{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T12:51:23Z","timestamp":1790167883544,"version":"4.1.0"},"reference-count":30,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T00:00:00Z","timestamp":1682553600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-17-CE12-0004-01"],"award-info":[{"award-number":["ANR-17-CE12-0004-01"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["SPF201909009274"],"award-info":[{"award-number":["SPF201909009274"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002915","name":"Fondation pour la Recherche M\u00e9dicale","doi-asserted-by":"publisher","award":["ANR-17-CE12-0004-01"],"award-info":[{"award-number":["ANR-17-CE12-0004-01"]}],"id":[{"id":"10.13039\/501100002915","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002915","name":"Fondation pour la Recherche M\u00e9dicale","doi-asserted-by":"publisher","award":["SPF201909009274"],"award-info":[{"award-number":["SPF201909009274"]}],"id":[{"id":"10.13039\/501100002915","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Spermiogenesis is the step during which post-meiotic cells, called spermatids, undergo numerous morphological changes and differentiate into spermatozoa. Thousands of genes have been described to be expressed at this stage and could contribute to spermatid differentiation. Genetically-engineered mouse models using Cre\/LoxP or CrispR\/Cas9 are the favored approaches to characterize gene function and better understand the genetic basis of male infertility. In the present study, we produced a new spermatid-specific Cre transgenic mouse line, in which the improved iCre recombinase is expressed under the control of the acrosomal vesicle protein 1 gene promoter (Acrv1-iCre). We show that Cre protein expression is restricted to the testis and only detected in round spermatids of stage V to VIII seminiferous tubules. The Acrv1-iCre line can conditionally knockout a gene during spermiogenesis with a &gt; 95% efficiency. Therefore, it could be useful to unravel the function of genes during the late stage of spermatogenesis, but it can also be used to produce an embryo with a paternally deleted allele without causing early spermatogenesis defects.<\/jats:p>","DOI":"10.3390\/genes14050983","type":"journal-article","created":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T02:50:00Z","timestamp":1682563800000},"page":"983","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Generation and Characterization of a Transgenic Mouse That Specifically Expresses the Cre Recombinase in Spermatids"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5242-7426","authenticated-orcid":false,"given":"Clara","family":"Gob\u00e9","sequence":"first","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, INSERM, CNRS, Institut Cochin, F-75014 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C\u00f4me","family":"Ialy-Radio","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, INSERM, CNRS, Institut Cochin, F-75014 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R\u00e9mi","family":"Pierre","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, INSERM, CNRS, Institut Cochin, F-75014 Paris, France"},{"name":"Homologous Recombination, Embryo Transfer and Cryopreservation Facility, Cochin Institute, University of Paris, F-75006 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6275-5412","authenticated-orcid":false,"given":"Julie","family":"Cocquet","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, INSERM, CNRS, Institut Cochin, F-75014 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/humupd\/dmab030","article-title":"A systematic review of the validated monogenic causes of human male infertility: 2020 update and a discussion of emerging gene-disease relationships","volume":"28","author":"Houston","year":"2022","journal-title":"Hum. Reprod. Update"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/978-1-60761-103-5_16","article-title":"Staging of mouse seminiferous tubule cross-sections","volume":"558","author":"Ahmed","year":"2009","journal-title":"Methods Mol. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1095\/biolreprod.113.111682","article-title":"Novel stage classification of human spermatogenesis based on acrosome development","volume":"89","author":"Muciaccia","year":"2013","journal-title":"Biol. Reprod."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"da Cruz, I., Rodriguez-Casuriaga, R., Santinaque, F.F., Farias, J., Curti, G., Capoano, C.A., Folle, G.A., Benavente, R., Sotelo-Silveira, J.R., and Geisinger, A. (2016). Transcriptome analysis of highly purified mouse spermatogenic cell populations: Gene expression signatures switch from meiotic-to postmeiotic-related processes at pachytene stage. BMC Genom., 17.","DOI":"10.1186\/s12864-016-2618-1"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1038\/s41594-020-0488-3","article-title":"Super-enhancer switching drives a burst in gene expression at the mitosis-to-meiosis transition","volume":"27","author":"Maezawa","year":"2020","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.ando.2014.04.006","article-title":"Disrupting the male germ line to find infertility and contraception targets","volume":"75","author":"Archambeault","year":"2014","journal-title":"Ann. Endocrinol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1126\/science.8016642","article-title":"Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting","volume":"265","author":"Gu","year":"1994","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1530\/REP-10-0404","article-title":"Good planning and serendipity: Exploiting the Cre\/Lox system in the testis","volume":"141","author":"Smith","year":"2011","journal-title":"Reproduction"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1002\/gene.20147","article-title":"A Cre gene directed by a human TSPY promoter is specific for germ cells and neurons","volume":"42","author":"Kido","year":"2005","journal-title":"Genesis"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"13702","DOI":"10.1073\/pnas.240471297","article-title":"Illegitimate Cre-dependent chromosome rearrangements in transgenic mouse spermatids","volume":"97","author":"Schmidt","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1002\/gene.10023","article-title":"Codon-improved Cre recombinase (iCre) expression in the mouse","volume":"32","author":"Shimshek","year":"2002","journal-title":"Genesis"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/S0012-1606(03)00349-X","article-title":"Spermatid-specific promoter of the SP-10 gene functions as an insulator in somatic cells","volume":"262","author":"Reddi","year":"2003","journal-title":"Dev. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1095\/biolreprod61.5.1256","article-title":"Round spermatid-specific transcription of the mouse SP-10 gene is mediated by a 294-base pair proximal promoter","volume":"61","author":"Reddi","year":"1999","journal-title":"Biol. Reprod."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1538\/expanim.55.137","article-title":"High-efficiency CAG-FLPe deleter mice in C57BL\/6J background","volume":"55","author":"Kanki","year":"2006","journal-title":"Exp. Anim."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Blanco, M., El Khattabi, L., Gob\u00e9, C., Crespo, M., Coul\u00e9e, M., De la Iglesia, A., Ialy-Radio, C., Lapoujade, C., Givelet, M., and Delessard, M. (Embo Reports bioRxiv, 2023). The histone methyltransferase DOT1L regulates chromatin reorganization and gene expression during the postmeiotic differentiation of male germ cells, Embo Reports bioRxiv, in press.","DOI":"10.15252\/embr.202256316"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1002\/dvg.20335","article-title":"A global double-fluorescent Cre reporter mouse","volume":"45","author":"Muzumdar","year":"2007","journal-title":"Genesis"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4759","DOI":"10.1182\/blood-2010-12-327668","article-title":"Requirement for Dot1l in murine postnatal hematopoiesis and leukemogenesis by MLL translocation","volume":"117","author":"Jo","year":"2011","journal-title":"Blood"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1571","DOI":"10.1111\/febs.12724","article-title":"SSTY proteins co-localize with the post-meiotic sex chromatin and interact with regulators of its expression","volume":"281","author":"Comptour","year":"2014","journal-title":"FEBS J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1016\/j.freeradbiomed.2015.10.419","article-title":"Oxidative DNA damage in mouse sperm chromosomes: Size matters","volume":"89","author":"Kocer","year":"2015","journal-title":"Free. Radic. Biol. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1995","DOI":"10.1038\/ncomms2995","article-title":"Dynamics of 5-hydroxymethylcytosine during mouse spermatogenesis","volume":"4","author":"Gan","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1038\/cdd.2017.32","article-title":"SLY regulates genes involved in chromatin remodeling and interacts with TBL1XR1 during sperm differentiation","volume":"24","author":"Moretti","year":"2017","journal-title":"Cell Death Differ."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Makela, J.A., Cisneros-Montalvo, S., Lehtiniemi, T., Olotu, O., La, H.M., Toppari, J., Hobbs, R.M., Parvinen, M., and Kotaja, N. (2020). Transillumination-Assisted Dissection of Specific Stages of the Mouse Seminiferous Epithelial Cycle for Downstream Immunostaining Analyses. J. Vis. Exp., e61800.","DOI":"10.3791\/61800"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1002\/dvg.20437","article-title":"Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice","volume":"46","author":"Payne","year":"2008","journal-title":"Genesis"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1002\/dvg.20310","article-title":"Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre","volume":"45","author":"Gallardo","year":"2007","journal-title":"Genesis"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.ydbio.2004.03.013","article-title":"Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types","volume":"270","author":"Schonhoff","year":"2004","journal-title":"Dev. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1002\/dvg.22389","article-title":"Incomplete cre-mediated excision leads to phenotypic differences between Stra8-iCre; Mov10l1(lox\/lox) and Stra8-iCre; Mov10l1(lox\/Delta) mice","volume":"51","author":"Bao","year":"2013","journal-title":"Genesis"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.devcel.2018.10.004","article-title":"SETDB1 Links the Meiotic DNA Damage Response to Sex Chromosome Silencing in Mice","volume":"47","author":"Hirota","year":"2018","journal-title":"Dev. Cell"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"467","DOI":"10.15252\/embr.201439379","article-title":"Distinct germline progenitor subsets defined through Tsc2-mTORC1 signaling","volume":"16","author":"Hobbs","year":"2015","journal-title":"EMBO Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1002\/dvg.20672","article-title":"Brain expression of Cre recombinase driven by pancreas-specific promoters","volume":"48","author":"Song","year":"2010","journal-title":"Genesis"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"14602","DOI":"10.1073\/pnas.94.26.14602","article-title":"Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells","volume":"94","author":"Dagenais","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/5\/983\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:24:11Z","timestamp":1760124251000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/14\/5\/983"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,27]]},"references-count":30,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["genes14050983"],"URL":"https:\/\/doi.org\/10.3390\/genes14050983","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,27]]}}}