{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T18:11:11Z","timestamp":1790532671606,"version":"4.1.0"},"reference-count":149,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,4,27]],"date-time":"2021-04-27T00:00:00Z","timestamp":1619481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of University and Research","award":["Grant PRIN to R. Pierantoni 2017"],"award-info":[{"award-number":["Grant PRIN to R. Pierantoni 2017"]}]},{"name":"Universit\u00e0 degli Studi della Campania Luigi Vanvitelli","award":["Grant VALERE, Vanvitelli per la Ricerca 2019 to G. Cobellis"],"award-info":[{"award-number":["Grant VALERE, Vanvitelli per la Ricerca 2019 to G. Cobellis"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Nuclear architecture undergoes an extensive remodeling during spermatogenesis, especially at levels of spermatocytes (SPC) and spermatids (SPT). Interestingly, typical events of spermiogenesis, such as nuclear elongation, acrosome biogenesis, and flagellum formation, need a functional cooperation between proteins of the nuclear envelope and acroplaxome\/manchette structures. In addition, nuclear envelope plays a key role in chromosome distribution. In this scenario, special attention has been focused on the LINC (linker of nucleoskeleton and cytoskeleton) complex, a nuclear envelope-bridge structure involved in the connection of the nucleoskeleton to the cytoskeleton, governing mechanotransduction. It includes two integral proteins: KASH- and SUN-domain proteins, on the outer (ONM) and inner (INM) nuclear membrane, respectively. The LINC complex is involved in several functions fundamental to the correct development of sperm cells such as head formation and head to tail connection, and, therefore, it seems to be important in determining male fertility. This review provides a global overview of the main LINC complex components, with a special attention to their subcellular localization in sperm cells, their roles in the regulation of sperm morphological maturation, and, lastly, LINC complex alterations associated to male infertility.<\/jats:p>","DOI":"10.3390\/genes12050658","type":"journal-article","created":{"date-parts":[[2021,4,27]],"date-time":"2021-04-27T21:18:20Z","timestamp":1619558300000},"page":"658","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["LINCking the Nuclear Envelope to Sperm Architecture"],"prefix":"10.3390","volume":"12","author":[{"given":"Francesco","family":"Manfrevola","sequence":"first","affiliation":[{"name":"Dipartimento di Medicina Sperimentale, Universit\u00e0 degli Studi della Campania L. Vanvitelli, Via Costantinopoli 16, 80138 Napoli, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7325-5317","authenticated-orcid":false,"given":"Florian","family":"Guillou","sequence":"additional","affiliation":[{"name":"PRC, CNRS, IFCE, INRAE, University of Tours, 37380 Nouzilly, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"Fasano","sequence":"additional","affiliation":[{"name":"Dipartimento di Medicina Sperimentale, Universit\u00e0 degli Studi della Campania L. Vanvitelli, Via Costantinopoli 16, 80138 Napoli, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Riccardo","family":"Pierantoni","sequence":"additional","affiliation":[{"name":"Dipartimento di Medicina Sperimentale, Universit\u00e0 degli Studi della Campania L. Vanvitelli, Via Costantinopoli 16, 80138 Napoli, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3631-1794","authenticated-orcid":false,"given":"Rosanna","family":"Chianese","sequence":"additional","affiliation":[{"name":"Dipartimento di Medicina Sperimentale, Universit\u00e0 degli Studi della Campania L. Vanvitelli, Via Costantinopoli 16, 80138 Napoli, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"69","DOI":"10.3389\/fendo.2014.00069","article-title":"Intra-testicular signals regulate germ cell progression and production of qualitatively mature spermatozoa in vertebrates","volume":"5","author":"Meccariello","year":"2014","journal-title":"Front. Endocrinol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"4071","DOI":"10.1007\/s00018-019-03201-6","article-title":"Mechanisms regulating mammalian spermatogenesis and fertility recovery following germ cell depletion","volume":"76","author":"La","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_3","unstructured":"Knobil, E., and Neill, J.D. (1999). Spermatogenesis: An overview. Encyclopedia of Reproduction, Academic Press."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"640","DOI":"10.3390\/jcm9030640","article-title":"Histone Post-Translational Modifications and CircRNAs in Mouse and Human Spermatozoa: Potential Epigenetic Marks to Assess Human Sperm Quality","volume":"9","author":"Chioccarelli","year":"2020","journal-title":"J. Clin. Med."},{"key":"ref_5","first-page":"112","article-title":"Meiosis: The chromosomal foundation of reproduction","volume":"9","author":"Handel","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_6","doi-asserted-by":"crossref","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":"Biochim. Biophys. Acta"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"92","DOI":"10.3390\/antiox10010092","article-title":"Mitochondrial Reactive Oxygen Species (ROS) Production Alters Sperm Quality","volume":"10","author":"Chianese","year":"2021","journal-title":"Antioxidants"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1111\/j.1742-4658.2009.07504.x","article-title":"From meiosis to postmeiotic events: The secrets of histone disappearance","volume":"277","author":"Gaucher","year":"2010","journal-title":"FEBS J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2013\/501350","article-title":"Estrogens and Spermiogenesis: New Insights from Type 1 Cannabinoid Receptor Knockout Mice","volume":"2013","author":"Cacciola","year":"2013","journal-title":"Int. J. Endocrinol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0962-8924(99)01708-0","article-title":"The nuclear envelope, muscular dystrophy and gene expression","volume":"10","author":"Wilson","year":"2000","journal-title":"Trends Cell Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1242\/jcs.019042","article-title":"The nuclear envelope at a glance","volume":"123","author":"Wilson","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/nrm3488","article-title":"The nuclear lamins: Flexibility in function","volume":"14","author":"Burke","year":"2013","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1038\/nrm.2016.153","article-title":"Mechanisms and functions of nuclear envelope remodelling","volume":"18","author":"Ungricht","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Link, J., Jahn, D., Schmitt, J., G\u00f6b, E., Baar, J., Ortega, S., Benavente, R., and Alsheimer, M. (2013). The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet., 9.","DOI":"10.1371\/journal.pgen.1003261"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1111\/brv.12498","article-title":"Nuclear envelope dynamics during mammalian spermatogenesis: New insights on male fertility","volume":"94","author":"Pereira","year":"2019","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2227","DOI":"10.1242\/jcs.111.15.2227","article-title":"Nuclear envelope remodelling during rat spermiogenesis: Distribution and expression pattern of LAP2\/thymopoietins","volume":"111","author":"Alsheimer","year":"1998","journal-title":"J. Cell Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.yexcr.2005.03.023","article-title":"Nuclear envelope remodeling during mouse spermiogenesis: Postmeiotic expression and redistribution of germline lamin B3","volume":"307","author":"Alsheimer","year":"2005","journal-title":"Exp. Cell Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"221","DOI":"10.4161\/spmg.1.3.18018","article-title":"Cytoskeletal track selection during cargo transport in spermatids is relevant to male fertility","volume":"1","author":"Kierszenbaum","year":"2011","journal-title":"Spermatogenesis"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/B978-0-12-416024-8.00005-2","article-title":"LINCing the nuclear envelope to gametogenesis","volume":"102","author":"Kracklauer","year":"2013","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1679\/aohc.67.271","article-title":"The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head","volume":"67","author":"Kierszenbaum","year":"2004","journal-title":"Arch. Histol. Cytol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/BF01790091","article-title":"Detection of chromosome aberrations in metaphase and interphase tumor cells by in situ hybridization using chromosome-specific library probes","volume":"80","author":"Cremer","year":"1988","journal-title":"Hum. Genet."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"4424","DOI":"10.1073\/pnas.072618599","article-title":"Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates","volume":"99","author":"Tanabe","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1363","DOI":"10.1242\/jcs.111.10.1363","article-title":"Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus","volume":"111","author":"Scherthan","year":"1998","journal-title":"J. Cell Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0070-2153(08)60328-2","article-title":"Sperm nuclear activation during fertilization","volume":"46","author":"Wright","year":"1999","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1002\/(SICI)1098-2795(200003)55:3<307::AID-MRD9>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":"Mol. Reprod. Dev."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1023\/B:CHRO.0000013166.04629.97","article-title":"Non-random positioning of chromosomes in human sperm nuclei","volume":"12","author":"Zalenskaya","year":"2004","journal-title":"Chromosome Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1242\/jcs.02301","article-title":"Non-random chromosome positioning in mammalian sperm nuclei, with migration of the sex chromosomes during late spermatogenesis","volume":"118","author":"Foster","year":"2005","journal-title":"J. Cell Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1006\/excr.1996.0315","article-title":"Change of karyoskeleton during mammalian spermatogenesis: Expression pattern of nuclear lamin C2 and its regulation","volume":"228","author":"Alsheimer","year":"1996","journal-title":"Exp. Cell Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.yexcr.2004.03.008","article-title":"The XY body: A specialized meiotic chromatin domain","volume":"296","author":"Handel","year":"2004","journal-title":"Exp. Cell Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/j.devcel.2009.10.018","article-title":"Nuclei take a position: Managing nuclear location","volume":"17","author":"Burke","year":"2009","journal-title":"Dev. Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1083\/jcb.200906068","article-title":"Bringing KASH under the SUN: The many faces of nucleo-cytoskeletal connections","volume":"186","author":"Razafsky","year":"2009","journal-title":"J. Cell Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1083\/jcb.200509124","article-title":"Coupling of the nucleus and cytoplasm: Role of the LINC complex","volume":"172","author":"Crisp","year":"2006","journal-title":"J. Cell Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1892","DOI":"10.1016\/j.yexcr.2008.02.022","article-title":"Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness","volume":"314","author":"Hale","year":"2008","journal-title":"Exp. Cell Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1016\/j.cell.2012.03.046","article-title":"LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins","volume":"149","author":"Sosa","year":"2012","journal-title":"Cell"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S1462399405009294","article-title":"Nesprins: Intracellular scaffolds that maintain cell architecture and coordinate cell function?","volume":"7","author":"Warren","year":"2005","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"25805","DOI":"10.1074\/jbc.M313157200","article-title":"Sun2 is a novel mammalian inner nuclear membrane protein","volume":"279","author":"Hodzic","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3419","DOI":"10.1242\/jcs.02471","article-title":"The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope","volume":"118","author":"Padmakumar","year":"2005","journal-title":"J. Cell Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1242\/jcs.037622","article-title":"A nuclear\u2014envelope bridge positions nuclei and moves chromosomes","volume":"122","author":"Starr","year":"2009","journal-title":"J. Cell Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1006\/dbio.1999.9297","article-title":"Spag4, a Novel Sperm Protein, Binds Outer Dense-Fiber Protein Odf1 and Localizes to Microtubules of Manchette and Axoneme","volume":"211","author":"Shao","year":"1999","journal-title":"Dev. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1515\/hsz-2014-0267","article-title":"Making the LINC: SUN and KASH protein interactions","volume":"396","author":"Kim","year":"2015","journal-title":"Biol. Chem."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1083\/jcb.200506083","article-title":"Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin","volume":"171","author":"Wilhelmsen","year":"2005","journal-title":"J. Cell Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.ceb.2010.11.006","article-title":"Nesprins LINC the nucleus and cytoskeleton","volume":"23","author":"Mellad","year":"2011","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e5","DOI":"10.1017\/erm.2013.6","article-title":"Nesprins: From the nuclear envelope and beyond","volume":"15","author":"Rajgor","year":"2013","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e60175","DOI":"10.7554\/eLife.60175","article-title":"A molecular mechanism for LINC complex branching by structurally diverse SUN-KASH 6:6 assemblies","volume":"10","author":"Gurusaran","year":"2021","journal-title":"eLife"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1242\/bio.015768","article-title":"The LINC complex component Sun4 plays a crucial role in sperm head formation and fertility","volume":"4","author":"Pasch","year":"2015","journal-title":"Biol. Open"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3219","DOI":"10.1242\/jcs.184184","article-title":"The LINC and NPC relationship\u2014it\u2019s complicated!","volume":"129","author":"Jahed","year":"2016","journal-title":"J. Cell Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1083\/jcb.200704108","article-title":"Functional association of Sun1 with nuclear pore complexes","volume":"178","author":"Liu","year":"2007","journal-title":"J. Cell Biol."},{"key":"ref_48","first-page":"9874","article-title":"Inner nuclear envelope protein SUN1 plays a prominent role in mammalian mRNA export","volume":"43","author":"Li","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1016\/j.devcel.2007.03.018","article-title":"SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice","volume":"12","author":"Ding","year":"2007","journal-title":"Dev. Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1083\/jcb.201304004","article-title":"A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton","volume":"202","author":"Horn","year":"2013","journal-title":"J. Cell Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"7426","DOI":"10.1073\/pnas.0609198104","article-title":"Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope","volume":"104","author":"Schmitt","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Link, J., Leubner, M., Schmitt, J., G\u00f6b, E., Benavente, R., Jeang, K.T., Xu, R., and Alsheimer, M. (2014). Analysis of Meiosis in SUN1 Deficient Mice Reveals a Distinct Role of SUN2 in Mammalian Meiotic LINC Complex Formation and Function. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004099"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s12610-018-0072-4","article-title":"The involvement of the nuclear lamina in human and rodent spermiogenesis: A systematic review","volume":"28","author":"Paci","year":"2018","journal-title":"Basic Clin. Androl."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1089\/dna.2010.1161","article-title":"SPAG4L, a novel nuclear envelope protein involved in the meiotic stage of spermatogenesis","volume":"30","author":"Jiang","year":"2011","journal-title":"DNA Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1093\/abbs\/gmz051","article-title":"SPAG4L\/SPAG4L\u03b2 interacts with Nesprin2 to participate in the meiosis of spermatogenesis","volume":"51","author":"Li","year":"2019","journal-title":"Acta Biochim. Biophys. Sin."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"G\u00f6b, E., Schmitt, J., Benavente, R., and Alsheimer, M. (2010). Mammalian Sperm Head Formation Involves Different Polarization of Two Novel LINC Complexes. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0012072"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Kmonickova, V., Frolikova, M., Steger, K., and Komrskova, K. (2020). The Role of the LINC Complex in Sperm Development and Function. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21239058"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.jmb.2014.09.008","article-title":"Cytoskeletal control of nuclear morphology and chromatin organization","volume":"427","author":"Ramdas","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"824","DOI":"10.3389\/fphys.2018.00824","article-title":"Cellular Mechanotransduction: From Tension to Function","volume":"9","author":"Martino","year":"2018","journal-title":"Front. Physiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1146\/annurev-bioeng-060418-052139","article-title":"The Driving Force: Nuclear Mechanotransduction in Cellular Function, Fate, and Disease","volume":"21","author":"Maurer","year":"2019","journal-title":"Annu. Rev. Biomed. Eng."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"4649","DOI":"10.1529\/biophysj.106.086454","article-title":"Mechanical properties of the cell nucleus and the effect of emerin deficiency","volume":"91","author":"Rowat","year":"2006","journal-title":"Biophys. J."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"26743","DOI":"10.1074\/jbc.M111.233700","article-title":"The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton","volume":"286","author":"Lombardi","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.tcb.2020.11.009","article-title":"Actin on and around the Nucleus","volume":"31","author":"Davidson","year":"2021","journal-title":"Trends Cell Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1093\/hmg\/ddq549","article-title":"KASH protein Syne-2\/Nesprin-2 and SUN proteins SUN1\/2 mediate nuclear migration during mammalian retinal development","volume":"20","author":"Yu","year":"2011","journal-title":"Hum. Mol. Genet."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1536","DOI":"10.1016\/S0960-9822(01)00475-4","article-title":"Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization","volume":"11","author":"Palazzo","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1126\/science.1189072","article-title":"Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement","volume":"329","author":"Luxton","year":"2010","journal-title":"Science"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"3097","DOI":"10.1016\/j.cub.2017.08.073","article-title":"Centrifugal displacement of nuclei reveals multiple LINC complex mechanisms for homeostatic nuclear positioning","volume":"27","author":"Zhu","year":"2017","journal-title":"Curr. Biol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1774","DOI":"10.1091\/mbc.E19-01-0027","article-title":"Mechanical stress triggers nuclear remodeling and the formation of transmembrane actin nuclear lines with associated nuclear pore complexes","volume":"31","author":"Hoffman","year":"2020","journal-title":"Mol. Biol. Cell"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"19017","DOI":"10.1073\/pnas.0908686106","article-title":"A perinuclear actin cap regulates nuclear shape","volume":"106","author":"Khatau","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.1038\/s41467-017-02217-5","article-title":"Nuclear lamin A\/C harnesses the perinuclear apical actin cables to protect nuclear morphology","volume":"8","author":"Kim","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/srep00555","article-title":"Actin cap associated focal adhesions and their distinct role in cellular mechanosensing","volume":"2","author":"Kim","year":"2012","journal-title":"Sci. Rep."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1038\/srep01087","article-title":"The LINC-anchored actin cap connects the extracellular milieu to the nucleus for ultrafast mechanotransduction","volume":"3","author":"Chambliss","year":"2013","journal-title":"Sci. Rep."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/j.tcb.2012.04.006","article-title":"The Hippo signaling pathway andstem cell biology","volume":"22","author":"Ramos","year":"2012","journal-title":"Trends Cell Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"157","DOI":"10.3389\/fmolb.2019.00157","article-title":"Hippo Signaling-Mediated Mechanotransduction in Cell Movement and Cancer Metastasis","volume":"6","author":"Chang","year":"2020","journal-title":"Front. Mol. Biosci."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"5072","DOI":"10.1002\/jcp.29455","article-title":"The role of Hippo signaling pathway and mechanotransduction in tuning embryoid body formation and differentiation","volume":"235","author":"Barzegari","year":"2020","journal-title":"J. Cell. Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/nrm3416","article-title":"Transduction of mechanical and cytoskeletal cues by YAP and TAZ","volume":"13","author":"Halder","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"798","DOI":"10.1101\/gad.274951.115","article-title":"\u03b1E-catenin inhibits a Src-YAP1 oncogenic module that couples tyrosine kinases and the effector of Hippo signaling pathway","volume":"30","author":"Li","year":"2016","journal-title":"Genes Dev."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Cobbaut, M., Karagil, S., Bruno, L., Diaz de la Loza, M.D.C., Mackenzie, F.E., Stolinski, M., and Elbediwy, A. (2020). Dysfunctional Mechanotransduction through the YAP\/TAZ\/Hippo Pathway as a Feature of Chronic Disease. Cells, 9.","DOI":"10.3390\/cells9010151"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/ncb3131","article-title":"Active diffusion positions the nucleus in mouse oocytes","volume":"17","author":"Almonacid","year":"2015","journal-title":"Nat. Cell Biol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"e46902","DOI":"10.7554\/eLife.46902","article-title":"Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis","volume":"8","author":"Booth","year":"2019","journal-title":"eLife"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/s13023-017-0698-x","article-title":"Nuclear envelopathies: A complex LINC between nuclear envelope and pathology","volume":"12","author":"Janin","year":"2017","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"e201908036","DOI":"10.1083\/jcb.201908036","article-title":"Nesprins are mechanotransducers that discriminate epithelial\u2013mesenchymal transition programs","volume":"219","author":"Carollo","year":"2020","journal-title":"J. Cell Biol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.tcb.2004.03.004","article-title":"BAF: Roles in chromatin, nuclear structure and retrovirus integration","volume":"14","author":"Wilson","year":"2004","journal-title":"Trends Cell Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1530\/REP-17-0358","article-title":"LEM-domain proteins are lost during human spermiogenesis but BAF and BAF-L persist","volume":"154","author":"Elkhatib","year":"2017","journal-title":"Reproduction"},{"key":"ref_85","doi-asserted-by":"crossref","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 Res."},{"key":"ref_86","doi-asserted-by":"crossref","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":"Nat. Genet."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"11626","DOI":"10.1074\/jbc.M311949200","article-title":"Temporal association of protamine 1 with the inner nuclear membrane protein lamin B receptor during spermiogenesis","volume":"279","author":"Mylonis","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"16610","DOI":"10.1073\/pnas.0909077106","article-title":"Barrier-to-autointegration factor (BAF) condenses DNA by looping","volume":"106","author":"Skoko","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"E544","DOI":"10.1073\/pnas.1118880109","article-title":"Active maintenance of nuclear actin by importin 9 supports transcription","volume":"109","author":"Dopie","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"107824","DOI":"10.1016\/j.celrep.2020.107824","article-title":"Zygotic Nuclear F-Actin Safeguards Embryonic Development","volume":"31","author":"Okuno","year":"2020","journal-title":"Cell Rep."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"925","DOI":"10.3389\/fphys.2018.00925","article-title":"The Effect of Cell Morphology on the Permeability of the Nuclear Envelope to Diffusive Factors","volume":"9","author":"Jacchetti","year":"2018","journal-title":"Front. Physiol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1240104","DOI":"10.1126\/science.1240104","article-title":"Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation","volume":"341","author":"Swift","year":"2013","journal-title":"Science"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.biomaterials.2015.01.023","article-title":"Cytoskeletal tension induces the polarized architecture of the nucleus","volume":"48","author":"Kim","year":"2015","journal-title":"Biomaterials"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1902","DOI":"10.1016\/j.bpj.2011.03.008","article-title":"Biophysical regulation of histone acetylation in mesenchymal stem cells","volume":"100","author":"Li","year":"2011","journal-title":"Biophys. J."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1038\/ncb3387","article-title":"Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment","volume":"18","author":"Le","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1016\/S0960-9822(03)00576-1","article-title":"Mechanical induction of Twist in the Drosophila foregut\/stomodeal primordium","volume":"13","author":"Farge","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1083\/jcb.99.3.1083","article-title":"Distinct cytoskeletal domains revealed in sperm cells","volume":"99","author":"Virtanen","year":"1984","journal-title":"J. Cell Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1095\/biolreprod.102.009233","article-title":"Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction","volume":"68","author":"Brener","year":"2003","journal-title":"Biol. Reprod."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1002\/j.1939-4640.2001.tb02154.x","article-title":"Actin and actin binding proteins in bovine spermatozoa: Potential role in membrane remodeling and intracellular signaling during epididymal maturation and the acrosome reaction","volume":"22","author":"Howes","year":"2001","journal-title":"J. Androl."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.bbrc.2017.11.001","article-title":"Actin cytoskeleton and sperm function","volume":"506","author":"Breitbart","year":"2018","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"2525","DOI":"10.1242\/jcs.108.6.2525","article-title":"Sperm exocytosis reconstructed in a cell-free system: Evidence for the involvement of phospholipase C and actin filaments in membrane fusion","volume":"108","author":"Spungin","year":"1995","journal-title":"J. Cell Sci."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1002\/(SICI)1097-0169(200005)46:1<43::AID-CM5>3.0.CO;2-1","article-title":"Involvement of an F-actin skeleton on the acrosome reaction in guinea pig spermatozoa","volume":"46","author":"Mujica","year":"2000","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.ydbio.2013.06.014","article-title":"Regulation of sperm motility by PIP2(4,5) and actin polymerization","volume":"381","author":"Finkelstein","year":"2013","journal-title":"Dev. Biol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.ydbio.2016.05.008","article-title":"CaMKII prevents spontaneous acrosomal exocytosis in sperm through induction of actin polymerization","volume":"415","author":"Shabtay","year":"2016","journal-title":"Dev. Biol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1007\/s00441-015-2229-1","article-title":"The role and importance of cofilin in human sperm capacitation and the acrosome reaction","volume":"362","author":"Megnagi","year":"2015","journal-title":"Cell Tissue Res."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"2865","DOI":"10.1128\/MCB.20.8.2865-2873.2000","article-title":"Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions","volume":"20","author":"Bouchard","year":"2000","journal-title":"Mol. Cell. Biol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1530\/rep.1.00549","article-title":"Cytoskeleton localization in the sperm head prior to fertilization","volume":"130","author":"Moore","year":"2005","journal-title":"Process. Prior Fertil. Reprod."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1530\/rep.0.1220519","article-title":"Hyperactivation of mammalian spermatozoa: Function and regulation","volume":"122","author":"Ho","year":"2001","journal-title":"Reproduction"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.ydbio.2011.12.002","article-title":"Hyper-activated motility in sperm capacitation is mediated by phospholipase D-dependent actin polymerization","volume":"362","author":"Itach","year":"2012","journal-title":"Dev. Biol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"39702","DOI":"10.1074\/jbc.M110.170951","article-title":"Role and regulation of sperm gelsolin prior to fertilization","volume":"285","author":"Finkelstein","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"jcs215897","DOI":"10.1242\/jcs.215897","article-title":"The actin cytoskeleton of the mouse sperm flagellum is organized in a helical structure","volume":"131","author":"Gervasi","year":"2018","journal-title":"J. Cell Sci."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1126\/science.aad0836","article-title":"Sperm calcineurin inhibition prevents mouse fertility with implications for male contraceptive","volume":"350","author":"Miyata","year":"2015","journal-title":"Science"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1679\/aohc.66.383","article-title":"Formation and organization of the mammalian sperm head","volume":"66","author":"Toshimori","year":"2003","journal-title":"Arch. Histol. Cytol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/2051-4190-24-6","article-title":"Recent knowledge concerning mammalian sperm chromatin organization and its potential weaknesses when facing oxidative challenge","volume":"24","author":"Noblanc","year":"2014","journal-title":"Basic Clin. Androl."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"195","DOI":"10.3389\/fcell.2019.00195","article-title":"Mechanism of Acrosome Biogenesis in Mammals","volume":"7","author":"Khawar","year":"2019","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1002\/aja.1001920202","article-title":"Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents","volume":"192","author":"Russell","year":"1991","journal-title":"Am. J. Anat."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3389\/fcell.2018.00072","article-title":"Molecular Basis of Human Sperm Capacitation","volume":"6","author":"Luque","year":"2018","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/biolre\/ioy045","article-title":"Sperm acrosome reaction: Its site and role in fertilization","volume":"99","author":"Hirohashi","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"1857","DOI":"10.2353\/ajpath.2009.080955","article-title":"The expression level of septin12 is critical for spermiogenesis","volume":"174","author":"Lin","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/nature06052","article-title":"Structural insight into filament formation by mammalian septins","volume":"449","author":"Sirajuddin","year":"2007","journal-title":"Nature"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1038\/nrm3284","article-title":"Septins: The fourth component of the cytoskeleton","volume":"13","author":"Mostowy","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Yeh, C.H., Kuo, P.L., Wang, Y.Y., Wu, Y.Y., Chen, M.F., Lin, D.Y., Lai, T.H., Chiang, H.S., and Lin, Y.H. (2015). SEPT12\/SPAG4\/LAMINB1 complexes are required for maintaining the integrity of the nuclear envelope in postmeiotic male germ cells. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0120722"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1093\/molehr\/gaq099","article-title":"SPAG4L\/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome","volume":"17","author":"Frohnert","year":"2011","journal-title":"Mol. Hum. Reprod."},{"key":"ref_124","doi-asserted-by":"crossref","unstructured":"Yassine, S., Escoffier, J., Abi Nahed, R., Pierre, V., Karaouzene, T., Ray, P.F., and Arnoult, C. (2015). Dynamics of Sun5 localization during spermatogenesis in wild type and Dpy19l2 knock-out mice indicates that Sun5 is not involved in acrosome attachment to the nuclear envelope. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0118698"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"2395","DOI":"10.1074\/jbc.RA117.000861","article-title":"Mechanistic insights into acephalic spermatozoa syndrome-associated mutations in the human SUN5 gene","volume":"293","author":"Shang","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1530\/REP-14-0012","article-title":"Lamin A\/C proteins in the spermatid acroplaxome are essential in mouse spermiogenesis","volume":"148","author":"Shen","year":"2014","journal-title":"Reproduction"},{"key":"ref_127","first-page":"2683","article-title":"Interphase phosphorylation of lamin A","volume":"127","author":"Kochin","year":"2014","journal-title":"J. Cell Sci."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"2955","DOI":"10.1242\/dev.077982","article-title":"Absence of Dpy19l2, a new inner nuclear membrane protein, causes globozoospermia in mice by preventing the anchoring of the acrosome to the nucleus","volume":"139","author":"Pierre","year":"2012","journal-title":"Development"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1093\/molehr\/gau099","article-title":"Dpy19l2-deficient globozoospermic sperm display altered genome packaging and DNA damage that compromises the initiation of embryo development","volume":"21","author":"Yassine","year":"2015","journal-title":"Mol. Hum. Reprod."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1083\/jcb.201204085","article-title":"A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis","volume":"198","author":"Morimoto","year":"2012","journal-title":"J. Cell Biol."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1093\/biolre\/iox096","article-title":"Formation and function of sperm tail structures in association with sperm motility defects","volume":"97","author":"Lehti","year":"2017","journal-title":"Biol. Reprod."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1002\/cm.21338","article-title":"Functional anatomy of the mammalian sperm flagellum","volume":"73","author":"Lindemann","year":"2016","journal-title":"Cytoskeleton"},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1002\/mrd.10197","article-title":"Motor Apparatus in Human Spermatozoa that Lack Central Pair Microtubules","volume":"63","author":"Ishijima","year":"2002","journal-title":"Mol. Reprod. Dev."},{"key":"ref_134","unstructured":"Neill, J.D. (2006). The Spermatozoon. Knobil and Neill\u2019s Physiology of Reproduction, Academic Press."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.fertnstert.2010.07.1086","article-title":"Altered ultrastructure of mitochondrial membranes is strongly associated with unexplained asthenozoospermia","volume":"95","author":"Pelliccione","year":"2011","journal-title":"Fertil. Steril."},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1111\/j.1365-2605.2011.01218.x","article-title":"The role of mitochondria in energy production for human sperm motility","volume":"35","author":"Piomboni","year":"2012","journal-title":"Int. J. Androl."},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"20613","DOI":"10.1074\/jbc.M115.664813","article-title":"Differences in ATP Generation via Glycolysis and Oxidative Phosphorylation and Relationships with Sperm Motility in Mouse Species","volume":"290","author":"Tourmente","year":"2015","journal-title":"J. Biol. Chem."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1093\/biolre\/ioaa016","article-title":"The coupling apparatus of the sperm head and tail","volume":"102","author":"Wu","year":"2020","journal-title":"Biol. Reprod."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s00418-018-1668-7","article-title":"Ultra-structure of the sperm head-to-tail linkage complex in the absence of the spermatid-specific LINC component SPAG4","volume":"150","author":"Yang","year":"2018","journal-title":"Histochem. Cell Biol."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"e28199","DOI":"10.7554\/eLife.28199","article-title":"Essential role for SUN5 in anchoring sperm head to the tail","volume":"6","author":"Shang","year":"2017","journal-title":"eLife"},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1242\/dev.029868","article-title":"Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA","volume":"136","author":"Chi","year":"2009","journal-title":"Development"},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"6289","DOI":"10.1074\/jbc.RA119.012375","article-title":"The testis-specific LINC component SUN3 is essential for sperm head shaping during mouse spermiogenesis","volume":"295","author":"Gao","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.ydbio.2015.09.010","article-title":"SUN4 is essential for nuclear remodeling during mammalian spermiogenesis","volume":"407","author":"Calvi","year":"2015","journal-title":"Dev. Biol."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1002\/humu.22028","article-title":"SEPT12 mutations cause male infertility with defective sperm annulus","volume":"33","author":"Kuo","year":"2012","journal-title":"Hum. Mutat."},{"key":"ref_145","doi-asserted-by":"crossref","unstructured":"Kuo, P.L. (2012). SEPTIN12 Genetic Variants Confer Susceptibility to Teratozoospermia. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0034011"},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1016\/j.ajhg.2016.08.004","article-title":"Biallelic SUN5 Mutations Cause Autosomal-Recessive Acephalic Spermatozoa Syndrome","volume":"99","author":"Zhu","year":"2016","journal-title":"Am. J. Hum. Genet."},{"key":"ref_147","first-page":"3167","article-title":"Homozygous deletion of SUN5 in three men with decapitated spermatozoa","volume":"26","author":"Elkhatib","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1093\/humrep\/dex382","article-title":"Patients with acephalic spermatozoa syndrome linked to SUN5 mutations have a favorable pregnancy outcome from ICSI","volume":"33","author":"Fang","year":"2018","journal-title":"Hum. Reprod."},{"key":"ref_149","doi-asserted-by":"crossref","unstructured":"Cescon, M., Chianese, R., and Tavares, R.S. (2020). Environmental Impact on Male (In)Fertility via Epigenetic Route. J. Clin. Med., 9.","DOI":"10.3390\/jcm9082520"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/12\/5\/658\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:53:32Z","timestamp":1760162012000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/12\/5\/658"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,27]]},"references-count":149,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["genes12050658"],"URL":"https:\/\/doi.org\/10.3390\/genes12050658","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,27]]}}}