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      An Epididymis-Specific Secretory Protein HongrES1 Critically Regulates Sperm Capacitation and Male Fertility

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          Abstract

          Mammalian sperm capacitation is an essential prerequisite to fertilizion. Although progress had been made in understanding the physiology and biochemistry of capacitation, little is known about the potential roles of epididymal proteins during this process. Here we report that HongrES1, a new member of the SERPIN (serine proteinase inhibitor) family exclusively expressed in the rat cauda epididymis and up-regulated by androgen, is secreted into the lumen and covers the sperm head. Co-culture of caudal sperms with HongrES1 antibody in vitro resulted in a significant increase in the percentage of capacitated spermatozoa. Furthermore, the percentage of capacitated spermatozoa clearly increased in rats when HongrES1 was down-regulated by RNAi in vivo. Remarkably, knockdown of HongrES1 in vivo led to reduced fertility accompanied with deformed appearance of fetuses and pups. These results identify HongrES1 as a novel and critical molecule in the regulation of sperm capacitation and male fertility.

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          Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.

          Geromy G. Moore, D Pan, Brett Olds … (1995)
          The molecular basis of mammalian sperm capacitation, defined functionally as those processes that confer on the sperm the acquisition of fertilization-competence either in vivo in the female reproductive tract or in vitro, is poorly understood. We demonstrate here that capacitation of caudal epididymal mouse sperm in vitro is accompanied by a time-dependent increase in the protein tyrosine phosphorylation of a subset of proteins of M(r) 40,000-120,000. Incubation of sperm in media devoid of bovine serum albumin, CaCl2 or NaHCO3, components which individually are required for capacitation, prevent the sperm from undergoing capacitation as assessed by the ability of the cells to acquire the pattern B chlortetracycline fluorescence, to undergo the zona pellucida-induced acrosome reaction and, in some cases, to fertilize metaphase II-arrested eggs in vitro. In each of these cases the protein tyrosine phosphorylation of the subset of capacitation-associated proteins does not occur. Protein tyrosine phosphorylation of these particular proteins, as well as sperm capacitation, can be recovered in media devoid of each of these three constituents (bovine serum albumin, CaCl2 or NaHCO3) by adding back the appropriate component in a concentration-dependent manner. The requirement of NaHCO3 for these phosphorylations is not due to an alkalinization of intracellular sperm pH or to an increase in media pH. Caput epididymal sperm, which lack the ability to undergo capacitation in vitro, do not display this capacitation-dependent subset of tyrosine phosphorylated proteins in complete media even after extended incubation periods, and do not fertilize metaphase II-arrested eggs in vitro.(ABSTRACT TRUNCATED AT 250 WORDS)
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            Observations on the penetration of the sperm in the mammalian egg.

            Christopher C. Austin (1951)
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              Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization.

              Denny Sakkas, Emre Seli, William B. Schoolcraft … (2004)
              To determine whether the extent of ongoing apoptotic cell death measured as the presence of DNA strand breaks in spermatozoa affects embryo development to the blastocyst stage in IVF. A prospective comparative study. A university IVF clinic and a private IVF clinic. Men (n = 49) undergoing infertility treatment with IVF. After density gradient centrifugation preparation, part of the sperm sample was used for infertility treatment, and the rest was fixed in paraformaldehyde. Strand breaks in DNA that are indicative of apoptosis were detected by the in situ DNA nick end labeling (TUNEL) technique. A total of 15,000 spermatozoa from each sample were evaluated for TUNEL reactivity by flow cytometry. Percentage of ejaculated spermatozoa with DNA strand breaks indicative of apoptosis, blastocyst development rate, and pregnancy rate. Blastocyst development showed a significant negative correlation with percentage TUNEL positivity in spermatozoa. When 20% was used as a cutoff for TUNEL positivity in sperm samples, the percentage of blastocyst development was 50% higher in the /=20% TUNEL positivity (n = 22; 44.7% blastocyst development vs. 29.8%). Clinical pregnancy rates in these two groups were 52% vs. 44%, respectively. The extent of nuclear DNA fragmentation in prepared ejaculated spermatozoa used in IVF negatively correlates with blastocyst development. A larger series of patients needs to be assessed to determine whether this paternal effect on blastocyst development may also affect pregnancy outcome.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2008
                Publication date (Electronic): 31 December 2008
                Volume: 3
                Issue: 12
                Electronic Location Identifier: e4106
                Affiliations
                [1 ]Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
                [2 ]Unit of Reproductive Physiology, Zhejiang Academy of Medical Sciences, Hangzhou, Zhejiang, China
                [3 ]Shanghai Institute of Planned Parenthood Research, Shanghai, China
                Yale University School of Medicine, United States of America
                Author notes

                Conceived and designed the experiments: YZ YZ. Performed the experiments: YZ MZ QS LZ WZ WC. Analyzed the data: YZ QS YZ. Wrote the paper: YZ YZ.

                Article
                Publisher ID: 08-PONE-RA-06629R1
                DOI: 10.1371/journal.pone.0004106
                PMC ID: 2606034
                PubMed ID: 19116669
                SO-VID: 113bfb9a-8976-4336-9ce5-67903573b977
                Copyright © Zhou et al. 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
                Date received : 29 September 2008
                Date accepted : 18 November 2008
                Page count
                Pages: 12
                Categories
                Subject: Research Article
                Subject: Biochemistry
                Subject: Immunology
                Subject: Molecular Biology
                Subject: Biochemistry/Cell Signaling and Trafficking Structures
                Subject: Biochemistry/Chemical Biology of the Cell
                Subject: Biochemistry/Protein Chemistry
                Subject: Biochemistry/Transcription and Translation
                Subject: Molecular Biology/DNA Methylation
                Subject: Urology/Infertility
                Subject: Urology/Testicular Cancer

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