{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T16:31:29Z","timestamp":1781627489668,"version":"3.54.5"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,9,7]],"date-time":"2024-09-07T00:00:00Z","timestamp":1725667200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2024,9,7]],"date-time":"2024-09-07T00:00:00Z","timestamp":1725667200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01EY031346"],"award-info":[{"award-number":["R01EY031346"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-024-71303-8","type":"journal-article","created":{"date-parts":[[2024,9,7]],"date-time":"2024-09-07T10:02:05Z","timestamp":1725703325000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["TUBB4B is essential for the expansion of differentiating spermatogonia"],"prefix":"10.1038","volume":"14","author":[{"given":"Urikhan","family":"Sanzhaeva","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalie R.","family":"Wonsettler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott B.","family":"Rhodes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Visvanathan","family":"Ramamurthy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,9,7]]},"reference":[{"key":"71303_CR1","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a022608","author":"HV Goodson","year":"2018","unstructured":"Goodson, H. V. & Jonasson, E. M. Microtubules and microtubule-associated proteins. Cold Spring Harb. Perspect. Biol. https:\/\/doi.org\/10.1101\/cshperspect.a022608 (2018).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"71303_CR2","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a025817","author":"K Barlan","year":"2017","unstructured":"Barlan, K. & Gelfand, V. I. Microtubule-based transport and the distribution, tethering, and organization of organelles. Cold Spring Harb. Perspect. Biol. https:\/\/doi.org\/10.1101\/cshperspect.a025817 (2017).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"71303_CR3","doi-asserted-by":"publisher","first-page":"1554","DOI":"10.1016\/j.celrep.2012.11.017","volume":"2","author":"M Breuss","year":"2012","unstructured":"Breuss, M. et al. Mutations in the \u03b2-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rep. 2, 1554\u20131562. https:\/\/doi.org\/10.1016\/j.celrep.2012.11.017 (2012).","journal-title":"Cell Rep."},{"key":"71303_CR4","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1016\/j.ajhg.2017.10.010","volume":"101","author":"R Luscan","year":"2017","unstructured":"Luscan, R. et al. Mutations in TUBB4B cause a distinctive sensorineural disease. Am. J. Hum. Genet. 101, 1006\u20131012. https:\/\/doi.org\/10.1016\/j.ajhg.2017.10.010 (2017).","journal-title":"Am. J. Hum. Genet."},{"key":"71303_CR5","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1056\/NEJMoa1510791","volume":"374","author":"R Feng","year":"2016","unstructured":"Feng, R. et al. Mutations in TUBB8 and human oocyte meiotic arrest. N. Engl. J. Med. 374, 223\u2013232. https:\/\/doi.org\/10.1056\/NEJMoa1510791 (2016).","journal-title":"N. Engl. J. Med."},{"key":"71303_CR6","doi-asserted-by":"publisher","first-page":"1676","DOI":"10.1093\/brain\/awu082","volume":"137","author":"N Bahi-Buisson","year":"2014","unstructured":"Bahi-Buisson, N. et al. The wide spectrum of tubulinopathies: What are the key features for the diagnosis?. Brain 137, 1676\u20131700. https:\/\/doi.org\/10.1093\/brain\/awu082 (2014).","journal-title":"Brain"},{"key":"71303_CR7","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1534\/genetics.110.116996","volume":"185","author":"DD Hurd","year":"2010","unstructured":"Hurd, D. D., Miller, R. M., N\u00fa\u00f1ez, L. & Portman, D. S. Specific \u03b1- and \u03b2-tubulin isotypes optimize the functions of sensory cilia in caenorhabditis elegans. Genetics 185, 883\u2013896. https:\/\/doi.org\/10.1534\/genetics.110.116996 (2010).","journal-title":"Genetics"},{"key":"71303_CR8","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1016\/j.cub.2017.02.039","volume":"27","author":"M Silva","year":"2017","unstructured":"Silva, M. et al. Cell-specific \u03b1-tubulin isotype regulates ciliary microtubule ultrastructure, intraflagellar transport, and extracellular vesicle biology. Curr. Biol. 27, 968\u2013980. https:\/\/doi.org\/10.1016\/j.cub.2017.02.039 (2017).","journal-title":"Curr. Biol."},{"key":"71303_CR9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1152\/physrev.00013.2015","volume":"96","author":"MD Griswold","year":"2016","unstructured":"Griswold, M. D. Spermatogenesis: The commitment to meiosis. Physiol. Rev. 96, 1\u201317. https:\/\/doi.org\/10.1152\/physrev.00013.2015 (2016).","journal-title":"Physiol. Rev."},{"key":"71303_CR10","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.scr.2018.04.009","volume":"29","author":"AP Fayomi","year":"2018","unstructured":"Fayomi, A. P. & Orwig, K. E. Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Res. 29, 207\u2013214. https:\/\/doi.org\/10.1016\/j.scr.2018.04.009 (2018).","journal-title":"Stem Cell Res."},{"key":"71303_CR11","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.semcdb.2014.01.003","volume":"30","author":"L O\u2019Donnell","year":"2014","unstructured":"O\u2019Donnell, L. & O\u2019Bryan, M. K. Microtubules and spermatogenesis. Semin. Cell Dev. Biol. 30, 45\u201354. https:\/\/doi.org\/10.1016\/j.semcdb.2014.01.003 (2014).","journal-title":"Semin. Cell Dev. Biol."},{"key":"71303_CR12","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.semcdb.2021.12.003","volume":"137","author":"S Gadadhar","year":"2023","unstructured":"Gadadhar, S., Hirschmugl, T. & Janke, C. The tubulin code in mammalian sperm development and function. Semin. Cell Dev. Biol. 137, 26\u201337. https:\/\/doi.org\/10.1016\/j.semcdb.2021.12.003 (2023).","journal-title":"Semin. Cell Dev. Biol."},{"key":"71303_CR13","doi-asserted-by":"publisher","first-page":"2023","DOI":"10.1083\/jcb.106.6.2023","volume":"106","author":"SA Lewis","year":"1988","unstructured":"Lewis, S. A. & Cowan, N. J. Complex regulation and functional versatility of mammalian alpha- and beta-tubulin isotypes during the differentiation of testis and muscle cells. J. Cell Biol. 106, 2023\u20132033. https:\/\/doi.org\/10.1083\/jcb.106.6.2023 (1988).","journal-title":"J. Cell Biol."},{"key":"71303_CR14","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1038\/ng1366","volume":"36","author":"FW Buaas","year":"2004","unstructured":"Buaas, F. W. et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36, 647\u2013652. https:\/\/doi.org\/10.1038\/ng1366 (2004).","journal-title":"Nat. Genet."},{"key":"71303_CR15","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1530\/rep-14-0653","volume":"149","author":"BA Niedenberger","year":"2015","unstructured":"Niedenberger, B. A., Busada, J. T. & Geyer, C. B. Marker expression reveals heterogeneity of spermatogonia in the neonatal mouse testis. Reproduction 149, 329\u2013338. https:\/\/doi.org\/10.1530\/rep-14-0653 (2015).","journal-title":"Reproduction"},{"key":"71303_CR16","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1369\/0022155414562045","volume":"63","author":"H Nakata","year":"2015","unstructured":"Nakata, H., Wakayama, T., Takai, Y. & Iseki, S. Quantitative analysis of the cellular composition in seminiferous tubules in normal and genetically modified infertile mice. J. Histochem. Cytochem. 63, 99\u2013113. https:\/\/doi.org\/10.1369\/0022155414562045 (2015).","journal-title":"J. Histochem. Cytochem."},{"key":"71303_CR17","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/1471-213X-9-38","volume":"9","author":"K Zheng","year":"2009","unstructured":"Zheng, K., Wu, X., Kaestner, K. H. & Wang, P. J. The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev. Biol. 9, 38\u201338. https:\/\/doi.org\/10.1186\/1471-213X-9-38 (2009).","journal-title":"BMC Dev. Biol."},{"key":"71303_CR18","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1095\/biolreprod.107.066795","volume":"79","author":"Q Zhou","year":"2008","unstructured":"Zhou, Q. et al. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol. Reprod. 79, 35\u201342. https:\/\/doi.org\/10.1095\/biolreprod.107.066795 (2008).","journal-title":"Biol. Reprod."},{"key":"71303_CR19","doi-asserted-by":"publisher","first-page":"R53","DOI":"10.1530\/rep-18-0457","volume":"157","author":"JEM Dunleavy","year":"2019","unstructured":"Dunleavy, J. E. M., O\u2019Bryan, M. K., Stanton, P. G. & O\u2019Donnell, L. The cytoskeleton in spermatogenesis. Reproduction 157, R53\u2013R72. https:\/\/doi.org\/10.1530\/rep-18-0457 (2019).","journal-title":"Reproduction"},{"key":"71303_CR20","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/0092-8674(82)90321-X","volume":"31","author":"KJ Kemphues","year":"1982","unstructured":"Kemphues, K. J., Kaufman, T. C., Raff, R. A. & Raff, E. C. The testis-specific \u03b2-tubulin subunit in drosophila melanogaster has multiple functions in spermatogenesis. Cell 31, 655\u2013670. https:\/\/doi.org\/10.1016\/0092-8674(82)90321-X (1982).","journal-title":"Cell"},{"key":"71303_CR21","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1016\/s0960-9822(01)00150-6","volume":"11","author":"MG Nielsen","year":"2001","unstructured":"Nielsen, M. G., Turner, F. R., Hutchens, J. A. & Raff, E. C. Axoneme-specific beta-tubulin specialization: A conserved C-terminal motif specifies the central pair. Curr. Biol. 11, 529\u2013533. https:\/\/doi.org\/10.1016\/s0960-9822(01)00150-6 (2001).","journal-title":"Curr. Biol."},{"key":"71303_CR22","doi-asserted-by":"publisher","first-page":"1391","DOI":"10.1016\/S0960-9822(00)00784-3","volume":"10","author":"EC Raff","year":"2000","unstructured":"Raff, E. C., Hutchens, J. A., Hoyle, H. D., Nielsen, M. G. & Turner, F. R. Conserved axoneme symmetry altered by a component \u03b2-tubulin. Curr. Biol. 10, 1391\u20131394. https:\/\/doi.org\/10.1016\/S0960-9822(00)00784-3 (2000).","journal-title":"Curr. Biol."},{"key":"71303_CR23","doi-asserted-by":"publisher","first-page":"2722","DOI":"10.1038\/s44319-024-00159-w","volume":"25","author":"GG Stathatos","year":"2024","unstructured":"Stathatos, G. G. et al. Epsilon tubulin is an essential determinant of microtubule-based structures in male germ cells. EMBO Rep. 25, 2722\u20132742. https:\/\/doi.org\/10.1038\/s44319-024-00159-w (2024).","journal-title":"EMBO Rep."},{"key":"71303_CR24","doi-asserted-by":"publisher","first-page":"e0174264","DOI":"10.1371\/journal.pone.0174264","volume":"12","author":"CP Diggle","year":"2017","unstructured":"Diggle, C. P. et al. A tubulin alpha 8 mouse knockout model indicates a likely role in spermatogenesis but not in brain development. PLoS ONE 12, e0174264. https:\/\/doi.org\/10.1371\/journal.pone.0174264 (2017).","journal-title":"PLoS ONE"},{"key":"71303_CR25","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1177\/0300985810363485","volume":"47","author":"P Vogel","year":"2010","unstructured":"Vogel, P., Hansen, G., Fontenot, G. & Read, R. Tubulin tyrosine ligase-like 1 deficiency results in chronic rhinosinusitis and abnormal development of spermatid flagella in mice. Vet. Pathol. 47, 703\u2013712. https:\/\/doi.org\/10.1177\/0300985810363485 (2010).","journal-title":"Vet. Pathol."},{"key":"71303_CR26","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.226951","author":"T Giordano","year":"2019","unstructured":"Giordano, T. et al. Loss of the deglutamylase CCP5 perturbs multiple steps of spermatogenesis and leads to male infertility. J. Cell Sci. https:\/\/doi.org\/10.1242\/jcs.226951 (2019).","journal-title":"J. Cell Sci."},{"key":"71303_CR27","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/b978-0-12-407699-0.00002-9","volume":"302","author":"RF Ludue\u00f1a","year":"2013","unstructured":"Ludue\u00f1a, R. F. A hypothesis on the origin and evolution of tubulin. Int. Rev. Cell Mol. Biol. 302, 41\u2013185. https:\/\/doi.org\/10.1016\/b978-0-12-407699-0.00002-9 (2013).","journal-title":"Int. Rev. Cell Mol. Biol."},{"key":"71303_CR28","doi-asserted-by":"publisher","DOI":"10.3390\/genes13061082","author":"M Feng","year":"2022","unstructured":"Feng, M. et al. Tubulin TUBB4B is involved in spermatogonia proliferation and cell cycle processes. Genes (Basel) https:\/\/doi.org\/10.3390\/genes13061082 (2022).","journal-title":"Genes (Basel)"},{"key":"71303_CR29","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1016\/j.devcel.2018.07.025","volume":"46","author":"CD Green","year":"2018","unstructured":"Green, C. D. et al. A comprehensive roadmap of murine spermatogenesis defined by single-cell RNA-seq. Dev. Cell 46, 651-667.e610. https:\/\/doi.org\/10.1016\/j.devcel.2018.07.025 (2018).","journal-title":"Dev. Cell"},{"key":"71303_CR30","doi-asserted-by":"publisher","DOI":"10.1242\/dev.201819","author":"MT Sewell","year":"2023","unstructured":"Sewell, M. T., Legu\u00e9, E. & Liem, K. F. Tubb4b is required for multi-ciliogenesis in the mouse. Development https:\/\/doi.org\/10.1242\/dev.201819 (2023).","journal-title":"Development"},{"key":"71303_CR31","doi-asserted-by":"publisher","first-page":"eadf5489","DOI":"10.1126\/science.adf5489","volume":"384","author":"DO Dodd","year":"2024","unstructured":"Dodd, D. O. et al. Ciliopathy patient variants reveal organelle-specific functions for TUBB4B in axonemal microtubules. Science 384, eadf5489. https:\/\/doi.org\/10.1126\/science.adf5489 (2024).","journal-title":"Science"},{"key":"71303_CR32","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.201907016","author":"K Sofroni","year":"2020","unstructured":"Sofroni, K. et al. CDKD-dependent activation of CDKA;1 controls microtubule dynamics and cytokinesis during meiosis. J. Cell Biol. https:\/\/doi.org\/10.1083\/jcb.201907016 (2020).","journal-title":"J. Cell Biol."},{"key":"71303_CR33","doi-asserted-by":"publisher","first-page":"102158","DOI":"10.1016\/j.ceb.2023.102158","volume":"81","author":"A Mytlis","year":"2023","unstructured":"Mytlis, A., Levy, K. & Elkouby, Y. M. The many faces of the bouquet centrosome MTOC in meiosis and germ cell development. Curr. Opin. Cell Biol. 81, 102158. https:\/\/doi.org\/10.1016\/j.ceb.2023.102158 (2023).","journal-title":"Curr. Opin. Cell Biol."},{"key":"71303_CR34","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1016\/j.celrep.2015.03.045","volume":"11","author":"CY Lee","year":"2015","unstructured":"Lee, C. Y. et al. Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes. Cell Rep. 11, 551\u2013563. https:\/\/doi.org\/10.1016\/j.celrep.2015.03.045 (2015).","journal-title":"Cell Rep."},{"key":"71303_CR35","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402\u2013408. https:\/\/doi.org\/10.1006\/meth.2001.1262 (2001).","journal-title":"Methods"},{"key":"71303_CR36","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2002-3-7-research0034","author":"J Vandesompele","year":"2002","unstructured":"Vandesompele, J. et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. https:\/\/doi.org\/10.1186\/gb-2002-3-7-research0034 (2002).","journal-title":"Genome Biol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-71303-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-71303-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-71303-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,10]],"date-time":"2024-09-10T14:11:07Z","timestamp":1725977467000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-71303-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,7]]},"references-count":36,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["71303"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-71303-8","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,7]]},"assertion":[{"value":"19 April 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 August 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 September 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"20889"}}