Oocyte Maturation and miRNAs: Studying a Complicate Interaction to Reveal Possible Biomarkers for Female Infertility
Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bendarska-Czerwinska, A.; Zmarzly, N.; Morawiec, E.; Panfil, A.; Brys, K.; Czarniecka, J.; Ostenda, A.; Dziobek, K.; Sagan, D.; Boron, D.; et al. Endocrine disorders and fertility and pregnancy: An update. Front. Endocrinol. 2022, 13, 970439. [Google Scholar] [CrossRef] [PubMed]
- Baird, D.T.; Collins, J.; Egozcue, J.; Evers, L.H.; Gianaroli, L.; Leridon, H.; Sunde, A.; Templeton, A.; Van Steirteghem, A.; Cohen, J.; et al. Fertility and ageing. Hum. Reprod. Update 2005, 11, 261–276. [Google Scholar] [CrossRef] [PubMed]
- Gougeon, A. Regulation of ovarian follicular development in primates: Facts and hypotheses. Endocr. Rev. 1996, 17, 121–155. [Google Scholar] [CrossRef] [PubMed]
- Vallee, M.; Gravel, C.; Palin, M.F.; Reghenas, H.; Stothard, P.; Wishart, D.S.; Sirard, M.A. Identification of novel and known oocyte-specific genes using complementary DNA subtraction and microarray analysis in three different species. Biol. Reprod. 2005, 73, 63–71. [Google Scholar] [CrossRef] [PubMed]
- Dalbies-Tran, R.; Mermillod, P. Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. Biol. Reprod. 2003, 68, 252–261. [Google Scholar] [CrossRef] [PubMed]
- Braw-Tal, R. The initiation of follicle growth: The oocyte or the somatic cells? Mol. Cell. Endocrinol. 2002, 187, 11–18. [Google Scholar] [CrossRef] [PubMed]
- Shah, J.S.; Sabouni, R.; Cayton Vaught, K.C.; Owen, C.M.; Albertini, D.F.; Segars, J.H. Biomechanics and mechanical signaling in the ovary: A systematic review. J. Assist. Reprod. Genet. 2018, 35, 1135–1148. [Google Scholar] [CrossRef] [PubMed]
- Dahl, K.D.; Czekala, N.M.; Hsueh, A.J. Estrogen-producing ovarian granulosa cells: Use of the granulosa cell aromatase bioassay (GAB) to monitor FSH levels in body fluids. Adv. Exp. Med. Biol. 1987, 219, 275–298. [Google Scholar] [CrossRef] [PubMed]
- Eppig, J.J. Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice: General conditions for expansion in vitro. J. Exp. Zool. 1979, 208, 111–120. [Google Scholar] [CrossRef]
- Gurtan, A.M.; Sharp, P.A. The role of miRNAs in regulating gene expression networks. J. Mol. Biol. 2013, 425, 3582–3600. [Google Scholar] [CrossRef] [PubMed]
- Griffiths-Jones, S.; Grocock, R.J.; van Dongen, S.; Bateman, A.; Enright, A.J. miRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006, 34, D140–D144. [Google Scholar] [CrossRef] [PubMed]
- Lim, L.P.; Glasner, M.E.; Yekta, S.; Burge, C.B.; Bartel, D.P. Vertebrate microRNA genes. Science 2003, 299, 1540. [Google Scholar] [CrossRef] [PubMed]
- Hutvagner, G.; McLachlan, J.; Pasquinelli, A.E.; Balint, E.; Tuschl, T.; Zamore, P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293, 834–838. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Radmark, O.; Kim, S.; et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425, 415–419. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, T.A.; Park, J.; Dang, T.L.; Choi, Y.G.; Kim, V.N. Microprocessor depends on hemin to recognize the apical loop of primary microRNA. Nucleic Acids Res. 2018, 46, 5726–5736. [Google Scholar] [CrossRef] [PubMed]
- Abd El Naby, W.S.; Hagos, T.H.; Hossain, M.M.; Salilew-Wondim, D.; Gad, A.Y.; Rings, F.; Cinar, M.U.; Tholen, E.; Looft, C.; Schellander, K.; et al. Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos. Zygote 2013, 21, 31–51. [Google Scholar] [CrossRef] [PubMed]
- Ardekani, A.M.; Naeini, M.M. The Role of MicroRNAs in Human Diseases. Avicenna J. Med. Biotechnol. 2010, 2, 161–179. [Google Scholar] [PubMed]
- Dell’Aversana, C.; Cuomo, F.; Longobardi, S.; D‘Hooghe, T.; Caprio, F.; Franci, G.; Santonastaso, M.; Colacurci, N.; Barone, S.; Pisaturo, V.; et al. Age-related miRNome landscape of cumulus oophorus cells during controlled ovarian stimulation protocols in IVF cycles. Hum. Reprod. 2021, 36, 1310–1325. [Google Scholar] [CrossRef] [PubMed]
- Gonella-Diaza, A.M.; Lopes, E.; Ribeiro da Silva, K.; Perecin Nociti, R.; Mamede Andrade, G.; Atuesta-Bustos, J.E.; Coelho da Silveira, J.; Vieira Meirelles, F.; Binelli, M. Steroidal Regulation of Oviductal microRNAs Is Associated with microRNA-Processing in Beef Cows. Int. J. Mol. Sci. 2021, 22, 953. [Google Scholar] [CrossRef] [PubMed]
- He, L.; Hannon, G.J. MicroRNAs: Small RNAs with a big role in gene regulation. Nat. Rev. Genet. 2004, 5, 522–531. [Google Scholar] [CrossRef] [PubMed]
- Moreno-Moya, J.M.; Vilella, F.; Simon, C. MicroRNA: Key gene expression regulators. Fertil. Steril. 2014, 101, 1516–1523. [Google Scholar] [CrossRef] [PubMed]
- Soifer, H.S.; Rossi, J.J.; Saetrom, P. MicroRNAs in disease and potential therapeutic applications. Mol. Ther. 2007, 15, 2070–2079. [Google Scholar] [CrossRef] [PubMed]
- Imbar, T.; Galliano, D.; Pellicer, A.; Laufer, N. Introduction: MicroRNAs in human reproduction: Small molecules with crucial regulatory roles. Fertil. Steril. 2014, 101, 1514–1515. [Google Scholar] [CrossRef] [PubMed]
- Li, P.; Zhu, W.J. Advance on Dicer gene and its role in female reproduction. Chin. J. Med. Genet. 2011, 28, 275–278. [Google Scholar] [CrossRef] [PubMed]
- Tatemoto, H.; Sakurai, N.; Muto, N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: Role of cumulus cells. Biol. Reprod. 2000, 63, 805–810. [Google Scholar] [CrossRef] [PubMed]
- Dompe, C.; Kulus, M.; Stefanska, K.; Kranc, W.; Chermula, B.; Bryl, R.; Pienkowski, W.; Nawrocki, M.J.; Petitte, J.N.; Stelmach, B.; et al. Human Granulosa Cells-Stemness Properties, Molecular Cross-Talk and Follicular Angiogenesis. Cells 2021, 10, 1396. [Google Scholar] [CrossRef] [PubMed]
- Jagarlamudi, K.; Rajkovic, A. Oogenesis: Transcriptional regulators and mouse models. Mol. Cell Endocrinol. 2012, 356, 31–39. [Google Scholar] [CrossRef] [PubMed]
- da Silveira, J.C.; Veeramachaneni, D.N.; Winger, Q.A.; Carnevale, E.M.; Bouma, G.J. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A possible new form of cell communication within the ovarian follicle. Biol. Reprod. 2012, 86, 71. [Google Scholar] [CrossRef] [PubMed]
- Sirotkin, A.V.; Laukova, M.; Ovcharenko, D.; Brenaut, P.; Mlyncek, M. Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J. Cell. Physiol. 2010, 223, 49–56. [Google Scholar] [CrossRef] [PubMed]
- Moreno, J.M.; Nunez, M.J.; Quinonero, A.; Martinez, S.; de la Orden, M.; Simon, C.; Pellicer, A.; Diaz-Garcia, C.; Dominguez, F. Follicular fluid and mural granulosa cells microRNA profiles vary in in vitro fertilization patients depending on their age and oocyte maturation stage. Fertil. Steril. 2015, 104, 1037–1046. [Google Scholar] [CrossRef]
- Santonocito, M.; Vento, M.; Guglielmino, M.R.; Battaglia, R.; Wahlgren, J.; Ragusa, M.; Barbagallo, D.; Borzi, P.; Rizzari, S.; Maugeri, M.; et al. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: Bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil. Steril. 2014, 102, 1751–1761.e1. [Google Scholar] [CrossRef] [PubMed]
- Hou, L.; Lu, Y.; Li, L. MiRNA-451 is a potential biomarker for estrogenicity in mouse uterus. Front. Environ. Sci. Eng. 2014, 8, 99–105. [Google Scholar] [CrossRef]
- Yang, X.; Zhou, Y.; Peng, S.; Wu, L.; Lin, H.Y.; Wang, S.; Wang, H. Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction 2012, 144, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Assou, S.; Al-edani, T.; Haouzi, D.; Philippe, N.; Lecellier, C.H.; Piquemal, D.; Commes, T.; Ait-Ahmed, O.; Dechaud, H.; Hamamah, S. MicroRNAs: New candidates for the regulation of the human cumulus-oocyte complex. Hum. Reprod. 2013, 28, 3038–3049. [Google Scholar] [CrossRef] [PubMed]
- Andrei, D.; Nagy, R.A.; van Montfoort, A.; Tietge, U.; Terpstra, M.; Kok, K.; van den Berg, A.; Hoek, A.; Kluiver, J.; Donker, R. Differential miRNA Expression Profiles in Cumulus and Mural Granulosa Cells from Human Pre-ovulatory Follicles. Microrna 2019, 8, 61–67. [Google Scholar] [CrossRef] [PubMed]
- Jenabi, M.; Khodarahmi, P.; Tafvizi, F.; Bostanabad, S.Z. Evaluation of the potential of miR-21 as a diagnostic marker for oocyte maturity and embryo quality in women undergoing ICSI. Sci. Rep. 2023, 13, 1440. [Google Scholar] [CrossRef] [PubMed]
- Almeida, C.P.; Ferreira, M.C.F.; Silveira, C.O.; Campos, J.R.; Borges, I.T.; Baeta, P.G.; Silva, F.H.S.; Reis, F.M.; Del Puerto, H.L. Clinical correlation of apoptosis in human granulosa cells-A review. Cell Biol. Int. 2018, 42, 1276–1281. [Google Scholar] [CrossRef] [PubMed]
- Carletti, M.Z.; Fiedler, S.D.; Christenson, L.K. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol. Reprod. 2010, 83, 286–295. [Google Scholar] [CrossRef]
- Han, X.; Xue, R.; Yuan, H.J.; Wang, T.Y.; Lin, J.; Zhang, J.; Liang, B.; Tan, J.H. MicroRNA-21 plays a pivotal role in the oocyte-secreted factor-induced suppression of cumulus cell apoptosis. Biol. Reprod. 2017, 96, 1167–1180. [Google Scholar] [CrossRef] [PubMed]
- Bartolucci, A.F.; Uliasz, T.; Peluso, J.J. MicroRNA-21 as a regulator of human cumulus cell viability and its potential influence on the developmental potential of the oocyte. Biol. Reprod. 2020, 103, 94–103. [Google Scholar] [CrossRef] [PubMed]
- Gaia-Oltean, A.I.; Braicu, C.; Gulei, D.; Ciortea, R.; Mihu, D.; Roman, H.; Irimie, A.; Berindan-Neagoe, I. Ovarian endometriosis, a precursor of ovarian cancer: Histological aspects, gene expression and microRNA alterations (Review). Exp. Ther. Med. 2021, 21, 243. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.; Lv, J.; Tang, R.; Feng, Y.; Zhao, Y.; Fei, X.; Chian, R.; Xie, Q. Association of exosomal microRNAs in human ovarian follicular fluid with oocyte quality. Biochem. Biophys. Res. Commun. 2021, 534, 468–473. [Google Scholar] [CrossRef] [PubMed]
- Muti, P.; Donzelli, S.; Sacconi, A.; Hossain, A.; Ganci, F.; Frixa, T.; Sieri, S.; Krogh, V.; Berrino, F.; Biagioni, F.; et al. MiRNA-513a-5p inhibits progesterone receptor expression and constitutes a risk factor for breast cancer: The hOrmone and Diet in the ETiology of breast cancer prospective study. Carcinogenesis 2018, 39, 98–108. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Tong, L.; Wang, M.; Chang, X.; Wang, S.; Li, K.; Xiao, J. miR-505-3p is a repressor of the puberty onset in female mice. J. Endocrinol. 2018, 240, 279–392. [Google Scholar] [CrossRef] [PubMed]
- Barragan, M.; Pons, J.; Ferrer-Vaquer, A.; Cornet-Bartolome, D.; Schweitzer, A.; Hubbard, J.; Auer, H.; Rodolosse, A.; Vassena, R. The transcriptome of human oocytes is related to age and ovarian reserve. Mol. Hum. Reprod. 2017, 23, 535–548. [Google Scholar] [CrossRef] [PubMed]
- Feng, R.; Sang, Q.; Zhu, Y.; Fu, W.; Liu, M.; Xu, Y.; Shi, H.; Xu, Y.; Qu, R.; Chai, R.; et al. MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro. Sci. Rep. 2015, 5, 8689. [Google Scholar] [CrossRef] [PubMed]
- Machtinger, R.; Rodosthenous, R.S.; Adir, M.; Mansour, A.; Racowsky, C.; Baccarelli, A.A.; Hauser, R. Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: An exploratory study. J. Assist. Reprod. Genet. 2017, 34, 525–533. [Google Scholar] [CrossRef]
- Sang, Q.; Yao, Z.; Wang, H.; Feng, R.; Wang, H.; Zhao, X.; Xing, Q.; Jin, L.; He, L.; Wu, L.; et al. Identification of microRNAs in human follicular fluid: Characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J. Clin. Endocrinol. Metab. 2013, 98, 3068–3079. [Google Scholar] [CrossRef] [PubMed]
- Conti, M.; Hsieh, M.; Zamah, A.M.; Oh, J.S. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol. Cell. Endocrinol. 2012, 356, 65–73. [Google Scholar] [CrossRef] [PubMed]
- Al-Edani, T.; Assou, S.; Ferrieres, A.; Bringer Deutsch, S.; Gala, A.; Lecellier, C.H.; Ait-Ahmed, O.; Hamamah, S. Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. Biomed. Res. Int. 2014, 2014, 964614. [Google Scholar] [CrossRef]
- Barragan, M.; Cornet-Bartolome, D.; Molina, N.; Vassena, R. The expression levels of NOS2, HMOX1, and VEGFC in cumulus cells are markers of oocyte maturation and fertilization rate. Mol. Reprod. Dev. 2023, 90, 369–377. [Google Scholar] [CrossRef] [PubMed]
- Yan, G.; Zhang, L.; Fang, T.; Zhang, Q.; Wu, S.; Jiang, Y.; Sun, H.; Hu, Y. MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Lett. 2012, 586, 3263–3270. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Yao, W.; Yao, Y.; Du, X.; Zhou, J.; Ma, B.; Liu, H.; Li, Q.; Pan, Z. MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene. FEBS Lett. 2014, 588, 4497–4503. [Google Scholar] [CrossRef] [PubMed]
- Sinha, P.B.; Tesfaye, D.; Rings, F.; Hossien, M.; Hoelker, M.; Held, E.; Neuhoff, C.; Tholen, E.; Schellander, K.; Salilew-Wondim, D. MicroRNA-130b is involved in bovine granulosa and cumulus cells function, oocyte maturation and blastocyst formation. J. Ovarian Res. 2017, 10, 37. [Google Scholar] [CrossRef] [PubMed]
- Cao, R.; Wu, W.; Zhou, X.; Liu, K.; Li, B.; Huang, X.; Zhang, Y.; Liu, H. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary. Int. J. Biochem. Cell Biol. 2015, 68, 148–157. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Wang, X.; Mu, H.; Mei, Q.; Liu, Y.; Min, Z.; Zhang, L.; Su, P.; Xiang, W. Mir-484 contributes to diminished ovarian reserve by regulating granulosa cell function via YAP1-mediated mitochondrial function and apoptosis. Int. J. Biol. Sci. 2022, 18, 1008–1021. [Google Scholar] [CrossRef] [PubMed]
- Eppig, J.J. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 1996, 8, 485–489. [Google Scholar] [CrossRef]
- Li, L.; Zheng, P.; Dean, J. Maternal control of early mouse development. Development 2010, 137, 859–870. [Google Scholar] [CrossRef] [PubMed]
- Otsuka, M.; Zheng, M.; Hayashi, M.; Lee, J.D.; Yoshino, O.; Lin, S.; Han, J. Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J. Clin. Investig. 2008, 118, 1944–1954. [Google Scholar] [CrossRef] [PubMed]
- Bernstein, E.; Kim, S.Y.; Carmell, M.A.; Murchison, E.P.; Alcorn, H.; Li, M.Z.; Mills, A.A.; Elledge, S.J.; Anderson, K.V.; Hannon, G.J. Dicer is essential for mouse development. Nat. Genet. 2003, 35, 215–217. [Google Scholar] [CrossRef]
- Yang, W.J.; Yang, D.D.; Na, S.; Sandusky, G.E.; Zhang, Q.; Zhao, G. Dicer is required for embryonic angiogenesis during mouse development. J. Biol. Chem. 2005, 280, 9330–9335. [Google Scholar] [CrossRef]
- Murchison, E.P.; Stein, P.; Xuan, Z.; Pan, H.; Zhang, M.Q.; Schultz, R.M.; Hannon, G.J. Critical roles for Dicer in the female germline. Genes Dev. 2007, 21, 682–693. [Google Scholar] [CrossRef] [PubMed]
- Tang, F.; Kaneda, M.; O‘Carroll, D.; Hajkova, P.; Barton, S.C.; Sun, Y.A.; Lee, C.; Tarakhovsky, A.; Lao, K.; Surani, M.A. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007, 21, 644–648. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.C.; Tang, Y.; He, Z.; Rosenwaks, Z. Dicer is a key player in oocyte maturation. J. Assist. Reprod. Genet. 2010, 27, 571–580. [Google Scholar] [CrossRef] [PubMed]
miRNA | Cell Type | Regulation | Regulatory Role | References |
---|---|---|---|---|
let-7a-5p | GCs and CCs | up | Proliferation of GCs and CCs | [35] |
let-7b | CCs | up | Steroidogenesis Apoptosis and proliferation of GCs | [34] |
let-7c | CCs | up | Steroidogenesis Apoptosis and proliferation of GCs | [34] |
let-7f-5p | GCs and CCs | up | Proliferation of GCs and CCs | [35] |
miR-21 | CCs | up | Oocyte maturation Steroidogenesis Apoptosis and proliferation of GCs | [34,35,36,37,38,39,52,53,54] |
miR-21 | CCs | down | Female infertility | [36] |
miR-21-5p | GCs and CCs | up | Apoptosis of GCs and CCs | [35] |
hsa-miR-320e | GCs | up | Proliferation of GCs affecting Oocyte degradation | [42] |
miR-99a | GCs and CCs | up | Poor oocyte quality | [31,49] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nazou, E.; Potiris, A.; Mavrogianni, D.; Drakaki, E.; Vogiatzis, A.-A.; Sarli, V.; Vrantza, T.; Zikopoulos, A.; Louis, K.; Skentou, C.; et al. Oocyte Maturation and miRNAs: Studying a Complicate Interaction to Reveal Possible Biomarkers for Female Infertility. Diseases 2024, 12, 121. https://doi.org/10.3390/diseases12060121
Nazou E, Potiris A, Mavrogianni D, Drakaki E, Vogiatzis A-A, Sarli V, Vrantza T, Zikopoulos A, Louis K, Skentou C, et al. Oocyte Maturation and miRNAs: Studying a Complicate Interaction to Reveal Possible Biomarkers for Female Infertility. Diseases. 2024; 12(6):121. https://doi.org/10.3390/diseases12060121
Chicago/Turabian StyleNazou, Eleni, Anastasios Potiris, Despoina Mavrogianni, Eirini Drakaki, Aris-Anargyros Vogiatzis, Vaia Sarli, Tereza Vrantza, Athanasios Zikopoulos, Konstantinos Louis, Chara Skentou, and et al. 2024. "Oocyte Maturation and miRNAs: Studying a Complicate Interaction to Reveal Possible Biomarkers for Female Infertility" Diseases 12, no. 6: 121. https://doi.org/10.3390/diseases12060121
APA StyleNazou, E., Potiris, A., Mavrogianni, D., Drakaki, E., Vogiatzis, A.-A., Sarli, V., Vrantza, T., Zikopoulos, A., Louis, K., Skentou, C., Panagopoulos, P., Drakakis, P., & Stavros, S. (2024). Oocyte Maturation and miRNAs: Studying a Complicate Interaction to Reveal Possible Biomarkers for Female Infertility. Diseases, 12(6), 121. https://doi.org/10.3390/diseases12060121