Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-08T14:28:32.231Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential expression of FSHR and LHR genes and proteins during development of rabbit ovarian follicles

Published online by Cambridge University Press:  02 May 2022

Eman Khalil ,
Mohamed Metwally ,
Hatem Bahgaat ,
Ahmed Kassab Open the ORCID record for Ahmed Kassab [Opens in a new window]  and
Anwar El-Shafey
Eman Khalil
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt
Mohamed Metwally
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt
Hatem Bahgaat
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt
Ahmed Kassab*
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt
Anwar El-Shafey
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt
*
Author for correspondence: Ahmed A. Kassab, Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Benha University, Egypt. Tel: +20 1117313734. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The development of an ovarian follicle is a complex process at the cellular and molecular level that is mainly regulated by follicle-stimulating hormone receptor (FSHR) and luteinizing hormone receptor (LHR). To elucidate the contribution of these receptors to ovarian follicle development, it is necessary to determine their expression profiles during this biological process. Therefore, this study aimed to investigate the relationship between ovarian development pattern and the differential ovarian expression pattern of FSHR and LHR genes as well as proteins at different developmental stages. Ovaries were collected from 30 New Zealand rabbits at day 0 (birth), week 2 (neonate), week 4 (cub), week 16 (maturity), and day 18 pregnancy. Ovarian histology, and gene as well as protein expression were determined using light microscopy, real-time PCR and western blotting, respectively. The results showed that the expression levels of FSHR mRNA and protein increased coincidently with age and the growth of ovarian follicles. The levels of LHR mRNA and protein remained low from the day of birth until week 4 and became significantly higher by week 16 coinciding with appearance of growing and antral follicles, which have a defined thecal layer. FSHR gene and protein expression decreased with pregnancy, whereas LHR increased, reaching a peak level during pregnancy. It can be concluded that changes in FSHR and LHR gene and protein expression could be related to the growth and development of follicles, indicating the regulatory role for these receptors in rabbit folliculogenesis.

Keywords

FolliculogenesisFSHRLHROvaryRabbit
Type
Research Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 577 - 583
Copyright
© The Author(s), 2022. 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

Abd-Allah, SH, Shalaby, SM, Abd-Elbary, E, Saleh, AA and El-Magd, MA (2015). Human peripheral blood CD34+ cells attenuate oleic acid–induced acute lung injury in rats. Cytotherapy 17, 443–53.CrossRefGoogle ScholarPubMed
Abd-Elkareem, M (2010). Histomorphological studies on the development of the ovary of the rabbits during the postnatal period. MSc thesis. Assiut Univ. Assiut.Google Scholar
Al-Saffar, FJ and Almayahi, MS (2018). Histomorphological postnatal developmental study of the ovaries of the local rabbits (Oryctolagus cuniculus). Bas J Vet Res 17, 124–46.Google Scholar
Chakraborty, P and Roy, SK (2015). Expression of FSH receptor in the hamster ovary during perinatal development. Mol Cell Endocrinol 400, 41–7.CrossRefGoogle ScholarPubMed
Daniel-Carlier, N, Harscoët, E, Thépot, D, Auguste, A, Pailhoux, E and Jolivet, G (2013). Gonad differentiation in the rabbit: evidence of species-specific features. PLoS ONE 8, e60451.CrossRefGoogle ScholarPubMed
Dias, JA, Cohen, BD, Lindau-Shepard, B, Nechamen, CA, Peterson, AJ and Schmidt, A (2002). Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam Horm 64, 249–322.CrossRefGoogle ScholarPubMed
Donaubauer, EM and Hunzicker-Dunn, ME (2016). Extracellular signal-regulated kinase (ERK)-dependent phosphorylation of Y-box-binding protein 1 (YB-1) enhances gene expression in granulosa cells in response to follicle-stimulating hormone (FSH). J Biol Chem 291, 12145–60.CrossRefGoogle Scholar
Durlej, M, Knapczyk-Stwora, K, Duda, M, Galas, J and Slomczynska, M (2011). The expression of FSH receptor (FSHR) in the neonatal porcine ovary and its regulation by flutamide. Reprod Domest Anim 46, 377–84.CrossRefGoogle ScholarPubMed
Fawzy, AM, Ibrahim, S, Mahmoud, K, Heleil, BA, Ismail, IE, Almadaly, EA, El-Magd, MA and Ramoun, AA (2021). Differential molecular and hormonal changes in oocytes, granulosa cells and follicular fluid of pregnant and non-pregnant camels. Zygote, 1–8. doi: 10.1017/S096719942000091X.Google ScholarPubMed
Feldman, AT and Wolfe, D (2014). Tissue processing and hematoxylin and eosin staining. Methods Mol Biol 1180, 31–43.CrossRefGoogle ScholarPubMed
Goodman, SB, Kugu, K, Chen, SH, Preutthipan, S, Tilly, KI, Tilly, JL and Dharmarajan, AM (1998). Estradiol-mediated suppression of apoptosis in the rabbit corpus luteum is associated with a shift in expression of bcl-2 family members favoring cellular survival. Biol Reprod 59, 820–7.CrossRefGoogle ScholarPubMed
Hillier, SG (2001). Gonadotropic control of ovarian follicular growth and development. Mol Cell Endocrinol 179, 39–46.CrossRefGoogle ScholarPubMed
Hu, S, Zhu, M, Wang, J, Li, L, He, H, Hu, B, Hu, J and Xia, L (2021). Histomorphology and gene expression profiles during early ovarian folliculogenesis in duck and goose. Poult Sci 100, 1098–108.CrossRefGoogle ScholarPubMed
Hunter, MG, Robinson, RS, Mann, GE and Webb, R (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim Reprod Sci 82–83, 461–77.CrossRefGoogle ScholarPubMed
Hutt, KJ, McLaughlin, EA and Holland, MK (2006). Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell Tissue Res 326, 809–22.CrossRefGoogle ScholarPubMed
Jin, H, Won, M, Shin, E, Kim, HM, Lee, K and Bae, J (2017). EGR2 is a gonadotropin-induced survival factor that controls the expression of IER3 in ovarian granulosa cells. Biochem Biophys Res Commun 482, 877–82.CrossRefGoogle ScholarPubMed
Johnson, AL and Woods, DC (2009). Dynamics of avian ovarian follicle development: cellular mechanisms of granulosa cell differentiation. Gen Comp Endocrinol 163, 12–7.CrossRefGoogle ScholarPubMed
Kishi, H, Kitahara, Y, Imai, F, Nakao, K and Suwa, H (2018). Expression of the gonadotropin receptors during follicular development. Reprod Med Biol 17, 11–9.CrossRefGoogle ScholarPubMed
Lan, RX, Liu, F, He, ZB, Chen, C, Liu, SJ, Shi, Y, Liu, YL, Yoshimura, Y and Zhang, M (2014). Immunolocalization of GnRHRI, gonadotropin receptors, PGR, and PGRMCI during follicular development in the rabbit ovary. Theriogenology 81, 1139–47.CrossRefGoogle ScholarPubMed
Lei, L, Jin, S, Mayo, KE and Woodruff, TK (2010). The interactions between the stimulatory effect of follicle-stimulating hormone and the inhibitory effect of estrogen on mouse primordial folliculogenesis. Biol Reprod 82, 13–22.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–8.CrossRefGoogle ScholarPubMed
Mehl, NS, Khalid, M, Srisuwatanasagul, S, Swangchan-uthai, T and Sirivaidyapong, S (2017). Comparison of the ovarian and uterine reproductive parameters, and the ovarian mRNA and protein expression of LHR and FSHR between the prepubertal and adult female cats. Reprod Domest Anim 52 (Supplement 2), 41–4.CrossRefGoogle Scholar
Narayan, P, Ulloa-Aguirre, A and Dias, JA (2018). Gonadotropin hormones and their receptors. In: Yen and Jaffe’s Reproductive Endocrinology (eds Strauss J, Barbieri A and Gargiulo A), pp. 25–57. Philadelphia: Elsevier.Google Scholar
Ni, Y, Zhou, Y, Lu, L, Grossmann, R and Zhao, R (2007). Developmental changes of FSH-R, LH-R, ER-β and GnRH-I expression in the ovary of prepubertal ducks (Anas platyrhynchos). Anim Reprod Sci 100, 318–28.CrossRefGoogle Scholar
Niswender, GD, Juengel, JL, Silva, PJ, Rollyson, MK and McIntush, EW (2000). Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 80, 1–29.CrossRefGoogle ScholarPubMed
O’Shaughnessy, PJ, Dudley, K and Rajapaksha, WR (1996). Expression of follicle stimulating hormone-receptor mRNA during gonadal development. Mol Cell Endocrinol 125, 169–75.CrossRefGoogle ScholarPubMed
O’Shaughnessy, PJ, McLelland, D and McBride, MW (1997). Regulation of luteinizing hormone-receptor and follicle-stimulating hormone-receptor messenger ribonucleic acid levels during development in the neonatal mouse ovary. Biol Reprod 57, 602–8.CrossRefGoogle ScholarPubMed
Picut, CA, Dixon, D, Simons, ML, Stump, DG, Parker, GA and Remick, AK (2015). Postnatal ovary development in the rat: morphologic study and correlation of morphology to neuroendocrine parameters. Toxicol Pathol 43, 343–53.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 (Thessalonike, Greece) 26, 3.CrossRefGoogle ScholarPubMed
Rannikki, AS, Zhang, FP and Huhtaniemi, IT (1995). Ontogeny of follicle-stimulating hormone receptor gene expression in the rat testis and ovary. Mol Cell Endocrinol 107, 199–208.CrossRefGoogle ScholarPubMed
Ricken, AM and Viebahn, C (2002). Stage-specific expression of the mitochondrial germ cell epitope PG2 during postnatal differentiation of rabbit germ cells. Biol Reprod 67, 196–203.CrossRefGoogle ScholarPubMed
Saleh, AM (2013). Histological study of ovary through last periods (Oryctolagus cuniculus) of pregnancy in domestic rabbit. Kufa J Vetmed Sci 4, 11–9.Google Scholar
Saraiva, MVA, Celestino, JJH, Araújo, VR, Chaves, RN, Almeida, AP, Lima-Verde, IB, Duarte, ABG, Silva, GM, Martins, FS, Bruno, JB, Matos, MH, Campello, CC, Silva, JR and Figueiredo, JR (2011). Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles. Zygote 19, 205–14.CrossRefGoogle ScholarPubMed
Scarlet, D, Walter, I, Hlavaty, J and Aurich, C (2015). Expression and immunolocalisation of follicle-stimulating hormone receptors in gonads of newborn and adult female horses. Reprod Fertil Dev 28, 1340–8.CrossRefGoogle Scholar
Takagi, K, Yamada, T, Miki, Y, Umegaki, T, Nishimura, M and Sasaki, J (2007). Histological observation of the development of follicles and follicular atresia in immature rat ovaries. Acta Med Okayama 61, 283–98.Google ScholarPubMed
Vogel, C and Marcotte, EM (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13, 227–32.CrossRefGoogle ScholarPubMed
Wear, HM, McPike, MJ and Watanabe, KH (2016). From primordial germ cells to primordial follicles: a review and visual representation of early ovarian development in mice. J Ovarian Res 9, 36.CrossRefGoogle ScholarPubMed
Wu, W, Han, J, Cao, R, Zhang, J, Li, B, Liu, Z, Liu, K, Li, Q, Pan, Z, Chen, J and Liu, H (2015). Sequence and regulation of the porcine FSHR gene promoter. Anim Reprod Sci 154, 95–104.CrossRefGoogle ScholarPubMed
Yang, P, Wang, J, Shen, Y and Roy, SK (2004). Developmental expression of estrogen receptor (ER) α and ERβ in the hamster ovary: regulation by follicle-stimulating hormone. Endocrinology 145, 5757–66.CrossRefGoogle ScholarPubMed
Zachos, NC, Billiar, RB, Albrecht, ED and Pepe, GJ (2003). Developmental regulation of follicle-stimulating hormone receptor messenger RNA expression in the baboon fetal ovary. Biol Reprod 68, 1911–7.CrossRefGoogle ScholarPubMed
Zhang, M, Shi, H, Segaloff, DL and Van Voorhis, BJ (2001). Expression and localization of luteinizing hormone receptor in the female mouse reproductive tract. Biol Reprod 64, 179–87.CrossRefGoogle ScholarPubMed
Zheng, W, Magid, MS, Kramer, EE and Chen, YT (1996). Follicle-stimulating hormone receptor is expressed in human ovarian surface epithelium and fallopian tube. Am J Pathol 148, 47–53.Google ScholarPubMed
Ziecik, AJ, Kaczmarek, MM, Blitek, A, Kowalczyk, AE, Li, X and Rahman, NA (2007). Novel biological and possible applicable roles of LH/hCG receptor. Mol Cell Endocrinol 269, 51–60.CrossRefGoogle ScholarPubMed