{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T05:21:18Z","timestamp":1790572878273,"version":"4.1.0"},"reference-count":62,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2024,11,8]],"date-time":"2024-11-08T00:00:00Z","timestamp":1731024000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,11,8]],"date-time":"2024-11-08T00:00:00Z","timestamp":1731024000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Death Dis"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Asthenoteratozoospermia is a major cause of male infertility. Thus far, the identified related genes can explain only a small share of asthenoteratozoospermia cases, suggesting the involvement of other genes. The transmembrane protein TMEM232 is highly expressed in mouse testes. In the present study, to determine its function of TMEM232 in testes, we constructed a <jats:italic>Tmem232<\/jats:italic>-null mouse model using CRISPR\u2013Cas9 technology. <jats:italic>Tmem232<\/jats:italic> knockout (KO) male mice was completely infertile, and their sperm were immotile, with morphological defects of the flagellum. Electron microscopy revealed an aberrant midpiece-principal junction and the loss of the fourth outer microtubule doublet in the sperm of <jats:italic>Tmem232<\/jats:italic><jats:sup>\u2212\/\u2212<\/jats:sup> mice. Sperm cells presented an 8\u2009+\u20092 conformation and an irregular arrangement of the mitochondrial sheath. Proteomic analysis revealed altered expression of proteins related to flagellar motility, sperm capacitation, the integrity and stability of sperm structure, especially an upregulated expression of multiple ribosome components in TMEM232-deficient spermatids. Additionally, TMEM232 was observed to be involved in autophagy by interacting with autophagy-related proteins, such as ATG14, to regulate ribosome homeostasis during spermiogenesis. These results suggest that TMEM232, as a potential scaffold protein involving in the correct assembly, distribution, and stability maintenance of certain functional complexes by recruiting key intracellular proteins, is essential for the formation of a highly structured flagellum and plays an important role in the autophagic elimination of cytosolic ribosomes to provide energy for sperm motility.<\/jats:p>","DOI":"10.1038\/s41419-024-07200-9","type":"journal-article","created":{"date-parts":[[2024,11,8]],"date-time":"2024-11-08T20:10:52Z","timestamp":1731096652000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["TMEM232 is required for the formation of sperm flagellum and male fertility in mice"],"prefix":"10.1038","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-4328-6999","authenticated-orcid":false,"given":"Xinying","family":"Cai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0468-3526","authenticated-orcid":false,"given":"Hui","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"Kong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weilong","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ning","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shupei","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiru","family":"Shen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zengyunou","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haijian","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fang","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shun","family":"Bai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fuxi","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1158-5190","authenticated-orcid":false,"given":"Fengli","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4664-9617","authenticated-orcid":false,"given":"Fengsong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,11,8]]},"reference":[{"key":"7200_CR1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1101\/cshperspect.a028076","volume":"9","author":"T Ishikawa","year":"2017","unstructured":"Ishikawa T. Axoneme Structure from Motile Cilia. Cold Spring Harb Perspect Biol. 2017;9:1.","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"7200_CR2","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1101\/cshperspect.a018325","volume":"9","author":"R Viswanadha","year":"2017","unstructured":"Viswanadha R, Sale WS, Porter ME. Ciliary Motility: Regulation of Axonemal Dynein Motors. Cold Spring Harb Perspect Biol. 2017;9:8.","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"7200_CR3","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1093\/biolre\/iox096","volume":"97","author":"MS Lehti","year":"2017","unstructured":"Lehti MS, Sironen A. Formation and function of sperm tail structures in association with sperm motility defects. Biol Reprod. 2017;97:522\u201336.","journal-title":"Biol Reprod"},{"key":"7200_CR4","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.ajhg.2021.11.022","volume":"109","author":"C Tan","year":"2022","unstructured":"Tan C, Meng L, Lv M, He X, Sha Y, Tang D, et al. Bi-allelic variants in DNHD1 cause flagellar axoneme defects and asthenoteratozoospermia in humans and mice. Am J Hum Genet. 2022;109:157\u201371.","journal-title":"Am J Hum Genet"},{"key":"7200_CR5","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/j.ajhg.2021.01.002","volume":"108","author":"C Liu","year":"2021","unstructured":"Liu C, Tu C, Wang L, Wu H, Houston BJ, Mastrorosa FK, et al. Deleterious variants in X-linked CFAP47 induce asthenoteratozoospermia and primary male infertility. Am J Hum Genet. 2021;108:309\u201323.","journal-title":"Am J Hum Genet"},{"key":"7200_CR6","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1093\/humupd\/dmp048","volume":"16","author":"TG Cooper","year":"2010","unstructured":"Cooper TG, Noonan E, von Eckardstein S, Auger J, Baker HW, Behre HM, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16:231\u201345.","journal-title":"Hum Reprod Update"},{"key":"7200_CR7","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1136\/archdischild-2013-304831","volume":"99","author":"JS Lucas","year":"2014","unstructured":"Lucas JS, Burgess A, Mitchison HM, Moya E, Williamson M, Hogg C. Diagnosis and management of primary ciliary dyskinesia. Arch Dis Child. 2014;99:850\u20136.","journal-title":"Arch Dis Child"},{"key":"7200_CR8","doi-asserted-by":"publisher","first-page":"551","DOI":"10.5534\/wjmh.210119","volume":"40","author":"BJ Zhuang","year":"2022","unstructured":"Zhuang BJ, Xu SY, Dong L, Zhang PH, Zhuang BL, Huang XP, et al. Novel DNAH1 Mutation Loci Lead to Multiple Morphological Abnormalities of the Sperm Flagella and Literature Review. World J Mens Health. 2022;40:551\u201360.","journal-title":"World J Mens Health"},{"key":"7200_CR9","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1038\/s41585-018-0051-8","volume":"15","author":"SC Esteves","year":"2018","unstructured":"Esteves SC, Roque M, Bedoschi G, Haahr T, Humaidan P. Intracytoplasmic sperm injection for male infertility and consequences for offspring. Nat Rev Urol. 2018;15:535\u201362.","journal-title":"Nat Rev Urol"},{"key":"7200_CR10","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1007\/978-1-4614-4015-4_7","volume":"757","author":"DS Chu","year":"2013","unstructured":"Chu DS, Shakes DC. Spermatogenesis. Adv Exp Med Biol. 2013;757:171\u2013203.","journal-title":"Adv Exp Med Biol"},{"key":"7200_CR11","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1038\/nrg3462","volume":"14","author":"G Meister","year":"2013","unstructured":"Meister G. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 2013;14:447\u201359.","journal-title":"Nat Rev Genet"},{"key":"7200_CR12","doi-asserted-by":"publisher","first-page":"1090","DOI":"10.1016\/j.cell.2017.04.034","volume":"169","author":"LT Gou","year":"2017","unstructured":"Gou LT, Kang JY, Dai P, Wang X, Li F, Zhao S, et al. Ubiquitination-Deficient Mutations in Human Piwi Cause Male Infertility by Impairing Histone-to-Protamine Exchange during Spermiogenesis. Cell. 2017;169:1090\u20131104.e1013.","journal-title":"Cell"},{"key":"7200_CR13","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-08182-x","volume":"10","author":"Y Shen","year":"2019","unstructured":"Shen Y, Zhang F, Li F, Jiang X, Yang Y, Li X, et al. Loss-of-function mutations in QRICH2 cause male infertility with multiple morphological abnormalities of the sperm flagella. Nat Commun. 2019;10:433.","journal-title":"Nat Commun"},{"key":"7200_CR14","doi-asserted-by":"publisher","DOI":"10.1186\/s12915-022-01368-2","volume":"20","author":"K Nozawa","year":"2019","unstructured":"Nozawa K, Fujihara Y, Devlin DJ, Deras RE, Kent K, Larina IV, et al. The testis-specific E3 ubiquitin ligase RNF133 is required for fecundity in mice. BMC Biol. 2019;20:161.","journal-title":"BMC Biol"},{"key":"7200_CR15","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1038\/cr.2013.168","volume":"24","author":"Y Feng","year":"2014","unstructured":"Feng Y, He D, Yao Z, Klionsky DJ. The machinery of macroautophagy. Cell Res. 2014;24:24\u201341.","journal-title":"Cell Res"},{"key":"7200_CR16","doi-asserted-by":"publisher","first-page":"1865","DOI":"10.3390\/ijms18091865","volume":"18","author":"SR Yoshii","year":"2017","unstructured":"Yoshii SR, Mizushima N. Monitoring and Measuring Autophagy. Int J Mol Sci. 2017;18:1865.","journal-title":"Int J Mol Sci"},{"key":"7200_CR17","doi-asserted-by":"publisher","first-page":"2313","DOI":"10.1016\/j.devcel.2021.07.015","volume":"56","author":"Y Lei","year":"2021","unstructured":"Lei Y, Zhang X, Xu Q, Liu S, Li C, Jiang H, et al. Autophagic elimination of ribosomes during spermiogenesis provides energy for flagellar motility. Dev Cell. 2021;56:2313\u201328.e2317.","journal-title":"Dev Cell"},{"key":"7200_CR18","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1038\/ng.851","volume":"43","author":"LD Sun","year":"2011","unstructured":"Sun LD, Xiao FL, Li Y, Zhou WM, Tang HY, Tang XF, et al. Genome-wide association study identifies two new susceptibility loci for atopic dermatitis in the Chinese Han population. Nat Genet. 2011;43:690\u20134.","journal-title":"Nat Genet"},{"key":"7200_CR19","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.gene.2017.03.034","volume":"617","author":"YY Wu","year":"2017","unstructured":"Wu YY, Tang JP, Liu Q, Zheng XD, Fang L, Yin XY, et al. Scanning indels in the 5q22.1 region and identification of the TMEM232 susceptibility gene that is associated with atopic dermatitis in the Chinese Han population. Gene. 2017;617:17\u201323.","journal-title":"Gene"},{"key":"7200_CR20","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1093\/bjd\/ljad078","volume":"189","author":"J Han","year":"2023","unstructured":"Han J, Cai X, Qin S, Zhang Z, Wu Y, Shi Y, et al. TMEM232 promotes the inflammatory response in atopic dermatitis via the nuclear factor-\u043aB and signal transducer and activator of transcription 3 signalling pathways. Br J Dermatol. 2023;189:195\u2013209.","journal-title":"Br J Dermatol"},{"key":"7200_CR21","doi-asserted-by":"publisher","first-page":"1141","DOI":"10.1038\/s41422-018-0099-2","volume":"28","author":"J Guo","year":"2018","unstructured":"Guo J, Grow EJ, Mlcochova H, Maher GJ, Lindskog C, Nie X, et al. The adult human testis transcriptional cell atlas. Cell Res. 2018;28:1141\u201357.","journal-title":"Cell Res"},{"key":"7200_CR22","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2016.344","volume":"7","author":"SR Chen","year":"2016","unstructured":"Chen SR, Batool A, Wang YQ, Hao XX, Chang CS, Cheng CY, et al. The control of male fertility by spermatid-specific factors: searching for contraceptive targets from spermatozoon\u2019s head to tail. Cell Death Dis. 2016;7:e2472.","journal-title":"Cell Death Dis"},{"key":"7200_CR23","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1126\/science.aai8764","volume":"356","author":"Z Xu","year":"2017","unstructured":"Xu Z, Schaedel L, Portran D, Aguilar A, Gaillard J, Marinkovich MP, et al. Microtubules acquire resistance from mechanical breakage through intralumenal acetylation. Science. 2017;356:328\u201332.","journal-title":"Science"},{"key":"7200_CR24","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1091\/mbc.e13-07-0387","volume":"25","author":"SC Howes","year":"2014","unstructured":"Howes SC, Alushin GM, Shida T, Nachury MV, Nogales E. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol Biol Cell. 2014;25:257\u201366.","journal-title":"Mol Biol Cell"},{"key":"7200_CR25","doi-asserted-by":"publisher","first-page":"9688","DOI":"10.1074\/jbc.M511481200","volume":"281","author":"LG Korotchkina","year":"2006","unstructured":"Korotchkina LG, Sidhu S, Patel MS. Characterization of testis-specific isoenzyme of human pyruvate dehydrogenase. J Biol Chem. 2006;281:9688\u201396.","journal-title":"J Biol Chem"},{"key":"7200_CR26","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/path.2697","volume":"221","author":"D Glick","year":"2010","unstructured":"Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3\u201312.","journal-title":"J Pathol"},{"key":"7200_CR27","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1093\/molehr\/gar034","volume":"17","author":"K Inaba","year":"2011","unstructured":"Inaba K. Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod. 2011;17:524\u201338.","journal-title":"Mol Hum Reprod"},{"key":"7200_CR28","doi-asserted-by":"publisher","first-page":"R45","DOI":"10.1530\/REP-14-0498","volume":"150","author":"CB Lindemann","year":"2015","unstructured":"Lindemann CB, Lesich KA. The geometric clutch at 20: stripping gears or gaining traction? Reproduction. 2015;150:R45\u201353.","journal-title":"Reproduction"},{"key":"7200_CR29","doi-asserted-by":"publisher","first-page":"2897","DOI":"10.1016\/j.cell.2023.05.009","volume":"186","author":"L Zhou","year":"2023","unstructured":"Zhou L, Liu H, Liu S, Yang X, Dong Y, Pan Y, et al. Structures of sperm flagellar doublet microtubules expand the genetic spectrum of male infertility. Cell. 2023;186:2897\u2013910.e2819.","journal-title":"Cell"},{"key":"7200_CR30","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1038\/s41594-022-00770-2","volume":"29","author":"M Gui","year":"2022","unstructured":"Gui M, Wang X, Dutcher SK, Brown A, Zhang R. Ciliary central apparatus structure reveals mechanisms of microtubule patterning. Nat Struct Mol Biol. 2022;29:483\u201392.","journal-title":"Nat Struct Mol Biol"},{"key":"7200_CR31","doi-asserted-by":"publisher","DOI":"10.1093\/nsr\/nwad181","volume":"10","author":"M Wang","year":"2023","unstructured":"Wang M, Kang J, Shen Z, Hu Y, Chen M, Cui X, et al. CCDC189 affects sperm flagellum formation by interacting with CABCOCO1. Natl Sci Rev. 2023;10:nwad181.","journal-title":"Natl Sci Rev"},{"key":"7200_CR32","doi-asserted-by":"publisher","first-page":"e1008954","DOI":"10.1371\/journal.pgen.1008954","volume":"16","author":"S Oura","year":"2020","unstructured":"Oura S, Kazi S, Savolainen A, Nozawa K, Casta\u00f1eda J, Yu Z, et al. Cfap97d1 is important for flagellar axoneme maintenance and male mouse fertility. PLoS Genet. 2020;16:e1008954.","journal-title":"PLoS Genet"},{"key":"7200_CR33","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.74993","volume":"11","author":"KF Lechtreck","year":"2022","unstructured":"Lechtreck KF, Liu Y, Dai J, Alkhofash RA, Butler J, Alford L, et al. Chlamydomonas ARMC2\/PF27 is an obligate cargo adapter for intraflagellar transport of radial spokes. Elife. 2022;11:e74993.","journal-title":"Elife"},{"key":"7200_CR34","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/j.ajhg.2018.12.013","volume":"104","author":"C Coutton","year":"2019","unstructured":"Coutton C, Martinez G, Kherraf ZE, Amiri-Yekta A, Boguenet M, Saut A, et al. Bi-allelic Mutations in ARMC2 Lead to Severe Astheno-Teratozoospermia Due to Sperm Flagellum Malformations in Humans and Mice. Am J Hum Genet. 2019;104:331\u201340.","journal-title":"Am J Hum Genet"},{"key":"7200_CR35","doi-asserted-by":"publisher","DOI":"10.1242\/dev.199805","volume":"148","author":"S Liu","year":"2021","unstructured":"Liu S, Zhang J, Kherraf ZE, Sun S, Zhang X, Cazin C, et al. CFAP61 is required for sperm flagellum formation and male fertility in human and mouse. Development. 2021;148:dev199805.","journal-title":"Development"},{"key":"7200_CR36","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1016\/j.ajhg.2013.07.013","volume":"93","author":"E Kott","year":"2013","unstructured":"Kott E, Legendre M, Copin B, Papon JF, Dastot-Le Moal F, Montantin G, et al. Loss-of-function mutations in RSPH1 cause primary ciliary dyskinesia with central-complex and radial-spoke defects. Am J Hum Genet. 2013;93:561\u201370.","journal-title":"Am J Hum Genet"},{"key":"7200_CR37","doi-asserted-by":"publisher","DOI":"10.15252\/embj.2020107410","volume":"40","author":"MR Leung","year":"2021","unstructured":"Leung MR, Roelofs MC, Ravi RT, Maitan P, Henning H, Zhang M, et al. The multi-scale architecture of mammalian sperm flagella and implications for ciliary motility. EMBO J. 2021;40:e107410.","journal-title":"EMBO J"},{"key":"7200_CR38","doi-asserted-by":"publisher","first-page":"5791","DOI":"10.1016\/j.cell.2021.10.007","volume":"184","author":"M Gui","year":"2021","unstructured":"Gui M, Farley H, Anujan P, Anderson JR, Maxwell DW, Whitchurch JB, et al. De novo identification of mammalian ciliary motility proteins using cryo-EM. Cell. 2021;184:5791\u2013806.e5719.","journal-title":"Cell"},{"key":"7200_CR39","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1016\/j.cell.2019.09.030","volume":"179","author":"M Ma","year":"2019","unstructured":"Ma M, Stoyanova M, Rademacher G, Dutcher SK, Brown A, Zhang R. Structure of the Decorated Ciliary Doublet Microtubule. Cell. 2019;179:909\u201322.e912.","journal-title":"Cell"},{"key":"7200_CR40","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2207605119","volume":"119","author":"M Gui","year":"2022","unstructured":"Gui M, Croft JT, Zabeo D, Acharya V, Kollman JM, Burgoyne T, et al. SPACA9 is a lumenal protein of human ciliary singlet and doublet microtubules. Proc Natl Acad Sci USA. 2022;119:e2207605119.","journal-title":"Proc Natl Acad Sci USA"},{"key":"7200_CR41","doi-asserted-by":"publisher","first-page":"2880","DOI":"10.1016\/j.cell.2023.05.026","volume":"186","author":"MR Leung","year":"2023","unstructured":"Leung MR, Zeng J, Wang X, Roelofs MC, Huang W, Zenezini Chiozzi R, et al. Structural specializations of the sperm tail. Cell. 2023;186:2880\u201396.e2817.","journal-title":"Cell"},{"key":"7200_CR42","doi-asserted-by":"publisher","first-page":"BSR20202442","DOI":"10.1042\/BSR20202442","volume":"40","author":"V Chawan","year":"2020","unstructured":"Chawan V, Yevate S, Gajbhiye R, Kulkarni V, Parte P. Acetylation\/deacetylation and microtubule associated proteins influence flagellar axonemal stability and sperm motility. Biosci Rep. 2020;40:BSR20202442.","journal-title":"Biosci Rep"},{"key":"7200_CR43","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.aax2705","volume":"5","author":"A Even","year":"2019","unstructured":"Even A, Morelli G, Broix L, Scaramuzzino C, Turchetto S, Gladwyn-Ng I, et al. ATAT1-enriched vesicles promote microtubule acetylation via axonal transport. Sci Adv. 2019;5:eaax2705.","journal-title":"Sci Adv"},{"key":"7200_CR44","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1016\/j.devcel.2004.12.005","volume":"8","author":"M Ihara","year":"2005","unstructured":"Ihara M, Kinoshita A, Yamada S, Tanaka H, Tanigaki A, Kitano A, et al. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell. 2005;8:343\u201352.","journal-title":"Dev Cell"},{"key":"7200_CR45","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.devcel.2005.01.021","volume":"8","author":"H Kissel","year":"2005","unstructured":"Kissel H, Georgescu MM, Larisch S, Manova K, Hunnicutt GR, Steller H. The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell. 2005;8:353\u201364.","journal-title":"Dev Cell"},{"key":"7200_CR46","first-page":"923","volume":"128","author":"YC Kuo","year":"2015","unstructured":"Kuo YC, Shen YR, Chen HI, Lin YH, Wang YY, Chen YR, et al. SEPT12 orchestrates the formation of mammalian sperm annulus by organizing core octameric complexes with other SEPT proteins. J Cell Sci. 2015;128:923\u201334.","journal-title":"J Cell Sci"},{"key":"7200_CR47","doi-asserted-by":"publisher","first-page":"799","DOI":"10.1515\/BC.2011.074","volume":"392","author":"A Toure","year":"2011","unstructured":"Toure A, Rode B, Hunnicutt GR, Escalier D, Gacon G. Septins at the annulus of mammalian sperm. Biol Chem. 2011;392:799\u2013803.","journal-title":"Biol Chem"},{"key":"7200_CR48","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1186\/1471-213X-9-23","volume":"9","author":"J Guan","year":"2009","unstructured":"Guan J, Kinoshita M, Yuan L. Spatiotemporal association of DNAJB13 with the annulus during mouse sperm flagellum development. BMC Dev Biol. 2009;9:23.","journal-title":"BMC Dev Biol"},{"key":"7200_CR49","doi-asserted-by":"publisher","first-page":"R163","DOI":"10.1530\/REP-13-0178","volume":"146","author":"A Amaral","year":"2013","unstructured":"Amaral A, Louren\u00e7o B, Marques M, Ramalho-Santos J. Mitochondria functionality and sperm quality. Reproduction. 2013;146:R163\u201374.","journal-title":"Reproduction"},{"key":"7200_CR50","doi-asserted-by":"publisher","first-page":"251","DOI":"10.3109\/19396368.2014.915360","volume":"60","author":"M Tang","year":"2014","unstructured":"Tang M, Liu BJ, Wang SQ, Xu Y, Han P, Li PC, et al. The role of mitochondrial aconitate (ACO2) in human sperm motility. Syst Biol Reprod Med. 2014;60:251\u20136.","journal-title":"Syst Biol Reprod Med"},{"key":"7200_CR51","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1136\/jmedgenet-2021-108137","volume":"60","author":"W Liu","year":"2023","unstructured":"Liu W, Wei X, Liu X, Chen G, Zhang X, Liang X, et al. Biallelic mutations in ARMC12 cause asthenozoospermia and multiple midpiece defects in humans and mice. J Med Genet. 2023;60:154\u201362.","journal-title":"J Med Genet"},{"key":"7200_CR52","doi-asserted-by":"publisher","first-page":"1753","DOI":"10.1080\/15548627.2020.1783822","volume":"17","author":"Q Huang","year":"2021","unstructured":"Huang Q, Liu Y, Zhang S, Yap YT, Li W, Zhang D, et al. Autophagy core protein ATG5 is required for elongating spermatid development, sperm individualization and normal fertility in male mice. Autophagy. 2021;17:1753\u201367.","journal-title":"Autophagy"},{"key":"7200_CR53","doi-asserted-by":"publisher","DOI":"10.1038\/s41419-022-05116-w","volume":"13","author":"FR Bai","year":"2022","unstructured":"Bai FR, Wu QQ, Wu YJ, Hu YQ, Jiang ZX, Lv H, et al. Germline FOXJ2 overexpression causes male infertility via aberrant autophagy activation by LAMP2A upregulation. Cell Death Dis. 2022;13:665.","journal-title":"Cell Death Dis"},{"key":"7200_CR54","doi-asserted-by":"publisher","first-page":"e109372","DOI":"10.1371\/journal.pone.0109372","volume":"9","author":"S Traikov","year":"2014","unstructured":"Traikov S, Stange C, Wassmer T, Paul-Gilloteaux P, Salamero J, Raposo G, et al. Septin6 and Septin7 GTP Binding Proteins Regulate AP-3- and ESCRT-Dependent Multivesicular Body Biogenesis. PLoS One. 2014;9:e109372.","journal-title":"PLoS One"},{"key":"7200_CR55","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1038\/cdd.2008.168","volume":"16","author":"CM Fader","year":"2009","unstructured":"Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 2009;16:70\u20138.","journal-title":"Cell Death Differ"},{"key":"7200_CR56","doi-asserted-by":"publisher","first-page":"21883","DOI":"10.1074\/jbc.273.34.21883","volume":"273","author":"TO Berg","year":"1998","unstructured":"Berg TO, Fengsrud M, Str\u00f8mhaug PE, Berg T, Seglen PO. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem. 1998;273:21883\u201392.","journal-title":"J Biol Chem"},{"key":"7200_CR57","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"9","author":"B Langmead","year":"2012","unstructured":"Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357\u20139.","journal-title":"Nat Methods"},{"key":"7200_CR58","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/nbt.3122","volume":"33","author":"M Pertea","year":"2015","unstructured":"Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33:290\u20135.","journal-title":"Nat Biotechnol"},{"key":"7200_CR59","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","volume":"30","author":"Y Liao","year":"2014","unstructured":"Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923\u201330.","journal-title":"Bioinformatics"},{"key":"7200_CR60","doi-asserted-by":"publisher","first-page":"D605","DOI":"10.1093\/nar\/gkaa1074","volume":"49","author":"D Szklarczyk","year":"2021","unstructured":"Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene\/measurement sets. Nucleic Acids Res. 2021;49:D605\u201312.","journal-title":"Nucleic Acids Res"},{"key":"7200_CR61","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-019-1758-4","volume":"20","author":"D Otasek","year":"2019","unstructured":"Otasek D, Morris JH, Bou\u00e7as J, Pico AR, Demchak B. Cytoscape Automation: empowering workflow-based network analysis. Genome Biol. 2019;20:185.","journal-title":"Genome Biol"},{"key":"7200_CR62","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1093\/bioinformatics\/btp101","volume":"25","author":"G Bindea","year":"2009","unstructured":"Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091\u20133.","journal-title":"Bioinformatics"}],"container-title":["Cell Death &amp; Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07200-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07200-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07200-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,8]],"date-time":"2024-11-08T21:11:30Z","timestamp":1731100290000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07200-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,8]]},"references-count":62,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["7200"],"URL":"https:\/\/doi.org\/10.1038\/s41419-024-07200-9","relation":{},"ISSN":["2041-4889"],"issn-type":[{"value":"2041-4889","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,8]]},"assertion":[{"value":"29 January 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 October 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 October 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 November 2024","order":4,"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"}},{"value":"All animal experiments were approved by the Animal Experimentation Ethics Committee of Anhui Medical University (Animal Ethics Committee approval no. 20190403).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics"}}],"article-number":"806"}}