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Luisa Gioia Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Barbara Barboni Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Maura Turriani Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Giulia Capacchietti Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Maria Gabriella Pistilli Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Paolo Berardinelli Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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Mauro Mattioli Dipartimento di Scienze Biomediche Comparate, Fisiologia Veterinaria, Università di Teramo, Piazza Aldo Moro 45, Teramo 64100, Italy

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The present experiments compared the ability of pig oocytes matured either in vivo or in vitro to structurally reorganize the penetrated sperm chromatin into male pronucleus (PN) and to carry out, in parallel, the epigenetic processes of global chromatin methylation and acetylation, 12–14 h after in vitro fertilization (IVF). In addition, PN distribution of histone deacetylase (HDAC), a major enzyme interfacing DNA methylation and histone acetylation, was investigated. The ability of the oocyte to operate an efficient block to polyspermy was markedly affected by maturation. The monospermic fertilization rate was significantly higher for in vivo than for in vitro matured (IVM) oocytes (P < 0.01) which, furthermore, showed a reduced ability to transform the chromatin of penetrated sperm into male PN (P < 0.01). Indirect immunofluorescence analysis of global DNA methylation, histone acetylation and HDAC distribution (HDAC-1, -2 and -3), carried out in monospermic zygotes that reached the late PN stage, showed that IVM oocytes also had a reduced epigenetic competence. In fact, while in about 80% of in vivo matured and IVF oocytes the male PN underwent a process of active demethylation and showed a condition of histone H4 hyperacetylation, only 40% of IVM/IVF zygotes displayed a similar PN remodelling asymmetry. Oocytes that carried out the first part of maturation in vivo (up to germinal vesicle breakdown; GVBD) and then completed the process in vitro, displayed the same PN asymmetry as oocytes matured entirely in vivo. A crucial role of HDAC in the establishment of PN acetylation asymmetry seems to be confirmed by the use of HDAC inhibitors as well as by the abnormal distribution of the enzyme between the two PN in IVM zygotes. Collectively, these data demonstrated that some pig IVM oocytes fail to acquire full remodelling competence which is independent from their ooplasmic ability to morphologically reorganize the sperm nucleus into PN.

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Luisa Gioia L Gioia, Department of Bioscience and Technology for Food, Agriculture and Environment, University of Teramo, Teramo, Italy

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Luca Palazzese L Palazzese, Laboratory of Embryology, University of Teramo Faculty of Veterinary Medicine, Teramo, Italy

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Marta Czernik M Czernik, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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Domenico Iuso D Iuso , Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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Helena Fulka H Fulka, Institute of Experimental Medicine , Czech Academy of Sciences, Praha, Czech Republic

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Josef Fulka J Fulka, Institute of Animal Science, Institute of Animal Science, Prague, Czech Republic

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Pasqualino Loi P Loi, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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The fertilizing spermatozoa induce a Ca2+ oscillatory pattern, the universal hallmark of oocyte activation, in all sexually reproducing animals. Assisted Reproductive Technologies (ARTs) like intracytoplasmic sperm injection (ICSI) bypass the physiological pathway; however, while a normal Ca2+ release pattern occurs in some species, particularly humans, artificial activation is compulsory for ICSI-fertilized oocytes to develop in most farm animals. Unlike the normal oscillatory pattern, most artificial activation protocols induce a single Ca2+ spike, undermining proper ICSI-derived embryo development in these species. Curiously, diploid parthenogenetic embryos activated by the same treatments develop normally at high frequencies and implant upon transfer in the uterus. We hypothesized that, at least in ruminant’s embryos, the oscillatory calcium waves late in the first cell cycle target preferentially the paternal pronucleus and are fundamentally important for paternal nuclear remodeling. We believe that Ca2+ signaling is central to full totipotency deployment of the paternal genome. Research in this area could highlight the asymmetry between the parental genome reprogramming timing/mechanisms in early development and impact ARTs like ICSI and cloning.

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Luisa Gioia Department of Bioscience and Technology for Food, Agriculture and Environment, University of Teramo, Teramo, Italy

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Luca Palazzese Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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Marta Czernik Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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Domenico Iuso Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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Helena Fulka Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic, Institute of Animal Science, Prague, Czech Republic

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Josef Fulka Jr Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic, Institute of Animal Science, Prague, Czech Republic

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Pasqualino Loi Department of Veterinary Medicine, University of Teramo, Teramo, Italy

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The fertilizing spermatozoa induce a Ca2+ oscillatory pattern, the universal hallmark of oocyte activation, in all sexually reproducing animals. Assisted reproductive technologies (ARTs) like intracytoplasmic sperm injection (ICSI) bypass the physiological pathway; however, while a normal Ca2+ release pattern occurs in some species, particularly humans, artificial activation is compulsory for ICSI-fertilized oocytes to develop in most farm animals. Unlike the normal oscillatory pattern, most artificial activation protocols induce a single Ca2+ spike, undermining proper ICSI-derived embryo development in these species. Curiously, diploid parthenogenetic embryos activated by the same treatments develop normally at high frequencies and implant upon transfer in the uterus. We hypothesized that, at least in ruminant embryos, the oscillatory calcium waves late in the first cell cycle target preferentially the paternal pronucleus and are fundamentally important for paternal nuclear remodeling. We believe that Ca2+ signaling is central to full totipotency deployment of the paternal genome. Research in this area could highlight the asymmetry between the parental genome reprogramming timing/mechanisms in early development and impact ARTs like ICSI and cloning.

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