Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T01:37:42.465Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression of steroidogenic enzymes and TGFβ superfamily members in follicular cells of prepubertal gilts with distinct endocrine profiles

Published online by Cambridge University Press:  10 May 2021

Veronica Hoyos-Marulanda ,
Cristina S. Haas ,
Karina L. Goularte ,
Monique T. Rovani ,
Rafael G. Mondadori ,
Arnaldo D. Vieira ,
Bernardo G. Gasperin  and
Thomaz Lucia Jr Open the ORCID record for Thomaz Lucia Jr [Opens in a new window]
Veronica Hoyos-Marulanda
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Cristina S. Haas
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Karina L. Goularte
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Monique T. Rovani
Affiliation:
Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Rafael G. Mondadori
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Instituto de Biologia, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Arnaldo D. Vieira
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Bernardo G. Gasperin
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas-RS, Brazil
Thomaz Lucia Jr*
Affiliation:
ReproPel, Universidade Federal de Pelotas, Pelotas-RS, Brazil Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas-RS, Brazil
*
Author for correspondence: Thomaz Lucia Jr. ReproPel, Faculdade de Veterinária, Universidade Federal de Pelotas, 96010-900, Pelotas-RS, Brazil. E-mails: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Regulation of the transforming growth factor beta (TGFβ) superfamily by gonadotrophins in swine follicular cells is not fully understood. This study evaluated the expression of steroidogenic enzymes and members of the TGFβ superfamily in prepubertal gilts allocated to three treatments: 1200 IU eCG at D −3 (eCG); 1200 IU eCG at D −6 plus 500 IU hCG at D −3 (eCG + hCG); and the control, composed of untreated gilts. Blood samples and ovaries were collected at slaughter (D0) and follicular cells were recovered thereafter. Relative gene expression was determined by real-time PCR. Serum progesterone levels were greater in the eCG + hCG group compared with the other groups (P < 0.01). No differences were observed in the expression of BMP15, BMPR1A, BMPR2, FSHR, GDF9, LHCGR and TGFBR1 (P > 0.05). Gilts from the eCG group presented numerically greater mean expression of CYP11A1 mRNA than in the control group that approached statistical significance (P = 0.08) and greater expression of CYP19A1 than in both the eCG and the control groups (P < 0.05). Expression of BMPR1B was lower in the eCG + hCG treatment group compared with the control (P < 0.05). In conclusion, eCG treatment increased the relative expression of steroidogenic enzymes, whereas treatment with eCG + hCG increased serum progesterone levels. Although most of the evaluated TGFβ members were not regulated after gonadotrophin treatment, the downregulation of BMPR1B observed after treatment with eCG + hCG and suggests a role in luteinization regulation.

Keywords

BMPR1BFollicleGenesGiltsGonadotrophinSteroids
Type
Research Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 65 - 71
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

Agca, C, Ries, JE, Kolath, SJ, Kim, JH, Forrester, LJ, Antoniou, E, Whitworth, KM, Mathialagan, N, Springer, GK, Prather, RS and Lucy, MC (2006). Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132, 133–45.10.1530/rep.1.01163CrossRefGoogle ScholarPubMed
Albrecht, BA and Daels, PF (1997). Immunolocalization of 3 beta-hydroxysteroid dehydrogenase, cytochrome P450 17 alpha-hydroxylase/17,20-lyase and cytochrome P450 aromatase in the equine corpus luteum of dioestrus and early pregnancy. J Reprod Fert 111, 127–33.CrossRefGoogle ScholarPubMed
Bao, B and Garverick, HA (1998). Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J Anim Sci 76, 1903–21.CrossRefGoogle ScholarPubMed
Bordignon, V, El-Beirouthi, N, Gasperin, BG, Albornoz, MS, Martinez-Diaz, MA, Schneider, C, Laurin, D, Zadworny, D and Agellon, LB (2013). Production of cloned pigs with targeted attenuation of gene expression. PLoS One, 8, e64613.10.1371/journal.pone.0064613CrossRefGoogle ScholarPubMed
Bramble, MS, Goldstein, EH, Lipson, A, Ngun, T, Eskin, A, Gosschalk, JE, Roach, L, Vashist, N, Barseghyan, H, Lee, E, Arboleda, VA, Vaiman, D, Yuksel, Z, Fellous, M and Vilain, E (2016). A novel follicle-stimulating hormone receptor mutation causing primary ovarian failure: a fertility application of whole exome sequencing. Hum Reprod 31, 905–14.CrossRefGoogle ScholarPubMed
Du, X, Zhang, L, Li, X, Pan, Z, Liu, H and Li, Q (2016). TGF-beta signaling controls FSHR signaling-reduced ovarian granulosa cell apoptosis through the SMAD4/miR-143 axis. Cell Death Dis 7, e2476.CrossRefGoogle ScholarPubMed
Edson, MA, Nalam, RL, Clementi, C, Franco, HL, Demayo, FJ, Lyons, KM, Pangas, SA and Matzuk, MM (2010). Granulosa cell-expressed BMPR1A and BMPR1B have unique functions in regulating fertility but act redundantly to suppress ovarian tumor development. Mol Endocrinol 24, 1251–66.CrossRefGoogle ScholarPubMed
Esbenshade, KL, Paterson, AM, Cantley, TC and Day, BN (1982). Changes in plasma hormone concentrations associated with the onset of puberty in the gilt. J Anim Sci 54, 320–4.CrossRefGoogle ScholarPubMed
Estienne, A, Pierre, A, di Clemente, N, Picard, JY, Jarrier, P, Mansanet, C, Monniaux, D and Fabre, S (2015). Anti-Müllerian hormone regulation by the bone morphogenetic proteins in the sheep ovary: deciphering a direct regulatory pathway. Endocrinology 156, 301–13.10.1210/en.2014-1551CrossRefGoogle ScholarPubMed
Foxcroft, GR, Silva, PV and Paradis, F (2016). Application of transcriptomic analyses to reproductive studies in contemporary commercial sows. Theriogenology 85, 145–51.CrossRefGoogle ScholarPubMed
Gasperin, BG, Ferreira, R, Rovani, MT, Bordignon, V, Duggavathi, R, Buratini, J, Oliveira, JFC and Gonçalves, PBD (2014). Expression of receptors for BMP15 is differentially regulated in dominant and subordinate follicles during follicle deviation in cattle. Anim Reprod Sci 144, 72–8.CrossRefGoogle ScholarPubMed
Gilchrist, RB, Lane, M and Thompson, JG (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14, 159–77.CrossRefGoogle ScholarPubMed
Gillio-Meina, C, Hui, YY and LaVoie, HA (2005). Expression of CCAAT/enhancer binding proteins alpha and beta in the porcine ovary and regulation in primary cultures of granulosa cells. Biol Reprod 72, 1194–204.CrossRefGoogle ScholarPubMed
Grzesiak, M, Knapczyk-Stwora, K, Duda, M and Słomczyńska, M (2012). Elevated level of 17β-estradiol is associated with overexpression of FSHR, CYP19A1, and CTNNB1 genes in porcine ovarian follicles after prenatal and neonatal flutamide exposure. Theriogenology 78, 2050–60.CrossRefGoogle ScholarPubMed
Haas, CS, Rovani, MT, Oliveira, FC, Vieira, AD, Bordignon, V, Gonçalves, PBD, Ferreira, R and Gasperin, BG (2016). Expression of growth and differentiation factor 9 and cognate receptors during final follicular growth in cattle. Anim Reprod 13, 756–61.10.21451/1984-3143-AR789CrossRefGoogle Scholar
Hanukoglu, I (1992). Steroidogenic enzymes: structure, function, and role in regulation of steroid hormone biosynthesis. J Steroid Biochem Mol Biol 43, 779–804.CrossRefGoogle ScholarPubMed
Hsieh, M, Lee, D, Panigone, S, Horner, K, Chen, R, Theologis, A, Lee, DC, Threadgill, DW and Conti, M (2007). Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27, 1914–24.CrossRefGoogle ScholarPubMed
Juengel, JL and McNatty, KP (2005). The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum   Reprod Update 11, 143–60.Google ScholarPubMed
Juengel, JL, Hudson, NL, Whiting, L and McNatty, KP (2004). Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization, and pregnancy in ewes. Biol Reprod 70, 557–61.CrossRefGoogle ScholarPubMed
Kandiel, MM, Watanabe, G and Taya, K (2010). Ovarian expression of inhibin-subunits, 3β-hydroxysteroid dehydrogenase, and cytochrome P450 aromatase during the estrous cycle and pregnancy of Shiba goats (Capra hircus). Exp Anim 59, 605–14.CrossRefGoogle Scholar
Lavery, K, Swain, P, Falb, D and Alaoui-Ismaili, MH (2008). BMP-2/4 and BMP-6/7 differentially utilize cell surface receptors to induce osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. J Biol Chem 283, 20948–58.CrossRefGoogle ScholarPubMed
LaVoie, HA (2017). Transcriptional control of genes mediating ovarian follicular growth, differentiation, and steroidogenesis in pigs. Mol Reprod Dev 84, 788–801.CrossRefGoogle ScholarPubMed
Liu, J, Aronow, BJ, Witte, DP, Pope, WF and La Barbera, AR (1998). Cyclic and maturation-dependent regulation of follicle-stimulating hormone receptor and luteinizing hormone receptor messenger ribonucleic acid expression in the porcine ovary. Biol Reprod 58, 648–58.10.1095/biolreprod58.3.648CrossRefGoogle ScholarPubMed
Lydon, JP, DeMayo, FJ, Funk, CR, Mani, SK, Hughes, AR, Montgomery, CA Jr, Shyamala, G, Connelly, OM and O’Malley, BW (1995). Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9, 2266–78.CrossRefGoogle ScholarPubMed
Małysz-Cymborska, I, Ziecik, A, Waclawik, A and Andronowska, A (2013). Effect of hCG and eCG treatments on prostaglandins synthesis in the porcine oviduct. Reprod Domest Anim 48, 1034–42.CrossRefGoogle ScholarPubMed
Manabe, N, Goto, Y, Matsuda-Minehata, F, Inoue, N, Maeda, A, Sakamaki, K and Miyano, T (2004). Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 50, 493–514.10.1262/jrd.50.493CrossRefGoogle ScholarPubMed
Mast, N, Annalora, AJ, Lodowski, DT, Palczewski, K, Stout, CD and Pikuleva, IA (2011). Structural basis for three-step sequential catalysis by the cholesterol side chain cleavage enzyme CYP11A1. J Biol Chem 286, 5607–13.CrossRefGoogle ScholarPubMed
McNatty, KP, Hudson, NL, Whiting, L, Reader, KL, Lun, S, Western, A, Heath, DA, Smith, P, Moore, LG and Juengel, JL (2007). The effects of immunizing sheep with different BMP15 or GDF9 peptide sequences on ovarian follicular activity and ovulation rate. Biol Reprod 76, 552–60.CrossRefGoogle ScholarPubMed
Ndiaye, K, Fayad, T, Silversides, DW, Sirois, J and Lussier, JG (2005). Identification of downregulated messenger RNAs in bovine granulosa cells of dominant follicles following stimulation with human chorionic gonadotropin. Biol Reprod 73, 324–33.CrossRefGoogle ScholarPubMed
Nogueira, MFG, Buratini, J Jr, Price, CA, Castilho, ACS, Pinto, MGL and Barros, CM (2007). Expression of LH receptor mRNA splice variants in bovine granulosa cells: changes with follicle size and regulation by FSH in vitro . Mol Reprod Dev 74, 680–6.CrossRefGoogle ScholarPubMed
Orisaka, M, Jiang, JY, 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
Pan, Z, Zhang, J, Lin, F, Ma, X, Wang, X and Liu, H (2012). Expression profiles of key candidate genes involved in steroidogenesis during follicular atresia in the pig ovary. Mol Biol Rep 39, 10823–32.CrossRefGoogle ScholarPubMed
Paradis, F, Novak, S, Murdoch, GK, Dyck, MK, Dixon, WT and Foxcroft, GR (2009). Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction 138, 115–29.CrossRefGoogle ScholarPubMed
Park, JY, Su, YQ, Ariga, M, Law, E, Jin, SL and Conti, M (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–4.CrossRefGoogle ScholarPubMed
Parvizi, N, Elsaesser, F, Smidt, D and Ellendorff, F (1976). Plasma luteinizing hormone and progesterone in the adult female pig during the oestrous cycle, late pregnancy and lactation, and after ovariectomy and pentobarbitone treatment. J Endocrinol 69, 193–203.CrossRefGoogle ScholarPubMed
Peng, X, Yang, M, Wang, L, Tong, C and Guo, Z (2010). In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium. J Assist Reprod Genet 27, 247–57.CrossRefGoogle Scholar
Quinn, RL, Shuttleworth, G and Hunter, MG (2004). Immunohistochemical localization of the bone morphogenetic protein receptors in the porcine ovary. J Anat 205, 15–23.CrossRefGoogle ScholarPubMed
Reader, KL, Haydon, LJ, Littlejohn, RP, Juengel, JL and McNatty, KP (2012). Booroola BMPR1B mutation alters early follicular development and oocyte ultrastructure in sheep. Reprod Fert Dev 24, 353–61.CrossRefGoogle ScholarPubMed
Samardzija, D, Pogrmic-Majkic, K, Fa, S, Glisic, B, Stanic, B and Andric, N (2016). Atrazine blocks ovulation via suppression of Lhr and Cyp19a1 mRNA and estradiol secretion in immature gonadotropin-treated rats. Reprod Toxicol 61, 10–18.CrossRefGoogle ScholarPubMed
Simões, RA, Satrapa, RA, Rosa, FS, Piagentini, M, Castilho, AC, Ereno, RL, Trinca, LA, Nogueira, MF, Buratini, J and Barros, CM (2012). Ovulation rate and its relationship with follicle diameter and gene expression of the LH receptor (LHR) in Nelore cows. Theriogenology 77, 139–47.CrossRefGoogle Scholar
Słomczyńska, M and Tabarowski, Z (2001). Localization of androgen receptor and cytochrome P450 aromatase in the follicle and corpus luteum of the porcine ovary. Anim Reprod Sci 65, 127–34.CrossRefGoogle ScholarPubMed
Słomczyńska, M, Szołtys, M, Duda, M, Sikora, K and Tabarowski, Z (2003). Androgens and FSH affect androgen receptor and aromatase distribution in the porcine ovary. Folia Biol 51, 63–8.Google ScholarPubMed
Spicer, LJ, Aad, PY, Allen, DT, Mazerbourg, S, Payne, AH and Hsueh, AJ (2008). Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol Reprod 78, 243–53.CrossRefGoogle ScholarPubMed
Sriperumbudur, R, Zorrilla, L and Gadsby, JE (2010). Transforming growth factor-β (TGFβ) and its signaling components in peri-ovulatory pig follicles. Anim Reprod Sci 120, 84–94.CrossRefGoogle ScholarPubMed
Statistix® (2013). Statistix® 10 Analytical Software. Tallahassee, FL, USA.Google Scholar
Su, YQ, Sugiura, K, Wigglesworth, K, O’Brien, MJ, Affourtit, JP, Pangas, SA, Matzuk, MM and Eppig, JJ (2008). Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–21.CrossRefGoogle ScholarPubMed
Tosca, L, Crochet, S, Ferré, P, Foufelle, F, Tesseraud, S and Dupont, J (2006). AMP-activated protein kinase activation modulates progesterone secretion in granulosa cells from hen preovulatory follicles. J Endocrinol 190, 85–97.CrossRefGoogle ScholarPubMed
Wang, W, Chen, X, Li, X, Wang, L, Zhang, H, He, Y, Wang, J, Zhao, Y, Zhang, B and Xu, Y (2011). Interference RNA-based silencing of endogenous SMAD4 in porcine granulosa cells resulted in decreased FSH-mediated granulosa cells proliferation and steroidogenesis. Reproduction 141, 643–51.CrossRefGoogle ScholarPubMed
Wilson, T, Wu, XY, Juengel, JL, Ross, IK, Lumsden, JM, Lord, EA, Dodds, KG, Walling, GA, McEwan, JC, O’Connell, AR, McNatty, KP and Montgomery, GW (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol Reprod 64, 1225–35.CrossRefGoogle ScholarPubMed
Wissing, ML, Kristensen, SG, Andersen, CY, Mikkelsen, AL, Høst, T, Borup, R and Grøndahl, ML (2014). Identification of new ovulation-related genes in humans by comparing the transcriptome of granulosa cells before and after ovulation triggering in the same controlled ovarian stimulation cycle. Human Reprod 29, 997–1010.CrossRefGoogle ScholarPubMed
Yuan, W and Lucy, MC (1996). Messenger ribonucleic acid expression for growth hormone receptor, luteinizing hormone receptor, and steroidogenic enzymes during the estrous cycle and pregnancy in porcine and bovine corpora lutea. Dom Anim Endocrinol 13, 431–444.CrossRefGoogle ScholarPubMed
Zhai, B, Liu, H, Li, X, Dai, L, Gao, Y, Li, C, Zhang, L, Ding, Y, Yu, X and Zhang, J (2013). BMP15 prevents cumulus cell apoptosis through CCL2 and FBN1 in porcine ovaries. Cell Physiol Biochem 32, 264–78.CrossRefGoogle ScholarPubMed
Zhao, YY, Li, XX, Wang, W, Chen, X, Yu, P, Wang, JJ and Xu, YX (2014). Effect of BMPRIB gene silencing by siRNA on apoptosis and steroidogenesis of porcine granulosa cells. Genet Mol Res 13, 9964–75.CrossRefGoogle ScholarPubMed
Ziecik, AJ, Biallowicz, M, Kaczmarek, M, Demianowicz, W, Rioperez, J, Wasielak, M and Bogacki, M (2005). Influence of estrus synchronization of prepubertal gilts on embryo quality. J Reprod Dev, 51, 379–84.CrossRefGoogle ScholarPubMed