

Nirupama, R., Devaki, M., and Yajurvedi, H. N. (2010). Repeated acute stress induced alterations in carbohydrate metabolism in rat. J. Stress Physiol. Biochem. 6, 44–55. open url image1

Ohkawa, H., Ohishi, N., and Yogi, K. (1979). Assay for LPO in animal tissue by thiobarbituric acid reaction. Anal. Biochem. 95, 351–358.
Assay for LPO in animal tissue by thiobarbituric acid reaction.CrossRef | 1:CAS:528:DyaE1MXksFaisbk%3D&md5=a58c04dcf7264317a4ad5482e83c4e93CAS | open url image1

Okada, A., Ohta, Y., Inoue, S., Hiroi, H., Muramatsu, M., and Iguchi, T. (2003). Expression of estrogen, progesterone and androgen receptors in the oviduct of developing, cycling and pre-implantation rats. J. Mol. Endocrinol. 30, 301–315.
Expression of estrogen, progesterone and androgen receptors in the oviduct of developing, cycling and pre-implantation rats.CrossRef | 1:CAS:528:DC%2BD3sXkslCgs7g%3D&md5=864d9c9b97f66f5eb9b9acd1baf4bf6cCAS | open url image1

Ozawa, M., Tabayashi, D., Latief, T. A., Shimizu, T., Oshima, I., and Kanai, Y. (2005). Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats. Reproduction 129, 621–630.
Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats.CrossRef | 1:CAS:528:DC%2BD2MXksFGku7Y%3D&md5=bb2333c394ba6e7291e29a5911aa2e37CAS | open url image1

Paredes, A., Galvez, A., Leyton, V., Aravena, G., Fiedler, J. L., Bustamante, D., and Lara, H. E. (1998). Stress promotes development of ovarian cysts in rats. Endocrine 8, 309–315.
Stress promotes development of ovarian cysts in rats.CrossRef | 1:CAS:528:DyaK1cXltFGnu7w%3D&md5=14ae200cebba70c24f12b4c1bdc90944CAS | open url image1

Pelletier, G., Labrie, C., and Labrie, F. (2000). Localization of oestrogen receptor α, oestrogen receptor β and androgen receptors in the rat reproductive organs. J. Endocrinol. 165, 359–370.
Localization of oestrogen receptor α, oestrogen receptor β and androgen receptors in the rat reproductive organs.CrossRef | 1:CAS:528:DC%2BD3cXjvFegt7o%3D&md5=9908bf6372af17943b67bac3efaa785eCAS | open url image1

Rabin, D. S., Johnson, E. O., Brandon, D. D., Liapi, C., and Chrousos, G. P. (1990). Glucocorticoid inhibit estradiol-mediated uterine growth: possible role of the uterine estradiol receptor. Biol. Reprod. 42, 74–80.
Glucocorticoid inhibit estradiol-mediated uterine growth: possible role of the uterine estradiol receptor.CrossRef | 1:CAS:528:DyaK3cXhsFajt78%3D&md5=7dc844172707906a908937bb5aa6b5f5CAS | open url image1

Rhen, T., and Cidlowski, J. A. (2006). Estrogens and glucocorticoids have opposing effects on the amount and latent activity of complement proteins in the rat uterus. Biol. Reprod. 74, 265–274.
Estrogens and glucocorticoids have opposing effects on the amount and latent activity of complement proteins in the rat uterus.CrossRef | 1:CAS:528:DC%2BD28Xot1Klsg%3D%3D&md5=4ccec8b6a0c0fcdda2606055493e42f3CAS | open url image1

Roozendaal, M. M., Swarts, H. J. M., Wiegant, V. M., and Mattheij, J. A. M. (1995). Effect of restraint stress on the preovulatory luteinizing homone profile and ovulation in the rat. Eur. J. Endocrinol. 133, 347–353.
Effect of restraint stress on the preovulatory luteinizing homone profile and ovulation in the rat.CrossRef | 1:CAS:528:DyaK2MXos1yhtLw%3D&md5=5b0fbdf7a10e19dd17a739797677d9caCAS | open url image1

Roth, Z., Meidan, R., Braw-Tal, R., and Wolfenson, D. (2000). Immediate and delayed effects of heat stress on follicular development and its association with plasma follicule stimulating hormone and inhibin concentration in cows. J. Reprod. Fertil. 120, 83–90.
| 1:CAS:528:DC%2BD3cXntlCiurs%3D&md5=dc1e1d82bef641535b48cf53ccbf0ac0CAS | open url image1

Said, R. S., Nada, A. S., and El-Demerdash, E. (2012). Sodium selenite improves folliculogenesis in radiation-induced ovarian failure: a mechanistic approach. PLoS One 7, e50928.
Sodium selenite improves folliculogenesis in radiation-induced ovarian failure: a mechanistic approach.CrossRef | 1:CAS:528:DC%2BC38XhvV2js7jK&md5=396c69dfdf46b0bd348b8debc04af9e0CAS | open url image1

Saraswathi, C. D., Gupta, S. K., and Sreemantula, S. (2012). Protective effect of Symplocos racemosa bark on cold restraint stress induced reproductive changes in female rats. J. Nat. Prod. 5, 251–258. open url image1

Shao, R., Egecioglu, E., Weijdegard, B., Kopchick, J. J., Fernandez-Rodriguez, J., Anderson, N., and Billig, H. (2007). Dynamic regulation of estrogen receptor α isoform expression in the mouse Fallopian tube: mechanistic insight into estrogen-dependent production and secretion of insulin-like growth factors. Am. J. Physiol. Endocrinol. Metab. 293, E1430–E1442.
Dynamic regulation of estrogen receptor α isoform expression in the mouse Fallopian tube: mechanistic insight into estrogen-dependent production and secretion of insulin-like growth factors.CrossRef | 1:CAS:528:DC%2BD2sXhtlenurjO&md5=473e84e098bd206db7a58b6d415bc4ceCAS | open url image1

Simitsidellis, I., Gibson, D. A., Cousins, F. L., Esnal-Zufiaurre, A., and Saunders, P. T. K. (2016). A role for androgens in epithelial proliferation and formation of glands in the mouse uterus. Endocrinology 157, 2116–2128.
A role for androgens in epithelial proliferation and formation of glands in the mouse uterus.CrossRef | 1:CAS:528:DC%2BC28XhsVGnsbrO&md5=7480114e192688a00d0ace956a157f10CAS | open url image1

Tappel, A. L. (1978). GPx and hydroperoxidase. Methods Enzymol. 52, 506–513.
GPx and hydroperoxidase.CrossRef | 1:CAS:528:DyaE1MXjsFertw%3D%3D&md5=715280d76d88ddafa260c2bd570c4034CAS | open url image1

Whirledge, S., and Cidlowski, J. A. (2010). Glucocorticoid, stress, and fertility. Minerva Endocrinol. 35, 109–125.
| 1:STN:280:DC%2BC3cnktl2ntw%3D%3D&md5=9997982dd10b1c1ec43cceb5469ad08aCAS | open url image1

Zhang, S. Y., Wang, J. Z., Li, J. J., Wei, D. L., Sui, H. S., Zhang, Z. H., Zhou, P., and Tan, J. H. (2011). Maternal restraint stress diminishes the developmental potential of oocytes. Biol. Reprod. 84, 672–681.
Maternal restraint stress diminishes the developmental potential of oocytes.CrossRef | 1:CAS:528:DC%2BC3MXjvFanur0%3D&md5=48978160cc1d0c47d6926611771aa371CAS | open url image1



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