journal article·2022-03-22Open access

Pregnancy Achievement by Medical Assisted Reproduction Is Correlated to the G Protein-Coupled Receptor 30 mRNA Abundance in Human Spermatozoa

Sara C. Pereira, Inês F. Esperança, Soraia Pinto, Alberto Barros, Mário Sousa, Marco G. Alves, Pedro F. Oliveira

Applied Sciences· Volume 12· Issue 7

Abstract

Estrogens, specifically 17β-estradiol (E2), play an important role in male health, including male fertility. The G protein-coupled receptor for estrogen 30 (GPR30) is essential for mediating the rapid non-genomic effects of E2 on a variety of testicular cells, including spermatozoa, although its molecular effects remain largely unknown. In this work, we hypothesized that the GPR30 mRNA abundance in spermatozoa could be correlated to sperm quality. Sperm GPR30 mRNA could also be carried into the oocyte, potentially impacting embryo development and the success of a pregnancy. For this study, 81 sperm samples were collected from couples seeking fertility treatment and undergoing medically assisted reproduction treatments (ART), following the World Health Organization guidelines. GPR30 mRNA abundance in spermatozoa was assessed with a quantitative polymerase chain reaction. The resulting data show that there is no correlation between the abundance of the GPR30 transcript with paternal BMI, age, or sperm quality parameters. Interestingly, we observed that higher levels of GPR30 mRNA abundance in spermatozoa were related to the achievement of biochemical pregnancy and clinical pregnancy (p < 0.05) by couples undergoing treatment. These results highlight the role of the sperm’s RNA cargo in offspring development, suggesting that spermatozoa mRNA content can influence ART success.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Estrogen and related hormone effects · Reproductive Biology and Fertility · Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Endocrine and Metabolic Research, Unit for Multidisciplinary Research in Biomedicine, Department of Anatomy, School of Medicine and Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal

Laboratory for Integrative and Translational Research in Population Health (ITR), University of Porto, 4099-002 Porto, Portugal

Department of Pathology, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal

QOPNA & LAQV, Department of Chemistry, Campus Universitario de Santiago, University of Aveiro, 3810-193 Aveiro, Portugal

Colégio Internato dos Carvalhos, Pedroso, 4415-133 Vila Nova de Gaia, Portugal

Centre for Reproductive Genetics Professor Alberto Barros, 4100-012 Porto, Portugal

Reproductive Genetics and Embryo-Fetal Development, i3S–Instituto de Investigação e Inovação em Saúde, University of Porto, 4200-135 Porto, Portugal

Laboratory of Cell Biology, Unit for Multidisciplinary Research in Biomedicine, Department of Microscopy, School of Medicine and Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal

Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain

Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, ES-17003 Girona, Spain

Funding

Fundação para a Ciência e Tecnologia

References (43)

Show source-provided references
1. Bernardino, R.L., Carrageta, D.F., Silva, A.M., Calamita, G., Alves, M.G., Soveral, G., and Oliveira, P.F. (2018). Estrogen Modulates Glycerol Permeability in Sertoli Cells through Downregulation of Aquaporin-9. Cells, 7.10.3390/cells7100153 ↗
2. Estrogen and Spermatogenesis
3. Estrogen Receptors α and β in Human Testis: Both Isoforms are Expressed10.3109/19396360902855733 ↗
4. Expression pattern of G protein-coupled receptor 30 in human seminiferous tubular cells10.1016/j.ygcen.2014.02.022 ↗
5. Identification of the estrogen receptor GPER in neoplastic and non-neoplastic human testes10.1186/1477-7827-9-135 ↗
6. Mechanisms linking obesity to male infertility10.5173/ceju.2015.01.435 ↗
7. RNA in spermatozoa: Implications for the alternative haploid genome10.1093/molehr/3.6.473 ↗
8. Nucleic acid metabolism of mammalian spermatozoa10.1042/bj0860298 ↗
9. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content10.1096/fj.12-224048 ↗
10. Inheritable testicular metabolic memory of high-fat diet causes transgenerational sperm defects in mice
11. A switch from high-fat to normal diet does not restore sperm quality but prevents metabolic syndrome10.1530/REP-19-0259 ↗
12. Diet during early life defines testicular lipid content and sperm quality in adulthood10.1152/ajpendo.00235.2020 ↗
13. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder10.1126/science.aad7977 ↗
14. Obesity, energy balance and spermatogenesis10.1530/REP-17-0018 ↗
15. Fertility and Sperm Quality in the Aging Male10.2174/1381612823666170503150313 ↗
16. Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology10.1016/j.fertnstert.2010.11.044 ↗
17. Men’s body mass index in relation to embryo quality and clinical outcomes in couples undergoing in vitro fertilization10.1016/j.fertnstert.2012.07.1102 ↗
18. The BMI of men and not sperm parameters impact on embryo quality and the IVF outcome10.1111/j.2047-2927.2012.00012.x ↗
19. Male age negatively impacts embryo development and reproductive outcome in donor oocyte art cycles10.1016/j.fertnstert.2007.07.255 ↗
20. The effect of advancing paternal age on pregnancy and live birth rates in couples undergoing in vitro fertilization or gamete intrafallopian transfer10.1016/j.ajog.2004.01.035 ↗
21. Expression of obesity-related genes in human spermatozoa affects the outcomes of reproductive treatments10.1016/j.xfss.2021.03.004 ↗
22. WHO Organization (2010). WHO Laboratory Manual for the Examination and Processing of Human Semen, World Health Organization.
23. Sperm swim-up: A simple and effective technique of semen processing for intrauterine insemination
24. Biochemical pregnancy during assisted conception: A little bit pregnant
25. Metformin and male reproduction: Effects on Sertoli cell metabolism10.1111/bph.12522 ↗
26. A new mathematical model for relative quantification in real-time RT-PCR10.1093/nar/29.9.e45 ↗
27. Identification of G protein-coupled estrogen receptor in human and pig spermatozoa10.1111/joa.12183 ↗
28. Sperm concentration and normal sperm morphology decrease and follicle-stimulating hormone level increases with age10.1111/j.1464-410X.2005.05806.x ↗
29. Impact of age, clinical conditions, and lifestyle on routine semen parameters and sperm kinematics10.1016/j.fertnstert.2018.03.016 ↗
30. 17β-Estradiol activates rapid signaling pathways involved in rat pachytene spermatocytes apoptosis through GPR30 and ERα10.1016/j.mce.2010.01.035 ↗
31. Vaucher, L., Funaro, M.G., Mehta, A., Mielnik, A., Bolyakov, A., Prossnitz, E.R., Schlegel, P.N., and Paduch, D.A. (2014). Activation of GPER-1 estradiol receptor downregulates production of testosterone in isolated rat Leydig cells and adult human testis. PLoS ONE, 9.10.1371/journal.pone.0092425 ↗
32. Expression of estrogen receptors alpha (ER-α), beta (ER-β), and G protein-coupled receptor 30 (GPR30) in testicular tissue of men with Klinefelter syndrome10.1055/s-0042-105151 ↗
33. Functional expression of G protein-coupled receptor 30 in immature rat epididymal epithelium10.1002/cbin.10709 ↗
34. Senescence and declining reproductive potential: Insight into molecular mechanisms through testicular metabolomics10.1016/j.bbadis.2018.07.028 ↗
35. GPR30 Mediates the Fast Effect of Estrogen on Mouse Blastocyst and its Role in Implantation10.1177/1933719115578921 ↗
36. Imbalance between proliferation and apoptosis−related impaired GPR30 expression is involved in preeclampsia10.1007/s00441-016-2466-y ↗
37. Restraint of Trophoblast Invasion of the Uterus by Decorin: Role in Pre-eclampsia10.1111/aji.12449 ↗
38. A possible role for sperm RNA in early embryo development10.1016/j.theriogenology.2007.05.058 ↗
39. Meiotic arrest in human oocytes is maintained by a Gs signaling pathway10.1095/biolreprod.107.066019 ↗
40. Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals10.1038/cddis.2017.82 ↗
41. Role of G-protein-coupled estrogen receptor (GPER/GPR30) in maintenance of meiotic arrest in fish oocytes10.1016/j.jsbmb.2016.12.005 ↗
42. Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications10.1038/nrg.2016.106 ↗
43. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals10.1126/science.aad6780 ↗