The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo

Romanato, Marina; Julianelli, Vanina Laura; Zappi, M.; Calvo, Lucrecia; Calvo, Juan

doi:10.1093/humrep/den028

Cited by 18 publications

(22 citation statements)

References 29 publications

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“…To date, the nature of the molecule required for the process of protamine replacement by oocyte-derived histone was still unknown. Some previous studies have reported that HS in concert with GSH leads to SCD induction in human spermatozoa [22,28,47]. The results of the present study are in line with these previous studies, demonstrating that HS was expressed in the mouse ooplasm and induced chromatin accessibility during SCD.…”

Section: Discussionsupporting

confidence: 93%

“…Heparin, a negatively charged compound, is made by secretory granules of mast cells, whereas no heparin is found in cumulus-oocyte complexes (COCs) and granulosa cells. In contrast, HS, a negatively charged polysaccharide with a qualitatively similar function and structure to heparin, is produced in all types of cells, including oocytes [21,22]. We also found that HS has the ability to decondense sperm chromatin.…”

Section: Discussionmentioning

confidence: 64%

“…Among these six genes, Gas6 silencing resulted in a marked reduction in Ndst1 (N-deacetylase/N-sulfotransferase 1), the first modification enzyme producing heparan sulfate (HS). HS, a member of glycosaminoglycans (GAGs), is produced by virtually all types of cells, including human and mouse oocytes [21,22]. Indeed, HS is highly negatively charged by sulfate and carboxyl groups, which bind to positively charged protamine [23].…”

Section: Introductionmentioning

confidence: 99%

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Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

Kim

Lee

et al. 2017

Cell Physiol Biochem

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Background/Aims: Previously, we found that silencing of growth arrest-specific gene 6 (Gas6) in oocytes impaired cytoplasmic maturation, resulting in failure of sperm chromatin decondensation (SCD) and pronuclear (PN) formation after fertilization. Thus, we conducted this study to determine the effect of Gas6 RNAi on downstream genes and to elucidate the working mechanism of Gas6 on oocyte cytoplasmic maturation and SCD. Methods: Using RT-PCR, Western blot and immunofluorescence, the expression levels of various target genes and the localization of heparan sulfate (HS) were analyzed after Gas6 RNAi. The roles of Gas6 in HS biosynthesis, production of ATP and GSH, ROS generation and ΔΨm were also investigated. SCD and micrococcal nuclease (MNase) analyses were used to examine the effects of HS on the open chromatin state in sperm and somatic cell nuclei, respectively. Results: Disruption of Gas6 expression led to the inhibition of HS biosynthesis through the reduction of several HS biosynthetic enzymes. The rescue experiment, HS treatment in vitro, significantly recovered SCD and PN formation, confirming that HS had the ability to induce sperm head remodeling during fertilization. Interestingly, excessive mitochondrial activation in Gas6-depleted MII oocytes caused ROS generation and glutathione (GSH) degradation via mitochondrial activation, such as elevated ΔΨm and ATP production. Indeed, HS-treated NIH3T3 cell nuclei showed an open chromatin state, as determined by diffuse DAPI staining and increased sensitivity to MNase. Conclusion: We propose that the addition of HS to sperm and/or oocyte maturation would improve the efficiency of in vitro fertilization and somatic cell nuclear transfer (SCNT) reprogramming.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 64%

Section: Introductionmentioning

confidence: 99%

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Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

Kim

Lee

et al. 2017

Cell Physiol Biochem

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“…This is consistent with and is likely facilitated by the GAGs, including heparin, in mammalian oocytes [Reyes et al 2004;Romanato et al 2008]. In this study we showed that histone H1 is present in the bull sperm nucleus and is released during nuclear decondensation mediated by the heparin-GSH.…”

Section: Discussionsupporting

confidence: 87%

Presence and Release of Bovine Sperm Histone H1 During Chromatin Decondensation by Heparin-Glutathione

Sánchez-Vázquez

Flores-Alonso

Merchant‐Larios

et al. 2008

Systems Biology in Reproductive Medicine

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During spermatogenesis, changes in sperm nuclear morphology are associated with the replacement of core somatic histones by protamines. Although protamines are the major nucleoproteins of mature sperm, not all species totally replace the histones. Histone H1, along with protamines, mediates chromatin condensation into an insoluble complex that is transcriptionally inactive. In vitro, heparin-reduced glutathione causes sperm decondensation, and the structures formed are morphologically similar to the in vivo male pronucleus. To study the participation of histone H1 in bovine sperm chromatin remodelling, we measured the presence and release of histone H1 by immunofluorescence, acetic acid-urea-triton-polyacrylamide gel electrophoresis, and immunoblotting. Nuclear decondensation was induced by 80 microM heparin and 15.0 mM reduced glutathione (GSH) for 7, 14, and 21 h at 37 degrees C. Additionally, nucleons, composed of nuclei isolated from the sperm, were decondensed with 20.0 microM heparin and 5.0 mM GSH for 4.0 h at 37 degrees C. Controls were incubated in buffer for similar periods of time. Immunofluorescent localization of histone H1 was carried out with mouse monoclonal antibody, and DNA localization was visualized by 0.001% quinacrine staining. Chromatin decondensation was accompanied by increased sperm nuclei and nucleon surface area. We observed that histone H1 was localized exclusively in the nuclei of intact sperm and nucleons. Histone H1 immunofluorescent intensity did not change in control samples but decreased over time in samples treated with heparin-GSH. There was a negative correlation between the surface area of sperm nuclei and immunohistochemical intensity of histone H1 (P < 0.05). Nucleon decondensation showed a similar relationship. By electrophoresis and immunoblotting, we verified the loss of histone H1 from the sperm and nucleons and its release into the incubation media. Based on these results, we propose that histone H1 is present in the bovine sperm nuclei. H1 depletion may participate in chromatin decondensation and nuclear swelling induced by heparin-GSH.

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“…В сперме плотная упаковка хроматина обеспечивается протаминами, а не гистонами. После оплодотворения ГС облегчают удаление протаминов, что способствует деконденсации хроматина сперматозоида и слиянию муж ского и жен-ского генетического материала [125]. ДС и гепарин также способствовали деконденсации хроматина в мы-шиных сперматозоидах in vitro, но активность гепари-на при этом была значительно выше.…”

Section: функциональная роль внутриядерных протеогликановunclassified

Proteoglycans in normal physiology and carcinogenesis

Суховских¹,

Григорьева²

2018

Usp. mol. onkol

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The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo

Abstract: The results presented in this paper demonstrate for the first time that HS is present in the mammalian oocyte and show that HS is necessary for fresh oocytes to express their sperm decondensing ability in vitro.

Cited by 18 publications

References 29 publications

Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

Presence and Release of Bovine Sperm Histone H1 During Chromatin Decondensation by Heparin-Glutathione

Proteoglycans in normal physiology and carcinogenesis

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