From Sperm Motility to Sperm-Borne microRNA Signatures: New Approaches to Predict Male Fertility Potential

Maíra Bianchi Rodrigues Alves, Eneiva Carla Carvalho Celeghini, Clémence Belleannée, Maíra Bianchi Rodrigues Alves, Eneiva Carla Carvalho Celeghini, Clémence Belleannée

Abstract

In addition to the paternal genome, spermatozoa carry several intrinsic factors, including organelles (e.g., centrioles and mitochondria) and molecules (e.g., proteins and RNAs), which are involved in important steps of reproductive biology such as spermatogenesis, sperm maturation, oocyte fertilization and embryo development. These factors constitute potential biomarkers of "viable sperm" and male fertility status and may become major assets for diagnosing instances of idiopathic male infertility in both humans and livestock animals. A better understanding of the mechanism of action of these sperm intrinsic factors in the regulation of reproductive and developmental processes still presents a major challenge that must be addressed. This review assembles the main data regarding morpho-functional and intrinsic sperm features that are associated with male infertility, with a particular focus on microRNA (miRNA) molecules.

Keywords: cattle; diagnosis; human; infertility; intrinsic factors; ncRNAs; semen; spermatozoa.

Copyright © 2020 Alves, Celeghini and Belleannée.

Figures

FIGURE 1
FIGURE 1
Concept of “healthy (viable) sperm.” Male fertility potential relies on structural, morpho-functional, and intrinsic sperm features that shape equally the concept of “healthy (viable) sperm.”
FIGURE 2
FIGURE 2
Structural sperm features. Spermatozoa are composed of two main parts: head and tail (or flagellum). The sperm head is constituted basically by the acrosome and nucleus. The sperm tail includes: the neck that contains mainly the proximal centriole; the midpiece which is composed by mitochondria, outer dense fibers (ODF) and axoneme; principal piece containing the fibrous sheath and axoneme; and terminal piece.
FIGURE 3
FIGURE 3
Morpho-functional sperm features. Schematic figure representing the spermatozoa with satisfactory (left) and unsatisfactory (right) morpho-functional features. Sperm acrosome membrane integrity, sperm plasma membrane integrity, sperm DNA integrity, low quantity of ROS, sperm mitochondrial membrane high activity, high sperm motility and normal sperm morphology characterize the satisfactory morpho-functional sperm features. Sperm acrosome membrane damage, sperm plasma membrane damage, sperm DNA fragmentation, high quantity of ROS, sperm mitochondrial membrane low activity, low sperm motility and abnormal sperm morphology characterize the unsatisfactory morpho-functional sperm features.
FIGURE 4
FIGURE 4
Intrinsic sperm features. Spermatozoon contributes early embryo development during mature oocyte fertilization, zygote formation and embryo cleavage potentially with intrinsic sperm features such as: sperm proteins (e.g., PLCζ, to promote oocyte activation); sperm RNAs and microRNAs (miRNAs); sperm DNA, to generate male pronucleus; sperm centrioles, to form sperm aster; and may contribute sperm mitochondria, promoting mtDNA heteroplasmy.
FIGURE 5
FIGURE 5
Schematic figure demonstrating the contribution of microRNAs (miRNAs) in the reproductive events. The sperm-related-miRNAs molecules display functions in spermatogenesis (testis), sperm maturation (epididymis caput, corpus, and cauda), sperm and seminal plasma interaction (e.g., epididymosomes) as well as modulating early embryo development.
FIGURE 6
FIGURE 6
Timeline of the new findings regarding sperm morpho-functional and intrinsic features. The paternal DNA was considered as the sole intrinsic sperm feature transferred from spermatozoon to oocyte until 1990s. In parallel, the sperm evaluation was limited to sperm conventional analyses (sperm motility and sperm morphology/abnormalities). Proximal centrioles were then shown to be transmitted by sperm to the oocytes during fertilization for the first time in 1991 (Sathananthan et al., 1991). The sperm-borne PLCζ protein was shown as a promotor of oocyte activation in 2002 (Saunders et al., 2002). The delivery of RNAs molecules was then revealed as transferred from sperm to the oocyte in 2004 (Ostermeier et al., 2004). In parallel, the sperm evaluation was updated to sperm functional analyses (e.g., sperm plasma membrane integrity). In 2010s, small sperm-borne RNAs molecules (microRNAs/miRNAs) were shown as important to early embryo development (Liu et al., 2012) potentially constituting a new group of sperm analyses composed by evaluation of molecular targets.

References

    1. Aarabi M., Balakier H., Bashar S., Moskovtsev S. I., Sutovsky P., Librach C. L., et al. (2014). Sperm content of postacrosomal WW binding protein is related to fertilization outcomes in patients undergoing assisted reproductive technology. Fertil. Steril. 102 440–447. 10.1016/j.fertnstert.2014.05.003
    1. Abu-Halima M., Hammadeh M., Schmitt J., Leidinger P., Keller A., Meese E., et al. (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril. 99 1249.e16–1255.e16. 10.1016/j.fertnstert.2012.11.054
    1. Agarwal A., Mulgund A., Hamada A., Chyatte M. R. (2015). A unique view on male infertility around the globe. Reprod. Biol. Endocrinol. 13 1–9. 10.1186/s12958-015-0032-1
    1. Aitken R. J., Wingate J. K., De Iuliis G. N., McLaughlin E. A. (2007). Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. MHR Basic Sci. Reprod. Med. 13 203–211. 10.1093/molehr/gal119
    1. Alves M. B. R., de Arruda R. P., De Bem T. H. C., Florez-Rodriguez S. A., Sá Filho M. F., de Belleannée C., et al. (2019). Sperm-borne miR-216b modulates cell proliferation during early embryo development via K-RAS. Sci. Rep. 9 1–14. 10.1038/s41598-019-46775-8
    1. Amann R. P., Hammerstedt R. H. (1993). In vitro evaluation of sperm quality: an opinion. J. Androl. 14 397–406. 10.1002/j.1939-4640.1993.tb03247.x
    1. Amaral A., Lourenço B., Marques M., Ramalho-Santos J. (2013). Mitochondria functionality and sperm quality. Reproduction 146 163–174. 10.1530/REP-13-0178
    1. Ambros V. (2004). The functions of animal microRNAs. Nature 431 350–355. 10.1038/nature02871
    1. Avidor-Reiss T., Fishman E. L. (2019). It takes two (centrioles) to tango. Reproduction 157 R33–R51. 10.1530/REP-18-0350
    1. Bahr G. F., Engler W. F. (1970). Considerations of volume, mass, DNA, and arrangement of mitochondria in the midpiece of bull spermatozoa. Exp. Cell Res. 60 338–340. 10.1016/0014-4827(70)90526-4
    1. Barceló M., Mata A., Bassas L., Larriba S. (2018). Exosomal microRNAs in seminal plasma are markers of the origin of azoospermia and can predict the presence of sperm in testicular tissue. Hum. Reprod. 33 1087–1098. 10.1093/humrep/dey072
    1. Bartel D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 281–297. 10.1016/S0092-8674(04)00045-5
    1. Bartel D. P. (2018). Metazoan MicroRNAs. Cell 173 20–51. 10.1016/j.cell.2018.03.006
    1. Belleannée C. (2015). Extracellular microRNAs from the epididymis as potential mediators of cell-to-cell communication. Asian J. Androl. 17 730–736.
    1. Belleannée C., Calvo É, Caballero J., Sullivan R. (2013). Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol. Reprod. 89:30. 10.1095/biolreprod.113.110486
    1. Betlach C., Erickson R. (1973). A unique RNA species from maturing mouse spermatozoa. Nature 242 114–115. 10.1038/242114a0
    1. Bianchi E., Doe B., Goulding D., Wright G. J. (2014). Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508 483–487. 10.1038/nature13203
    1. Björkgren I., Saastamoinen L., Krutskikh A., Huhtaniemi I., Poutanen M., Sipilä P. (2012). Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PLoS One 7:e38457. 10.1371/journal.pone.0038457
    1. Blom E. (1973). The ultrastructure of some characteristic sperm defects and a proposal for a new classification of the bull spermiogram. Nord. Vet. Med. 25 383–391.
    1. Boerke A., Dieleman S. J., Gadella B. M. (2007). A possible role for sperm RNA in early embryo development. Theriogenology 68(Suppl. 1) S147–S155. 10.1016/j.theriogenology.2007.05.058
    1. Bouhallier F., Allioli N., Lavial F., Chalmel F., Perrard M.-H., Durand P., et al. (2010). Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 16 720–731. 10.1261/rna.1963810
    1. Caballero J., Frenette G., Amours O., Belleannée C., Lacroix-Pepin N., Robert C., et al. (2012). Bovine sperm raft membrane associated Glioma Pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. J. Cell. Physiol. 227 3876–3886. 10.1002/jcp.24099
    1. Capra E., Turri F., Lazzari B., Cremonesi P., Gliozzi T. M., Fojadelli I., et al. (2017). Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between High- and Low-motile sperm populations. BMC Genomics 18:14. 10.1186/s12864-016-3394-7
    1. Celeghini E. C. C., Alves M. B. R., de Arruda R. P., de Rezende G. M., Florez-Rodriguez S. A., de Sá Filho M. F. (2019). Efficiency of CellROX deep red ® and CellROX orange ® fluorescent probes in identifying reactive oxygen species in sperm samples from high and low fertility bulls. Anim. Biotechnol. [Epub ahead of print].
    1. Celeghini E. C. C., de Arruda R. P., de Andrade A. F. C., Nascimento J., Raphael C. F. (2007). Practical techniques for bovine sperm simultaneous fluorimetric assessment of plasma, acrosomal and mitochondrial membranes. Reprod. Domest. Anim. 42 479–488. 10.1111/j.1439-0531.2006.00810.x
    1. Comazzetto S., Di Giacomo M., Rasmussen K. D., Much C., Azzi C., Perlas E., et al. (2014). Oligoasthenoteratozoospermia and Infertility in Mice Deficient for miR-34b/c and miR-449 Loci. PLoS Genet. 10:e1004597. 10.1371/journal.pgen.1004597
    1. Conine C. C., Sun F., Song L., Rivera-Pérez J. A., Rando O. J. (2018). Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. Dev. Cell 46 470.e3–480.e3. 10.1016/j.devcel.2018.06.024
    1. Conine C. C., Sun F., Song L., Rivera-Pérez J. A., Rando O. J. (2019). MicroRNAs absent in caput sperm are required for normal embryonic development. Dev. Cell 50 7–8. 10.1016/j.devcel.2019.06.007
    1. Cooper T. G., Yeung C.-H. (2003). Acquisition of volume regulatory response of sperm upon maturation in the epididymis and the role of the cytoplasmic droplet. Microsc. Res. Tech. 61 28–38. 10.1002/jemt.10314
    1. Correa J. R., Pace M. M., Zavos P. M. (1997). Relationships among frozen-thawed sperm characteristics assessed via the routine semen analysis, sperm functional tests and fertility of bulls in an artificial insemination program. Theriogenology 48 721–731. 10.1016/S0093-691X(97)00296-3
    1. Cui L., Fang L., Shi B., Qiu S., Ye Y. (2015). Spermatozoa micro ribonucleic acid–34c level is correlated with intracytoplasmic sperm injection outcomes. Fertil. Steril. 104 312.e1–317.e1. 10.1016/j.fertnstert.2015.05.003
    1. Curry E., Safranski T. J., Pratt S. L. (2011). Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76 1532–1539. 10.1016/j.theriogenology.2011.06.025
    1. D’Amours O., Frenette G., Bordeleau L.-J., Allard N., Leclerc P., Blondin P., et al. (2012). Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biol. Reprod. 87 1–11. 10.1095/biolreprod.112.100990
    1. Evenson D. P., Wixon R. (2006). Clinical aspects of sperm DNA fragmentation detection and male infertility. Theriogenology 65 979–991. 10.1016/j.theriogenology.2005.09.011
    1. Fagerlind M., Stalhammar H., Olsson B., Klinga-Levan K. (2015). Expression of miRNAs in bull spermatozoa correlates with fertility rates. Reprod. Domest. Anim. 50 587–594. 10.1111/rda.12531
    1. Farrell P. B., Presicce G. A., Brockett C. C., Foote R. H. (1998). Quantification of bull sperm characteristics measured by computer-assisted sperm analysis (CASA) and the relationship to fertility. Theriogenology 49 871–879. 10.1016/S0093-691X(98)00036-3
    1. Feugang J. M., Rodriguez-Osorio N., Kaya A., Wang H., Page G., Ostermeier G. C., et al. (2010). Transcriptome analysis of bull spermatozoa: implications for male fertility. Reprod. Biomed. Online 21 312–324. 10.1016/j.rbmo.2010.06.022
    1. Fishman E. L., Jo K., Nguyen Q. P. H., Kong D., Royfman R., Cekic A. R., et al. (2018). A novel atypical sperm centriole is functional during human fertilization. Nat. Commun. 9:2210. 10.1038/s41467-018-04678-8
    1. Gadea J., Parrington J., Kashir J., Coward K. (2013). “The male reproductive tract and spermatogenesis,” in Textbook of Clinical Embryology, eds Coward K., Wells D. (Cambridge: Cambridge University Press; ), 18–26. 10.1017/cbo9781139192736.005
    1. Gillan L., Evans G., Maxwell W. M. C. (2005). Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63 445–457. 10.1016/j.theriogenology.2004.09.024
    1. Gillan L., Kroetsch T., Chis Maxwell W. M., Evans G. (2008). Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls. Anim. Reprod. Sci. 103 201–214. 10.1016/j.anireprosci.2006.12.010
    1. Gyllensten U., Wharton D., Josefsson A., Wilson A. C. (1991). Paternal inheritance of mitochondrial DNA in mice. Nature 352 255–257. 10.1038/352255a0
    1. Hayashi K., Chuva de Sousa Lopes S. M., Kaneda M., Tang F., Hajkova P., Lao K., et al. (2008). MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3:e0001738. 10.1371/journal.pone.0001738
    1. Hecht N. B., Liem H., Kleene K. C., Distel R. J., Ho S. (1984). Maternal inheritance of the mouse mitochondrial genome is not mediated by a loss or gross alteration of the paternal mitochondrial DNA or by methylation of the oocyte mitochondrial DNA. Dev. Biol. 102 452–461. 10.1016/0012-1606(84)90210-0
    1. Hermo L., Oka R., Morales C. R. (1994). Secretion and endocytosis in the male reproductive tract: a role in sperm maturation. Int. Rev. Cytol. 154 106–189. 10.1016/S0074-7696(08)62199-3
    1. Hirohashi N., Yanagimachi R. (2018). Sperm acrosome reaction: its site and role in fertilization. Biol. Reprod. 99 127–133. 10.1093/biolre/ioy045
    1. Inaba K. (2003). Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool. Sci. 20 1043–1056. 10.2108/zsj.20.1043
    1. Irvine D. S. (1998). Epidemiology and aetiology of male infertility. Hum. Reprod. 13 33–38. 10.1093/humrep/13.1.33
    1. Jerczynski O., Lacroix-Pépin N., Boilard E., Calvo E., Bernet A., Fortier M. A., et al. (2016). Role of Dicer1-dependent factors in the paracrine regulation of epididymal gene expression. PLoS One 11:e0163876. 10.1371/journal.pone.0163876
    1. Jodar M., Selvaraju S., Sendler E., Diamond M. P., Krawetz S. A. (2013). The presence, role and clinical use of spermatozoal RNAs. Hum. Reprod. Update 19 604–624. 10.1093/humupd/dmt031
    1. Kashir J., Heindryckx B., Jones C., De Sutter P., Parrington J., Coward K. (2010). Oocyte activation, phospholipase C zeta and human infertility. Hum. Reprod. Update 16 690–703. 10.1093/humupd/dmq018
    1. Kasimanickam V., Kasimanickam R., Arangasamy A., Saberivand A., Stevenson J. S., Kastelic J. P. (2012). Association between mRNA abundance of functional sperm function proteins and fertility of Holstein bulls. Theriogenology 78 2007–2019. 10.1016/j.theriogenology.2012.07.016
    1. Kotaja N. (2014). MicroRNAs and spermatogenesis. Fertil. Steril. 101 1552–1562. 10.1016/j.fertnstert.2014.04.025
    1. Krawetz S. A. (2005). Paternal contribution: new insights and future challenges. Nat. Rev. Genet. 6 633–642. 10.1038/nrg1654
    1. Kwon W.-S., Rahman M., Lee J.-S., Kim J., Yoon S.-J., Park Y.-J., et al. (2014). A comprehensive proteomic approach to identifying capacitation related proteins in boar spermatozoa. BMC Genomics 15:897. 10.1186/1471-2164-15-897
    1. Kwon W.-S., Rahman M. S., Lee J.-S., You Y.-A., Pang M.-G. (2015). Improving litter size by boar spermatozoa: application of combined H33258/CTC staining in field trial with artificial insemination. Andrology 3 552–557. 10.1111/andr.12020
    1. Li Y., Li R. H., Ran M. X., Zhang Y., Liang K., Ren Y. N., et al. (2018). High throughput small RNA and transcriptome sequencing reveal capacitation-related microRNAs and mRNA in boar sperm. BMC Genomics 19:1–12. 10.1186/s12864-018-5132-9
    1. Liu W., Pang R. T. K., Chiu P. C. N., Wong B. P. C., Lao K., Lee K. (2012). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc. Natl. Acad. Sci. U.S.A. 109 490–494. 10.1073/pnas.1110368109
    1. Luo S., Valencia C. A., Zhang J., Lee N.-C., Slone J., Gui B., et al. (2018). Biparental Inheritance of Mitochondrial DNA in Humans. Proc. Natl. Acad. Sci. U.S.A. 115 13039–13044. 10.1073/pnas.1810946115
    1. Mattick J. S. (2001). Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep. 2 986–991. 10.1093/embo-reports/kve230
    1. Menezes E. S. B., Badial P. R., El Debaky H., Husna A. U., Ugur M. R., Kaya A., et al. (2019). Sperm miR-15a and miR-29b are associated with bull fertility. Andrologia 52:e13412. 10.1111/and.13412
    1. Morrell J. M., Valeanu A. S., Lundeheim N., Johannisson A. (2018). Sperm quality in frozen beef and dairy bull semen. Acta Vet. Scand. 60 1–10. 10.1186/s13028-018-0396-2
    1. Navara C. S., Hewitson L. C., Simerly C. R., Sutovsky P., Schatten G. (1997). The implications of a paternally derived centrosome during human fertilization: consequences for reproduction and the treatment of male factor infertility. Am. J. Reprod. Immunol. 37 39–49. 10.1111/j.1600-0897.1997.tb00191.x
    1. Nixon B., Stanger S. J., Mihalas B. P., Reilly J. N., Anderson A. L., Tyagi S., et al. (2015). The MicroRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biol. Reprod. 93 1–20. 10.1095/biolreprod.115.132209
    1. Odia M., Swanson G., Krawetz S. A. (2018). A history of why fathers’ RNA matters. Biol. Reprod. 99 147–159. 10.1093/biolre/ioy007
    1. Oliveira B. M., Arruda R. P., Thomé H. E., Maturana Filho M., Oliveira G., Guimarães C., et al. (2014). Fertility and uterine hemodynamic in cows after artificial insemination with semen assessed by fluorescent probes. Theriogenology 82 767–772. 10.1016/j.theriogenology.2014.06.007
    1. Ostermeier G. C., Goodrich R. J., Diamond M. P., Dix D. J., Krawetz S. A. (2005). Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil. Steril. 83 1687–1694. 10.1016/j.fertnstert.2004.12.046
    1. Ostermeier G. C., Miller D., Huntriss J. D., Diamond M. P., Krawetz S. A. (2004). Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429:2603. 10.1038/nature02602
    1. Papaioannou M. D., Pitetti J. L., Ro S., Park C., Aubry F., Schaad O., et al. (2009). Sertoli cell Dicer is essential for spermatogenesis in mice. Dev. Biol. 326 250–259. 10.1016/j.ydbio.2008.11.011
    1. Paul J., Duerksen J. D. (1975). Chromatin-associated RNA content of heterochromatin and euchromatin. Mol. Cell. Biochem. 9 9–16. 10.1007/BF01731728
    1. Piomboni P., Focarelli R., Stendardi A., Ferramosca A., Zara V. (2012). The role of mitochondria in energy production for human sperm motility. Int. J. Androl. 35 109–124. 10.1111/j.1365-2605.2011.01218.x
    1. Ran M., Weng B., Cao R., Li Z., Peng F., Luo H., et al. (2018). miR-26a inhibits proliferation and promotes apoptosis in porcine immature Sertoli cells by targeting the PAK2 gene. Reprod. Domest. Anim. 53 1375–1385. 10.1111/rda.13254
    1. Raposo G., Stoorvogel W. (2013). Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200 373–383. 10.1083/jcb.201211138
    1. Reilly J. N., McLaughlin E. A., Stanger S. J., Anderson A. L., Hutcheon K., Church K., et al. (2016). Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Sci. Rep. 6 1–15. 10.1038/srep31794
    1. Rodgers A. B., Morgan C. P., Bronson S. L., Revello S., Bale T. L. (2013). Paternal stress exposure alters sperm MicroRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33 9003–9012. 10.1523/JNEUROSCI.0914-13.2013
    1. Rodgers A. B., Morgan C. P., Leu N. A., Bale T. L. (2015). Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. U.S.A. 112 13699–13704. 10.1073/pnas.1508347112
    1. Rompala G. R., Simons A., Kihle B., Homanics G. E. (2018). Paternal preconception chronic variable stress confers attenuated ethanol drinking behavior selectively to male offspring in a pre-stress environment dependent manner. Front. Behav. Neurosci. 12:257. 10.3389/fnbeh.2018.00257
    1. Salas-Huetos A., Blanco J., Vidal F., Godo A., Grossmann M., Pons M. C., et al. (2015). Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertil. Steril. 104 591–601. 10.1016/j.fertnstert.2015.06.015
    1. Salas-Huetos A., Blanco J., Vidal F., Grossmann M., Pons M. C., Garrido N., et al. (2016). Sperm from normozoospermic fertile and infertile individuals convey a distinct miRNA cargo. Andrology 4 1–9. 10.1111/andr.12276
    1. Samans B., Yang Y., Krebs S., Sarode G. V., Blum H., Reichenbach M., et al. (2014). Uniformity of nucleosome preservation pattern in mammalian sperm and Its connection to repetitive DNA elements. Dev. Cell 30 23–35. 10.1016/j.devcel.2014.05.023
    1. Sathananthan A. H., Kola I., Osborne J., Trounson A., Ng S. C., Bongso A., et al. (1991). Centrioles in the beginning of human development. Proc. Natl. Acad. Sci. U.S.A. 88 4806–4810. 10.1073/pnas.88.11.4806
    1. Satouh Y., Inoue N., Ikawa M., Okabe M. (2012). Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. J. Cell Sci. 125 4985–4990. 10.1242/jcs.100867
    1. Saunders C. M., Larman M. G., Parrington J., Cox L. J., Royse J., Blayney L. M., et al. (2002). PLC ζ: a sperm-specific trigger of Ca 2 + oscillations in eggs and embryo development. Development 3544 3533–3544.
    1. Schatten H., Sun Q.-Y. (2009). The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol. Hum. Reprod. 15 531–538. 10.1093/molehr/gap049
    1. Schuster A., Skinner M. K., Yan W. (2016). Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ. Epigenet. 2:dvw001. 10.1093/eep/dvw001
    1. Sellem E., Broekhuijse M. L. W. J., Chevrier L., Camugli S., Schmitt E., Schibler L., et al. (2015). Use of combinations of in vitro quality assessments to predict fertility of bovine semen. Theriogenology 84 1447.e5–1454.e5. 10.1016/j.theriogenology.2015.07.035
    1. Sharma U., Conine C. C., Shea J. M., Boskovic A., Derr A. G., Bing X. Y., et al. (2016). Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351 391–396. 10.1126/science.aad6780
    1. Sharma U., Sun F., Conine C. C., Reichholf B., Kukreja S., Herzog V. A., et al. (2018). Small RNAs are trafficked from the epididymis to developing mammalian sperm. Dev. Cell 46 481–494. 10.1016/j.devcel.2018.06.023
    1. Simerly C., Manil-Ségalen M., Castro C., Hartnett C., Kong D., Verlhac M. H., et al. (2018). Separation and loss of centrioles from primordidal germ cells to mature oocytes in the mouse. Sci. Rep. 8 1–17. 10.1038/s41598-018-31222-x
    1. Simerly C., Wu G.-J., Zoran S., Ord T., Rawlins R., Jones J., et al. (1995). The paternal inheritance of the centrosome, the cell’s microtubule-organizing center, in humans, and the implications for infertility. Nat. Med. 1 47–52. 10.1038/nm0195-47
    1. Sipilä P., Björkgren I. (2016). Segment-specific regulation of epididymal gene expression. Reproduction 152 R91–R99. 10.1530/REP-15-0533
    1. Smorag L., Zheng Y., Nolte J., Zechner U., Engel W., Pantakani D. V. K. (2012). MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221, -203 and -34b-5p mediated spermatogenesis regulation. Biol. Cell 104 677–692. 10.1111/boc.201200014
    1. Song G. J., Lewis V. (2008). Mitochondrial DNA integrity and copy number in sperm from infertile men. Fertil. Steril. 90 2238–2244. 10.1016/j.fertnstert.2007.10.059
    1. Sullivan R. (2015). Epididymosomes: a heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J. Androl. 17 726–729. 10.4103/1008-682X.155255
    1. Sullivan R., Frenette G., Girouard J. (2007). Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J. Androl. 9 483–491. 10.1111/j.1745-7262.2007.00281.x
    1. Sullivan R., Saez F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 146 R21–35. 10.1530/REP-13-0058
    1. Tang F., Kaneda M., O’Carroll D., Hajkova P., Barton S. C., Sun Y. A., et al. (2007). Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 21 644–648. 10.1101/gad.418707
    1. Tscherner A., Gilchrist G., Smith N., Blondin P., Gillis D., LaMarre J. (2014). MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reprod. Biol. Endocrinol. 12:85. 10.1186/1477-7827-12-85
    1. Vincent P., Underwood S. L., Dolbec C., Bouchard N., Kroetsch T., Blondin P. (2012). Bovine semen quality control in artificial insemination centers. Anim. Reprod. 9 153–165.
    1. Wang C., Yang C., Chen X., Yao B., Yang C., Zhu C., et al. (2011). Altered profile of seminal plasma microRNAs in the molecular diagnosis of male infertility. Clin. Chem. 57 1722–1731. 10.1373/clinchem.2011.169714
    1. Wang M., Gao Y., Qu P., Qing S., Qiao F., Zhang Y., et al. (2017). Sperm-borne miR-449b influences cleavage, epigenetic reprogramming and apoptosis of SCNT embryos in bovine. Sci. Rep. 7 1–12. 10.1038/s41598-017-13899-8
    1. Weinhold B. (2006). Epigenetics: the science of change. Environ. Health Perspect. 114 160–167.
    1. Wightman B., Ha I., Ruvkun G. (1993). Posttranscriptional regulation of the heterochronic gene lin- 14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75 855–862. 10.1016/0092-8674(93)90530-4
    1. Wu A. T. H., Sutovsky P., Manandhar G., Xu W., Katayama M., Day B. N., et al. (2007). PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J. Biol. Chem. 282 12164–12175. 10.1074/jbc.M609132200
    1. Wu J., Bao J., Kim M., Yuan S., Tang C., Zheng H., et al. (2014). Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc. Natl. Acad. Sci. U.S.A. 111 E2851–E2857. 10.1073/pnas.1407777111
    1. Yuan S., Schuster A., Tang C., Yu T., Ortogero N., Bao J., et al. (2016). Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143 635–647. 10.1242/dev.131755
    1. Zegers-Hochschild F., Adamson G. D., Dyer S., Racowsky C., De Mouzon J., Sokol R., et al. (2017). The international glossary on infertility and fertility care, 2017. Hum. Reprod. 32 1786–1801. 10.1093/humrep/dex234
    1. Zhou J.-H., Zhou Q.-Z., Yang J.-K., Lyu X.-M., Bian J., Guo W.-B., et al. (2017). MicroRNA-27a-mediated repression of cysteine-rich secretory protein 2 translation in asthenoteratozoospermic patients. Asian J. Androl. 19:591. 10.4103/1008-682X.185001
    1. Zhou W., Stanger S. J., Anderson A. L., Bernstein I. R., De Iuliis G. N., McCluskey A., et al. (2019). Mechanisms of tethering and cargo transfer during epididymosome-sperm interactions. BMC Biol. 17:1–18. 10.1186/s12915-019-0653-5
    1. Zimmermann C., Romero Y., Warnefors M., Bilican A., Borel C., Smith L. B., et al. (2014). Germ cell-specific targeting of DICER or DGCR8 reveals a novel role for endo-siRNAs in the progression of mammalian spermatogenesis and male fertility. PLoS One 9:e107023. 10.1371/journal.pone.0107023
    1. Zini A., Agarwal A. (2011). Sperm Chromatin. New York, NY: Springer.
    1. Ziyyat A. (2001). Differential gene expression in pre-implantation embryos from mouse oocytes injected with round spermatids or spermatozoa. Hum. Reprod. 16 1449–1456. 10.1093/humrep/16.7.1449

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