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      Storage and Release of Spermatozoa from the Pre-Uterine Tube Reservoir

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          Abstract

          In mammals, after coitus a small number of spermatozoa enter the uterine tube and following attachment to uterine tube epithelium are arrested in a non-capacitated state until peri-ovulatory signalling induces their detachment. Whilst awaiting release low numbers of spermatozoa continually detach from the epithelium and the uterine tube reservoir risks depletion. There is evidence of attachment of spermatozoa to uterine epithelium in several species which might form a potential pre-uterine tube reservoir. In this study we demonstrate that: (1) dog spermatozoa attach to uterine epithelium and maintain flagellar activity, (2) in non-capacitating conditions spermatozoa progressively detach with a variety of motility characteristics, (3) attachment is not influenced by epithelial changes occurring around ovulation, (4) attachment to uterine epithelium slows capacitation, (5) capacitated spermatozoa have reduced ability to attach to uterine epithelium, (6) under capacitating conditions increased numbers of spermatozoa detach and exhibit transitional and hyperactive motility which differ to those seen in non-capacitating conditions, (7) detachment of spermatozoa and motility changes can be induced by post-ovulation but not pre-ovulation uterine tube flush fluid and by components of follicular fluid and solubilised zona pellucida, (8) prolonged culture does not change the nature of the progressive detachment seen in non-capacitating conditions nor the potential for increased detachment in capacitating conditions. We postulate that in some species binding of spermatozoa to uterine epithelium is an important component of the transport of spermatozoa. Before ovulation low numbers of spermatozoa continually detach, including those which are non-capacitated with fast forward progressive motility allowing the re-population of the uterine tube, whilst around the time of ovulation, signalling from as-yet unknown factors associated with follicular fluid, oocytes and uterine tube secretion promotes the detachment of large numbers of capacitated spermatozoa with hyperactive motility that may contribute to the fertilising pool.

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          Most cited references25

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          Regulation of sperm storage and movement in the mammalian oviduct.

          The oviduct plays a vital role in ensuring successful fertilization and normal early embryonic development. The male inseminates many thousands or even millions of sperm, but this alone does not ensure that fertilization will be successful. The female tract, particularly the oviduct, provides filters that select for normal vigorously motile sperm. In conjunction with molecules in the seminal plasma and on sperm, the female tract regulates how and when sperm pass though the tract to reach the site of fertilization. Various regulatory processes control sperm passage into and through the oviduct. In some species, the uterotubal junction opens and closes to regulate when sperm may enter; furthermore, passage through the junction requires certain proteins on the sperm surface. Most of the sperm that manage to enter the oviduct soon become trapped and held in a reservoir. In marsupials and insectivores, this involves trapping sperm in mucosal crypts; while in most other mammalian species, this involves binding sperm to the oviductal epithelium. As the time of ovulation approaches, the sperm in the reservoir undergo capacitation, including motility hyperactivation. Capacitating sperm shed proteins that bind them to the mucosal epithelium, while hyperactivation assists the sperm in pulling off of the epithelium and escaping out of mucosal pockets. The process of sperm release is gradual, reducing chances of polyspermic fertilization. Released sperm may be guided towards the oocyte by secretions of the oviduct, cumulus cells, or oocyte. Hyperactivation likely assists sperm in penetrating the cumulus matrix and is absolutely required for penetrating the oocyte zona pellucida and achieving fertilization.
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            Hyperactivated sperm progress in the mouse oviduct.

            Sperm from naturally mated mice were observed and videotaped moving within mouse oviducts. The typical pattern of sperm progress involved intermittently breaking free and swimming a short distance, then reattaching to the epithelium. The proportion of sperm that swam freely (were not attached to the epithelium) was calculated and analyzed for effects of oviductal region, ovulation status, and sperm location relative to the lumen. A significantly higher proportion of sperm were free in the ampulla than in the isthmus (26.3% +/- 0.8% vs. 11.8% +/- 1.0%; p less than 0.0001) and in post-ovulatory than pre-ovulatory (16.2% +/- 2.0% vs. 10.6% +/- 1.6%; p less than 0.05) oviducts. Flagellar curvature ratio values showed that free sperm (0.716 +/- 0.024) had more sharply curved tails than stuck sperm (0.782 +/- 0.013). While this difference is significant (p = 0.01), the effect of attachment status interacted significantly (p less than 0.05) with the oviductal region such that there was a greater difference in the isthmus than in the ampulla. Only sperm using the more curved tail beats of hyperactivation were seen to break free from the epithelium and to progress along the oviduct. These results indicate that hyperactivation plays a role in moving sperm out of the isthmic reservoir and to the site of fertilization.
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              Attachment and release of spermatozoa from the caudal isthmus of the hamster oviduct.

              Female hamsters were mated shortly after the onset of oestrus. At 3 or 6 h after mating, the right oviduct was flushed in situ with 30, 90 or 180 microliters medium to remove spermatozoa from the lumen, leaving only those firmly attached to the isthmic mucosa of the oviduct. When eggs were recovered from oviducts at 20 h after flushing the majority were fertilized, indicating that the spermatozoa that were firmly attached to the mucosa were capable of detaching and ascending to the ampulla to fertilize eggs. Neither the time of flushing nor the volume of flushing medium had a significant effect on the percentage of spermatozoa that remained in the isthmus after flushing. These results suggest that there is no change in the surface of the oviduct mucosa that causes the release of spermatozoa from the caudal isthmus near the time of ovulation. When incapacitated spermatozoa were introduced into the oviduct, many of them attached to oviductal mucosa, while capacitated spermatozoa did not. This indicates that it is a change in the sperm surface, rather than the mucosal surface, that causes the release of spermatozoa, i.e. spermatozoa remain attached to the isthmic mucosa until they become capacitated and then detach and migrate to the ampulla to fertilize the eggs.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                25 February 2013
                : 8
                : 2
                : e57006
                Affiliations
                [1]Division of Veterinary Surgery, School of Veterinary Medicine and Science, Faculty of Medicine and Health Sciences, University of Nottingham, Sutton Bonington Campus, Leicestershire, United Kingdom
                Institute of Zoology, Chinese Academy of Sciences, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SLF GCWE. Performed the experiments: SLF GCWE. Analyzed the data: GCWE. Contributed reagents/materials/analysis tools: SLF GCWE. Wrote the paper: SLF GCWE.

                Article
                PONE-D-12-38028
                10.1371/journal.pone.0057006
                3581566
                23451135
                026a7f21-a5cc-4106-bd4a-04352982563e
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 December 2012
                : 17 January 2013
                Page count
                Pages: 10
                Funding
                No external funding was received for this work.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Reproductive System
                Reproductive Physiology
                Comparative Anatomy
                Developmental Biology
                Fertilization
                Zoology
                Comparative Anatomy
                Medicine
                Anatomy and Physiology
                Reproductive System
                Reproductive Physiology
                Veterinary Science
                Veterinary Anatomy and Physiology
                Animal Genital Anatomy

                Uncategorized
                Uncategorized

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