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Article: Absence of paternal accessory sex gland secretions disturbs epigenetic reprogramming and expression of Igf2 and Dlk1 in golden hamster embryos

TitleAbsence of paternal accessory sex gland secretions disturbs epigenetic reprogramming and expression of Igf2 and Dlk1 in golden hamster embryos
Authors
Issue Date2009
PublisherElsevier Inc. The Journal's web site is located at http://www.elsevier.com/locate/theriogenology
Citation
Theriogenology, 2009, v. 71 n. 9, p. 1367-1380 How to Cite?
AbstractAccessory sex gland (ASG) secretion is known to exert an effect on sperm that is heritable in hamster embryos. We hypothesized that ASG secretion changes the sperm epigenome, which in turn is propagated in sired embryos. To test our hypothesis, we produced male hamsters that were devoid of either all ASG (TX) or only the ventral lobe of the prostate gland (VPX). A sham-operated control group (SH) was also established. These males were mated with normal females; uterine sperm, fertilized oocytes, and pre-implantation embryos were harvested from the females after mating. Epididymal sperm were collected at the end of experiments. Immunofluorescent staining was performed on these harvested specimens using antibodies against 5-methylcytosine, Dnmt1, Dnmt3a, Dnmt3b, protamine 1, protamine 2, and aectyl-H4K5. Expression of Igf2 and Dlk1 were analyzed by real-time RT PCR and in situ hybridization. We demonstrated that the DNA methylation pattern changed dynamically in SH, TX, and VPX fertilized oocytes. In VPX and TX embryos, DNA demethylation was slower and remethylation was delayed when compared with SH embryos. In addition, Dnmt3b expression was also abnormal. When sperm from VPX and TX males were exposed to whole ASG secretion in vivo, the resulting embryos all methylated normally. Immunofluorescent staining revealed that there was no difference in protamine packaging of uterine sperm from VPX and TX males. The staining also showed a lower level of acetyl-H4K5 expression in the male pronuclei of TX produced embryos. Furthermore, the VPX and TX embryos also expressed higher levels Igf2, and Dlk1. We concluded that interactions between ASG and sperm affected: (1) histone acetylation in male pronuclei; (2) DNA methylation in fertilized oocytes; and (3) Igf2 and Dlk1 expression embryos. © 2009 Elsevier Inc. All rights reserved.
Persistent Identifierhttp://hdl.handle.net/10722/149712
ISSN
2015 Impact Factor: 1.838
2015 SCImago Journal Rankings: 0.842
ISI Accession Number ID
Funding AgencyGrant Number
Competitive Earmark Grant (CUHK4419/03)
Hong Kong Special Administrative Region
Funding Information:

We thank Dr. Anne C Ferguson-Smith of the Department of Anatomy at University of Cambridge for her invaluable contribution in formulating this research and preparation of the manuscript. We also thank Dr. Alex Chan for his constructive discussions. This work was supported by a Competitive Earmark Grant (CUHK4419/03) awarded to PHC, ASF and WSO by the Research Grant Council of the Hong Kong Special Administrative Region.

References

 

DC FieldValueLanguage
dc.contributor.authorPoon, HKen_US
dc.contributor.authorLee, KHen_US
dc.contributor.authorWong, CLen_US
dc.contributor.authorO, WSen_US
dc.contributor.authorChow, PHen_US
dc.date.accessioned2012-06-26T05:57:29Z-
dc.date.available2012-06-26T05:57:29Z-
dc.date.issued2009en_US
dc.identifier.citationTheriogenology, 2009, v. 71 n. 9, p. 1367-1380en_US
dc.identifier.issn0093-691Xen_US
dc.identifier.urihttp://hdl.handle.net/10722/149712-
dc.description.abstractAccessory sex gland (ASG) secretion is known to exert an effect on sperm that is heritable in hamster embryos. We hypothesized that ASG secretion changes the sperm epigenome, which in turn is propagated in sired embryos. To test our hypothesis, we produced male hamsters that were devoid of either all ASG (TX) or only the ventral lobe of the prostate gland (VPX). A sham-operated control group (SH) was also established. These males were mated with normal females; uterine sperm, fertilized oocytes, and pre-implantation embryos were harvested from the females after mating. Epididymal sperm were collected at the end of experiments. Immunofluorescent staining was performed on these harvested specimens using antibodies against 5-methylcytosine, Dnmt1, Dnmt3a, Dnmt3b, protamine 1, protamine 2, and aectyl-H4K5. Expression of Igf2 and Dlk1 were analyzed by real-time RT PCR and in situ hybridization. We demonstrated that the DNA methylation pattern changed dynamically in SH, TX, and VPX fertilized oocytes. In VPX and TX embryos, DNA demethylation was slower and remethylation was delayed when compared with SH embryos. In addition, Dnmt3b expression was also abnormal. When sperm from VPX and TX males were exposed to whole ASG secretion in vivo, the resulting embryos all methylated normally. Immunofluorescent staining revealed that there was no difference in protamine packaging of uterine sperm from VPX and TX males. The staining also showed a lower level of acetyl-H4K5 expression in the male pronuclei of TX produced embryos. Furthermore, the VPX and TX embryos also expressed higher levels Igf2, and Dlk1. We concluded that interactions between ASG and sperm affected: (1) histone acetylation in male pronuclei; (2) DNA methylation in fertilized oocytes; and (3) Igf2 and Dlk1 expression embryos. © 2009 Elsevier Inc. All rights reserved.en_US
dc.languageengen_US
dc.publisherElsevier Inc. The Journal's web site is located at http://www.elsevier.com/locate/theriogenologyen_US
dc.relation.ispartofTheriogenologyen_US
dc.subject.mesh5-Methylcytosine - Analysisen_US
dc.subject.meshAcetylationen_US
dc.subject.meshAnimalsen_US
dc.subject.meshBlastocyst - Chemistryen_US
dc.subject.meshCricetinaeen_US
dc.subject.meshDna (Cytosine-5-)-Methyltransferaseen_US
dc.subject.meshDna Methylationen_US
dc.subject.meshDna Modification Methylases - Analysisen_US
dc.subject.meshEmbryonic Developmenten_US
dc.subject.meshEpigenesis, Genetic - Genetics - Physiologyen_US
dc.subject.meshFemaleen_US
dc.subject.meshFluorescent Antibody Techniqueen_US
dc.subject.meshGene Expressionen_US
dc.subject.meshGenitalia, Male - Secretionen_US
dc.subject.meshHistones - Chemistryen_US
dc.subject.meshIn Situ Hybridizationen_US
dc.subject.meshInsulin-Like Growth Factor Ii - Geneticsen_US
dc.subject.meshIntracellular Signaling Peptides And Proteinsen_US
dc.subject.meshMaleen_US
dc.subject.meshMembrane Proteins - Geneticsen_US
dc.subject.meshMesocricetus - Embryology - Physiologyen_US
dc.subject.meshPregnancyen_US
dc.subject.meshReverse Transcriptase Polymerase Chain Reactionen_US
dc.subject.meshSpermatozoa - Chemistryen_US
dc.titleAbsence of paternal accessory sex gland secretions disturbs epigenetic reprogramming and expression of Igf2 and Dlk1 in golden hamster embryosen_US
dc.typeArticleen_US
dc.identifier.emailO, WS:owaisum@hkucc.hku.hken_US
dc.identifier.authorityO, WS=rp00315en_US
dc.description.naturelink_to_subscribed_fulltexten_US
dc.identifier.doi10.1016/j.theriogenology.2008.12.016en_US
dc.identifier.pmid19201017-
dc.identifier.scopuseid_2-s2.0-65449160149en_US
dc.identifier.hkuros155436-
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-65449160149&selection=ref&src=s&origin=recordpageen_US
dc.identifier.volume71en_US
dc.identifier.issue9en_US
dc.identifier.spage1367en_US
dc.identifier.epage1380en_US
dc.identifier.isiWOS:000266141600004-
dc.publisher.placeUnited Statesen_US
dc.identifier.scopusauthoridPoon, HK=7007103075en_US
dc.identifier.scopusauthoridLee, KH=7501505976en_US
dc.identifier.scopusauthoridWong, CL=26535204400en_US
dc.identifier.scopusauthoridO, WS=6701729369en_US
dc.identifier.scopusauthoridChow, PH=7202656919en_US
dc.identifier.citeulike5206759-

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