Molecular basis of spermatogenesis and sperm quality

https://doi.org/10.1016/j.ygcen.2016.04.026Get rights and content

Highlights

  • Non-coding RNAs are crucial in the control of germline development.

  • The chromatoid body (CB) is crucial for successful spermatogenesis.

  • mRNA profile could be used as a predictor of fertilization ability in fish.

  • Novel methods allow the quantification of the lesions in particular genome regions.

  • Environmental or nutritional conditions could modify the epigenetic landmarks.

Abstract

Spermatozoan quality can be evaluated in different ways, here we focus on the analysis of DNA, RNA and epigenetic status of germ cells. These characterizations also can be the bases for explaining sperm quality at other levels, so we will see how some of these molecules could affect other sperm quality markers. Moreover, we consider the possibility of using some of these molecules as predictors of sperm quality in terms of the ability to produce healthy offspring. The relevant effect of different types of RNA molecules in germ line specification and spermatogenesis and the importance of germ cell DNA integrity and a proper epigenetic pattern will be also discussed. Although most studies at this level have been performed in mammals, some information is available for fish; these recent discoveries in fish models are included. We provide a general overview on how these molecules could have a deep influence in the final sperm quality.

Section snippets

Functions of non-coding RNAs in the control of germline development: miRNAs, piRNAs and lncRNAs

RNAs are crucial from very early stages in germline development. Primordial germ cells (PGCs) (the precursors of gametes) acquire a specific gene expression program in which non-coding RNAs and ribonucleoproteins play an important role. Some ribonucleoproteins (RBPs) such as DND1 are from very early stages mainly expressed in germ cells having an essential role in germline development. They are such important proteins that if in zebrafish embryos their translation is blocked by using

The chromatoid body

The chromatoid body (CB) was described more than a hundred years ago (Benda, 1891, Kotaja, 2006). It is known that CB is involved in RNA storage and metabolism (Nagamori and Sassone-Corsi, 2008) being crucial for successful spermatogenesis.

The CB contains male-germ-cell-specific components, such as the mouse VASA homolog (MVH) and MIWI, as well as components of both the microRNA (miRNA) pathway (such as Argonaute proteins and the endonuclease Dicer) and the RNA-decay pathway (such as the

mRNAs

From the first part of this review, it seems clear that the role of small and long non- coding RNAs in post-transcriptional regulation is completely necessary for successful spermatogenesis. However, mRNA are also crucial molecules that could be directly related to sperm quality. We have already pointed to the possible role of CB as a centre, not only for processing but also for the storage of mRNAs. This storage prevents mRNA from degradation; it is really interesting because recently it has

DNA

In addition to RNAs, DNA is also a crucial molecule in sperm quality. A correlation between DNA integrity and motility, and even fertility has been reported (Sheikh et al., 2009). Comet assay and Sperm Chromatin Dispersion tests have been widely used in order to determine DNA integrity (Bungum, 2012). However, DNA damage could produce not only poor fertilization rates but also impaired embryo development. In addition to DNA fragmentation, there are several types of DNA damage that could not be

Epigenetic status

Epigenetic modifications or reprogramming is essential for development of sperm cells (Güneş and Kulaç, 2013, Schagdarsurengin et al., 2012). The best characterized epigenetic change is PGC reprogramming, deeply affecting DNA methylation which is almost globally erased in these cells (Messerschmidt et al., 2014). Interestingly, a recent study in zebrafish confirmed that cryopreservation of these cells could induce hypermethylation in the promoters of important genes such as vasa (Riesco and

Conclusions

Understanding the subjacent molecular regulation that control sperm quality would provide very interesting information on reproductive biology. Recent studies pointed to relatively new discovered molecules as principal actors in this respect. Although most of the knowledge is only available in mammals, recent studies in fish suggests a similar scenario. However, we are still far from understanding this complex network of molecular pathway interactions. Comparative studies analyzing all these

Acknowledgments

Authors would like to acknowledge financial support of MINECO AGL2015-68330-C2-1-R as well as COST Office (Food and Agriculture COST Action FA1205: AQUAGAMETE), Fundación Ramón Areces, Ministerio de Ciencia e Innovación MICINN AGL2009-06994, AGL2014-53167-C3-3-R, Ramón y Cajal Program RYC-2008-02339, Junta de Castilla y León E-24-2009-0036681 EDU/1084/2012, Fondo Social Europeo, the Ministry of Education, Youth and Sports of the Czech Republic — projects CENAKVA (No. CZ.1.05/2.1.00/01.0024) and

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