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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Male reproductive dysfunction in Solea senegalensis: new insights into an unsolved question

Marta F. Riesco A , David G. Valcarce A , Juan Manuel Martínez-Vázquez A , Ignacio Martín A , Andrés Ángel Calderón-García B , Verónica Gonzalez-Nunez B and Vanesa Robles https://orcid.org/0000-0002-7917-7700 A C
+ Author Affiliations
- Author Affiliations

A Spanish Institute of Oceanography (IEO), Planta de Cultivos el Bocal, Barrio Corbanera, Monte, 39012 Santander, Spain.

B Instituto de Neurociencias de Castilla y León (INCyL), Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Salamanca, Institute of Biomedical Research of Salamanca (IBSAL), E-37007 Salamanca, Spain.

C Corresponding author. Email: robles.vanesa@gmail.com

Reproduction, Fertility and Development 31(6) 1104-1115 https://doi.org/10.1071/RD18453
Submitted: 23 November 2018  Accepted: 25 January 2019   Published: 4 April 2019

Abstract

Senegalese sole (Solea senegalensis) is a species with a high commercial value that exhibits a reproductive dysfunction in males born and raised in captivity (F1) that hinders their sustainable culture. The present study evaluates the sperm quality and dopaminergic pathway of males born in the wild environment and of F1 males. Traditional sperm analyses were performed, finding only significant differences in curvilinear velocity (VCL) and no significant differences in viability and total motility. No differences in global sperm methylation were observed either in spermatozoa or brain between the two groups (F1 and wild-born males). However, our results point to a different sperm molecular signature between wild fish and fish born in captivity, specifically the differential expression in miR-let7-d and miR-200a-5p between these two groups. miR-let7-d has been correlated with spermatogenesis and sex preferences, whereas the miR-200 family is implied in target innervation of dopaminergic neurons in zebrafish. When we analysed the dopaminergic pathway, no differences were found in terms of different mRNA expression of dopaminergic markers. However, some differences were detected in terms of tyrosine hydroxylase protein expression by western blot analysis, thus suggesting an altered post-transcriptional regulation in F1 males. The results of this study suggest that an altered sperm miRNA signature in F1 males could be one possible mode of transmission of reproductive dysfunction to the progeny.

Additional keywords: dopamine signalling, miRNAs, molecular assays, mRNA, Senegalese sole, sperm quality.


References

Abu-Halima, M., Hammadeh, M., Schmitt, J., Leidinger, P., Keller, A., Meese, E., and Backes, C. (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril. 99, 1249–1255.e16.
Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments.Crossref | GoogleScholarGoogle Scholar | 23312218PubMed |

Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.
MicroRNAs: genomics, biogenesis, mechanism, and function.Crossref | GoogleScholarGoogle Scholar | 14744438PubMed |

Beny-Shefer, Y., Zilkha, N., Lavi-Avnon, Y., Bezalel, N., Rogachev, I., Brandis, A., Dayan, M., and Kimchi, T. (2017). Nucleus accumbens dopamine signaling regulates sexual preference for females in male mice. Cell Reports 21, 3079–3088.
Nucleus accumbens dopamine signaling regulates sexual preference for females in male mice.Crossref | GoogleScholarGoogle Scholar | 29241537PubMed |

Borrelli, L., Aceto, S., Agnisola, C., De Paolo, S., Dipineto, L., Stilling, R. M., Dinan, T. G., Cryan, J. F., Menna, L. F., and Fioretti, A. (2016). Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish. Sci. Rep. 6, 30046.
Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish.Crossref | GoogleScholarGoogle Scholar | 27416816PubMed |

Cabrita, E., Soares, F., and Dinis, M. T. (2006). Characterization of Senegalese sole, Solea senegalensis, male broodstock in terms of sperm production and quality. Aquaculture 261, 967–975.
Characterization of Senegalese sole, Solea senegalensis, male broodstock in terms of sperm production and quality.Crossref | GoogleScholarGoogle Scholar |

Cabrita, E., Soares, F., Beirão, J., García-López, A., Martínez-Rodríguez, G., and Dinis, M. T. (2011). Endocrine and milt response of Senegalese sole, Solea senegalensis, males maintained in captivity. Theriogenology 75, 1–9.
Endocrine and milt response of Senegalese sole, Solea senegalensis, males maintained in captivity.Crossref | GoogleScholarGoogle Scholar | 20833416PubMed |

Cabrita, E., Martínez-Páramo, S., Gavaia, P. J., Riesco, M. F., Valcarce, D. G., Sarasquete, C., Herráez, M. P., and Robles, V. (2014). Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432, 389–401.
Factors enhancing fish sperm quality and emerging tools for sperm analysis.Crossref | GoogleScholarGoogle Scholar |

Carazo, I., Martin, I., Hubbard, P., Chereguini, O., Maatanas, E., Canario, A., and Duncan, N. (2011). Reproductive behaviour, the absence of reproductive behaviour in cultured (G1 generation) and chemical communication in the Senegalese sole (Solea senegalensis). Indian J. Sci. Technol. 4, 96–97.
Reproductive behaviour, the absence of reproductive behaviour in cultured (G1 generation) and chemical communication in the Senegalese sole (Solea senegalensis).Crossref | GoogleScholarGoogle Scholar |

Carazo, I., Norambuena, F., Oliveira, C., Sánchez-Vázquez, F. J., and Duncan, N. J. (2013). The effect of night illumination, red and infrared light, on locomotor activity, behaviour and melatonin of Senegalese sole (Solea senegalensis) broodstock. Physiol. Behav. 118, 201–207.
The effect of night illumination, red and infrared light, on locomotor activity, behaviour and melatonin of Senegalese sole (Solea senegalensis) broodstock.Crossref | GoogleScholarGoogle Scholar | 23711567PubMed |

Chauvigné, F., Fatsini, E., Duncan, N., Ollé, J., Zanuy, S., Gómez, A., and Cerdà, J. (2016). Plasma levels of follicle-stimulating and luteinizing hormones during the reproductive cycle of wild and cultured Senegalese sole (Solea senegalensis). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 191, 35–43.
Plasma levels of follicle-stimulating and luteinizing hormones during the reproductive cycle of wild and cultured Senegalese sole (Solea senegalensis).Crossref | GoogleScholarGoogle Scholar | 26419696PubMed |

Chauvigné, F., Ollé, J., González, W., Duncan, N., Giménez, I., and Cerdà, J. (2017). Toward developing recombinant gonadotropin-based hormone therapies for increasing fertility in the flatfish Senegalese sole. PLoS One 12, e0174387.
Toward developing recombinant gonadotropin-based hormone therapies for increasing fertility in the flatfish Senegalese sole.Crossref | GoogleScholarGoogle Scholar | 28329024PubMed |

Corral-Vazquez, C., Blanco, J., Salas-Huetos, A., Vidal, F., and Anton, E. (2017). Normalization matters: tracking the best strategy for sperm miRNA quantification. Mol. Hum. Reprod. 23, 45–53.
Normalization matters: tracking the best strategy for sperm miRNA quantification.Crossref | GoogleScholarGoogle Scholar | 27932553PubMed |

Daubner, S. C., Le, T., and Wang, S. (2011). Tyrosine hydroxylase and regulation of dopamine synthesis. Arch. Biochem. Biophys. 508, 1–12.
Tyrosine hydroxylase and regulation of dopamine synthesis.Crossref | GoogleScholarGoogle Scholar | 21176768PubMed |

Dickson, D. A., Paulus, J. K., Mensah, V., Lem, J., Saavedra-Rodriguez, L., Gentry, A., Pagidas, K., and Feig, L. A. (2018). Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress. Transl. Psychiatry 8, 101.
Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress.Crossref | GoogleScholarGoogle Scholar | 29795112PubMed |

Eisenberg, I., Kotaja, N., Goldman-Wohl, D., and Imbar, T. (2015). microRNA in human reproduction. Adv. Exp. Med. Biol. 888, 353–387.
microRNA in human reproduction.Crossref | GoogleScholarGoogle Scholar | 26663192PubMed |

Fatsini, E., Bautista, R., Manchado, M., and Duncan, N. J. (2016). Transcriptomic profiles of the upper olfactory rosette in cultured and wild Senegalese sole (Solea senegalensis) males. Comp. Biochem. Physiol. Part D Genomics Proteomics 20, 125–135.
Transcriptomic profiles of the upper olfactory rosette in cultured and wild Senegalese sole (Solea senegalensis) males.Crossref | GoogleScholarGoogle Scholar | 27689822PubMed |

Forné, I., Castellana, B., Marín-Juez, R., Cerdà, J., Abián, J., and Planas, J. V. (2011). Transcriptional and proteomic profiling of flatfish (Solea senegalensis) spermatogenesis. Proteomics 11, 2195–2211.
Transcriptional and proteomic profiling of flatfish (Solea senegalensis) spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 21538881PubMed |

Gallego, V., Herranz-Jusdado, J. G., Rozenfeld, C., Pérez, L., and Asturiano, J. F. (2018). Subjective and objective assessment of fish sperm motility: when the technique and technicians matter. Fish Physiol. Biochem. 44, 1457–1467.
Subjective and objective assessment of fish sperm motility: when the technique and technicians matter.Crossref | GoogleScholarGoogle Scholar | 29713849PubMed |

García-Herrero, S., Garrido, N., Martínez-Conejero, J. A., Remohí, J., Pellicer, A., and Meseguer, M. (2011). Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI. Reprod. Biomed. Online 22, 25–36.
Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI.Crossref | GoogleScholarGoogle Scholar | 21123116PubMed |

Grunewald, S., Paasch, U., Glander, H.-J., and Anderegg, U. (2005). Mature human spermatozoa do not transcribe novel RNA. Andrologia 37, 69–71.
Mature human spermatozoa do not transcribe novel RNA.Crossref | GoogleScholarGoogle Scholar | 16026427PubMed |

Guerra, S. M., Valcarce, D. G., Cabrita, E., and Robles, V. (2013). Analysis of transcripts in gilthead seabream sperm and zebrafish testicular cells: mRNA profile as a predictor of gamete quality. Aquaculture 406–407, 28–33.
Analysis of transcripts in gilthead seabream sperm and zebrafish testicular cells: mRNA profile as a predictor of gamete quality.Crossref | GoogleScholarGoogle Scholar |

Gunes, S., Arslan, M. A., Hekim, G. N. T., and Asci, R. (2016). The role of epigenetics in idiopathic male infertility. J. Assist. Reprod. Genet. 33, 553–569.
The role of epigenetics in idiopathic male infertility.Crossref | GoogleScholarGoogle Scholar | 26941097PubMed |

Guzmán, J. M., Norberg, B., Ramos, J., Mylonas, C. C., and Mañanós, E. L. (2008). Vitellogenin, steroid plasma levels and spawning performance of cultured female Senegalese sole (Solea senegalensis). Gen. Comp. Endocrinol. 156, 285–297.
Vitellogenin, steroid plasma levels and spawning performance of cultured female Senegalese sole (Solea senegalensis).Crossref | GoogleScholarGoogle Scholar | 18342314PubMed |

Guzmán, J. M., Rubio, M., Ortiz-Delgado, J. B., Klenke, U., Kight, K., Cross, I., Sánchez-Ramos, I., Riaza, A., Rebordinos, L., Sarasquete, C., Zohar, Y., and Mañanós, E. L. (2009). Comparative gene expression of gonadotropins (FSH and LH) and peptide levels of gonadotropin-releasing hormones (GnRHs) in the pituitary of wild and cultured Senegalese sole (Solea senegalensis) broodstocks. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 153, 266–277.
Comparative gene expression of gonadotropins (FSH and LH) and peptide levels of gonadotropin-releasing hormones (GnRHs) in the pituitary of wild and cultured Senegalese sole (Solea senegalensis) broodstocks.Crossref | GoogleScholarGoogle Scholar | 19264148PubMed |

Guzmán, J. M., Cal, R., García-López, Á., Chereguini, O., Kight, K., Olmedo, M., Sarasquete, C., Mylonas, C. C., Peleteiro, J. B., Zohar, Y., and Mañanós, E. L. (2011). Effects of in vivo treatment with the dopamine antagonist pimozide and gonadotropin-releasing hormone agonist (GnRHa) on the reproductive axis of Senegalese sole (Solea senegalensis). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 158, 235–245.
Effects of in vivo treatment with the dopamine antagonist pimozide and gonadotropin-releasing hormone agonist (GnRHa) on the reproductive axis of Senegalese sole (Solea senegalensis).Crossref | GoogleScholarGoogle Scholar | 21112410PubMed |

Hertel, J., Bartschat, S., Wintsche, A., Otto, C., Students of the Bioinformatics Computer Lab Stadler, P. F. (2012). Evolution of the let-7 microRNA family. RNA Biol. 9, 231–241.
Evolution of the let-7 microRNA family.Crossref | GoogleScholarGoogle Scholar | 22617875PubMed |

Howell, B., Conceição, L., Prickett, R., Cañavate, J. P., and Mañanós, E. L. (2009). Sole farming: nearly there but not quite? Aquaculture Europe 34, 24–27.

Infante, C., Matsuoka, M. P., Asensio, E., Canavate, J. P., Reith, M., and Manchado, M. (2008). Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol. Biol. 9, 28.
Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR.Crossref | GoogleScholarGoogle Scholar | 18325098PubMed |

Ji, J., Qin, Y., Ren, J., Lu, C., Wang, R., Dai, X., Zhou, R., Huang, Z., Xu, M., Chen, M., Wu, W., Song, L., Shen, H., Hu, Z., Miao, D., Xia, Y., and Wang, X. (2015). Mitochondria-related miR-141-3p contributes to mitochondrial dysfunction in HFD-induced obesity by inhibiting PTEN. Sci. Rep. 5, 16262.
Mitochondria-related miR-141-3p contributes to mitochondrial dysfunction in HFD-induced obesity by inhibiting PTEN.Crossref | GoogleScholarGoogle Scholar | 26548909PubMed |

Jia, K.-T., Zhang, J., Jia, P., Zeng, L., Jin, Y., Yuan, Y., Chen, J., Hong, Y., and Yi, M. (2015). Identification of MicroRNAs in zebrafish spermatozoa. Zebrafish 12, 387–397.
Identification of MicroRNAs in zebrafish spermatozoa.Crossref | GoogleScholarGoogle Scholar | 26418264PubMed |

Jiang, L., Zhang, J., Wang, J.-J., Wang, L., Zhang, L., Li, G., Yang, X., Ma, X., Sun, X., Cai, J., Zhang, J., Huang, X., Yu, M., Wang, X., Liu, F., Wu, C.-I., He, C., Zhang, B., Ci, W., and Liu, J. (2013). Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153, 773–784.
Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos.Crossref | GoogleScholarGoogle Scholar | 23663777PubMed |

Jodar, M., Selvaraju, S., Sendler, E., Diamond, M. P., Krawetz, S. A., Reproductive Medicine Network (2013). The presence, role and clinical use of spermatozoal RNAs. Hum. Reprod. Update 19, 604–624.
The presence, role and clinical use of spermatozoal RNAs.Crossref | GoogleScholarGoogle Scholar | 23856356PubMed |

Kotaja, N. (2014). MicroRNAs and spermatogenesis. Fertil. Steril. 101, 1552–1562.
MicroRNAs and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 24882619PubMed |

Kurtz, K., Saperas, N., Ausió, J., and Chiva, M. (2009). Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear spermiogenesis. J. Exp. Zool. B Mol. Dev. Evol. 312B, 149–163.
Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 19132734PubMed |

Labbé, C., Robles, V., and Herraez, M. P. (2017). Epigenetics in fish gametes and early embryo. Aquaculture 472, 93–106.
Epigenetics in fish gametes and early embryo.Crossref | GoogleScholarGoogle Scholar |

Lima Giacobbo, B., Doorduin, J., Klein, H. C., Dierckx, R. A. J. O., Bromberg, E., and de Vries, E. F. J. (2018). Brain-derived neurotrophic factor in brain disorders: focus on neuroinflammation. Mol. Neurobiol , .
Brain-derived neurotrophic factor in brain disorders: focus on neuroinflammation.Crossref | GoogleScholarGoogle Scholar | 30117106PubMed |

Liu, W.-M., Pang, R. T. K., Chiu, P. C. N., Wong, B. P. C., Lao, K., Lee, K.-F., and Yeung, W. S. B. (2012). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc. Natl Acad. Sci. USA 109, 490–494.
Sperm-borne microRNA-34c is required for the first cleavage division in mouse.Crossref | GoogleScholarGoogle Scholar | 22203953PubMed |

Mañanós, E., Ferreiro, I., Bolón, D., Guzmán, J., Mylonas, C., and Riaza, A. (2007). Different responses of Senegalese sole Solea senegalensis broodstock to a hormonal spawning induction therapy, depending on their wild or captive-reared origin. In ‘Proceedings of Aquaculture Europe 07’, Istanbul, Turkey. pp. 330–331. (European Aquaculture Society.)

McIver, S. C., Roman, S. D., Nixon, B., and McLaughlin, E. A. (2012). miRNA and mammalian male germ cells. Hum. Reprod. Update 18, 44–59.
miRNA and mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar | 21989172PubMed |

Meseguer, M., Garrido, N., Simón, C., Pellicer, A., and Remohí, J. (2004). Concentration of glutathione and expression of glutathione peroxidases 1 and 4 in fresh sperm provide a forecast of the outcome of cryopreservation of human spermatozoa. J. Androl. 25, 773–780.
Concentration of glutathione and expression of glutathione peroxidases 1 and 4 in fresh sperm provide a forecast of the outcome of cryopreservation of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 15292110PubMed |

Niu, Z., Goodyear, S. M., Rao, S., Wu, X., Tobias, J. W., Avarbock, M. R., and Brinster, R. L. (2011). MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc. Natl Acad. Sci. USA 108, 12740–12745.
MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells.Crossref | GoogleScholarGoogle Scholar | 21768389PubMed |

Nixon, B., Stanger, S. J., Mihalas, B. P., Reilly, J. N., Anderson, A. L., Tyagi, S., Holt, J. E., and McLaughlin, E. A. (2015). The microRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biol. Reprod. 93, 91.
The microRNA signature of mouse spermatozoa is substantially modified during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 26333995PubMed |

Ostermeier, G. C., Dix, D. J., Miller, D., Khatri, P., and Krawetz, S. A. B. (2002). Spermatozoal RNA profiles of normal fertile men. Lancet 360, 772–777.
Spermatozoal RNA profiles of normal fertile men.Crossref | GoogleScholarGoogle Scholar | 12241836PubMed |

Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B., Müller, P., Spring, J., Srinivasan, A., Fishman, M., Finnerty, J., Corbo, J., Levine, M., Leahy, P., Davidson, E., and Ruvkun, G. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89.
Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA.Crossref | GoogleScholarGoogle Scholar | 11081512PubMed |

Patrizio, P., Sanguineti, F., and Sakkas, D. (2008). Modern andrology: from semen analysis to postgenomic studies of the male gametes. Ann. N. Y. Acad. Sci. 1127, 59–63.
Modern andrology: from semen analysis to postgenomic studies of the male gametes.Crossref | GoogleScholarGoogle Scholar | 18443330PubMed |

Peterson, S. M., Thompson, J. A., Ufkin, M. L., Sathyanarayana, P., Liaw, L., and Congdon, C. B. (2014). Common features of microRNA target prediction tools. Front. Genet. 5, 23.
Common features of microRNA target prediction tools.Crossref | GoogleScholarGoogle Scholar | 24600468PubMed |

Potok, M. E., Nix, D. A., Parnell, T. J., and Cairns, B. R. (2013). Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern. Cell 153, 759–772.
Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern.Crossref | GoogleScholarGoogle Scholar | 23663776PubMed |

Pratt, S. L., and Calcatera, S. M. (2017). Expression of microRNA in male reproductive tissues and their role in male fertility. Reprod. Fertil. Dev. 29, 24.
Expression of microRNA in male reproductive tissues and their role in male fertility.Crossref | GoogleScholarGoogle Scholar |

Presslauer, C., Tilahun Bizuayehu, T., Kopp, M., Fernandes, J. M. O., and Babiak, I. (2017). Dynamics of miRNA transcriptome during gonadal development of zebrafish. Sci. Rep. 7, 43850.
Dynamics of miRNA transcriptome during gonadal development of zebrafish.Crossref | GoogleScholarGoogle Scholar | 28262836PubMed |

Rasines, I., Gómez, M., Martín, I., Rodríguez, C., Mañanós, E., and Chereguini, O. (2012). Artificial fertilization of Senegalese sole (Solea senegalensis): hormone therapy administration methods, timing of ovulation and viability of eggs retained in the ovarian cavity. Aquaculture 326–329, 129–135.
Artificial fertilization of Senegalese sole (Solea senegalensis): hormone therapy administration methods, timing of ovulation and viability of eggs retained in the ovarian cavity.Crossref | GoogleScholarGoogle Scholar |

Rasines, I., Gómez, M., Martín, I., Rodríguez, C., Mañanós, E., and Chereguini, O. (2013). Artificial fertilisation of cultured Senegalese sole (Solea senegalensis): effects of the time of day of hormonal treatment on inducing ovulation. Aquaculture 392–395, 94–97.
Artificial fertilisation of cultured Senegalese sole (Solea senegalensis): effects of the time of day of hormonal treatment on inducing ovulation.Crossref | GoogleScholarGoogle Scholar |

Riesco, M. F., Oliveira, C., Soares, F., Gavaia, P. J., Dinis, M. T., and Cabrita, E. (2017). Solea senegalensis sperm cryopreservation: new insights on sperm quality. PLoS One 12, e0186542.
Solea senegalensis sperm cryopreservation: new insights on sperm quality.Crossref | GoogleScholarGoogle Scholar | 29053706PubMed |

Robles, V., Herráez, P., Labbé, C., Cabrita, E., Pšenička, M., Valcarce, D. G., and Riesco, M. F. (2017). Molecular basis of spermatogenesis and sperm quality. Gen. Comp. Endocrinol. 245, 5–9.
Molecular basis of spermatogenesis and sperm quality.Crossref | GoogleScholarGoogle Scholar | 27131389PubMed |

Schulman, B. R. M., Esquela-Kerscher, A., and Slack, F. J. (2005). Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev. Dyn. 234, 1046–1054.
Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis.Crossref | GoogleScholarGoogle Scholar |

Schuster, A., Tang, C., Xie, Y., Ortogero, N., Yuan, S., and Yan, W. (2016). SpermBase: a database for sperm-borne RNA contents. Biol. Reprod. 95, 99.
SpermBase: a database for sperm-borne RNA contents.Crossref | GoogleScholarGoogle Scholar | 27628216PubMed |

Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. (2004). Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13.
Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation.Crossref | GoogleScholarGoogle Scholar | 15003116PubMed |

Thomson, J. M., Parker, J., Perou, C. M., and Hammond, S. M. (2004). A custom microarray platform for analysis of microRNA gene expression. Nat. Methods 1, 47–53.
A custom microarray platform for analysis of microRNA gene expression.Crossref | GoogleScholarGoogle Scholar | 15782152PubMed |

Thomson, J. M., Newman, M., Parker, J. S., Morin-Kensicki, E. M., Wright, T., and Hammond, S. M. (2006). Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 20, 2202–2207.
Extensive post-transcriptional regulation of microRNAs and its implications for cancer.Crossref | GoogleScholarGoogle Scholar | 16882971PubMed |

Vacher, C., Mañanos, E. L., Breton, B., Marmignon, M. H., and Saligaut, C. (2000). Modulation of pituitary dopamine D1 or D2 receptors and secretion of follicle stimulating hormone and luteinizing hormone during the annual reproductive cycle of female rainbow trout. J. Neuroendocrinol. 12, 1219–1226.
Modulation of pituitary dopamine D1 or D2 receptors and secretion of follicle stimulating hormone and luteinizing hormone during the annual reproductive cycle of female rainbow trout.Crossref | GoogleScholarGoogle Scholar | 11106981PubMed |

Valcarce, D. G., and Robles, V. (2016). Effect of captivity and cryopreservation on ROS production in Solea senegalensis spermatozoa. Reproduction 152, 439–446.
Effect of captivity and cryopreservation on ROS production in Solea senegalensis spermatozoa.Crossref | GoogleScholarGoogle Scholar | 27528770PubMed |

Valcarce, D. G., Cartón-García, F., Herráez, M. P., and Robles, V. (2013). Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development. Cryobiology 67, 84–90.
Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development.Crossref | GoogleScholarGoogle Scholar | 23727067PubMed |

Valcarce, D. G., Pardo, M. Á., Riesco, M. F., Cruz, Z., and Robles, V. (2015). Effect of diet supplementation with a commercial probiotic containing Pediococcus acidilactici (Lindner, 1887) on the expression of five quality markers in zebrafish (Danio rerio (Hamilton, 1822)) testis. J. Appl. Ichthyology 31, 18–21.
Effect of diet supplementation with a commercial probiotic containing Pediococcus acidilactici (Lindner, 1887) on the expression of five quality markers in zebrafish (Danio rerio (Hamilton, 1822)) testis.Crossref | GoogleScholarGoogle Scholar |

Valcarce, D. G., Herráez, M. P., Chereguini, O., Rodríguez, C., and Robles, V. (2016). Selection of nonapoptotic sperm by magnetic-activated cell sorting in Senegalese sole (Solea senegalensis). Theriogenology 86, 1195–1202.
Selection of nonapoptotic sperm by magnetic-activated cell sorting in Senegalese sole (Solea senegalensis).Crossref | GoogleScholarGoogle Scholar | 27173958PubMed |

Wienholds, E., Koudijs, M. J., van Eeden, F. J. M., Cuppen, E., and Plasterk, R. H. A. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat. Genet. 35, 217–218.
The microRNA-producing enzyme Dicer1 is essential for zebrafish development.Crossref | GoogleScholarGoogle Scholar | 14528306PubMed |

Woods, L. C., Li, Y., Ding, Y., Liu, J., Reading, B. J., Fuller, S. A., and Song, J. (2018). DNA methylation profiles correlated to striped bass sperm fertility. BMC Genomics 19, 244.
DNA methylation profiles correlated to striped bass sperm fertility.Crossref | GoogleScholarGoogle Scholar | 29636007PubMed |

Wu, S.-F., Zhang, H., and Cairns, B. R. (2011). Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res. 21, 578–589.
Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm.Crossref | GoogleScholarGoogle Scholar | 21383318PubMed |

Wulczyn, F. G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A., Schumacher, S., and Nitsch, R. (2007). Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 21, 415–426.
Post-transcriptional regulation of the let-7 microRNA during neural cell specification.Crossref | GoogleScholarGoogle Scholar | 17167072PubMed |

Xiong, S., Ma, W., Jing, J., Zhang, J., Dan, C., Gui, J.-F., and Mei, J. (2018). An miR-200 cluster on chromosome 23 regulates sperm motility in zebrafish. Endocrinology 159, 1982–1991.
An miR-200 cluster on chromosome 23 regulates sperm motility in zebrafish.Crossref | GoogleScholarGoogle Scholar | 29579206PubMed |

Yamamoto, K., and Vernier, P. (2011). The evolution of dopamine systems in chordates. Front. Neuroanat. 5, 21.
The evolution of dopamine systems in chordates.Crossref | GoogleScholarGoogle Scholar | 21483723PubMed |

Yang, T., Cao, C., Yang, J., Liu, T., Lei, X. G., Zhang, Z., and Xu, S. (2018a). miR-200a-5p regulates myocardial necroptosis induced by Se deficiency via targeting RNF11. Redox Biol. 15, 159–169.
miR-200a-5p regulates myocardial necroptosis induced by Se deficiency via targeting RNF11.Crossref | GoogleScholarGoogle Scholar | 29248830PubMed |

Yang, S., Toledo, E. M., Rosmaninho, P., Peng, C., Uhlén, P., Castro, D. S., and Arenas, E. (2018b). A Zeb2–miR-200c loop controls midbrain dopaminergic neuron neurogenesis and migration. Commun. Biol. 1, 75.
A Zeb2–miR-200c loop controls midbrain dopaminergic neuron neurogenesis and migration.Crossref | GoogleScholarGoogle Scholar | 30271956PubMed |

Yuan, J. S., Reed, A., Chen, F., and Stewart, C. N. (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.
Statistical analysis of real-time PCR data.Crossref | GoogleScholarGoogle Scholar | 16504059PubMed |