{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T13:54:30Z","timestamp":1793973270905,"version":"4.8.0"},"reference-count":81,"publisher":"Springer Science and Business Media LLC","issue":"7941","license":[{"start":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T00:00:00Z","timestamp":1670976000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T00:00:00Z","timestamp":1670976000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2022,12,22]]},"DOI":"10.1038\/s41586-022-05508-0","type":"journal-article","created":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T17:02:52Z","timestamp":1671037372000},"page":"725-731","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":133,"title":["A male germ-cell-specific ribosome controls male fertility"],"prefix":"10.1038","volume":"612","author":[{"given":"Huiling","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4970-8080","authenticated-orcid":false,"given":"Yangao","family":"Huo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liping","family":"Yao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7043-5438","authenticated-orcid":false,"given":"Hao","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiqiang","family":"Cui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huijuan","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenxiu","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dejiu","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yue","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shu","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haixia","family":"Tu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiwei","family":"Cheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yueshuai","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xintao","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunfei","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0475-5705","authenticated-orcid":false,"given":"Xuejiang","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3660-0636","authenticated-orcid":false,"given":"Yan","family":"Qin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahao","family":"Sha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,12,14]]},"reference":[{"key":"5508_CR1","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1016\/j.molcel.2018.07.018","volume":"71","author":"NR Genuth","year":"2018","unstructured":"Genuth, N. R. & Barna, M. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. Mol. Cell 71, 364\u2013374 (2018).","journal-title":"Mol. Cell"},{"key":"5508_CR2","doi-asserted-by":"publisher","first-page":"1954","DOI":"10.1093\/nar\/gkz1183","volume":"48","author":"MM Ghulam","year":"2020","unstructured":"Ghulam, M. M., Catala, M. & Abou Elela, S. Differential expression of duplicated ribosomal protein genes modifies ribosome composition in response to stress. Nucleic Acids Res. 48, 1954\u20131968 (2020).","journal-title":"Nucleic Acids Res."},{"key":"5508_CR3","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1016\/j.stem.2018.08.007","volume":"23","author":"M Wang","year":"2018","unstructured":"Wang, M. et al. Single-cell RNA sequencing analysis reveals sequential cell fate transition during human spermatogenesis. Cell Stem Cell 23, 599\u2013614 (2018).","journal-title":"Cell Stem Cell"},{"key":"5508_CR4","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/j.molcel.2017.05.021","volume":"67","author":"Z Shi","year":"2017","unstructured":"Shi, Z. et al. Heterogeneous ribosomes preferentially translate distinct subpools of mRNAs genome-wide. Mol. Cell 67, 71\u201383 (2017).","journal-title":"Mol. Cell"},{"key":"5508_CR5","doi-asserted-by":"publisher","first-page":"1004","DOI":"10.1261\/rna.043653.113","volume":"20","author":"V Gupta","year":"2014","unstructured":"Gupta, V. & Warner, J. R. Ribosome-omics of the human ribosome. RNA 20, 1004\u20131013 (2014).","journal-title":"RNA"},{"key":"5508_CR6","doi-asserted-by":"publisher","first-page":"1894","DOI":"10.1002\/jcp.25294","volume":"231","author":"T Chaillou","year":"2016","unstructured":"Chaillou, T., Zhang, X. & McCarthy, J. J. Expression of muscle-specific ribosomal protein L3-like impairs myotube growth. J. Cell. Physiol. 231, 1894\u2013902 (2016).","journal-title":"J. Cell. Physiol."},{"key":"5508_CR7","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1089\/nat.2020.0928","volume":"31","author":"BR Kao","year":"2021","unstructured":"Kao, B. R. et al. Knockdown of muscle-specific ribosomal protein L3-like enhances muscle function in healthy and dystrophic mice. Nucleic Acid Ther. 31, 457\u2013464 (2021).","journal-title":"Nucleic Acid Ther."},{"key":"5508_CR8","doi-asserted-by":"publisher","first-page":"e1003708","DOI":"10.1371\/journal.pgen.1003708","volume":"9","author":"MN O'Leary","year":"2013","unstructured":"O\u2019Leary, M. N. et al. The ribosomal protein Rpl22 controls ribosome composition by directly repressing expression of its own paralog, Rpl22l1. PLoS Genet. 9, e1003708 (2013).","journal-title":"PLoS Genet."},{"key":"5508_CR9","doi-asserted-by":"publisher","first-page":"e0222392","DOI":"10.1371\/journal.pone.0222392","volume":"14","author":"S Rao","year":"2019","unstructured":"Rao, S. et al. RPL22L1 induction in colorectal cancer is associated with poor prognosis and 5-FU resistance. PLoS ONE 14, e0222392 (2019).","journal-title":"PLoS ONE"},{"key":"5508_CR10","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.cell.2011.03.028","volume":"145","author":"N Kondrashov","year":"2011","unstructured":"Kondrashov, N. et al. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145, 383\u2013397 (2011).","journal-title":"Cell"},{"key":"5508_CR11","doi-asserted-by":"publisher","first-page":"1051","DOI":"10.1016\/j.cell.2017.05.022","volume":"169","author":"D Simsek","year":"2017","unstructured":"Simsek, D. et al. The mammalian ribo-interactome reveals ribosome functional diversity and heterogeneity. Cell 169, 1051\u20131065 (2017).","journal-title":"Cell"},{"key":"5508_CR12","doi-asserted-by":"publisher","first-page":"865","DOI":"10.1016\/j.celrep.2015.09.056","volume":"13","author":"N Slavov","year":"2015","unstructured":"Slavov, N., Semrau, S., Airoldi, E., Budnik, B. & van Oudenaarden, A. Differential stoichiometry among core ribosomal proteins. Cell Rep. 13, 865\u2013873 (2015).","journal-title":"Cell Rep."},{"key":"5508_CR13","doi-asserted-by":"publisher","first-page":"1498","DOI":"10.1016\/j.cub.2017.04.017","volume":"27","author":"L Jiang","year":"2017","unstructured":"Jiang, L. et al. RPL10L is required for male meiotic division by compensating for RPL10 during meiotic sex chromosome inactivation in mice. Curr. Biol. 27, 1498\u20131505 (2017).","journal-title":"Curr. Biol."},{"key":"5508_CR14","doi-asserted-by":"publisher","first-page":"1725","DOI":"10.1261\/rna.046649.114","volume":"20","author":"M Gamalinda","year":"2014","unstructured":"Gamalinda, M. & Woolford Jr, J. L. Deletion of L4 domains reveals insights into the importance of ribosomal protein extensions in eukaryotic ribosome assembly. RNA 20, 1725\u20131731 (2014).","journal-title":"RNA"},{"key":"5508_CR15","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1038\/nature12104","volume":"497","author":"AM Anger","year":"2013","unstructured":"Anger, A. M. et al. Structures of the human and Drosophila 80S ribosome. Nature 497, 80\u201385 (2013).","journal-title":"Nature"},{"key":"5508_CR16","doi-asserted-by":"crossref","first-page":"4379","DOI":"10.1242\/jcs.193151","volume":"129","author":"SA Young","year":"2016","unstructured":"Young, S. A. et al. CABYR is essential for fibrous sheath integrity and progressive motility in mouse spermatozoa. J. Cell Sci. 129, 4379\u20134387 (2016).","journal-title":"J. Cell Sci."},{"key":"5508_CR17","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s00418-018-1668-7","volume":"150","author":"K Yang","year":"2018","unstructured":"Yang, K., Adham, I. M., Meinhardt, A. & Hoyer-Fender, S. Ultra-structure of the sperm head-to-tail linkage complex in the absence of the spermatid-specific LINC component SPAG4. Histochem. Cell Biol. 150, 49\u201359 (2018).","journal-title":"Histochem. Cell Biol."},{"key":"5508_CR18","doi-asserted-by":"publisher","first-page":"e28199","DOI":"10.7554\/eLife.28199","volume":"6","author":"Y Shang","year":"2017","unstructured":"Shang, Y. et al. Essential role for SUN5 in anchoring sperm head to the tail. eLife 6, e28199 (2017).","journal-title":"eLife"},{"key":"5508_CR19","doi-asserted-by":"publisher","first-page":"E430","DOI":"10.1073\/pnas.1424648112","volume":"112","author":"S Yuan","year":"2015","unstructured":"Yuan, S. et al. Spata6 is required for normal assembly of the sperm connecting piece and tight head-tail conjunction. Proc. Natl Acad. Sci. USA 112, E430\u2013E439 (2015).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5508_CR20","doi-asserted-by":"publisher","first-page":"e1009020","DOI":"10.1371\/journal.pgen.1009020","volume":"16","author":"YY Wang","year":"2020","unstructured":"Wang, Y. Y. et al. Deficiency of the Tbc1d21 gene causes male infertility with morphological abnormalities of the sperm mitochondria and flagellum in mice. PLoS Genet. 16, e1009020 (2020).","journal-title":"PLoS Genet."},{"key":"5508_CR21","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1002\/1873-3468.12504","volume":"591","author":"JA Farias-Rico","year":"2017","unstructured":"Farias-Rico, J. A., Goetz, S. K., Marino, J. & von Heijne, G. Mutational analysis of protein folding inside the ribosome exit tunnel. FEBS Lett. 591, 155\u2013163 (2017).","journal-title":"FEBS Lett."},{"key":"5508_CR22","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1038\/nsmb.1614","volume":"16","author":"G Kramer","year":"2009","unstructured":"Kramer, G., Boehringer, D., Ban, N. & Bukau, B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589\u2013597 (2009).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"5508_CR23","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1146\/annurev-biochem-062917-012226","volume":"89","author":"AME Cassaignau","year":"2020","unstructured":"Cassaignau, A. M. E., Cabrita, L. D. & Christodoulou, J. How does the ribosome fold the proteome. Annu. Rev. Biochem. 89, 389\u2013415 (2020).","journal-title":"Annu. Rev. Biochem."},{"key":"5508_CR24","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1146\/annurev-biochem-060815-014334","volume":"85","author":"M Ott","year":"2016","unstructured":"Ott, M., Amunts, A. & Brown, A. Organization and regulation of mitochondrial protein synthesis. Annu. Rev. Biochem. 85, 77\u2013101 (2016).","journal-title":"Annu. Rev. Biochem."},{"key":"5508_CR25","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1038\/nsmb.1756","volume":"17","author":"S Bhushan","year":"2010","unstructured":"Bhushan, S. et al. \u03b1-Helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 17, 313\u2013317 (2010).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"5508_CR26","doi-asserted-by":"publisher","first-page":"aac4354","DOI":"10.1126\/science.aac4354","volume":"353","author":"D Balchin","year":"2016","unstructured":"Balchin, D., Hayer-Hartl, M. & Hartl, F. U. In vivo aspects of protein folding and quality control. Science 353, aac4354 (2016).","journal-title":"Science"},{"key":"5508_CR27","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-04520-z","volume":"7","author":"B Li","year":"2017","unstructured":"Li, B. et al. A comprehensive mouse transcriptomic BodyMap across 17 tissues by RNA-seq. Sci. Rep. 7, 4200 (2017).","journal-title":"Sci. Rep."},{"key":"5508_CR28","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1093\/biolre\/ioaa018","volume":"102","author":"D Wang","year":"2020","unstructured":"Wang, D. et al. LYPD4, mouse homolog of a human acrosome protein, is essential for sperm fertilizing ability and male fertility. Biol. Reprod. 102, 1033\u20131044 (2020).","journal-title":"Biol. Reprod."},{"key":"5508_CR29","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/j.molcel.2019.06.041","volume":"75","author":"E Mordret","year":"2019","unstructured":"Mordret, E. et al. Systematic detection of amino acid substitutions in proteomes reveals mechanistic basis of ribosome errors and selection for translation fidelity. Mol. Cell 75, 427\u2013441 (2019).","journal-title":"Mol. Cell"},{"key":"5508_CR30","doi-asserted-by":"publisher","first-page":"103396","DOI":"10.1016\/j.isci.2021.103396","volume":"24","author":"Q Zou","year":"2021","unstructured":"Zou, Q. et al. Proteostasis regulated by testis-specific ribosomal protein RPL39L maintains mouse spermatogenesis. iScience 24, 103396 (2021).","journal-title":"iScience"},{"key":"5508_CR31","doi-asserted-by":"publisher","first-page":"16549","DOI":"10.1073\/pnas.0801795105","volume":"105","author":"PM Petrone","year":"2008","unstructured":"Petrone, P. M., Snow, C. D., Lucent, D. & Pande, V. S. et al. Side-chain recognition and gating in the ribosome exit tunnel. Proc. Natl Acad. Sci. USA 105, 16549\u201316554 (2008).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5508_CR32","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.jmb.2008.08.089","volume":"384","author":"J Lu","year":"2008","unstructured":"Lu, J. & Deutsch, C. Electrostatics in the ribosomal tunnel modulate chain elongation rates. J. Mol. Biol. 384, 73\u201386 (2008).","journal-title":"J. Mol. Biol."},{"key":"5508_CR33","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","volume":"596","author":"J Jumper","year":"2021","unstructured":"Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583\u2013589 (2021).","journal-title":"Nature"},{"key":"5508_CR34","doi-asserted-by":"publisher","first-page":"D439","DOI":"10.1093\/nar\/gkab1061","volume":"50","author":"M Varadi","year":"2022","unstructured":"Varadi, M. et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 50, D439\u2013D444 (2022).","journal-title":"Nucleic Acids Res."},{"key":"5508_CR35","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/j.molcel.2016.01.008","volume":"61","author":"F Buhr","year":"2016","unstructured":"Buhr, F. et al. Synonymous codons direct cotranslational folding toward different protein conformations. Mol. Cell 61, 341\u2013351 (2016).","journal-title":"Mol. Cell"},{"key":"5508_CR36","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1038\/nrc1669","volume":"5","author":"AJ Simpson","year":"2005","unstructured":"Simpson, A. J., Caballero, O. L., Jungbluth, A., Chen, Y. T. & Old, L. J. Cancer\/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 5, 615\u2013625 (2005).","journal-title":"Nat. Rev. Cancer"},{"key":"5508_CR37","doi-asserted-by":"publisher","first-page":"1141","DOI":"10.1016\/j.cmet.2019.08.021","volume":"30","author":"S Chen","year":"2019","unstructured":"Chen, S. et al. Trimethylamine N-oxide binds and activates PERK to promote metabolic dysfunction. Cell Metab. 30, 1141\u20131151 (2019).","journal-title":"Cell Metab."},{"key":"5508_CR38","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1126\/science.1209038","volume":"334","author":"P Walter","year":"2011","unstructured":"Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081\u20131086 (2011).","journal-title":"Science"},{"key":"5508_CR39","doi-asserted-by":"crossref","unstructured":"Pallares, I. & Ventura, S. Understanding and predicting protein misfolding and aggregation: insights from proteomics. Proteomics 16, 2570\u20132581 (2016).","DOI":"10.1002\/pmic.201500529"},{"key":"5508_CR40","doi-asserted-by":"publisher","first-page":"1460","DOI":"10.1021\/bi901896b","volume":"49","author":"R Piatek","year":"2010","unstructured":"Piatek, R., Bruzdziak, P., Wojciechowski, M., Zalewska-Piatek, B. & Kur, J. The noncanonical disulfide bond as the important stabilizing element of the immunoglobulin fold of the Dr Fimbrial DraE subunit. Biochemistry 49, 1460\u20131468 (2010).","journal-title":"Biochemistry"},{"key":"5508_CR41","doi-asserted-by":"publisher","first-page":"e1000712","DOI":"10.1371\/journal.pgen.1000712","volume":"5","author":"K Tokuhiro","year":"2009","unstructured":"Tokuhiro, K. et al. OAZ-t\/OAZ3 is essential for rigid connection of sperm tails to heads in mouse. PLoS Genet. 5, e1000712 (2009).","journal-title":"PLoS Genet."},{"key":"5508_CR42","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1146\/annurev.genet.39.073003.114725","volume":"39","author":"EV Koonin","year":"2005","unstructured":"Koonin, E. V. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39, 309\u2013338 (2005).","journal-title":"Annu. Rev. Genet."},{"key":"5508_CR43","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1016\/j.cell.2007.08.037","volume":"131","author":"S Komili","year":"2007","unstructured":"Komili, S., Farny, N. G., Roth, F. P. & Silver, P. A. Functional specificity among ribosomal proteins regulates gene expression. Cell 131, 557\u2013571 (2007).","journal-title":"Cell"},{"key":"5508_CR44","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1016\/j.tig.2018.08.004","volume":"34","author":"JE Gerst","year":"2018","unstructured":"Gerst, J. E. Pimp my ribosome: ribosomal protein paralogs specify translational control. Trends Genet. 34, 832\u2013845 (2018).","journal-title":"Trends Genet."},{"key":"5508_CR45","doi-asserted-by":"publisher","first-page":"22567","DOI":"10.1073\/pnas.1912060116","volume":"116","author":"S Amirbeigiarab","year":"2019","unstructured":"Amirbeigiarab, S. et al. Invariable stoichiometry of ribosomal proteins in mouse brain tissues with aging. Proc. Natl Acad. Sci. USA 116, 22567\u201322572 (2019).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5508_CR46","doi-asserted-by":"publisher","first-page":"e55474","DOI":"10.7554\/eLife.55474","volume":"9","author":"VD Rinaldi","year":"2020","unstructured":"Rinaldi, V. D. et al. An atlas of cell types in the mouse epididymis and vas deferens. eLife 9, e55474 (2020).","journal-title":"eLife"},{"key":"5508_CR47","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1101\/gad.367606","volume":"20","author":"Y Gur","year":"2006","unstructured":"Gur, Y. & Breitbart, H. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 20, 411\u2013416 (2006).","journal-title":"Genes Dev."},{"key":"5508_CR48","doi-asserted-by":"publisher","unstructured":"Bryant, J. M., Meyer-Ficca, M. L., Dang, V. M., Berger, S. L. & Meyer, R. G. Separation of spermatogenic cell types using STA-PUT velocity sedimentation. J. Vis. Exp. https:\/\/doi.org\/10.3791\/50648 (2013).","DOI":"10.3791\/50648"},{"key":"5508_CR49","doi-asserted-by":"publisher","first-page":"2911","DOI":"10.1093\/hmg\/ddi322","volume":"14","author":"JP Wang","year":"2005","unstructured":"Wang, J. P., Page, D. C. & McCarrey, J. R. Differential expression of sex-linked and autosomal germ-cell-specific genes during spermatogenesis in the mouse. Hum. Mol. Genet. 14, 2911\u20132918 (2005).","journal-title":"Hum. Mol. Genet."},{"key":"5508_CR50","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1002\/pmic.200900726","volume":"11","author":"X Guo","year":"2011","unstructured":"Guo, X. et al. Proteomic analysis of male 4C germ cell proteins involved in mouse meiosis. Proteomics 11, 298\u2013308 (2011).","journal-title":"Proteomics"},{"key":"5508_CR51","doi-asserted-by":"publisher","first-page":"974","DOI":"10.3390\/genes10120974","volume":"10","author":"W Zheng","year":"2019","unstructured":"Zheng, W. et al. DDB1 regulates sertoli cell proliferation and testis cord remodeling by TGF\u03b2 pathway. Genes 10, 974 (2019).","journal-title":"Genes"},{"key":"5508_CR52","first-page":"11755","volume":"47","author":"R Hua","year":"2019","unstructured":"Hua, R. et al. FBXO47 regulates telomere-inner nuclear envelope integration by stabilizing TRF2 during meiosis. Nucleic Acids Res. 47, 11755\u201311770 (2019).","journal-title":"Nucleic Acids Res."},{"key":"5508_CR53","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/978-1-60761-103-5_25","volume":"558","author":"SK Mahadevaiah","year":"2009","unstructured":"Mahadevaiah, S. K., Costa, Y. & Turner, J. M. Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol. Biol. 558, 433\u2013444 (2009).","journal-title":"Methods Mol. Biol."},{"key":"5508_CR54","doi-asserted-by":"publisher","first-page":"1104","DOI":"10.1074\/mcp.M114.045468","volume":"14","author":"J Wang","year":"2015","unstructured":"Wang, J. et al. Quantitative phosphoproteomics analysis reveals a key role of insulin growth factor 1 receptor (IGF1R) tyrosine kinase in human sperm capacitation. Mol. Cell Proteom. 14, 1104\u20131112 (2015).","journal-title":"Mol. Cell Proteom."},{"key":"5508_CR55","doi-asserted-by":"publisher","first-page":"1554","DOI":"10.1161\/CIRCULATIONAHA.119.040747","volume":"141","author":"Y Fan","year":"2020","unstructured":"Fan, Y. et al. Phosphoproteomic analysis of neonatal regenerative myocardium revealed important roles of checkpoint kinase 1 via activating mammalian target of rapamycin C1\/ribosomal protein S6 kinase b-1 pathway. Circulation 141, 1554\u20131569 (2020).","journal-title":"Circulation"},{"key":"5508_CR56","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.jprot.2013.02.008","volume":"82","author":"P Hao","year":"2013","unstructured":"Hao, P., Ren, Y., Dutta, B. & Sze, S. K. Comparative evaluation of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) and high-pH reversed phase (Hp-RP) chromatography in profiling of rat kidney proteome. J. Proteom. 82, 254\u2013262 (2013).","journal-title":"J. Proteom."},{"key":"5508_CR57","doi-asserted-by":"publisher","first-page":"2301","DOI":"10.1038\/nprot.2016.136","volume":"11","author":"S Tyanova","year":"2016","unstructured":"Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301\u20132319 (2016).","journal-title":"Nat. Protoc."},{"key":"5508_CR58","doi-asserted-by":"publisher","first-page":"2847","DOI":"10.1093\/bioinformatics\/btw313","volume":"32","author":"Z Gu","year":"2016","unstructured":"Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847\u20132849 (2016).","journal-title":"Bioinformatics"},{"key":"5508_CR59","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1089\/omi.2011.0118","volume":"16","author":"G Yu","year":"2012","unstructured":"Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16, 284\u2013287 (2012).","journal-title":"OMICS"},{"key":"5508_CR60","doi-asserted-by":"publisher","first-page":"1475","DOI":"10.1074\/mcp.O112.020131","volume":"11","author":"AC Peterson","year":"2012","unstructured":"Peterson, A. C., Russell, J. D., Bailey, D. J., Westphall, M. S. & Coon, J. J. Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol. Cell. Proteom. 11, 1475\u20131488 (2012).","journal-title":"Mol. Cell. Proteom."},{"key":"5508_CR61","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1038\/nmeth.4193","volume":"14","author":"SQ Zheng","year":"2017","unstructured":"Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331\u2013332 (2017).","journal-title":"Nat. Methods"},{"key":"5508_CR62","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1016\/j.jsb.2015.08.008","volume":"192","author":"A Rohou","year":"2015","unstructured":"Rohou, A. & N G, CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216\u2013221 (2015).","journal-title":"J. Struct. Biol."},{"key":"5508_CR63","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1107\/S2059798316019276","volume":"73","author":"R Fernandez-Leiro","year":"2017","unstructured":"Fernandez-Leiro, R. & Scheres, S. H. W. A pipeline approach to single-particle processing in RELION. Acta Crystallogr. D 73, 496\u2013502 (2017).","journal-title":"Acta Crystallogr. D"},{"key":"5508_CR64","doi-asserted-by":"publisher","first-page":"e42166","DOI":"10.7554\/eLife.42166","volume":"7","author":"J Zivanov","year":"2018","unstructured":"Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018).","journal-title":"eLife"},{"key":"5508_CR65","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1016\/j.jmb.2003.07.013","volume":"333","author":"PB Rosenthal","year":"2003","unstructured":"Rosenthal, P. B. & Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721\u2013745 (2003).","journal-title":"J. Mol. Biol."},{"key":"5508_CR66","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1038\/nmeth.2727","volume":"11","author":"A Kucukelbir","year":"2014","unstructured":"Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63\u201365 (2014).","journal-title":"Nat. Methods"},{"key":"5508_CR67","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1107\/S0907444910007493","volume":"66","author":"P Emsley","year":"2010","unstructured":"Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486\u2013501 (2010).","journal-title":"Acta Crystallogr. D"},{"key":"5508_CR68","doi-asserted-by":"publisher","first-page":"472","DOI":"10.1038\/nature24482","volume":"551","author":"SK Natchiar","year":"2017","unstructured":"Natchiar, S. K., Myasnikov, A. G., Kratzat, H., Hazemann, I. & Klaholz, B. P. Visualization of chemical modifications in the human 80S ribosome structure. Nature 551, 472\u2013477 (2017).","journal-title":"Nature"},{"key":"5508_CR69","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1107\/S2059798319011471","volume":"75","author":"D Liebschner","year":"2019","unstructured":"Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D 75, 861\u2013877 (2019).","journal-title":"Acta Crystallogr. D"},{"key":"5508_CR70","doi-asserted-by":"publisher","first-page":"3211","DOI":"10.1093\/bioinformatics\/bts611","volume":"28","author":"E Kopylova","year":"2012","unstructured":"Kopylova, E., Noe, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211\u20133217 (2012).","journal-title":"Bioinformatics"},{"key":"5508_CR71","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","volume":"12","author":"D Kim","year":"2015","unstructured":"Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357\u2013360 (2015).","journal-title":"Nat. Methods"},{"key":"5508_CR72","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","volume":"30","author":"Y Liao","year":"2014","unstructured":"Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923\u2013930 (2014).","journal-title":"Bioinformatics"},{"key":"5508_CR73","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).","journal-title":"Genome Biol."},{"key":"5508_CR74","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2010","unstructured":"Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139\u2013140 (2010).","journal-title":"Bioinformatics"},{"key":"5508_CR75","doi-asserted-by":"publisher","first-page":"781","DOI":"10.3390\/insects11110781","volume":"11","author":"S Tokumoto","year":"2020","unstructured":"Tokumoto, S. et al. Development of a Tet-on inducible expression system for the anhydrobiotic cell line, Pv11. Insects 11, 781 (2020).","journal-title":"Insects"},{"key":"5508_CR76","doi-asserted-by":"publisher","first-page":"2153","DOI":"10.1101\/gad.268722.115","volume":"29","author":"WX Hao Zeng","year":"2015","unstructured":"Hao Zeng, W. X. Ctr9, a key subunit of PAFc, affects global estrogen signaling and drives ER\u03b1-positive breast tumorigenesis. Genes Dev. 29, 2153\u20132167 (2015).","journal-title":"Genes Dev."},{"key":"5508_CR77","doi-asserted-by":"publisher","first-page":"1435","DOI":"10.1080\/15548627.2018.1474314","volume":"14","author":"M Mauthe","year":"2018","unstructured":"Mauthe, M. et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy 14, 1435\u20131455 (2018).","journal-title":"Autophagy"},{"key":"5508_CR78","doi-asserted-by":"crossref","unstructured":"Go, Y. M. & Jones, D. P. Thioredoxin redox western analysis. Curr. Protoc. Toxicol. 41, 17.12.1\u201317.12.12 (2009).","DOI":"10.1002\/0471140856.tx1712s41"},{"key":"5508_CR79","doi-asserted-by":"publisher","first-page":"11248","DOI":"10.1021\/bi0491898","volume":"43","author":"M Manning","year":"2004","unstructured":"Manning, M. & Col\u00f3n, W. Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure. Biochemistry 43, 11248\u201311254 (2004).","journal-title":"Biochemistry"},{"key":"5508_CR80","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1128\/IAI.73.1.135-145.2005","volume":"73","author":"R Piatek","year":"2005","unstructured":"Piatek, R. et al. Molecular aspects of biogenesis of Escherichia coli Dr Fimbriae: characterization of DraB-DraE complexes. Infect. Immun. 73, 135\u2013145 (2005).","journal-title":"Infect. Immun."},{"key":"5508_CR81","doi-asserted-by":"crossref","unstructured":"Hu, M. L. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol. 233, 380\u2013385 (1994).","DOI":"10.1016\/S0076-6879(94)33044-1"}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41586-022-05508-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-022-05508-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-022-05508-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,10]],"date-time":"2024-10-10T10:37:37Z","timestamp":1728556657000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41586-022-05508-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,14]]},"references-count":81,"journal-issue":{"issue":"7941","published-print":{"date-parts":[[2022,12,22]]}},"alternative-id":["5508"],"URL":"https:\/\/doi.org\/10.1038\/s41586-022-05508-0","relation":{},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,14]]},"assertion":[{"value":"6 September 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 November 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 December 2022","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"}}]}}