{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T01:07:57Z","timestamp":1788138477532,"version":"build-2803163510"},"reference-count":172,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2022,7,26]],"date-time":"2022-07-26T00:00:00Z","timestamp":1658793600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":["rep.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2022,9,1]]},"abstract":"<jats:title>\u2003<\/jats:title>\n                  <jats:sec>\n                    <jats:title>In brief<\/jats:title>\n                    <jats:p>Protamines package and shield the paternal DNA in the sperm nucleus and have been studied in many mouse models over decades. This review recapitulates and updates our knowledge about protamines and reveals a surprising complexity in protamine function and their interactions with other sperm nuclear proteins.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Abstract<\/jats:title>\n                    <jats:p>The packaging and safeguarding of paternal DNA in the sperm cell nucleus is a critical feature of proper sperm function. Histones cannot mediate the necessary hypercondensation and shielding of chromatin required for motility and transit through the reproductive tracts. Paternal chromatin is therefore reorganized and ultimately packaged by protamines. In most mammalian species, one protamine is present in mature sperm (PRM1). In rodents and primates among others, however, mature sperm contain a second protamine (PRM2). Unlike PRM1, PRM2 is cleaved at its N-terminal end. Although protamines have been studied for decades due to their role in chromatin hypercondensation and involvement in male infertility, key aspects of their function are still unclear. This review updates and integrates our knowledge of protamines and their function based on lessons learned from mouse models and starts to answer open questions. The combined insights from recent work reveal that indeed both protamines are crucial for the production of functional sperm and indicate that the two protamines perform distinct functions beyond simple DNA compaction. Loss of one allele of PRM1 leads to subfertility whereas heterozygous loss of PRM2 does not. Unprocessed PRM2 seems to play a distinct role related to the eviction of intermediate DNA-bound proteins and the incorporation of both protamines into chromatin. For PRM1, on the other hand, heterozygous loss leads to strongly reduced sperm motility as the main phenotype, indicating that PRM1 might be important for processes ensuring correct motility, apart from DNA compaction.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1530\/rep-22-0107","type":"journal-article","created":{"date-parts":[[2022,7,7]],"date-time":"2022-07-07T09:28:45Z","timestamp":1657186125000},"page":"R57-R74","update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-11","source":"Crossref","is-referenced-by-count":38,"title":["Protamines: lessons learned from mouse models"],"prefix":"10.1093","volume":"164","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0681-0392","authenticated-orcid":false,"given":"Lena","family":"Ar\u00e9valo","sequence":"first","affiliation":[{"name":"Department of Developmental Pathology , Institute of Pathology, University Hospital Bonn, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5805-965X","authenticated-orcid":false,"given":"Gina","family":"Esther Merges","sequence":"additional","affiliation":[{"name":"Department of Developmental Pathology , Institute of Pathology, University Hospital Bonn, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9894-5608","authenticated-orcid":false,"given":"Simon","family":"Schneider","sequence":"additional","affiliation":[{"name":"Department of Developmental Pathology , Institute of Pathology, University Hospital Bonn, Bonn, Germany"},{"name":"Bonn Technology Campus , Core Facility \u2018Gene-Editing\u2019, University Hospital Bonn, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8272-0076","authenticated-orcid":false,"given":"Hubert","family":"Schorle","sequence":"additional","affiliation":[{"name":"Department of Developmental Pathology , Institute of Pathology, University Hospital Bonn, Bonn, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,7,26]]},"reference":[{"key":"2026010712074114300_bib1","doi-asserted-by":"publisher","first-page":"1096","DOI":"10.2164\/jandrol.112.016535","article-title":"Reactive oxygen species and sperm function \u2013 in sickness and in health","volume":"33","author":"Aitken","year":"2012","journal-title":"Journal of Andrology"},{"key":"2026010712074114300_bib2","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1080\/15216549800201332","article-title":"Transition protein 1 from boar late spermatid nuclei having DNA-melting activity is a dimeric protein","volume":"44","author":"Akama","year":"1998","journal-title":"Biochemistry and Molecular Biology International"},{"key":"2026010712074114300_bib3","doi-asserted-by":"publisher","first-page":"741","DOI":"10.2164\/jandrol.05063","article-title":"DNA integrity is compromised in protamine-deficient human sperm","volume":"26","author":"Aoki","year":"2005","journal-title":"Journal of Andrology"},{"key":"2026010712074114300_bib4","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1093\/molehr\/gah258","article-title":"A novel mechanism of protamine expression deregulation highlighted by abnormal protamine transcript retention in infertile human males with sperm protamine deficiency","volume":"12","author":"Aoki","year":"2006","journal-title":"Molecular Human Reproduction"},{"key":"2026010712074114300_bib5","doi-asserted-by":"publisher","first-page":"1408","DOI":"10.1016\/j.fertnstert.2006.04.024","article-title":"Sperm protamine 1\/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability","volume":"86","author":"Aoki","year":"2006","journal-title":"Fertility and Sterility"},{"key":"2026010712074114300_bib6","doi-asserted-by":"publisher","first-page":"2124","DOI":"10.1111\/evo.14305","article-title":"Sexual selection towards a protamine expression ratio optimum in two rodent groups?","volume":"75","author":"Ar\u00e9valo","year":"2021","journal-title":"Evolution; International Journal of Organic Evolution"},{"key":"2026010712074114300_bib7","doi-asserted-by":"publisher","first-page":"e1010272","DOI":"10.1371\/journal.pgen.1010272","article-title":"Loss of the cleaved-protamine 2 domain leads to incomplete histone-to-protamine exchange and infertility in mice","volume":"18","author":"Ar\u00e9valo","year":"2022","journal-title":"PLoS Genetics"},{"key":"2026010712074114300_bib8","doi-asserted-by":"publisher","first-page":"1338","DOI":"10.1101\/gr.094953.109","article-title":"Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences","volume":"19","author":"Arpanahi","year":"2009","journal-title":"Genome Research"},{"key":"2026010712074114300_bib9","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1016\/j.jsb.2014.09.004","article-title":"Comparative structure of vertebrate sperm chromatin","volume":"188","author":"Ausio","year":"2014","journal-title":"Journal of Structural Biology"},{"key":"2026010712074114300_bib10","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1083\/jcb.93.2.298","article-title":"A model for the structure of chromatin in mammalian sperm","volume":"93","author":"Balhorn","year":"1982","journal-title":"Journal of Cell Biology"},{"key":"2026010712074114300_bib11","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2007-8-9-227","article-title":"The protamine family of sperm nuclear proteins","volume":"8","author":"Balhorn","year":"2007","journal-title":"Genome Biology"},{"key":"2026010712074114300_bib12","doi-asserted-by":"publisher","first-page":"4074","DOI":"10.1021\/bi00637a021","article-title":"Mouse sperm chromatin proteins: quantitative isolation and partial characterization","volume":"16","author":"Balhorn","year":"1977","journal-title":"Biochemistry"},{"key":"2026010712074114300_bib13","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1007\/BF01960243","article-title":"Aberrant protamine 1\/protamine 2 ratios in sperm of infertile human males","volume":"44","author":"Balhorn","year":"1988","journal-title":"Experientia"},{"key":"2026010712074114300_bib14","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1016\/0003-9861(9290588-n","article-title":"Formation of intraprotamine disulfides in vitro","volume":"296","author":"Balhorn","year":"1992","journal-title":"Archives of Biochemistry and Biophysics"},{"key":"2026010712074114300_bib15","author":"Balhorn","year":"1995","journal-title":"Importance of Protamine Phosphorylation to Histone Displacement in Spermatids: Can the Disruption of This Process Be Used for Male Contraception"},{"issue":"Supplement","key":"2026010712074114300_bib16","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1002\/(SICI)1098-2795(200006)56:2+&lt;230::AID-MRD3&gt;3.0.CO;2-V","article-title":"DNA condensation by protamine and arginine-rich peptides: analysis of toroid stability using single DNA molecules","volume":"56","author":"Balhorn","year":"2000","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib17","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1080\/19396368.2018.1510063","article-title":"New monoclonal antibodies specific for mammalian protamines P1 and P2","volume":"64","author":"Balhorn","year":"2018","journal-title":"Systems Biology in Reproductive Medicine"},{"key":"2026010712074114300_bib18","doi-asserted-by":"publisher","first-page":"89.e8","DOI":"10.1016\/j.molcel.2017.02.025","article-title":"Histone variant HA.L.2 guides transition protein-dependent protamine assembly in male germ cells","volume":"66","author":"Barral","year":"2017","journal-title":"Molecular Cell"},{"key":"2026010712074114300_bib19","doi-asserted-by":"publisher","first-page":"21039","DOI":"10.1016\/S0021-9258(1745324-5","article-title":"Interaction of spermatid-specific protein TP2 with nucleic acids, in vitro. A comparative study with TP1","volume":"265","author":"Baskaran","year":"1990","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib20","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1002\/mrd.1080340109","article-title":"Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin","volume":"34","author":"Belokopytova","year":"1993","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib21","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1002\/(SICI)1098-2795(199807)50:3&lt;345::AID-MRD11&gt;3.0.CO;2-3","article-title":"Protein and DNA contents in sperm from an infertile human male possessing protamine defects that vary over time","volume":"50","author":"Bench","year":"1998","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib22","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1002\/1098-2795(200008)56:4&lt;512::AID-MRD9&gt;3.0.CO;2-M","article-title":"Zinc is sufficiently abundant within mammalian sperm nuclei to bind stoichiometrically with protamine 2","volume":"56","author":"Bench","year":"2000","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-1-4614-7783-9_1","article-title":"Structure of chromatin in spermatozoa","volume":"791","author":"Bjorndahl","year":"2014","journal-title":"Advances in Experimental Medicine and Biology"},{"key":"2026010712074114300_bib24","doi-asserted-by":"publisher","first-page":"110964","DOI":"10.1016\/j.mce.2020.110964","article-title":"Paternal epigenetics: mammalian sperm provide much more than DNA at fertilization","volume":"518","author":"Bl\u00e9vec","year":"2020","journal-title":"Molecular and Cellular Endocrinology"},{"key":"2026010712074114300_bib25","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/0003-9861(7590269-6","article-title":"The histones of rat testis","volume":"168","author":"Branson","year":"1975","journal-title":"Archives of Biochemistry and Biophysics"},{"key":"2026010712074114300_bib26","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1038\/ng0501-10","article-title":"Packaging paternal chromosomes with protamine","volume":"28","author":"Braun","year":"2001","journal-title":"Nature Genetics"},{"key":"2026010712074114300_bib27","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1126\/science.286.5437.120","article-title":"Protamine-induced condensation and decondensation of the same DNA molecule","volume":"286","author":"Brewer","year":"1999","journal-title":"Science"},{"key":"2026010712074114300_bib28","doi-asserted-by":"publisher","first-page":"38895","DOI":"10.1074\/jbc.M204755200","article-title":"Condensation of DNA by spermatid basic nuclear proteins","volume":"277","author":"Brewer","year":"2002","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib29","doi-asserted-by":"publisher","DOI":"10.1186\/1756-8935-7-2","article-title":"Epigenetic marking of sperm by post-translational modification of histones and protamines","volume":"7","author":"Brunner","year":"2014","journal-title":"Epigenetics and Chromatin"},{"key":"2026010712074114300_bib30","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1038\/nsmb.1821","article-title":"Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa","volume":"17","author":"Brykczynska","year":"2010","journal-title":"Nature Structural and Molecular Biology"},{"issue":"Supplement 13","key":"2026010712074114300_bib31","first-page":"65","article-title":"Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis","volume":"13","author":"Calvin","year":"1971","journal-title":"Journal of Reproduction and Fertility: Supplement"},{"key":"2026010712074114300_bib32","doi-asserted-by":"publisher","first-page":"5506","DOI":"10.1016\/S0021-9258(2081134-X","article-title":"Trout testis cells. 3. Acetylation of histones in different cell types from developing trout testis","volume":"247","author":"Candido","year":"1972","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib33","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1002\/1098-2795(20010401)58:4&lt;437::AID-MRD12&gt;3.0.CO;2-Q","article-title":"Stimulation of DNA repair by the spermatidal TP1 protein","volume":"58","author":"Caron","year":"2001","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib34","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.devcel.2014.05.024","article-title":"High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm","volume":"30","author":"Carone","year":"2014","journal-title":"Developmental Cell"},{"key":"2026010712074114300_bib35","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1042\/bj2770039","article-title":"Processing of the precursor of protamine P2 in mouse. Peptide mapping and N -terminal sequence analysis of intermediates","volume":"277","author":"Carr\u00e9-Eus\u00e8be","year":"1991","journal-title":"Biochemical Journal"},{"key":"2026010712074114300_bib36","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1002\/j.1939-4640.2001.tb02220.x","article-title":"Altered protamine 2 expression is uncommon in donors of known fertility, but common among men with poor fertilizing capacity, and may reflect other abnormalities of spermiogenesis","volume":"22","author":"Carrell","year":"2001","journal-title":"Journal of Andrology"},{"key":"2026010712074114300_bib37","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1093\/humupd\/dml057","article-title":"Altered protamine expression and diminished spermatogenesis: what is the link?","volume":"13","author":"Carrell","year":"2007","journal-title":"Human Reproduction Update"},{"key":"2026010712074114300_bib38","doi-asserted-by":"publisher","first-page":"601","DOI":"10.4103\/1008-682X.153302","article-title":"Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility","volume":"17","author":"Castillo","year":"2015","journal-title":"Asian Journal of Andrology"},{"key":"2026010712074114300_bib39","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/0014-4827(7190308-9","article-title":"\u2018Unscheduled\u2019 DNA synthesis in human germ cells following UV irradiation","volume":"69","author":"Chandley","year":"1971","journal-title":"Experimental Cell Research"},{"key":"2026010712074114300_bib40","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1111\/j.1432-1033.1992.tb16691.x","article-title":"Molecular characterization of six intermediate proteins in the processing of mouse protamine P2 precursor","volume":"204","author":"Chauvi\u00e8re","year":"1992","journal-title":"European Journal of Biochemistry"},{"key":"2026010712074114300_bib41","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1016\/s0022-2836(0300091-3","article-title":"Recognition of nucleic acid bases and base-pairs by hydrogen bonding to amino acid side-chains","volume":"327","author":"Cheng","year":"2003","journal-title":"Journal of Molecular Biology"},{"key":"2026010712074114300_bib42","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/0167-4838(9390043-q","article-title":"Phosphorylation of human sperm protamines HP1 and HP2: identification of phosphorylation sites","volume":"1203","author":"Chira","year":"1993","journal-title":"Biochimica et Biophysica Acta"},{"key":"2026010712074114300_bib43","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1038\/ng0501-82","article-title":"Haploinsufficiency of protamine-1 or -2 causes infertility in mice","volume":"28","author":"Cho","year":"2001","journal-title":"Nature Genetics"},{"key":"2026010712074114300_bib44","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1095\/biolreprod.102.015115","article-title":"Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice","volume":"69","author":"Cho","year":"2003","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib45","doi-asserted-by":"publisher","first-page":"7637","DOI":"10.1128\/MCB.25.17.7637-7644.2005","article-title":"The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability","volume":"25","author":"Conrad","year":"2005","journal-title":"Molecular and Cellular Biology"},{"key":"2026010712074114300_bib46","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1002\/mrd.10105","article-title":"Protamine 1: protamine 2 stoichiometry in the sperm of eutherian mammals","volume":"61","author":"Corzett","year":"2002","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib47","doi-asserted-by":"publisher","first-page":"802","DOI":"10.2174\/092986611795713943","article-title":"Single molecule studies of DNA-protamine interactions","volume":"18","author":"Cree","year":"2011","journal-title":"Protein and Peptide Letters"},{"key":"2026010712074114300_bib48","doi-asserted-by":"publisher","first-page":"2170","DOI":"10.1038\/nprot.2016.130","article-title":"Remodeling somatic nuclei via exogenous expression of protamine 1 to create spermatid-like structures for somatic nuclear transfer","volume":"11","author":"Czernik","year":"2016","journal-title":"Nature Protocols"},{"key":"2026010712074114300_bib49","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/s1642-431x(1260077-1","article-title":"Impact of protamine transcripts and their proteins on the quality and fertilization ability of sperm and the development of preimplantation embryos","volume":"12","author":"Depa-Martynow","year":"2012","journal-title":"Reproductive Biology"},{"key":"2026010712074114300_bib50","doi-asserted-by":"publisher","first-page":"6387","DOI":"10.1074\/jbc.M111.288167","article-title":"Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodeling in mammalian spermiogenesis","volume":"287","author":"Dhar","year":"2012","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib51","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1038\/nsmb.2599","article-title":"Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa","volume":"20","author":"Erkek","year":"2013","journal-title":"Nature Structural and Molecular Biology"},{"key":"2026010712074114300_bib52","doi-asserted-by":"publisher","first-page":"80","DOI":"10.3109\/14647273.2014.915347","article-title":"Aberrant protamine content in sperm and consequential implications for infertility treatment","volume":"17","author":"Francis","year":"2014","journal-title":"Human Fertility"},{"key":"2026010712074114300_bib53","doi-asserted-by":"publisher","first-page":"3350","DOI":"10.1128\/MCB.18.6.3350","article-title":"Histone- and protamine-DNA association: conservation of different patterns within the \u03b2-globin domain in human sperm","volume":"18","author":"Gardiner-Garden","year":"1998","journal-title":"Molecular and Cellular Biology"},{"key":"2026010712074114300_bib54","doi-asserted-by":"publisher","first-page":"3809","DOI":"10.1038\/emboj.2012.233","article-title":"Bromodomain-dependent stage-specific male genome programming by Brdt","volume":"31","author":"Gaucher","year":"2012","journal-title":"EMBO Journal"},{"key":"2026010712074114300_bib55","doi-asserted-by":"publisher","first-page":"540","DOI":"10.2164\/jandrol.107.004390","article-title":"A common protamine 1 promoter polymorphism (\u2212190 C\u2192A) correlates With abnormal sperm morphology and increased protamine P1\/P2 ratio in infertile patients","volume":"29","author":"G\u00e1zquez","year":"2008","journal-title":"Journal of Andrology"},{"key":"2026010712074114300_bib56","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1002\/mrd.21394","article-title":"Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species","volume":"78","author":"Gos\u00e1lvez","year":"2011","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib57","doi-asserted-by":"publisher","first-page":"1212.e14","DOI":"10.1016\/j.cell.2020.02.020","article-title":"Initiation of parental genome reprogramming in fertilized oocyte by splicing kinase SRPK1-catalyzed protamine phosphorylation","volume":"180","author":"Gou","year":"2020","journal-title":"Cell"},{"key":"2026010712074114300_bib58","doi-asserted-by":"publisher","first-page":"3342","DOI":"10.1016\/j.jmb.2014.02.023","article-title":"Genome-scale acetylation-dependent histone eviction during spermatogenesis","volume":"426","author":"Goudarzi","year":"2014","journal-title":"Journal of Molecular Biology"},{"key":"2026010712074114300_bib59","doi-asserted-by":"publisher","first-page":"3459","DOI":"10.1111\/j.1432-1033.2004.04266.x","article-title":"The role of histones in chromatin remodelling during mammalian spermiogenesis","volume":"271","author":"Govin","year":"2004","journal-title":"European Journal of Biochemistry"},{"key":"2026010712074114300_bib60","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1083\/jcb.200604141","article-title":"Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis","volume":"176","author":"Govin","year":"2007","journal-title":"Journal of Cell Biology"},{"key":"2026010712074114300_bib61","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1139\/o01-075","article-title":"Phosphorylation of histone variant regions in chromatin: unlocking the linker?","volume":"79","author":"Green","year":"2001","journal-title":"Biochemistry and Cell Biology"},{"key":"2026010712074114300_bib62","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/0304-4165(8690235-7","article-title":"Purification and characterization of nuclear basic proteins of human sperm","volume":"884","author":"Gusse","year":"1986","journal-title":"Biochimica et Biophysica Acta"},{"key":"2026010712074114300_bib63","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1038\/nature08162","article-title":"Distinctive chromatin in human sperm packages genes for embryo development","volume":"460","author":"Hammoud","year":"2009","journal-title":"Nature"},{"key":"2026010712074114300_bib64","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1111\/j.1439-0272.2008.00890.x","article-title":"Protamine ratio and the level of histone retention in sperm selected from a density gradient preparation","volume":"41","author":"Hammoud","year":"2009","journal-title":"Andrologia"},{"key":"2026010712074114300_bib65","doi-asserted-by":"publisher","first-page":"1728","DOI":"10.1016\/j.fertnstert.2009.09.010","article-title":"Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility","volume":"94","author":"Hammoud","year":"2010","journal-title":"Fertility and Sterility"},{"key":"2026010712074114300_bib66","doi-asserted-by":"publisher","first-page":"2558","DOI":"10.1093\/humrep\/der192","article-title":"Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men","volume":"26","author":"Hammoud","year":"2011","journal-title":"Human Reproduction"},{"key":"2026010712074114300_bib67","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1002\/(SICI)1098-2795(200003)55:3&lt;307::AID-MRD9&gt;3.0.CO;2-P","article-title":"Genome organization in the human sperm nucleus studied by FISH and confocal microscopy","volume":"55","author":"Hazzouri","year":"2000","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib68","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1016\/j.rbmo.2012.09.005","article-title":"PRM1 variant rs35576928 (ArgSer) is associated with defective spermatogenesis in the Chinese Han population","volume":"25","author":"He","year":"2012","journal-title":"Reproductive Biomedicine Online"},{"key":"2026010712074114300_bib69","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/0014-4827(8690465-9","article-title":"Evidence for haploid expression of mouse testicular genes","volume":"164","author":"Hecht","year":"1986","journal-title":"Experimental Cell Research"},{"key":"2026010712074114300_bib70","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1007\/BF01560667","article-title":"Mapping of haploid expressed genes: genes for both mouse protamines are located on chromosome 16","volume":"12","author":"Hecht","year":"1986","journal-title":"Somatic Cell and Molecular Genetics"},{"key":"2026010712074114300_bib71","doi-asserted-by":"publisher","first-page":"13309","DOI":"10.1016\/S0021-9258(1845202-7","article-title":"Transcriptional and translational control of the message for transition protein 1, a major chromosomal protein of mammalian spermatids","volume":"262","author":"Heidaran","year":"1987","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib72","doi-asserted-by":"publisher","DOI":"10.3390\/cells9020474","article-title":"RNA-guided genomic localization of H2A.L.2 histone variant","volume":"9","author":"Hoghoughi","year":"2020","journal-title":"Cells"},{"key":"2026010712074114300_bib73","doi-asserted-by":"publisher","first-page":"1925","DOI":"10.1016\/j.bpj.2017.08.050","article-title":"Role of disulfide bonds on DNA packaging forces in bull sperm chromatin","volume":"113","author":"Hutchison","year":"2017","journal-title":"Biophysical Journal"},{"key":"2026010712074114300_bib74","doi-asserted-by":"publisher","first-page":"733","DOI":"10.1093\/molehr\/gap056","article-title":"Mutations in the protamine locus: association with spermatogenic failure?","volume":"15","author":"Imken","year":"2009","journal-title":"Molecular Human Reproduction"},{"key":"2026010712074114300_bib75","doi-asserted-by":"publisher","DOI":"10.4103\/2277-9175.124666","article-title":"The effects of protamine deficiency on ultrastructure of human sperm nucleus","volume":"3","author":"Iranpour","year":"2014","journal-title":"Advanced Biomedical Research"},{"key":"2026010712074114300_bib76","doi-asserted-by":"publisher","DOI":"10.1126\/scisignal.aao7232","article-title":"Dephosphorylation of protamine 2 at serine 56 is crucial for murine sperm maturation in vivo","volume":"12","author":"Itoh","year":"2019","journal-title":"Science Signaling"},{"key":"2026010712074114300_bib77","doi-asserted-by":"publisher","first-page":"1765","DOI":"10.1016\/j.celrep.2015.10.066","article-title":"Exogenous expression of human protamine 1 (hPrm1) remodels fibroblast nuclei into spermatid-like structures","volume":"13","author":"Iuso","year":"2015","journal-title":"Cell Reports"},{"key":"2026010712074114300_bib78","doi-asserted-by":"publisher","first-page":"1074","DOI":"10.1126\/science.1063127","article-title":"Translating the histone code","volume":"293","author":"Jenuwein","year":"2001","journal-title":"Science"},{"key":"2026010712074114300_bib79","doi-asserted-by":"publisher","DOI":"10.1038\/srep15300","article-title":"Polymorphisms in protamine 1 and protamine 2 predict the risk of male infertility: a meta-analysis","volume":"5","author":"Jiang","year":"2015","journal-title":"Scientific Reports"},{"key":"2026010712074114300_bib80","doi-asserted-by":"publisher","DOI":"10.1111\/and.12990","article-title":"Systematic review and meta-analysis of the genetic association between protamine polymorphism and male infertility","volume":"50","author":"Jiang","year":"2018","journal-title":"Andrologia"},{"key":"2026010712074114300_bib81","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1111\/j.1365-2605.2010.01115.x","article-title":"Polymorphisms, haplotypes and mutations in the protamine 1 and 2 genes","volume":"34","author":"Jodar","year":"2011","journal-title":"International Journal of Andrology"},{"key":"2026010712074114300_bib82","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1016\/j.celrep.2017.01.034","article-title":"Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes","volume":"18","author":"Jung","year":"2017","journal-title":"Cell Reports"},{"key":"2026010712074114300_bib83","doi-asserted-by":"publisher","first-page":"755","DOI":"10.2174\/092986611795713989","article-title":"Protamines: structural complexity, evolution and chromatin patterning","volume":"18","author":"Kasinsky","year":"2011","journal-title":"Protein and Peptide Letters"},{"key":"2026010712074114300_bib84","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1007\/BF02765830","article-title":"Human protamines and male infertility","volume":"14","author":"Khara","year":"1997","journal-title":"Journal of Assisted Reproduction and Genetics"},{"key":"2026010712074114300_bib85","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1083\/jcb.65.2.258","article-title":"Structural and transcriptional features of the mouse spermatid genome","volume":"65","author":"Kierszenbaum","year":"1975","journal-title":"Journal of Cell Biology"},{"key":"2026010712074114300_bib86","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/0012-1606(8790455-6","article-title":"Molecular cloning and differential expression of somatic and testis-specific H2B histone genes during rat spermatogenesis","volume":"124","author":"Kim","year":"1987","journal-title":"Developmental Biology"},{"key":"2026010712074114300_bib87","doi-asserted-by":"publisher","first-page":"1847","DOI":"10.1016\/S0021-9258(1941772-9","article-title":"The amino acid sequence of a testis-specific basic protein that is associated with spermatogenesis","volume":"250","author":"Kistler","year":"1975","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib88","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.115.137620","article-title":"Murine and human spermatids are characterized by numerous, newly synthesized and differentially expressed transcription factors and bromodomain-containing proteins","volume":"95","author":"Klaus","year":"2016","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib89","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1242\/dev.106.2.367","article-title":"Poly(A) shortening accompanies the activation of translation of five mRNAs during spermiogenesis in the mouse","volume":"106","author":"Kleene","year":"1989","journal-title":"Development"},{"key":"2026010712074114300_bib90","doi-asserted-by":"publisher","first-page":"17272","DOI":"10.1016\/S0021-9258(1845373-2","article-title":"Characterization of a cDNA clone encoding a basic protein, TP2, involved in chromatin condensation during spermiogenesis in the mouse","volume":"262","author":"Kleene","year":"1987","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib91","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/0012-1606(8490262-8","article-title":"Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse","volume":"105","author":"Kleene","year":"1984","journal-title":"Developmental Biology"},{"key":"2026010712074114300_bib92","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1080\/014850190518134","article-title":"Chromatin remodeling in spermatids: a sensitive step for the genetic integrity of the male gamete","volume":"51","author":"Laberge","year":"2005","journal-title":"Archives of Andrology"},{"key":"2026010712074114300_bib93","doi-asserted-by":"publisher","first-page":"12451","DOI":"10.1073\/pnas.92.26.12451","article-title":"Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice","volume":"92","author":"Lee","year":"1995","journal-title":"PNAS"},{"key":"2026010712074114300_bib94","doi-asserted-by":"publisher","first-page":"3619","DOI":"10.1242\/dev.113027","article-title":"Poised chromatin in the mammalian germ line","volume":"141","author":"Lesch","year":"2014","journal-title":"Development"},{"key":"2026010712074114300_bib95","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1006\/bbrc.1998.9687","article-title":"Architectural DNA-binding properties of the spermatidal transition proteins 1 and 2","volume":"252","author":"L\u00e9vesque","year":"1998","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2026010712074114300_bib96","doi-asserted-by":"publisher","first-page":"4148","DOI":"10.1073\/pnas.0308721101","article-title":"Histone H1 and the origin of protamines","volume":"101","author":"Lewis","year":"2004","journal-title":"PNAS"},{"key":"2026010712074114300_bib97","doi-asserted-by":"publisher","first-page":"7962","DOI":"10.1016\/S0021-9258(2081796-7","article-title":"Kinetics of enzymatic modification of the protamines and a proposal for their binding to chromatin","volume":"247","author":"Louie","year":"1972","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712074114300_bib98","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0029247","article-title":"Sexual selection halts the relaxation of protamine 2 among rodents","volume":"6","author":"L\u00fcke","year":"2011","journal-title":"PLoS ONE"},{"key":"2026010712074114300_bib99","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1095\/biolreprod.113.115956","article-title":"Evolution of protamine genes and changes in sperm head phenotype in rodents","volume":"90","author":"L\u00fcke","year":"2014","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib100","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2013.3359","article-title":"Sexual selection on protamine and transition nuclear protein expression in mouse species","volume":"281","author":"L\u00fcke","year":"2014","journal-title":"Proceedings of the Royal Society of London: Series B"},{"key":"2026010712074114300_bib101","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-016-0588-1","article-title":"Selective constraints on protamine 2 in primates and rodents","volume":"16","author":"L\u00fcke","year":"2016","journal-title":"BMC Evolutionary Biology"},{"key":"2026010712074114300_bib102","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1093\/molbev\/msv209","article-title":"Sexual selection of protamine 1 in mammals","volume":"33","author":"L\u00fcke","year":"2016","journal-title":"Molecular Biology and Evolution"},{"key":"2026010712074114300_bib103","doi-asserted-by":"publisher","first-page":"910","DOI":"10.1095\/biolreprod.103.022541","article-title":"Transient DNA strand breaks during mouse and human spermiogenesis: new insights in stage specificity and link to chromatin remodeling","volume":"70","author":"Marcon","year":"2004","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib104","doi-asserted-by":"publisher","DOI":"10.1038\/srep03355","article-title":"Generation of mutant mice by pronuclear injection of circular plasmid expressing Cas9 and single guided RNA","volume":"3","author":"Mashiko","year":"2013","journal-title":"Scientific Reports"},{"key":"2026010712074114300_bib105","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1006\/dbio.1993.1173","article-title":"Nicking of rat spermatid and spermatozoa DNA: possible involvement of DNA topoisomerase II","volume":"158","author":"McPherson","year":"1993","journal-title":"Developmental Biology"},{"key":"2026010712074114300_bib106","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1002\/mrd.1080310303","article-title":"Highly acetylated H4 is associated with histone displacement in rat spermatids","volume":"31","author":"Meistrich","year":"1992","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712074114300_bib107","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1007\/s00412-002-0227-z","article-title":"Roles of transition nuclear proteins in spermiogenesis","volume":"111","author":"Meistrich","year":"2003","journal-title":"Chromosoma"},{"key":"2026010712074114300_bib108","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1002\/j.1939-4640.2003.tb02692.x","article-title":"Marked differences in protamine content and P1\/P2 ratios in sperm cells from Percoll fractions between patients and controls","volume":"24","author":"Mengual","year":"2003","journal-title":"Journal of Andrology"},{"key":"2026010712074114300_bib109","doi-asserted-by":"publisher","first-page":"dev200330","DOI":"10.1242\/dev.200330","article-title":"Loss of Prm1 leads to defective chromatin protamination, impaired PRM2 processing, reduced sperm motility and subfertility in male mice","volume":"149","author":"Merges","year":"2022","journal-title":"Development"},{"key":"2026010712074114300_bib110","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1007\/BF01302341","article-title":"Das protamin \u2013 eine neue organische Basis aus den Samenf\u00e4den des Rheinlachses","volume":"13","author":"Miescher","year":"1874","journal-title":"Zeitschrift f\u00fcr Analytische Chemie"},{"key":"2026010712074114300_bib111","doi-asserted-by":"publisher","first-page":"1680","DOI":"10.1101\/gad.220095.113","article-title":"Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B","volume":"27","author":"Montellier","year":"2013","journal-title":"Genes and Development"},{"key":"2026010712074114300_bib112","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1515\/BC.2003.070","article-title":"Testis-specific expression of the nuclear form of phospholipid hydroperoxide glutathione peroxidase (PHGPx)","volume":"384","author":"Moreno","year":"2003","journal-title":"Biological Chemistry"},{"key":"2026010712074114300_bib113","doi-asserted-by":"publisher","DOI":"10.1101\/2021.09.16.460631","article-title":"Single residue substitution in protamine 1 disrupts sperm genome packaging and embryonic development in mice","author":"Moritz","year":"2021","journal-title":"bioRxiv"},{"key":"2026010712074114300_bib114","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1016\/s1472-6483(1061776-2","article-title":"Effect of protamine-2 deficiency on ICSI outcome","volume":"9","author":"Nasr-Esfahani","year":"2004","journal-title":"Reproductive Biomedicine Online"},{"key":"2026010712074114300_bib115","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1111\/andr.12216","article-title":"The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis","volume":"4","author":"Ni","year":"2016","journal-title":"Andrology"},{"key":"2026010712074114300_bib116","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1093\/humupd\/dml009","article-title":"Protamines and male infertility","volume":"12","author":"Oliva","year":"2006","journal-title":"Human Reproduction Update"},{"key":"2026010712074114300_bib117","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/s0079-6603(0860839-9","article-title":"Vertebrate protamine genes and the histone-to-protamine replacement reaction","volume":"40","author":"Oliva","year":"1991","journal-title":"Progress in Nucleic Acid Research and Molecular Biology"},{"key":"2026010712074114300_bib118","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/s0092-8674(0081073-9","article-title":"Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4","volume":"85","author":"Olson","year":"1996","journal-title":"Cell"},{"key":"2026010712074114300_bib119","doi-asserted-by":"publisher","first-page":"2972","DOI":"10.1093\/nar\/27.14.2972","article-title":"SR protein-specific kinase 1 is highly expressed in testis and phosphorylates protamine 1","volume":"27","author":"Papoutsopoulou","year":"1999","journal-title":"Nucleic Acids Research"},{"key":"2026010712074114300_bib120","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1095\/biolreprod39.1.157","article-title":"Interspecies differences in the stability of mammalian sperm nuclei assessed in vivo by sperm microinjection and in vitro by flow cytometry","volume":"39","author":"Perreault","year":"1988","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib121","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.1096\/fj.00-0655fje","article-title":"Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation","volume":"15","author":"Pfeifer","year":"2001","journal-title":"FASEB Journal"},{"key":"2026010712074114300_bib122","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1095\/biolreprod50.5.981","article-title":"Identification of phosphoseryl residues in protamines from mature mammalian spermatozoa","volume":"50","author":"Pirhonen","year":"1994","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib123","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1111\/j.1432-1033.1994.tb18979.x","article-title":"P2 protamines are phosphorylated in vitro by protein kinase C, whereas P1 protamines prefer cAMP-dependent protein kinase. A comparative study of five mammalian species","volume":"223","author":"Pirhonen","year":"1994","journal-title":"European Journal of Biochemistry"},{"key":"2026010712074114300_bib124","doi-asserted-by":"publisher","first-page":"3537","DOI":"10.1242\/jcs.112.20.3537","article-title":"A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA","volume":"112","author":"Pittoggi","year":"1999","journal-title":"Journal of Cell Science"},{"key":"2026010712074114300_bib125","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1038\/s41580-021-00341-1","article-title":"The roles of Polycomb repressive complexes in mammalian development and cancer","volume":"22","author":"Piunti","year":"2021","journal-title":"Nature Reviews: Molecular Cell Biology"},{"key":"2026010712074114300_bib126","doi-asserted-by":"publisher","first-page":"5354","DOI":"10.1128\/MCB.23.15.5354-5365.2003","article-title":"Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein","volume":"23","author":"Pivot-Pajot","year":"2003","journal-title":"Molecular and Cellular Biology"},{"key":"2026010712074114300_bib127","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/0014-4827(8190044-6","article-title":"DNA and protein content of mouse sperm Implications regarding sperm chromatin structure","volume":"136","author":"Pogany","year":"1981","journal-title":"Experimental Cell Research"},{"key":"2026010712074114300_bib128","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1002\/mrd.1120180208","article-title":"Phosphorylation state of protamines 1 and 2 in human spermatids and spermatozoa","volume":"18","author":"Pruslin","year":"1987","journal-title":"Gamete Research"},{"key":"2026010712074114300_bib129","doi-asserted-by":"publisher","DOI":"10.4161\/spmg.28460","article-title":"The nuclear form of glutathione peroxidase 4 colocalizes and directly interacts with protamines in the nuclear matrix during mouse sperm chromatin assembly","volume":"4","author":"Puglisi","year":"2014","journal-title":"Spermatogenesis"},{"key":"2026010712074114300_bib130","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.bbagrm.2013.08.004","article-title":"Chromatin dynamics during spermiogenesis","volume":"1839","author":"Rathke","year":"2014","journal-title":"Biochimica et Biophysica Acta"},{"key":"2026010712074114300_bib131","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1093\/molehr\/gam031","article-title":"Mutations in the protamine 1 gene associated with male infertility","volume":"13","author":"Ravel","year":"2007","journal-title":"Molecular Human Reproduction"},{"key":"2026010712074114300_bib132","doi-asserted-by":"publisher","DOI":"10.1093\/molehr\/gaac004","article-title":"Direct visualization of pre-protamine 2 detects protamine assembly failures and predicts ICSI success","volume":"28","author":"Rezaei-Gazik","year":"2022","journal-title":"Molecular Human Reproduction"},{"key":"2026010712074114300_bib133","doi-asserted-by":"publisher","first-page":"969","DOI":"10.1093\/humrep\/des471","article-title":"The sperm protamine mRNA ratio as a clinical parameter to estimate the fertilizing potential of men taking part in an ART programme","volume":"28","author":"Rogenhofer","year":"2013","journal-title":"Human Reproduction"},{"key":"2026010712074114300_bib134","doi-asserted-by":"publisher","first-page":"278","DOI":"10.1093\/oxfordjournals.molbev.a026307","article-title":"An unusual form of purifying selection in a sperm protein","volume":"17","author":"Rooney","year":"2000","journal-title":"Molecular Biology and Evolution"},{"key":"2026010712074114300_bib135","doi-asserted-by":"publisher","first-page":"2541","DOI":"10.1098\/rspb.2010.0333","article-title":"Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate","volume":"277","author":"Ruiz-L\u00f3pez","year":"2010","journal-title":"Proceedings: Biological Sciences"},{"key":"2026010712074114300_bib136","first-page":"1","article-title":"Uniformity of nucleosome preservation pattern in mammalian sperm and its connection to repetitive DNA elements","volume":"1","author":"Samans","year":"2014","journal-title":"Developmental Cell"},{"key":"2026010712074114300_bib137","doi-asserted-by":"publisher","DOI":"10.1038\/srep36764","article-title":"Re-visiting the protamine-2 locus: deletion, but not haploinsufficiency, renders male mice infertile","volume":"6","author":"Schneider","year":"2016","journal-title":"Scientific Reports"},{"key":"2026010712074114300_bib138","doi-asserted-by":"publisher","DOI":"10.3390\/cells9081789","article-title":"Protamine-2 deficiency initiates a reactive oxygen species (ROS)-mediated destruction cascade during epididymal sperm maturation in mice","volume":"9","author":"Schneider","year":"2020","journal-title":"Cells"},{"key":"2026010712074114300_bib139","doi-asserted-by":"publisher","first-page":"4955","DOI":"10.1073\/pnas.71.12.4955","article-title":"Unscheduled DNA synthesis in the germ cells of male mice exposed in vivo to the chemical mutagen ethyl methanesulfonate","volume":"71","author":"Sega","year":"1974","journal-title":"PNAS"},{"key":"2026010712074114300_bib140","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1095\/biolreprod.104.028035","article-title":"Tyrosine phosphorylation, thiol status, and protein tyrosine phosphatase in rat epididymal spermatozoa","volume":"71","author":"Seligman","year":"2004","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib141","doi-asserted-by":"publisher","first-page":"3507","DOI":"10.1242\/dev.004481","article-title":"The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation","volume":"134","author":"Shang","year":"2007","journal-title":"Development"},{"key":"2026010712074114300_bib142","doi-asserted-by":"publisher","first-page":"1287","DOI":"10.1242\/dev.121830","article-title":"Disruption of Th2a and Th2b genes causes defects in spermatogenesis","volume":"142","author":"Shinagawa","year":"2015","journal-title":"Development"},{"key":"2026010712074114300_bib143","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1262\/jrd.2014-018","article-title":"Histone H4 modification during mouse spermatogenesis","volume":"60","author":"Shirakata","year":"2014","journal-title":"Journal of Reproduction and Development"},{"key":"2026010712074114300_bib144","doi-asserted-by":"publisher","first-page":"2714","DOI":"10.1073\/pnas.72.7.2714","article-title":"New histones found in mature mammalian testes","volume":"72","author":"Shires","year":"1975","journal-title":"PNAS"},{"key":"2026010712074114300_bib145","doi-asserted-by":"publisher","first-page":"1220","DOI":"10.1095\/biolreprod.104.029363","article-title":"Abnormalities and reduced reproductive potential of sperm from Tnp1- and Tnp2-null double mutant mice","volume":"71","author":"Shirley","year":"2004","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib146","first-page":"701","article-title":"Interaction of rat testis protein, TP, with nucleosome core particle","volume":"17","author":"Singh","year":"1988","journal-title":"Biochemistry International"},{"key":"2026010712074114300_bib147","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1021\/acs.jproteome.9b00499","article-title":"Characterization of human sperm protamine proteoforms through a combination of top-down and bottom-up mass spectrometry approaches","volume":"19","author":"Soler-Ventura","year":"2020","journal-title":"Journal of Proteome Research"},{"key":"2026010712074114300_bib148","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1007\/s004290050245","article-title":"Transcriptional and translational regulation of gene expression in haploid spermatids","volume":"199","author":"Steger","year":"1999","journal-title":"Anatomy and Embryology"},{"key":"2026010712074114300_bib149","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1111\/ahe.12361","article-title":"Sperm nuclear protamines: a checkpoint to control sperm chromatin quality","volume":"47","author":"Steger","year":"2018","journal-title":"Anatomia, Histologia, Embryologia"},{"key":"2026010712074114300_bib150","doi-asserted-by":"publisher","first-page":"709","DOI":"10.1093\/humrep\/16.4.709","article-title":"Round spermatids from infertile men exhibit decreased protamine-1 and -2 mRNA","volume":"16","author":"Steger","year":"2001","journal-title":"Human Reproduction"},{"key":"2026010712074114300_bib151","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1093\/molehr\/gag041","article-title":"Decreased protamine-1 transcript levels in testes from infertile men","volume":"9","author":"Steger","year":"2003","journal-title":"Molecular Human Reproduction"},{"key":"2026010712074114300_bib152","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1093\/humrep\/dem363","article-title":"Both protamine-1 to protamine-2 mRNA ratio and Bcl2 mRNA content in testicular spermatids and ejaculated spermatozoa discriminate between fertile and infertile men","volume":"23","author":"Steger","year":"2008","journal-title":"Human Reproduction"},{"key":"2026010712074114300_bib153","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1038\/nrg733","article-title":"The rapid evolution of reproductive proteins","volume":"3","author":"Swanson","year":"2002","journal-title":"Nature Reviews: Genetics"},{"key":"2026010712074114300_bib154","doi-asserted-by":"publisher","DOI":"10.1038\/srep27409","article-title":"Viable offspring obtained from Prm1-deficient sperm in mice","volume":"6","author":"Takeda","year":"2016","journal-title":"Scientific Reports"},{"key":"2026010712074114300_bib155","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1095\/biolreprod.103.015867","article-title":"Novel actin-like proteins T-actin 1 and T-actin 2 are differentially expressed in the cytoplasm and nucleus of mouse haploid germ cells","volume":"69","author":"Tanaka","year":"2003","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib156","doi-asserted-by":"publisher","first-page":"2084","DOI":"10.1093\/humrep\/del114","article-title":"Protamine 2 precursors, protamine 1\/protamine 2 ratio, DNA integrity and other sperm parameters in infertile patients","volume":"21","author":"Torregrosa","year":"2006","journal-title":"Human Reproduction"},{"key":"2026010712074114300_bib157","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1093\/humupd\/dmn004","article-title":"Oxidative stress and male infertility \u2013 a clinical perspective","volume":"14","author":"Tremellen","year":"2008","journal-title":"Human Reproduction Update"},{"key":"2026010712074114300_bib158","doi-asserted-by":"publisher","first-page":"2075","DOI":"10.1534\/genetics.107.085902","article-title":"Comparative analysis of testis protein evolution in rodents","volume":"179","author":"Turner","year":"2008","journal-title":"Genetics"},{"key":"2026010712074114300_bib159","doi-asserted-by":"publisher","first-page":"e240","DOI":"10.1111\/j.1365-2605.2009.01003.x","article-title":"A common haplotype of protamine 1 and 2 genes is associated with higher sperm counts","volume":"33","author":"T\u00fcttelmann","year":"2010","journal-title":"International Journal of Andrology"},{"key":"2026010712074114300_bib160","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1095\/biolreprod44.4.569","article-title":"DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells","volume":"44","author":"Ward","year":"1991","journal-title":"Biology of Reproduction"},{"key":"2026010712074114300_bib161","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1038\/78153","article-title":"Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4","volume":"25","author":"Wu","year":"2000","journal-title":"Nature Genetics"},{"key":"2026010712074114300_bib162","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1038\/35002070","article-title":"Rapid evolution of male reproductive genes in the descent of man","volume":"403","author":"Wyckoff","year":"2000","journal-title":"Nature"},{"key":"2026010712074114300_bib163","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1021\/acsnano.7b06398","article-title":"Sperm-hybrid micromotor for targeted drug delivery","volume":"12","author":"Xu","year":"2018","journal-title":"ACS Nano"},{"key":"2026010712074114300_bib164","doi-asserted-by":"publisher","first-page":"3920","DOI":"10.1016\/j.celrep.2018.05.094","article-title":"Re-evaluating the localization of sperm-retained histones revealed the modification-dependent accumulation in specific genome regions","volume":"23","author":"Yamaguchi","year":"2018","journal-title":"Cell Reports"},{"key":"2026010712074114300_bib165","doi-asserted-by":"publisher","first-page":"10546","DOI":"10.1073\/pnas.1837812100","article-title":"HILS1 is a spermatid-specific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis","volume":"100","author":"Yan","year":"2003","journal-title":"PNAS"},{"key":"2026010712074114300_bib166","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1006\/abio.1993.1104","article-title":"Rapid analysis of mammalian sperm nuclear proteins","volume":"209","author":"Yebra","year":"1993","journal-title":"Analytical Biochemistry"},{"key":"2026010712074114300_bib167","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/s0015-0282(9800012-0","article-title":"Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels","volume":"69","author":"Yebra de","year":"1998","journal-title":"Fertility and Sterility"},{"key":"2026010712074114300_bib168","doi-asserted-by":"publisher","first-page":"2173","DOI":"10.1128\/mcb.7.6.2173-2179.1987","article-title":"Mouse protamine 2 is synthesized as a precursor whereas mouse protamine 1 is not","volume":"7","author":"Yelick","year":"1987","journal-title":"Molecular and Cellular Biology"},{"key":"2026010712074114300_bib169","doi-asserted-by":"publisher","first-page":"4683","DOI":"10.1073\/pnas.97.9.4683","article-title":"Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice","volume":"97","author":"Yu","year":"2000","journal-title":"PNAS"},{"key":"2026010712074114300_bib170","first-page":"314","article-title":"Association of PRM1-190C- &gt; a polymorphism with teratozoospermia","volume":"18","author":"Yu","year":"2012","journal-title":"Zhonghua Nan Ke Xue"},{"key":"2026010712074114300_bib171","doi-asserted-by":"publisher","first-page":"7243","DOI":"10.1128\/MCB.21.21.7243-7255.2001","article-title":"Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice","volume":"21","author":"Zhao","year":"2001","journal-title":"Molecular and Cellular Biology"},{"key":"2026010712074114300_bib172","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1002\/gene.20019","article-title":"Transition nuclear proteins are required for normal chromatin condensation and functional sperm development","volume":"38","author":"Zhao","year":"2004","journal-title":"Genesis"}],"container-title":["Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rep.bioscientifica.com\/view\/journals\/rep\/164\/3\/REP-22-0107.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/rep.bioscientifica.com\/downloadpdf\/journals\/rep\/164\/3\/REP-22-0107.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/reproduction\/article-pdf\/164\/3\/R57\/64064385\/rep-22-0107.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/reproduction\/article-pdf\/164\/3\/R57\/64064385\/rep-22-0107.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,7]],"date-time":"2026-01-07T17:07:52Z","timestamp":1767805672000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/reproduction\/article\/164\/3\/R57\/8217052"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,26]]},"references-count":172,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2022,9,1]]}},"URL":"https:\/\/doi.org\/10.1530\/rep-22-0107","relation":{},"ISSN":["1470-1626","1741-7899"],"issn-type":[{"value":"1470-1626","type":"print"},{"value":"1741-7899","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,9,1]]},"published":{"date-parts":[[2022,7,26]]}}}