Prenatally administered dexamethasone impairs folliculogenesis in spiny mouse offspring
Monika Hułas-Stasiak A C , Piotr Dobrowolski A and Ewa Tomaszewska B
+ Author Affiliations
- Author Affiliations
A Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Akademicka St.19, 20-033 Lublin, Poland.
B Department of Animal Biochemistry and Physiology, Faculty of Veterinary Medicine, University of Life Sciences, Akademicka St. 12, 20-950 Lublin, Poland.
C Corresponding author. Email: monsta1976@wp.pl
Reproduction, Fertility and Development 28(7) 1038-1048 https://doi.org/10.1071/RD14224
Submitted: 23 June 2014 Accepted: 21 November 2014 Published: 7 January 2015
Abstract
This study was designed to determine whether prenatal dexamethasone treatment has an effect on follicular development and atresia in the ovary of spiny mouse (Acomys cahirinus) offspring. Dexamethasone (125 µg kg–1 bodyweight per day) was administered to pregnant spiny mice from Day 20 of gestation to parturition. The processes of follicle loss were analysed using classical markers of apoptosis (terminal deoxynucleotidyl transferase-mediated dUTP nick end-labelling reaction, active caspase-3) and autophagy (Lamp1). The present study indicated that dexamethasone reduced the pool of healthy primordial follicles. Moreover, the oocytes from these follicles showed intensive caspase-3 and Lamp1 staining. Surprisingly, dexamethasone caused an increase in the number of secondary follicles; however, most of these follicles were characterised by extensive degeneration of the oocyte and caspase-3 and Lamp1 labelling. Western-blot analysis indicated that the glucocorticoid receptor as well as apoptosis and autophagy markers were more strongly expressed in the DEX-treated group than in the control. On the basis of these findings, we have concluded that dexamethasone impairs spiny mouse folliculogenesis and enhances follicular atresia through induction of autophagy or combined autophagy and apoptosis.
Additional keywords: apoptosis, autophagy, follicular atresia, ovary, prenatal development.
References
Amsterdam, A., Tajima, K., and Sasson, R. (2002). Cell-specific regulation of apoptosis by glucocorticoids: implication to their anti-inflammatory action. Biochem. Pharmacol. 64, 843–850.| Cell-specific regulation of apoptosis by glucocorticoids: implication to their anti-inflammatory action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1ymsrk%3D&md5=178548531501ea54c948abe1711b50c0CAS | 12213578PubMed |
Audette, M. C., Challis, J. R., Jones, R. L., Sibley, C. P., and Matthews, S. G. (2011). Antenatal dexamethasone treatment in midgestation reduces system A-mediated transport in the late-gestation murine placenta. Endocrinology 152, 3561–3570.
| Antenatal dexamethasone treatment in midgestation reduces system A-mediated transport in the late-gestation murine placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFOht7fP&md5=0ed5b6887d02b199dcef6763e54c3ec2CAS | 21733830PubMed |
Bradford, M. M. (1976). A rapid and sensitive method for quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for quantification of microgram quantities of protein utilising the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=84aec28e8a212c17872b05093c0cb556CAS | 942051PubMed |
Brunjes, P. C. (1984). Hippocampal maturation in the precocial murid rodent Acomys cahirinus. Brain Behav. Evol. 24, 58–64.
| Hippocampal maturation in the precocial murid rodent Acomys cahirinus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7nvFylsA%3D%3D&md5=5357a7c83658a2959c84129ba6d814b5CAS | 6713169PubMed |
Dickinson, H., Walker, D. W., Cullen-McEwen, L., Wintour, E. M., and Moritz, K. (2005). The spiny mouse (Acomys cahirinus) completes nephrogenesis before birth. Am. J. Physiol. Renal Physiol. 289, F273–F279.
| The spiny mouse (Acomys cahirinus) completes nephrogenesis before birth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXotFejtbs%3D&md5=f4e4231ec60e37f5690722a4ba40fee8CAS | 15741606PubMed |
Dickinson, H., Walker, D. W., Wintour, E. M., and Moritz, K. (2007). Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R453–R461.
| Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisFGhsrk%3D&md5=8626f68333ff07cc97c22bc68cb147c5CAS | 16946081PubMed |
Eisenberg-Lerner, A., Bialik, S., Simon, H. U., and Kimchi, A. (2009). Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 16, 966–975.
| Life and death partners: apoptosis, autophagy and the cross-talk between them.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsV2qs7o%3D&md5=e6ac22a70e7e76fefe49f36e49b14361CAS | 19325568PubMed |
Escobar, M. L., Echeverria, O. M., Ortiz, R., and Vasquez-Nin, G. H. (2008). Combined apoptosis and autophagy, the process that eliminates the oocytes of atretic follicles in immature rats. Apoptosis 13, 1253–1266.
| Combined apoptosis and autophagy, the process that eliminates the oocytes of atretic follicles in immature rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cngtFSntg%3D%3D&md5=661aa3b8a4e1bc974328e02311f4e745CAS | 18690537PubMed |
Eskelinen, E. L. (2006). Roles of Lamp-1 and Lamp-2 in lysosome biogenesis and autophagy. Mol. Asp. Med. 27, 495–502.
| Roles of Lamp-1 and Lamp-2 in lysosome biogenesis and autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVagtbvE&md5=619f7730890593357ae173704624e509CAS |
Evans, A. C., Mossa, F., Walsh, S. W., Scheetz, D., Jimenez-Krassel, F., Ireland, J. L., Smith, G. W., and Ireland, J. J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod. Domest. Anim. 47, 31–37.
| Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar | 22827347PubMed |
Gandolfi, F., Pocar, P., Brevini, T. A., and Fischer, B. (2002). Impact of endocrine disrupters on ovarian function and embryonic development. Domest. Anim. Endocrinol. 23, 189–201.
| Impact of endocrine disrupters on ovarian function and embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1WktLc%3D&md5=ed67d0af9a18d258563d1c4a7d48ee07CAS | 12142237PubMed |
Gao, H. B., Tong, M. T., Hu, H. Y., You, H. Y., Guo, Q. S., and Ge, R. S. (2002). Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 143, 130–138.
| Glucocorticoid induces apoptosis in rat Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVOrtQ%3D%3D&md5=74e20d309f0953cf4eab28d20a75c901CAS | 11751601PubMed |
Gao, H. B., Tong, M. T., Hu, H. Y., You, H. Y., Guo, Q. S., and Ge, R. S. (2003). Mechanism of glucocorticoid-induced Leydig cell apoptosis. Mol. Cell. Endocrinol. 199, 153–163.
| Mechanism of glucocorticoid-induced Leydig cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVCrt7c%3D&md5=8fe66becee2d412a98e4b2781de8b86cCAS | 12581887PubMed |
Ghafari, F., Gutierrez, C. G., and Hartshorne, G. M. (2007). Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one. BMC Dev. Biol. 7, 87.
| Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one.Crossref | GoogleScholarGoogle Scholar | 17650311PubMed |
González-Polo, R-A., Boya, P., Pauleau, A.-L., Jalil, P., Larochette, N., Souquère, S., Eskelinen, E.-L., Pierron, G., Saftig, P., and Kroemer, G. (2005). The apoptosis–autophagy paradox: autophagic vacuolisation before apoptotic death. J. Cell Sci. 118, 3091–3102.
| The apoptosis–autophagy paradox: autophagic vacuolisation before apoptotic death.Crossref | GoogleScholarGoogle Scholar | 15985464PubMed |
Gruver-Yates, A. L., and Cidlowski, J. A. (2013). Tissue-specific actions of glucocorticoids on apoptosis: a double-edged sword. Cells 2, 202–223.
| Tissue-specific actions of glucocorticoids on apoptosis: a double-edged sword.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKlu73J&md5=b4de768e71ace45d016869ea4605e3c0CAS | 24709697PubMed |
Hashemitabar, M., Orazizadeh, M., Khorsandi, L., and Albughobeish, N. (2009). Dexamethasone effects on Bax expression in the mouse testicular germ cells. Folia Histochem. Cytobiol. 47, 237–241.
Hulas, M., Gawron, A., and Orfin, G. (2003). A comparative study of ovary development in the precocial spiny mouse (Acomys cahirinus) and the altricial Norway rat (Rattus Norvegicus). Isr. J. Zool. 49, 307–313.
| A comparative study of ovary development in the precocial spiny mouse (Acomys cahirinus) and the altricial Norway rat (Rattus Norvegicus).Crossref | GoogleScholarGoogle Scholar |
Hułas-Stasiak, M., and Gawron, A. (2011). Follicular atresia in the prepubertal spiny mouse (Acomys cahirinus) ovary. Apoptosis 16, 967–975.
| Follicular atresia in the prepubertal spiny mouse (Acomys cahirinus) ovary.Crossref | GoogleScholarGoogle Scholar | 21739276PubMed |
Illera, J. C., Silvàn, G., Martinez, M. M., Blass, A., and Peña, L. (2005). The effect of dexamethasone on disruption of ovarian steroid levels and receptors in female rats. J. Physiol. Biochem. 61, 429–438.
| The effect of dexamethasone on disruption of ovarian steroid levels and receptors in female rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Gqs7w%3D&md5=e41939d64205a40b8b1239151a8e4e55CAS | 16440597PubMed |
Laane, E., Tamm, K.P., Buentke, E., Ito, K., Kharaziha, P., Oscarsson, J., Corcoran, M., Björklund, A.C., Hultenby, K., Lundin, J., Heyman, M., Söderhäll, S., Mazur, J., Porwit, A., Pandolfi, P. P., Zhivotovsky, B., Panaretakis, T., and Grandér, D. (2009). Cell death induced by dexamethasone in lymphoid leukaemia is mediated through initiation of autophagy. Cell Death Differ. 16, 1018–1029.
| Cell death induced by dexamethasone in lymphoid leukaemia is mediated through initiation of autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsV2qs78%3D&md5=c0b606f937f4108eab49fe6d8a5916bfCAS | 19390558PubMed |
Lamers, W. H., Mooren, P. G., and Charles, R. (1985a). Perinatal development of the small intestine and pancreas in rat and spiny mouse. Its relation to altricial and precocial timing of birth. Biol. Neonate 47, 153–162.
| Perinatal development of the small intestine and pancreas in rat and spiny mouse. Its relation to altricial and precocial timing of birth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSms7Y%3D&md5=1bc99e2309edc509cdc908a14ba1a615CAS | 3921064PubMed |
Lamers, W. H., Mooren, P. G., De Graaf, A., and Charles, R. (1985b). Perinatal development of the liver in rat and spiny mouse. Its relation to altricial and precocial timing of birth. Eur. J. Biochem. 146, 475–480.
| Perinatal development of the liver in rat and spiny mouse. Its relation to altricial and precocial timing of birth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXns1eqsg%3D%3D&md5=2505d3fa618ffcdd57b4dc15cd8b8e19CAS | 3967668PubMed |
Lamers, W. H., Mooren, P. G., Griep, H., Endert, E., Degenhart, H. J., and Charles, R. (1986). Hormones in perinatal rat and spiny mouse: relation to altricial and precocial timing of birth. Am. J. Physiol. 251, E78–E85.
| 1:CAS:528:DyaL28XkvFajs7Y%3D&md5=bfdc82c8681f8bb03eaf496514036dedCAS | 3524260PubMed |
Lee, C. Y., and Baehrecke, E. (2001). Steroid regulation of autophagic programmed cell death during development. Development 128, 1443–1455.
| 1:CAS:528:DC%2BD3MXjsFCjsrk%3D&md5=a603458a5f9402ff0f5d93f23fcf1853CAS | 11262243PubMed |
O’Connell, B. A., Moritz, K. M., Roberts, C. T., Walker, D. W., and Dickinson, H. (2011). The placental response to excess maternal glucocorticoid exposure differs between the male and female conceptus in spiny mouse. Biol. Reprod. 85, 1040–1047.
| The placental response to excess maternal glucocorticoid exposure differs between the male and female conceptus in spiny mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2is7fI&md5=87eb2126351e47bbf5f60e0707bb18baCAS | 21795670PubMed |
O’Connell, B. A., Moritz, K. M., Walker, D. W., and Dickinson, H. (2013a). Sexually dimorphic placental development throughout gestation in the spiny mouse (Acomys cahirinus). Placenta 34, 119–126.
| Sexually dimorphic placental development throughout gestation in the spiny mouse (Acomys cahirinus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s3ktVCnsA%3D%3D&md5=8dc217774a2e91bdec032337f6491e41CAS | 23260227PubMed |
O’Connell, B. A., Moritz, K. M., Walker, D. W., and Dickinson, H. (2013b). Synthetic glucocorticoid dexamethasone inhibits branching morphogenesis in the spiny mouse placenta. Biol. Reprod. 88, 26.
| Synthetic glucocorticoid dexamethasone inhibits branching morphogenesis in the spiny mouse placenta.Crossref | GoogleScholarGoogle Scholar | 23242523PubMed |
Orazizadeh, M., Khorsandi, L. S., and Hashemitabar, M. (2010). Toxic effects of dexamethasone on mouse testicular germ cells. Andrologia 42, 247–253.
| Toxic effects of dexamethasone on mouse testicular germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOntLfN&md5=b65492089955314ee75c6cd6ec956636CAS | 20629648PubMed |
Ortiz, R., Echeverria, O. M., Salgado, R., Escobar, M. L., and Vasquez-Nin, G. H. (2006). Fine structural and cytochemical analysis of the process of cell death of oocytes in atretic follicles in newborn and prepubertal rats. Apoptosis 11, 25–37.
| Fine structural and cytochemical analysis of the process of cell death of oocytes in atretic follicles in newborn and prepubertal rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFyntg%3D%3D&md5=d1059d02dc460d1b8f1f8915ca40edefCAS | 16374541PubMed |
Pattingre, S., Tassa, A., Qu, X., Garugi, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., and Levine, B. (2005). Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927–939.
| Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOrurbP&md5=15fe76e798d241412f9e0a9e7c6943a0CAS | 16179260PubMed |
Pedersen, T., and Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555–557.
| Proposal for a classification of oocytes and follicles in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M7jsFSgtw%3D%3D&md5=fc6c5a8cea7344ad0e15eeb31248c2cfCAS | 5715685PubMed |
Peters, H. (1969). The development of the mouse ovary from birth to maturity. Acta Endocrinol. (Copenh.) 62, 98–116.
| 1:STN:280:DyaF1M3psl2lsg%3D%3D&md5=34891d428a1fb05e11007b309f377962CAS | 5394354PubMed |
Poulain, M., Frydman, N., Duquenne, C., N’Tumba-Byn, T., Benachi, A., Habert, R., Rouiller-Fabre, V., and Livera, G. (2012). Dexamethasone induces germ-cell apoptosis in the human fetal ovary. J. Clin. Endocrinol. Metab. 97, E1890–E1897.
| Dexamethasone induces germ-cell apoptosis in the human fetal ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKku77P&md5=638dfae26c833384b1f137aa686bb19cCAS | 22802086PubMed |
Qin, W., Pan, J., Wu, Y., Bauman, W. A., and Cardozo, C. H. (2010). Protection against dexamethasone-induced muscle atrophy is related to modulation by testosterone of FOXO1 and PGC-1 α. Biochem. Biophys. Res. Commun. 403, 473–478.
| Protection against dexamethasone-induced muscle atrophy is related to modulation by testosterone of FOXO1 and PGC-1 α.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2mtL3K&md5=c4ec441b3a8f6dba42a0d0db850f8d13CAS | 21094144PubMed |
Quinn, T. A., Ratnayake, U., Dickinson, H., Nguyen, T. H., Mclntosh, M., Castillo-Melendez, M., Conley, A. J., and Walker, D. W. (2013). Ontogeny of the adrenal gland in the spiny mouse, with particular reference to production of the steroids cortisol and dehydroepiandrosterone. Endocrinology 154, 1190–1201.
| Ontogeny of the adrenal gland in the spiny mouse, with particular reference to production of the steroids cortisol and dehydroepiandrosterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsF2rtrg%3D&md5=90f3753745ba781df8c9ec2fb45e3cf7CAS | 23354096PubMed |
Ristić, N., Nestorović, N., Manojlović-Stojanoski, M., Filipović, B., Šošić-Jurjević, B., Milošević, V., and Sekulić, M. (2008). Maternal dexamethasone treatment reduces ovarian follicle number in neonatal rat offspring. J. Microsc. 232, 549–557.
| Maternal dexamethasone treatment reduces ovarian follicle number in neonatal rat offspring.Crossref | GoogleScholarGoogle Scholar | 19094039PubMed |
Rodrigues, P., Limback, D., McGinnis, L. K., Plancha, C. E., and Albertini, D. F. (2009). Multiple mechanisms of germ-cell loss in the perinatal mouse ovary. Reproduction 137, 709–720.
| Multiple mechanisms of germ-cell loss in the perinatal mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2ntbs%3D&md5=951a6b743973cc91e109148005b506a6CAS | 19176312PubMed |
Sasson, R., and Amsterdam, A. (2002). Stimulation of apoptosis in human granulosa cells from in vitro fertilisation patients and its prevention by dexamethasone: involvement of cell contact and Bcl-2 expression. J. Clin. Endocrinol. Metab. 87, 3441–3451.
| Stimulation of apoptosis in human granulosa cells from in vitro fertilisation patients and its prevention by dexamethasone: involvement of cell contact and Bcl-2 expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVGisrg%3D&md5=9bd98f702fdbca040729ccec7416c13eCAS | 12107264PubMed |
Shi, Y. (2002). Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 9, 459–470.
| Mechanisms of caspase activation and inhibition during apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVyltr0%3D&md5=cfbee9aedfbc9a6bf77465cad992efa6CAS | 11931755PubMed |
Singh, R. R., Cuffe, J. M., and Moritz, K. M. (2012). Short- and long-term effects of exposure to natural and synthetic glucocorticoids during development. Clin. Exp. Pharmacol. Physiol. 39, 979–989.
| Short- and long-term effects of exposure to natural and synthetic glucocorticoids during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFOqurnF&md5=514c5474802e49e5ddc9b0cc04ad98cfCAS | 22971052PubMed |
Śliwa, E., Tatara, M. R., Nowakowski, H., Pierzynowski, S. G., and Studziński, T. (2006). Effect of maternal dexamethasone and alpha-ketoglutarate administration on skeletal development during the last three weeks of prenatal life in pigs. J. Matern. Fetal Neonatal Med. 19, 489–493.
| Effect of maternal dexamethasone and alpha-ketoglutarate administration on skeletal development during the last three weeks of prenatal life in pigs.Crossref | GoogleScholarGoogle Scholar | 16966114PubMed |
Swanson, M. S. (2006). Autophagy: eating for good health. J. Immunol. 177, 4945–4951.
| Autophagy: eating for good health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVansr3N&md5=23e0c32872f8c176764a2db40b0c04fcCAS | 17015674PubMed |
Swerdlow, S., McColl, K., Rong, Y., Lam, M., Gupta, A., and Distelhorst, C. W. (2008). Apoptosis inhibition by Bcl-2 gives way to autophagy in glucocorticoid-treated lymphocytes. Autophagy 4, 612–620.
| Apoptosis inhibition by Bcl-2 gives way to autophagy in glucocorticoid-treated lymphocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVCkt7w%3D&md5=20964cb389152c4e71def92620e46954CAS | 18362516PubMed |
Tetsuka, M. (2007). Actions of glucocorticoid and their regulatory mechanisms in the ovary. Anim. Sci. J. 78, 112–120.
| Actions of glucocorticoid and their regulatory mechanisms in the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVOku74%3D&md5=58a07d628df16fbdd3739e045a71b86cCAS |
Tilly, J. L. (2003). Ovarian follicle counts – not as simple as 1, 2, 3. Reprod. Biol. Endocrinol. 1, 11.
| Ovarian follicle counts – not as simple as 1, 2, 3.Crossref | GoogleScholarGoogle Scholar | 12646064PubMed |
Tomaszewska, E., Dobrowolski, P., and Puzio, I. (2012). Postnatal administration of 2-oxoglutaric acid improves the intestinal barrier affected by the prenatal action of dexamethasone in pigs. Nutrition 28, 190–196.
| Postnatal administration of 2-oxoglutaric acid improves the intestinal barrier affected by the prenatal action of dexamethasone in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFynsQ%3D%3D&md5=1a7cce20e4e20df9592719d865153270CAS | 22018909PubMed |
Tomaszewska, E., Dobrowolski, P., and Puzio, I. (2013). Morphological changes of the cartilage and bone in newborn piglets evoked by experimentally induced glucocorticoid excess during pregnancy. J. Anim. Physiol. Anim. Nutr. (Berl.) 97, 785–796.
| Morphological changes of the cartilage and bone in newborn piglets evoked by experimentally induced glucocorticoid excess during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVersLfK&md5=46bc1efec14944df4a7e0a4f2aab23beCAS | 22716040PubMed |
Vackova, Z., Vagnerova, K., Libra, A., Miksik, I., Pacha, J., and Staud, F. (2009). Dexamethasone and betamethasone administration during pregnancy affects expression and function of 11β-hydroxysteroid dehydrogenase type 2 in the rat placenta. Reprod. Toxicol. 28, 46–51.
| Dexamethasone and betamethasone administration during pregnancy affects expression and function of 11β-hydroxysteroid dehydrogenase type 2 in the rat placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1KmtLc%3D&md5=e1d13c92d543d6b0559f2a7fb7071d5fCAS | 19490994PubMed |
Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, Ph. M., and Fowden, A. L. (2013). Adaptations in placental phenotype depend on route and timing of maternal dexamethasone administration in mice. Biol. Reprod. , .
| Adaptations in placental phenotype depend on route and timing of maternal dexamethasone administration in mice.Crossref | GoogleScholarGoogle Scholar | 23986571PubMed |
Wahbah, N. S., Abd El-Fattah, E. A., Ahmed, F. E., and Hassan, E. Z. (2010). Histological study of the effect of exogenous glucocorticoids on the testis of prepubertal albino rat. Egypt. J. Histol. 33, 353–364.
Yazawa, H., Sasagawa, I., and Nakada, T. (2000). Apoptosis of testicular germ cells induced by exogenous glucocorticoid in rat. Hum. Reprod. 15, 1917–1920.
| Apoptosis of testicular germ cells induced by exogenous glucocorticoid in rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvFOisb4%3D&md5=ebd7607b0794585f3710067fcceef250CAS | 10966986PubMed |
Young, D. A. (1976). Breeding and fertility of the Egyptian spiny mouse. Acomys cahirinus: effect of different environments. Lab. Anim. 10, 15–24.
| Breeding and fertility of the Egyptian spiny mouse. Acomys cahirinus: effect of different environments.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE287kvVWluw%3D%3D&md5=349b7713636717994a8e270c5021e6b8CAS | 1256010PubMed |
Yu, L., Lenardo, M., and Baehrecke, E. (2004). Autophagy and caspases a new cell death program. Cell Cycle 3, 1122–1124.
| Autophagy and caspases a new cell death program.Crossref | GoogleScholarGoogle Scholar |
