Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T21:41:36.710Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential molecular and hormonal changes in oocytes, granulosa cells and follicular fluid of pregnant and non-pregnant camels

Published online by Cambridge University Press:  07 April 2021

Ahmed M. Fawzy ,
Sally Ibrahim ,
Karima Mahmoud ,
Bassiouni A. Heleil ,
I. El-Kon Ismail ,
Essam A. Almadaly ,
Mohammed A. El-Magd Open the ORCID record for Mohammed A. El-Magd [Opens in a new window]  and
Adel A. Ramoun
Ahmed M. Fawzy
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
Sally Ibrahim
Affiliation:
Department of Animal Reproduction and Artificial Insemination, Veterinary Research Division, National Research Center, Dokki, Egypt
Karima Mahmoud
Affiliation:
Department of Animal Reproduction and Artificial Insemination, Veterinary Research Division, National Research Center, Dokki, Egypt
Bassiouni A. Heleil
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
I. El-Kon Ismail
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
Essam A. Almadaly
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
Mohammed A. El-Magd*
Affiliation:
Department of Anatomy & Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
Adel A. Ramoun
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
*
Author for correspondence: Mohammed A. El-Magd. Department of Anatomy & Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt. Email: mohamed.abouelmagd@vet.kfs.edu.eg
Get access Rights & Permissions [Opens in a new window]

Summary

This study aimed to compare the expression of genes regulating follicles development, survival and steroid hormones secretion in oocytes and granulosa cells (GCs) and study the correlation between their expression and follicular fluid (FF) levels of progesterone (P4) in pregnant and non-pregnant camels. In total, 138 ovarian pairs from slaughtered camels were used. Gene expression and hormonal assay were determined using real-time polymerase chain reaction (PCR) and enzyme-linked immunosorbent assay (ELISA), respectively. The obtained results revealed that the number of follicles (3–8 mm) was significantly (P < 0.05) lower in pregnant, compared with non-pregnant, camels. P4 level in the FF was significantly (P < 0.05) higher in pregnant, compared with non-pregnant, camels. However, no significant (P > 0.05) difference was noticed in the oestradiol (E2) level. STAR, PTEN, IGF1 and BCL2 mRNA levels were significantly higher in GCs and significantly lower in oocytes of pregnant, compared with non-pregnant, camels. However, follicle-stimulating hormone receptor (FSHR) mRNA level was significantly lower in GCs and oocytes, and the BMP15 mRNA level was significantly lower in oocytes of pregnant, compared with non-pregnant, camels. P4 level in FF was positively correlated with STAR, PTEN, IGF1 and BCL2 mRNA levels in GCs and negatively correlated with BMP15 mRNA levels in oocytes and FSHR mRNA levels in GCs and oocytes of pregnant camels. It could be concluded that pregnancy-induced variations in oocytes and GC expression of BMP15, IGF1, FSHR, STAR, BCL2, and PTEN genes might be associated with a decrease in the number of follicles and an increase in the FF level of P4.

Keywords

CamelsGene expressionGranulosa cellsOocytePregnancy
Type
Research Article
Information
Zygote , Volume 29 , Issue 6 , December 2021 , pp. 427 - 434
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdoon, A (2001). Factors affecting follicular population, oocyte yield and quality in camels (Camelus dromedarius) ovary with special reference to maturation time in vitro. Anim Reprod Sci 66, 71–9.CrossRefGoogle ScholarPubMed
Adam, M, Gholib, G, Hafizuddin, H, Zamzami, RS and Bahi, M (2019). Characteristic of ovarian and estradiol concentrations in the follicular fluid of slaughtered Aceh cattle. J Kedokt Hewan 13, 71–5.Google Scholar
Andersen, CL, Jensen, JL and Ørntoft, TF (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, 5245–50.CrossRefGoogle ScholarPubMed
Assidi, M, Dufort, I, Ali, A, Hamel, M, Algriany, O, Dielemann, S and Sirard, M-A (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol Reprod 79, 209–22.CrossRefGoogle ScholarPubMed
Basiouni, GF (2007). Follicular wave pattern, folliculogenesis and assisted reproductive techniques in the non-pregnant female dromedary camel (Camelus dromedarius): a review. J Biol Sci 7, 1038–45.CrossRefGoogle Scholar
Boruszewska, D, Sinderewicz, E, Kowalczyk-Zieba, I, Grycmacher, K and Woclawek-Potocka, I (2015). The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus–oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence. Reprod Biol Endocrinol 13, 1–18.CrossRefGoogle ScholarPubMed
Braw-Tal, R and Roth, Z (2005). Gene expression for LH receptor, 17α-hydroxylase and StAR in the theca interna of preantral and early antral follicles in the bovine ovary. Reproduction 129, 453–61.CrossRefGoogle Scholar
Caixeta, ES, Ripamonte, P, Franco, MM, Junior, JB and Dode, MAN (2009). Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reprod Fertil Dev 21, 655–64.CrossRefGoogle ScholarPubMed
Carpintero, NL, Suárez, OA, Mangas, CC, Varea, CG and Rioja, RG (2014). Follicular steroid hormones as markers of oocyte quality and oocyte development potential. J Hum Reprod Sci 7, 187.CrossRefGoogle ScholarPubMed
de Figueiredo, JR, de Lima, LF, Silva, JRV and Santos, RR (2018). Control of growth and development of preantral follicle: insights from in vitro culture. Anim Reprod 15, 648–59.CrossRefGoogle Scholar
Dube, JL, Wang, P, Elvin, J, Lyons, KM, Celeste, AJ and Matzuk, MM (1998). The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 12, 1809–17.CrossRefGoogle ScholarPubMed
El-Magd, MA, Ghoniem, AM, Helmy, NM, Abdelfattah-Hassan, A, Saleh, AA, Abd Allah, EA, Essawi, WM and Kahilo, KA (2019). Effect of myostatin inhibitor (myostatin pro-peptide) microinjection on in vitro maturation and subsequent early developmental stages of buffalo embryo. Theriogenology 126, 230–8.CrossRefGoogle ScholarPubMed
Emori, C and Sugiura, K (2014). Role of oocyte-derived paracrine factors in follicular development. Animal Sci J 85, 627–33.CrossRefGoogle ScholarPubMed
Fan, H, Ren, D and Hou, Y (2018). TLR7, a third signal for the robust generation of spontaneous germinal center B cells in systemic lupus erythematosus. Cell Mol Immunol 15, 286–8.CrossRefGoogle ScholarPubMed
Froment, P, Bontoux, M, Pisselet, C, Monget, P and Dupont, J (2005). PTEN expression in ovine granulosa cells increases during terminal follicular growth. FEBS Lett 579, 2376–82.CrossRefGoogle ScholarPubMed
George, JW, Dille, EA and Heckert, LL (2011). Current concepts of follicle-stimulating hormone receptor gene regulation. Biol Reprod 84, 7–17.CrossRefGoogle ScholarPubMed
Gong, H, Chen, Y, Xu, J, Xie, X, Yu, D, Yang, B and Kuang, H (2017). The regulation of ovary and conceptus on the uterine natural killer cells during early pregnancy. Reprod Biol Endocrinol 15, 73.CrossRefGoogle ScholarPubMed
Grimard, B, Marquant-Leguienne, B, Remy, D, Richard, C, Nuttinck, F, Humblot, P and Ponter, A (2013). Postpartum variations of plasma IGF and IGFBPs, oocyte production and quality in dairy cows: relationships with parity and subsequent fertility. Reprod Domest Anim 48, 183–94.CrossRefGoogle ScholarPubMed
Huang, J, Liu, Z, Xu, P, Zhang, Z, Yin, D, Liu, J, He, H and He, M (2018). Capsaicin prevents mitochondrial damage, protects cardiomyocytes subjected to anoxia/reoxygenation injury mediated by 14–3-3η/Bcl-2. Eur J Pharmacol 819, 43–50.CrossRefGoogle ScholarPubMed
Humblot, P, Holm, P, Lonergan, P, Wrenzycki, C, Lequarré, AS, Joly, CG, Herrmann, D, Lopes, A, Rizos, D, Niemann, H and Callesen, H (2005). Effect of stage of follicular growth during superovulation on developmental competence of bovine oocytes. Theriogenology 63, 1149–66.CrossRefGoogle ScholarPubMed
Ipsa, E, Cruzat, VF, Kagize, JN, Yovich, JL and Keane, KN (2019). Growth hormone and insulin-like growth factor action in reproductive tissues. Front Endocrinol 10, 777.CrossRefGoogle ScholarPubMed
Kafi, M, Mesbah, SF, Davoodian, N and Kadivar, A (2014). Fine structures of the oocyte in relation to serum, follicular fluid steroid hormones and IGF-I in the ovulatory-sized follicles in one-humped camel (Camelus dromedarius). Avicenna J Med Biotechnol 6, 57.Google Scholar
Khatir, H, Anouassi, A and Tibary, A (2007). Effect of follicular size on in vitro developmental competence of oocytes and viability of embryos after transfer in the dromedary (Camelus dromedarius). Anim Reprod Sci 99, 413–20.CrossRefGoogle Scholar
LaVoie, HA and King, SR (2009). Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B . Exp Biol Med 234, 880–907.CrossRefGoogle ScholarPubMed
Li, Y, Li, R-Q, Ou, S-B, Zhang, N-F, Ren, L, Wei, L-N, Zhang, Q-X and Yang, D-Z (2014). Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod Biol Endocrinol 12, 1–9.CrossRefGoogle ScholarPubMed
Ling, YH, Guo, XF, Chen, T, Ding, JP, Ma, YH, Chu, MX, Di, R, Zhang, YH and Zhang, XR (2016). Characterization and analysis of differentially expressed microRNAs in hircine ovaries during the follicular and luteal phases. Anim Reprod Sci 166, 47–57.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–DDCt method. Methods 25, 402–8.CrossRefGoogle Scholar
Lonergan, P, Rizos, D, Gutierrez-Adan, A, Fair, T and Boland, M (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod Domest Anim 38, 259–67.CrossRefGoogle ScholarPubMed
Mani, AM, Fenwick, MA, Cheng, Z, Sharma, MK, Singh, D and Wathes, DC (2010). IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction 139, 139.CrossRefGoogle ScholarPubMed
Melo, E, Cordeiro, D, Pellegrino, R, Wei, Z, Daye, ZJ, Nishimura, R and Dode, M (2017). Identification of molecular markers for oocyte competence in bovine cumulus cells. Anim Genet 48, 19–29.CrossRefGoogle ScholarPubMed
Moawad, AR, Ghoneim, IM, Darwish, GM, Badr, MR, El-Badry DA and EL-Wishy ABA (2020). Factors affecting in vitro embryo production: insights into dromedary camel. J Anim Reprod Biotechnol 35, 119–41.CrossRefGoogle Scholar
Moore, K and Thatcher, W (2006). Major advances associated with reproduction in dairy cattle. J Dairy Sci 89, 1254–66.CrossRefGoogle ScholarPubMed
Moulavi, F and Hosseini, S (2018). Diverse patterns of cumulus cell expansion during in vitro maturation reveal heterogeneous cellular and molecular features of oocyte competence in dromedary camel. Theriogenology 119, 259–67.CrossRefGoogle ScholarPubMed
Ola, SI and Sun, Q-Y (2012). Factors influencing the biochemical markers for predicting mammalian oocyte quality. J Reprod Dev 58, 385–92.CrossRefGoogle ScholarPubMed
Orisaka, M, Jiang, J-Y, Orisaka, S, Kotsuji, F and Tsang, BK (2009). Growth differentiation factor 9 promotes rat preantral follicle growth by up-regulating follicular androgen biosynthesis. Endocrinology 150, 2740–8.CrossRefGoogle ScholarPubMed
Otsuka, F, Yamamoto, S, Erickson, GF and Shimasaki, S (2001). Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J Biol Chem 276, 11387–92.CrossRefGoogle ScholarPubMed
Pieterse, M, Kappen, K, Kruip, TA and Taverne, M (1988). Aspiration of bovine oocytes during transvaginal ultrasound scanning of the ovaries. Theriogenology 30, 751–62.CrossRefGoogle ScholarPubMed
Quan, Q, Zheng, Q, Ling, Y, Fang, F, Chu, M, Zhang, X, Liu, Y and Li, W (2019). Comparative analysis of differentially expressed genes between the ovaries from pregnant and nonpregnant goats using RNA-seq. J Biol Res (Thessalon) 26, 3.CrossRefGoogle ScholarPubMed
Reddy, P, Liu, L, Adhikari, D, Jagarlamudi, K, Rajareddy, S, Shen, Y, Du, C, Tang, W, Hämäläinen, T and Peng, SL (2008). Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319, 611–3.CrossRefGoogle ScholarPubMed
Richards, JS (1994). Hormonal control of gene expression in the ovary. Endocr Rev 15, 725–51.CrossRefGoogle ScholarPubMed
Sargent, KM, Lu, N, Clopton, DT, Pohlmeier, WE, Brauer, VM, Ferrara, N, Silversides, DW and Cupp, AS (2015). Loss of vascular endothelial growth factor A (VEGFA) isoforms in granulosa cells using pDmrt-1-Cre or Amhr2-Cre reduces fertility by arresting follicular development and by reducing litter size in female mice. PLoS One 10, e0116332.CrossRefGoogle ScholarPubMed
Shimasaki, S, Moore, RK, Otsuka, F and Erickson, GF (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25, 72–101.CrossRefGoogle ScholarPubMed
Silva, J, Figueiredo, J and Van den Hurk, R (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–208.CrossRefGoogle ScholarPubMed
Silva, J, Van Den Hurk, R and Figueiredo, J (2016). Ovarian follicle development in vitro and oocyte competence: advances and challenges for farm animals. Domest Anim Endocrinol 55, 123–35.CrossRefGoogle ScholarPubMed
Tibary, A (2018). Monitoring and controlling follicular activity in camelids. Theriogenology 109, 22–30.CrossRefGoogle ScholarPubMed
Torner, H, Heleil, B, Alm, H, Ghoneim, I, Srsen, V, Kanitz, W, Tuchscherer, A and Fattouh, E (2003). Changes in cumulus–oocyte complexes of pregnant and non-pregnant camels (Camelus dromedarius) during maturation in vitro. Theriogenology 60, 977–87.CrossRefGoogle ScholarPubMed
Yamashita, Y, Okamoto, M, Kawashima, I, Okazaki, T, Nishimura, R, Gunji, Y, Hishinuma, M and Shimada, M (2011). Positive feedback loop between prostaglandin E2 and EGF-like factors is essential for sustainable activation of MAPK3/1 in cumulus cells during in vitro maturation of porcine cumulus–oocyte complexes. Biol Reprod 85, 1073–82.CrossRefGoogle ScholarPubMed
Yang, MY and Rajamahendran, R (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro . Anim Reprod Sci 70, 159–69.CrossRefGoogle ScholarPubMed
Zi, X-D, Chen, D-W and Wang, H-M (2012). Molecular characterization, mRNA expression of prolactin receptor (PRLR) gene during pregnancy, nonpregnancy in the yak (Bos grunniens). Gen Comp Endocrinol 175, 384–8.CrossRefGoogle Scholar