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      Molecular Alterations in Spermatozoa of a Family Case Living in the Land of Fires—A First Look at Possible Transgenerational Effects of Pollutants

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          Abstract

          In our previous work, we reported alterations in protamines/histones ratio, in DNA binding of these proteins and their involvement in DNA oxidative damage in 84% of the young men living in the Land of Fires. In the present work, we extended our findings, evaluating any alterations in spermatozoa of a family case, a father and son, living in this area, to also give a first look at the possibility of transgenerational inherited effects of environmental contaminants on the molecular alterations of sperm nuclear basic proteins (SNBP), DNA and semen parameters. In the father and son, we found a diverse excess of copper and chromium in the semen, different alterations in SNBP content and low DNA binding affinity of these proteins. In addition, DNA damage, in the presence of CuCl 2 and H 2O 2, increased by adding both the father and son SNBP. Interestingly, son SNBP, unlike his father, showed an unstable DNA binding and were able to produce DNA damage even without external addition of CuCl 2, in line with a lower seminal antioxidant activity than the father. The peculiarity of some characteristics of son semen could be a basis for possible future studies on transgenerational effects of pollutants on fertility.

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          Most cited references74

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          Temporal trends in sperm count: a systematic review and meta-regression analysis

          Reported declines in sperm counts remain controversial today and recent trends are unknown. A definitive meta-analysis is critical given the predictive value of sperm count for fertility, morbidity and mortality.
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            Chromatin dynamics during spermiogenesis.

            The function of sperm is to safely transport the haploid paternal genome to the egg containing the maternal genome. The subsequent fertilization leads to transmission of a new unique diploid genome to the next generation. Before the sperm can set out on its adventurous journey, remarkable arrangements need to be made during the post-meiotic stages of spermatogenesis. Haploid spermatids undergo extensive morphological changes, including a striking reorganization and compaction of their chromatin. Thereby, the nucleosomal, histone-based structure is nearly completely substituted by a protamine-based structure. This replacement is likely facilitated by incorporation of histone variants, post-translational histone modifications, chromatin-remodeling complexes, as well as transient DNA strand breaks. The consequences of mutations have revealed that a protamine-based chromatin is essential for fertility in mice but not in Drosophila. Nevertheless, loss of protamines in Drosophila increases the sensitivity to X-rays and thus supports the hypothesis that protamines are necessary to protect the paternal genome. Pharmaceutical approaches have provided the first mechanistic insights and have shown that hyperacetylation of histones just before their displacement is vital for progress in chromatin reorganization but is clearly not the sole inducer. In this review, we highlight the current knowledge on post-meiotic chromatin reorganization and reveal for the first time intriguing parallels in this process in Drosophila and mammals. We conclude with a model that illustrates the possible mechanisms that lead from a histone-based chromatin to a mainly protamine-based structure during spermatid differentiation. This article is part of a Special Issue entitled: Chromatin and epigenetic regulation of animal development. © 2013. Published by Elsevier B.V. All rights reserved.
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              Distinctive Chromatin in Human Sperm Packages Genes for Embryo Development

              Summary As nucleosomes are widely replaced by protamine in mature human sperm, epigenetic contributions of sperm chromatin to embryo development have been considered highly limited. However, we find the retained nucleosomes significantly enriched at loci of developmental importance including imprinted gene clusters, miRNA clusters, HOX gene clusters, and the promoters of stand-alone developmental transcription and signaling factors. Importantly, histone modifications localize to particular developmental loci. H3K4me2 is enriched at certain developmental promoters, whereas large blocks of H3K4me3 localize to a subset of developmental promoters, regions in HOX clusters, certain non-coding RNAs, and generally to paternally-expressed imprinted loci, but not paternally-repressed loci. Notably, H3K27me3 is significantly enriched at developmental promoters that are repressed in early embryos, including many bivalent (H3K4me3/H3K27me3) promoters in embryonic stem cells. Finally, developmental promoters are generally DNA hypomethylated in sperm, but acquire methylation during differentiation. Taken together, epigenetic marking in sperm is extensive, and correlated with developmental regulators.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                13 September 2020
                September 2020
                : 21
                : 18
                : 6710
                Affiliations
                [1 ]Department of Biology, University of Naples Federico II, 80126 Napoli, Italy; gennarole@ 123456outlook.com (G.L.); federicamarra14@ 123456gmail.com (F.M.); cla_mar97@ 123456hotmail.it (C.M.); marina.prisco@ 123456unina.it (M.P.)
                [2 ]Check Up—Day Surgery, Polydiagnostic and Research Centre, Reproductive Medicine Unit, 84131 Salerno, Italy; tiziananotari7@ 123456gmail.com
                [3 ]Department of Chemical Sciences, University of Naples Federico II, Via Cinthia, 21, 80126 Naples, Italy; marco.trifuoggi@ 123456unina.it (M.T.); antonella.giarra@ 123456unina.it (A.G.)
                [4 ]Department of Biological, Chemistry and Pharmaceutical Sciences and Technologies, University of Palermo, Viale delle Scienze Ed.16, 90128 Palermo, Italy; liana.bosco@ 123456unipa.it
                [5 ]Andrology Unit of the “S. Francesco d’Assisi” Hospital, Local Health Authority (ASL) Salerno, EcoFoodFertility Project Coordination Unit, 84020 Oliveto Citra, Italy
                Author notes
                [* ]Correspondence: l.montano@ 123456aslsalerno.it (L.M.); marina.piscopo@ 123456unina.it (M.P.); Tel.: +39-082-879-7111 (ext. 271) (L.M.); +39-081-679-081 (M.P.)
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-0141-3320
                https://orcid.org/0000-0002-6424-8676
                https://orcid.org/0000-0003-1623-164X
                https://orcid.org/0000-0003-1538-3983
                https://orcid.org/0000-0001-5670-9439
                https://orcid.org/0000-0003-0560-6952
                Article
                ijms-21-06710
                10.3390/ijms21186710
                7555199
                32933216
                cee976c4-fd39-4b2d-98e6-a1f56a010d6b
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 July 2020
                : 11 September 2020
                Categories
                Article

                Molecular biology
                human spermatozoa,human protamines,land of fires,dna oxidative damage,protein-dna binding,heavy metals,emsa,transgenerational effects

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