Expression Profiles of the Progesterone Receptor, Cyclooxygenase-2, Growth Differentiation Factor 9, and Bone Morphogenetic Protein 15 Transcripts in the Canine Oviducts during the Oestrous Cycle
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Recovery of the Oviductal Cells
2.3. RNA Extraction and Quantitative Real-Time RT-qPCR Analysis
2.4. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wollenhaupt, K.; Tomek, W.; Brüssow, K.P.; Tiemann, U.; Viergutz, T.; Schneider, F.; Nürnberg, G. Effects of ovarian steroids and epidermal growth factor (EGF) on expression and bioactivation of specific regulators of transcription and translation in oviductal tissue in pigs. Reproduction 2002, 123, 87–96. [Google Scholar] [CrossRef]
- Cerny, K.L.; Garrett, E.; Walton, A.J.; Anderson, L.H.; Bridges, P.J. A transcriptomal analysis of bovine oviductal epithelial cells collected during the follicular phase versus the luteal phase of the estrous cycle. Reprod. Biol. Endocrinol. 2015, 13, 84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barton, B.E.; Herrera, G.G.; Anamthathmakula, P.; Rock, J.K.; Willie, A.M.; Harris, E.A.; Takemaru, K.; Winuthayanon, W. Roles of steroid hormones in oviductal function. Reproduction 2020, 159, R125–R137. [Google Scholar] [CrossRef] [PubMed]
- Hermoso, M.; Barrera, N.; Morales, B.; Perez, S.; Villalon, M. Platelet-activating factor increases ciliary activity in the hamster oviduct through epithelial production of prostaglandin E2. Pflugers Arch. 2001, 442, 336–345. [Google Scholar] [CrossRef] [PubMed]
- Gauvreau, D.; Moisan, V.; Roy, M.; Fortier, M.A.; Bilodeau, J.F. Expression of prostaglandin E synthases in the bovine oviduct. Theriogenology 2010, 73, 103–111. [Google Scholar] [CrossRef] [PubMed]
- Wijayagunawardane, M.P.; Kodithuwakku, S.P.; Yamamoto, D.; Miyamoto, A. Vascular endothelial growth factor system in the cow oviduct: Possible involvement in the regulation of the oviductal motility and embryo transport. Mol. Reprod. Dev. 2005, 72, 511–520. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Martínez, S.; Hermoso, M.; Farina, M.; Ribeiro, M.L.; Rapanelli, M.; Espinosa, M.; Villalón, M.; Franchi, A. 17-β-Estradiol upregulates COX-2 in the rat oviduct. Prostaglandins Lipid Mediat. 2006, 80, 155–164. [Google Scholar]
- Hunter, R.H. Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 2012, 87, 244–255. [Google Scholar] [CrossRef]
- Concannon, P.W. Endocrinologic control of normal canine ovarian function. Reprod. Domest. Anim. 2009, 44 (Suppl. 2), 3–15. [Google Scholar] [CrossRef]
- Hardy, D.B.; Janowski, B.A.; Corey, D.R.; Mendelson, C.R. Progesterone receptor plays a major anti-inflammatory role in human myometrial cells by antagonism of nuclear factor-B activation of cyclooxygenase 2 expressions. Mol. Endocrinol. 2006, 20, 2724–2733. [Google Scholar] [CrossRef]
- Akison, L.K.; Boden, M.J.; Kennaway, D.J.; Russell, D.L.; Rocker, R.L. Progesterone receptor-dependent regulation of genes in the oviducts of female mice. Physiol. Genom. 2014, 46, 583–592. [Google Scholar] [CrossRef] [Green Version]
- Kaya, H.S.; Hantak, A.M.; Stubbs, L.J.; Taylor, R.N.; Bagchi, I.C.; Bagchi, M.K. Roles of progesterone receptor A and B isoforms during human endometrial decidualization. Mol. Endocrinol. 2015, 29, 882–895. [Google Scholar] [CrossRef] [Green Version]
- Teilmann, S.C.; Clement, C.A.; Thorup, J.; Byskov, A.G.; Christensen, S.T. Expression and localization of the progesterone receptor in mouse and human reproductive organs. J. Endocrinol. 2006, 191, 525–535. [Google Scholar] [CrossRef]
- Akison, L.K.; Robker, R.L. The critical roles of progesterone receptor (PGR) in ovulation, oocyte developmental competence and oviductal transport in mammalian reproduction. Reprod. Domest. Anim. 2012, 47 (Suppl. 4), 288–296. [Google Scholar] [CrossRef]
- Tahir, M.; Reynaud, K.; Grimard, B.; Thoumire, S.; Chastant-Maillard, S.; Saint-Dizier, M. Expression of nuclear and membrane progesterone receptors in the canine oviduct during the periovulatory period. Reprod. Fertil. Dev. 2013, 25, 1065–1076. [Google Scholar] [CrossRef]
- Kim, J.; Bagchi, I.C.; Bagchi, M.K. Control of ovulation in mice by progesterone receptor-regulated gene networks. Mol. Hum. Reprod. 2009, 15, 821–828. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, W.L.; DeWitt, D.L.; Garavito, R.M. Cyclooxygenases: Structural, cellular, and molecular biology. Annu. Rev. Biochem. 2000, 69, 145–182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tai, H.H.; Ensor, C.M.; Tong, M.; Zhou, H.; Yan, F. Prostaglandin catabolizing enzymes. Prostaglandins Lipid Mediat. 2002, 68–69, 483–493. [Google Scholar] [CrossRef]
- Odau, S.; Gabler, C.; Holder, C.; Einspanie, R. Differential expression of cyclooxygenase 1 and cyclooxygenase 2 in the bovine oviduct. J. Endocrinol. 2006, 191, 263–274. [Google Scholar] [CrossRef]
- Kowalewski, M.P.; Fox, B.; Gram, A.; Boos, A.; Reichler, I. Prostaglandin E2 functions as a luteotrophic factor in the dog. Reproduction 2013, 145, 213–226. [Google Scholar] [CrossRef] [Green Version]
- De los Reyes, M.; Araujo, A.; Flores, J.; Ramirez, G.; Palomino, J.; Parraguez, V.H.; Aspee, K. Cyclooxygenase-2 messenger RNA levels in canine follicular cells: Interrelationship with GDF-9, BMP-15 and progesterone. Domest. Anim. Endocrinol. 2021, 74, 106529. [Google Scholar] [CrossRef]
- Takahashi, T.; Jason, D.; Morrow, J.D.; Wang, H.; Dey, S.K. Cyclooxygenase-2-derived Prostaglandin E2 Directs Oocyte Maturation by Differentially Influencing Multiple Signaling Pathways. J. Biol. Chem. 2007, 281, 37117–37129. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, T.; Igarashi, H.; Amita, M.; Hara, S.; Kurachi, H. Roles of prostaglandins during oocyte maturation: Lessons from Knockout mice. J. Mamm. Ova Res. 2010, 27, 11–20. [Google Scholar] [CrossRef]
- Viggiano, M.; Cebral, E.; Gimeno, A.L.; Gimeno, M.A. Probable influence of ova and embryo prostaglandins in the differential ovum transport in pregnant and cycling rats. Prostaglandins Leukot. Essent. Fat. Acids 1992, 45, 211–215. [Google Scholar] [CrossRef]
- Zhao, Y.; Chegini, N.; Flanders, K.C. Human fallopian tube expresses transforming growth factor (TGF beta) isoforms, TGF beta type I-III receptor messenger ribonucleic acid and protein, and contains [125I] TGF beta-binding sites. J. Clin. Endocrinol. Metab. 1994, 79, 1177–1184. [Google Scholar] [PubMed]
- Lee, S.H.; Oh, H.J.; Kim, M.J.; Kim, G.A.; Choi, Y.B.; Jo, Y.K.; Nugraha, E.M.; Setyawan, N.; Lee, B.C. Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes. J. Assist. Reprod. Genet. 2017, 34, 929–938. [Google Scholar] [CrossRef] [PubMed]
- Eppig, J.J. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 2008, 135, 111–121. [Google Scholar]
- Chang, H.M.; Qiao, J.; Leung, P.C. Oocyte-somatic cell interactions in the human ovary-novel role of bone morphogenetic proteins and growth differentiation factors. Hum. Reprod. Update 2016, 23, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Belli, M.; Shimasaki, S. Molecular aspects and clinical Relevance of GDF9 and BMP15 in ovarian function. Vitam. Horm. 2018, 107, 317–348. [Google Scholar]
- Garcia, P.; Aspee, K.; Ramirez, G.; Dettleff, P.; Palomino, J.; Peralta, O.A.; Parraguez, V.H.; De los Reyes, M. Influence of growth differentiation factor 9 and bone morphogenetic protein 15 on in vitro maturation of canine oocytes. Reprod. Domest. Anim. 2019, 54, 373–380. [Google Scholar] [CrossRef]
- Elvin, J.A.; Clarck, A.T.; Wang, P.; Wolfman, N.M.; Matzuk, M.M. Paracrine Actions of Growth Differentiation Factor-9 in the mammalian ovary. Mol. Endocrinol. 1999, 13, 1035–1048. [Google Scholar] [CrossRef] [PubMed]
- Goncalves, J.S.A.; Vannucchi, C.I.; Braga, F.C.; Paula-Lopes, F.F.; Milazzotto, M.P.; Assumpcao, M.E.O.A.; Visintin, J.A. Oestrogen and Progesterone receptor gene expression in canine oocytes and cumulus cells throughout the oestrous cycle. Reprod. Domest. Anim. 2009, 44 (Suppl. 2), 239–242. [Google Scholar] [CrossRef] [PubMed]
- Palomino, J.; De los Reyes, M. Temporal expression of GDF-9 and BMP-15 in canine ovarian follicles. Theriogenology 2016, 86, 1541–1549. [Google Scholar] [CrossRef] [PubMed]
- Ramirez, G.; Palomino, J.; Aspee, K.; De los Reyes, M. GDF-9 and BMP-15 mRNA levels in canine cumulus cells related to cumulus expansion and the maturation process. Animals 2020, 10, 462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brugger, N.; Otzdorff, C.; Walter, B.; Hoffmann, B.; Braun, J. Quantitative determination of progesterone (P4) in canine blood serum using an enzyme-linked fluorescence assay. Reprod. Domest. Anim. 2011, 46, 870–873. [Google Scholar] [CrossRef]
- Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, research0034.1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fuentealba, B.; Nieto, M.; Croxatto, H.B. Estrogen and Progesterone Receptors in the Oviduct during Egg Transport in Cyclic and Pregnant Rats. Biol. Reprod. 1988, 9, 751–757. [Google Scholar] [CrossRef] [Green Version]
- Vermeirsch, H.; Van Den Broec, W.; Coryn, M.; Simoens, P. Immunolocalization of sex steroid hormone receptors in the canine uterine tube and their relation to sex steroid hormone concentrations levels. Reprod. Fertil. Dev. 2002, 14, 241–250. [Google Scholar] [CrossRef]
- Slobodin, B.; Han, R.; Calderone, V.; Oude, V.; Loayza-Puch, F.; Elkon, R.; Agami, R. Transcription Impacts the Efficiency of mRNA Translation via co-transcriptional N6-adenosine Methylation. Cell 2017, 169, 326–337. [Google Scholar] [CrossRef] [Green Version]
- Pasqualini, J.R.; Nguyen, B.L. Progesterone receptors in the foetal uterus of guinea-pig: Its stimulation after oestradiol treatment. Endocrinology 1980, 106, 1160–1165. [Google Scholar] [CrossRef]
- Fortune, J.E.; Willis, E.L.; Bridges, P.J.; Yang, C.S. The periovulatory period in cattle: Progesterone, prostaglandins, oxytocin and ADAMTS proteases. Anim. Reprod. 2009, 6, 60–71. [Google Scholar] [PubMed]
- Reynaud, K.; Saint-Dizier, M.; Tahir, M.Z.; Havard, T.; Harichaux, G.; Labas, V.; Thoumire, S.; Fontbonne, A.; Grimard, B.; Chastant-Maillard, S. Progesterone plays a critical role in canine oocyte maturation and fertilization. Biol. Reprod. 2015, 93, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.J.; Park, K.B.; Choi, E.J.; Hyun, S.H.; Kim, N.H.; Jeong, Y.W.; Hwang, W.S. Relationship between time post-ovulation and progesterone on oocyte maturation and pregnancy in canine cloning. Anim. Reprod. Sci. 2018, 185, 75–82. [Google Scholar] [CrossRef] [PubMed]
- Morrill, G.A.; Chien, E.J.; Kostellow, A.B. Progesterone induction of phospholipid methylation and arachidonic acid turnover during the first meiotic division in amphibian oocytes. Life Sci. 1986, 27, 1501–1508. [Google Scholar]
- Wanggren, K.; Lalitkumar, P.G.; Stavreus-Evers, A.; Stabi, B.; Gemzell-Danielsson, K. Prostaglandin E2 and F2alpha receptors in the human Fallopian tube before and after mifepristone treatment. Mol. Hum. Reprod. 2006, 12, 577–585. [Google Scholar] [CrossRef]
- Herschman, H.R. Review: Prostaglandin synthase-2. Biochim. Biophys. Acta 1996, 1299, 125–140. [Google Scholar] [CrossRef]
- Sirois, J.; Simmons, D.L.; Richards, J.S. Hormonal regulation of messenger ribonucleic acid encoding a novel isoform of prostaglandin endo-peroxide H synthase in rat preovulatory follicles Induction in vivo and in vitro. J. Biol. Chem. 1992, 267, 11586–11592. [Google Scholar] [CrossRef]
- Bridges, P.J.; Komar, C.M.; Fortune, J.E. Gonadotropin-Induced Expression of Messenger Ribonucleic Acid for Cyclooxygenase-2 and Production of Prostaglandins E and F2a in Bovine Preovulatory Follicles Are Regulated by the Progesterone Receptor. Endocrinology 2006, 147, 4713–4722. [Google Scholar] [CrossRef] [Green Version]
- Salleh, N. Diverse Roles of Prostaglandins in Blastocyst Implantation. Sci. World J. 2014, 2014, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pan, Z.Y.; Di, R.; Tang, Q.Q.; Jin, H.H.; Chu, M.X.; Huang, D.W.; He, J.N.; Liu, Q.Y.; Hu, W.P.; Wang, X.Y.; et al. Tissue-specific mRNA expression profiles of GDF9, BMP15, and BMPR1B genes in prolific and non-prolific goat breeds. Czech J. Anim. Sci. 2015, 60, 452–458. [Google Scholar] [CrossRef] [Green Version]
- Hussein, T.S.; Sutton-McDowall, M.L.; Gilchrist, R.B.; Thompson, J.G. Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM. Reprod. Fertil. Dev. 2011, 23, 576–584. [Google Scholar] [CrossRef]
- Yeo, C.X.; Gilchrist, R.B.; Thompson, J.G.; Lane, M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 2008, 23, 67–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elvin, J.A.; Yan, C.; Matzuk, M.M. Growth differentiation factor-9 stimulates progesterone synthesis in granulosa cells via a prostaglandin E2-EP2 receptor pathway. Proc. Natl. Acad. Sci. USA 2000, 97, 10288–10293. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hou, X.; Arvisais, E.W.; Davis, J.S. Luteinizing hormone stimulates mammalian target of rapamycin signalling in bovine luteal cells via pathways independent of Akt and Mitogen-activated protein kinase: Modulation of glycogen synthase kinase 3 and amp-activated protein kinase. Endocrinology 2010, 151, 2846–2857. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Norris, R.P.; Freudzon, M.; Mehlmann, L.M.; Cowan, A.E.; Simon, A.M.; Paul, D.; Jaffe, L.A. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: One of two paths to meiotic resumption. Development 2008, 135, 3229–3238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mester, B.; Ritter, L.; Pitman, J.L.; Bibby, A.H.; Gilchrist, R.B.; McNatty, K.P.; Juengel, J.L.; McIntosh, C.J. Oocyte expression, secretion and somatic cell interaction of mouse bone morphogenetic protein 15 during the peri-ovulatory period. Reprod. Fertil. Dev. 2014, 27, 801–811. [Google Scholar] [CrossRef]
- Yoshino, O.; Osuga, J.S.; Harada, M.; Nishii, O.Y.; Taketani, Y. The function of bone morphogenetic proteins in the human ovary. Reprod. Med. Biol. 2011, 10, 1–7. [Google Scholar] [CrossRef]
- Garciía, E.V.; Valdecantos, P.A.; Barrera, D.; Roldaán-Olarte, M.; Miceli, D.C. Bone morphogenetic proteins in the bovine oviduct: Differential expression of BMP-5 in the isthmus during the estrous cycle. Theriogenology 2014, 81, 1032–1041. [Google Scholar]
Gene | Sequence 5′-3′ | Size (bp) | Reference |
---|---|---|---|
ACTB | F:ATTGTCATGGACTCTGGGGATG R:TCCTTGATGTCACGCACGAT | 191 | [33] |
GDF-9 | F: CAGAAGGGAGGTCTGTCTGC R: TGTTGGGGGAAAAGAAAGTG | 170 | [33] |
BMP-15 | F: CCCTGCCCCTGATTCGGGAG R: CCGCAAAGGATGCCCAAGGAC | 82 | [33] |
COX-2 | F:TGAGCGGTTATTCCAGACGAGCAG R:CCAACCCCGCAGCCATTTCCTTCT | 500 | [21] |
PGR | F:GATGCTATATTTTGCACCTGA R: CTCCTTTTTGCCTCAAGCCA | 266 | [15] |
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Palomino, J.; Flores, J.; Ramirez, G.; Parraguez, V.H.; De los Reyes, M. Expression Profiles of the Progesterone Receptor, Cyclooxygenase-2, Growth Differentiation Factor 9, and Bone Morphogenetic Protein 15 Transcripts in the Canine Oviducts during the Oestrous Cycle. Animals 2021, 11, 454. https://doi.org/10.3390/ani11020454
Palomino J, Flores J, Ramirez G, Parraguez VH, De los Reyes M. Expression Profiles of the Progesterone Receptor, Cyclooxygenase-2, Growth Differentiation Factor 9, and Bone Morphogenetic Protein 15 Transcripts in the Canine Oviducts during the Oestrous Cycle. Animals. 2021; 11(2):454. https://doi.org/10.3390/ani11020454
Chicago/Turabian StylePalomino, Jaime, Javiera Flores, Georges Ramirez, Victor H. Parraguez, and Monica De los Reyes. 2021. "Expression Profiles of the Progesterone Receptor, Cyclooxygenase-2, Growth Differentiation Factor 9, and Bone Morphogenetic Protein 15 Transcripts in the Canine Oviducts during the Oestrous Cycle" Animals 11, no. 2: 454. https://doi.org/10.3390/ani11020454
APA StylePalomino, J., Flores, J., Ramirez, G., Parraguez, V. H., & De los Reyes, M. (2021). Expression Profiles of the Progesterone Receptor, Cyclooxygenase-2, Growth Differentiation Factor 9, and Bone Morphogenetic Protein 15 Transcripts in the Canine Oviducts during the Oestrous Cycle. Animals, 11(2), 454. https://doi.org/10.3390/ani11020454