{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T18:21:40Z","timestamp":1791570100215,"version":"4.3.4"},"reference-count":73,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T00:00:00Z","timestamp":1775174400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32472978"],"award-info":[{"award-number":["32472978"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32472978"],"award-info":[{"award-number":["32472978"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004608","name":"Natural Science Foundation of Jiangsu Province","doi-asserted-by":"publisher","award":["BK20250131"],"award-info":[{"award-number":["BK20250131"]}],"id":[{"id":"10.13039\/501100004608","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Sexual reproduction is the predominant mode of reproduction in animals, and spermatogenesis is the fundamental step in this process. As the model organism for lepidopteran, the silkworm Bombyx mori exhibits typical dichotomous spermatogenesis, producing both nucleated (eupyrene) and anucleate (apyrene) sperm. Leucylaminopeptidases (LAPs), members of the M17 metalloprotease family, are characterized by their ability to cleave leucine residues from the N-terminus of peptides. In addition to this canonical function, they have been implicated in male fertility in mammals and Diptera. Nevertheless, whether LAPs are required for dimorphic spermatogenesis in Lepidoptera remains to be clarified. Here, we demonstrated that Sperm-Leucylaminopeptidase (S-LAP) plays vital roles in the silkworm eupyrene sperm development. Similar to the testis-specific expression pattern of eight S-LAPs in Drosophila melanogaster, BmS-LAP was also predominantly expressed in testis. Depletion of BmS-LAP via CRISPR\/Cas9 system resulted in male sterility, while the fertility of female mutant was unaffected. Notably, male mutants displayed severe defects in the formation and migration of eupyrene sperm, whereas apyrene sperm development appeared normal. In addition, RNA-seq and qRT-PCR analyses demonstrated that spermatogenesis defects were associated with energy metabolism and flagellar assembly. Our study provides the first evidence that LAP is necessary for dimorphic spermatogenesis in Lepidopteran, offering new insights into the molecular basis of male infertility.<\/jats:p>","DOI":"10.3390\/insects17040389","type":"journal-article","created":{"date-parts":[[2026,4,6]],"date-time":"2026-04-06T03:11:28Z","timestamp":1775445088000},"page":"389","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["The Development of Eupyrene Sperm Is Dependent on Sperm-Leucylaminopeptidase in Bombyx mori"],"prefix":"10.3390","volume":"17","author":[{"given":"Hongxia","family":"Kang","sequence":"first","affiliation":[{"name":"Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China"},{"name":"Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guan","family":"Man","sequence":"additional","affiliation":[{"name":"Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China"},{"name":"Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yutong","family":"Liu","sequence":"additional","affiliation":[{"name":"Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China"},{"name":"Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anjiang","family":"Tan","sequence":"additional","affiliation":[{"name":"Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China"},{"name":"Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2199-297X","authenticated-orcid":false,"given":"Kai","family":"Chen","sequence":"additional","affiliation":[{"name":"Jiangsu Key Laboratory of Sericultural and Animal Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang 212100, China"},{"name":"Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Scientific Research Center, Chinese Academy of Agricultural Sciences, Zhenjiang 212100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,4,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1038\/nrg3294","article-title":"Genetics of germ cell development","volume":"13","author":"Lesch","year":"2012","journal-title":"Nat. Rev. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e2520991123","DOI":"10.1073\/pnas.2520991123","article-title":"Programmed meiotic errors facilitate dichotomous sperm production in the silkworm, Bombyx mori","volume":"123","author":"Benner","year":"2026","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1093\/molehr\/gan002","article-title":"Identification and characterization of novel mammalian spermatogenic genes conserved from fly to human","volume":"14","author":"Bonilla","year":"2008","journal-title":"Mol. Hum. Reprod."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e24376","DOI":"10.4161\/spmg.24376","article-title":"Protamines and spermatogenesis in Drosophila and Homo sapiens: A comparative analysis","volume":"3","author":"Kanippayoor","year":"2013","journal-title":"Spermatogenesis"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Fairchild, M.J., Islam, F., and Tanentzapf, G. (2017). Identification of genetic networks that act in the somatic cells of the testis to mediate the developmental program of spermatogenesis. PLoS Genet., 13.","DOI":"10.1371\/journal.pgen.1007026"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/jmor.1051930102","article-title":"The spermatophore and its structural changes with time in the bursa copulatrix of the silkworm, Bombyx mori","volume":"193","author":"Osanai","year":"1987","journal-title":"J. Morphol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"10412","DOI":"10.1073\/pnas.1820101116","article-title":"Dimorphic sperm formation by Sex-lethal","volume":"116","author":"Sakai","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1038\/s41421-020-00194-6","article-title":"Dysfunction of dimorphic sperm impairs male fertility in the silkworm","volume":"6","author":"Chen","year":"2020","journal-title":"Cell Discov."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.ibmb.2019.03.012","article-title":"Maelstrom regulates spermatogenesis of the silkworm, Bombyx mori","volume":"109","author":"Chen","year":"2019","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.ibmb.2017.05.007","article-title":"Deletion of the Bombyx mori odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms","volume":"86","author":"Liu","year":"2017","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"11659","DOI":"10.1074\/jbc.M117.777797","article-title":"The FOXO transcription factor controls insect growth and development by regulating juvenile hormone degradation in the silkworm, Bombyx mori","volume":"292","author":"Zeng","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Xu, J., Chen, S., Zeng, B., James, A.A., Tan, A., and Huang, Y. (2017). Bombyx mori P-element Somatic Inhibitor (BmPSI) Is a Key Auxiliary Factor for Silkworm Male Sex Determination. PLoS Genet., 13.","DOI":"10.1371\/journal.pgen.1006576"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/978-1-0716-3016-7_27","article-title":"Genome Editing of Silkworms","volume":"2637","author":"Tsubota","year":"2023","journal-title":"Methods Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e2306322120","DOI":"10.1073\/pnas.2306322120","article-title":"Engineering a complex, multiple enzyme-mediated synthesis of natural plant pigments in the silkworm, Bombyx mori","volume":"120","author":"Chen","year":"2023","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1038\/s41467-023-44444-z","article-title":"Leucine aminopeptidase1 controls egg deposition and hatchability in male Aedes aegypti mosquitoes","volume":"15","author":"Sun","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Zhang, Z., Liu, X., Hu, B., Chen, K., Yu, Y., Sun, C., Zhu, D., Bai, H., Palli, S.R., and Tan, A. (2024). The mechanoreceptor Piezo is required for spermatogenesis in Bombyx mori. BMC Biol., 22.","DOI":"10.1186\/s12915-024-01916-y"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1111\/imb.12988","article-title":"Depletion of Gtsf1L impairs development of eupyrene sperm and ovary in Bombyx mori","volume":"34","author":"Chen","year":"2025","journal-title":"Insect Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1002\/jmor.1051380104","article-title":"The fate of the normal-anucleated spermatozoa in inseminated females of the silkworm Bombyx mori","volume":"138","author":"Gitay","year":"1972","journal-title":"J. Morphol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1002\/1097-4687(200011)246:2<53::AID-JMOR1>3.0.CO;2-P","article-title":"Peristaltic squeezing of sperm bundles at the late stage of spermatogenesis in the silkworm, Bombyx mori","volume":"246","author":"Kawamura","year":"2000","journal-title":"J. Morphol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1046\/j.1440-169X.1997.t01-5-00007.x","article-title":"Behaviors of nucleus, basal bodies and microtubules during eupyrene and apyrene spermiogenesis in the silkworm, Bombyx mori (Lepidoptera)","volume":"39","author":"Yamashiki","year":"1997","journal-title":"Dev. Growth Differ."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/jmor.10168","article-title":"Roles of actin networks in peristaltic squeezing of sperm bundles in Bombyx mori","volume":"259","author":"Sahara","year":"2004","journal-title":"J. Morphol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Chen, K., Yu, Y., Yang, D., Yang, X., Tang, L., Liu, Y., Luo, X., Walter, J.R., Liu, Z., and Jun, X. (2020). Gtsf1 is essential for proper female sex determination and transposon silencing in the silkworm, Bombyx mori. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1009194"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.1515\/BC.2006.191","article-title":"Leucine aminopeptidases: Diversity in structure and function","volume":"387","author":"Matsui","year":"2006","journal-title":"Biol. Chem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.biochi.2019.01.007","article-title":"M17 aminopeptidases diversify function by moderating their macromolecular assemblies and active site environment","volume":"166","author":"Drinkwater","year":"2019","journal-title":"Biochimie"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Liu, J., and Cui, T. (2023). Expression, Characterisation, Homology Modelling and Molecular Docking of a Novel M17 Family Leucyl-Aminopeptidase from Bacillus cereus CZ. Int. J. Mol. Sci., 24.","DOI":"10.20944\/preprints202309.2178.v1"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1096\/fasebj.7.2.8440407","article-title":"Aminopeptidases: Structure and function","volume":"7","author":"Taylor","year":"1993","journal-title":"FASEB J."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5006","DOI":"10.1073\/pnas.90.11.5006","article-title":"Differentiation and identification of the two catalytic metal binding sites in bovine lens leucine aminopeptidase by x-ray crystallography","volume":"90","author":"Kim","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"14792","DOI":"10.1021\/bi00045a021","article-title":"Two-metal ion mechanism of bovine lens leucine aminopeptidase: Active site solvent structure and binding mode of L-leucinal, a gem-diolate transition state analogue, by X-ray crystallography","volume":"34","author":"Lipscomb","year":"1995","journal-title":"Biochemistry"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1111\/j.1574-6976.1996.tb00247.x","article-title":"Bacterial aminopeptidases: Properties and functions","volume":"18","author":"Gonzales","year":"1996","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1630","DOI":"10.1046\/j.1432-1327.2002.02795.x","article-title":"Identification of residues critical for activity of the wound-induced leucine aminopeptidase (LAP-A) of tomato","volume":"269","author":"Gu","year":"2002","journal-title":"Eur. J. Biochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e23745","DOI":"10.1002\/mrd.23745","article-title":"Proteomic diversification of spermatostyles among six species of whirligig beetles","volume":"91","author":"Gomez","year":"2024","journal-title":"Mol. Reprod. Dev."},{"key":"ref_32","first-page":"139","article-title":"Seminal plasma leucine aminopeptidase in male fertility","volume":"17","author":"Navajo","year":"1985","journal-title":"Andrologia"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Laurinyecz, B., Vedelek, V., Kov\u00e1cs, A.L., Szilasi, K., Lipinszki, Z., Slez\u00e1k, C., Darula, Z., Juh\u00e1sz, G., and Sinka, R. (2019). Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm. PLoS Genet., 15.","DOI":"10.1371\/journal.pgen.1007987"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1440","DOI":"10.1038\/ng1915","article-title":"Genomic and functional evolution of the Drosophila melanogaster sperm proteome","volume":"38","author":"Dorus","year":"2006","journal-title":"Nat. Genet."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2171","DOI":"10.1016\/j.jprot.2010.09.002","article-title":"The Drosophila melanogaster sperm proteome-II (DmSP-II)","volume":"73","author":"Wasbrough","year":"2010","journal-title":"J. Proteom."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Whittington, E., Forsythe, D., Borziak, K., Karr, T.L., Walters, J.R., and Dorus, S. (2017). Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera. BMC Genom., 18.","DOI":"10.1186\/s12864-017-4293-2"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1002\/pmic.200701020","article-title":"The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS\/MS identification","volume":"8","author":"Baker","year":"2008","journal-title":"Proteomics"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Skerget, S., Rosenow, M.A., Petritis, K., and Karr, T.L. (2015). Sperm Proteome Maturation in the Mouse Epididymis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0140650"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1838","DOI":"10.1093\/gbe\/evz080","article-title":"Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs","volume":"11","author":"Whittington","year":"2019","journal-title":"Genome Biol Evol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"100281","DOI":"10.1016\/j.mcpro.2022.100281","article-title":"Functional Diversity and Evolution of the Drosophila Sperm Proteome","volume":"21","author":"Garlovsky","year":"2022","journal-title":"Mol. Cell. Proteom."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1083\/jcb.44.2.243","article-title":"Insect sperm: Their structure and morphogenesis","volume":"44","author":"Phillips","year":"1970","journal-title":"J. Cell Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"20907","DOI":"10.1038\/s41598-020-77683-x","article-title":"Destination of apyrene sperm following migration from the bursa copulatrix in the monandrous swallowtail butterfly Byasa alcinous","volume":"10","author":"Konagaya","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"16308","DOI":"10.1074\/jbc.M112.400978","article-title":"Heat shock protein 90 functions to stabilize and activate the testis-specific serine\/threonine kinases, a family of kinases essential for male fertility","volume":"288","author":"Jha","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s11934-019-0911-7","article-title":"Sperm Morphology: History, Challenges, and Impact on Natural and Assisted Fertility","volume":"20","author":"Danis","year":"2019","journal-title":"Curr. Urol. Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0022-5320(73)80055-3","article-title":"The mitochondrial derivative of the spermatozoon of Drosophila before and after fertilization","volume":"44","author":"Perotti","year":"1973","journal-title":"J. Ultrastruct. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/S0022-5320(75)80089-X","article-title":"Dynamics of spermiogenesis in Drosophila melanogaster. VI. Significance of \u201conion\u201d nebenkern formation","volume":"53","author":"Tokuyasu","year":"1975","journal-title":"J. Ultrastruct. Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1111\/1744-7917.13096","article-title":"Spindle-E is essential for gametogenesis in the silkworm, Bombyx mori","volume":"30","author":"Chen","year":"2023","journal-title":"Insect Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"103906","DOI":"10.1016\/j.ibmb.2022.103906","article-title":"The morphogen Hedgehog is essential for proper adult morphogenesis in Bombyx mori","volume":"153","author":"Chen","year":"2023","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1038\/nature09715","article-title":"The developmental transcriptome of Drosophila melanogaster","volume":"471","author":"Graveley","year":"2011","journal-title":"Nature"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1016\/S0022-1910(97)00044-9","article-title":"Control of the eupyrene\u2014Apyrene sperm dimorphism in Lepidoptera","volume":"43","year":"1997","journal-title":"J. Insect Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Seth, R.K., Yadav, P., and Reynolds, S.E. (2023). Dichotomous sperm in Lepidopteran insects: A biorational target for pest management. Front. Insect Sci., 3.","DOI":"10.3389\/finsc.2023.1198252"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Yang, X., Chen, D., Zheng, S., Yi, M., Wang, S., Liu, Y., Jing, L., Liu, Z., Yang, D., and Liu, Y. (2023). The Prmt5-Vasa module is essential for spermatogenesis in Bombyx mori. PLoS Genet., 19.","DOI":"10.1371\/journal.pgen.1010600"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"103874","DOI":"10.1016\/j.ibmb.2022.103874","article-title":"BmHen1 is essential for eupyrene sperm development in Bombyx mori but PIWI proteins are not","volume":"151","author":"Yang","year":"2022","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1007\/978-3-031-82990-1_17","article-title":"Intraflagellar Transport (IFT) and Sperm Formation","volume":"1469","author":"Liu","year":"2025","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1002\/dvdy.22563","article-title":"GMAP210 and IFT88 are present in the spermatid golgi apparatus and participate in the development of the acrosome-acroplaxome complex, head-tail coupling apparatus and tail","volume":"240","author":"Kierszenbaum","year":"2011","journal-title":"Dev. Dyn."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3705","DOI":"10.1091\/mbc.e16-05-0318","article-title":"Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice","volume":"27","author":"Zhang","year":"2016","journal-title":"Mol. Biol. Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.ydbio.2017.09.023","article-title":"Intraflagellar transporter protein (IFT27), an IFT25 binding partner, is essential for male fertility and spermiogenesis in mice","volume":"432","author":"Zhang","year":"2017","journal-title":"Dev. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"18408","DOI":"10.1074\/jbc.M111.309500","article-title":"Plant leucine aminopeptidases moonlight as molecular chaperones to alleviate stress-induced damage","volume":"287","author":"Scranton","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/0003-2697(85)90421-X","article-title":"Purification, preliminary characterization, and immunological comparison of hog lens leucine aminopeptidase (EC 3.4.11.1) with hog kidney and beef lens aminopeptidases","volume":"146","author":"Oettgen","year":"1985","journal-title":"Anal. Biochem."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Dorus, S., Wilkin, E.C., and Karr, T.L. (2011). Expansion and functional diversification of a leucyl aminopeptidase family that encodes the major protein constituents of Drosophila sperm. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-177"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1111\/imb.12921","article-title":"GASZ is indispensable for gametogenesis in the silkworm, Bombyx mori","volume":"33","author":"Guo","year":"2024","journal-title":"Insect Mol. Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"104714","DOI":"10.1016\/j.dci.2023.104714","article-title":"Characterization of the pro-inflammatory roles of the goldfish (Carassius auratus L.) M17 protein","volume":"145","author":"Gouife","year":"2023","journal-title":"Dev. Comp. Immunol."},{"key":"ref_63","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 (BBA) Gene Regul. Mech."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Shimada, Y., Kanazawa-Takino, N., and Nishimura, H. (2023). Spermiogenesis in Caenorhabditis elegans: An Excellent Model to Explore the Molecular Basis for Sperm Activation. Biomolecules, 13.","DOI":"10.3390\/biom13040657"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"dev202838","DOI":"10.1242\/dev.202838","article-title":"Development of functional spermatozoa in mammalian spermiogenesis","volume":"151","author":"Miyata","year":"2024","journal-title":"Development"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"7342","DOI":"10.1002\/anie.200501023","article-title":"Protein posttranslational modifications: The chemistry of proteome diversifications","volume":"44","author":"Walsh","year":"2005","journal-title":"Angew. Chem. Int. Ed."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1038\/s41392-024-01886-1","article-title":"Glycosylation: Mechanisms, biological functions and clinical implications","volume":"9","author":"He","year":"2024","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_68","first-page":"195","article-title":"Intraflagellar transport is essential for spermiogenesis","volume":"25","author":"Zhang","year":"2019","journal-title":"Zhonghua Nan Ke Xue"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"e920","DOI":"10.1002\/mgg3.920","article-title":"Novel IFT140 variants cause spermatogenic dysfunction in humans","volume":"7","author":"Wang","year":"2019","journal-title":"Mol. Genet. Genom. Med."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1530\/REP-17-0789","article-title":"Murine germ cell-specific disruption of Ift172 causes defects in spermiogenesis and male fertility","volume":"159","author":"Zhang","year":"2020","journal-title":"Reproduction"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1007\/s00018-025-05710-z","article-title":"Role of intraflagellar transport protein IFT140 in the formation and function of motile cilia in mammals","volume":"82","author":"Yap","year":"2025","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"113273","DOI":"10.1016\/j.yexcr.2022.113273","article-title":"The intraflagellar transport protein IFT52 associated with short-rib thoracic dysplasia is essential for ciliary function in osteogenic differentiation in vitro and for sensory perception in Drosophila","volume":"418","author":"Guleria","year":"2022","journal-title":"Exp. Cell Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1111\/1744-7917.13140","article-title":"IFT52 plays an essential role in sensory cilia formation and neuronal sensory function in Drosophila","volume":"30","author":"Hou","year":"2023","journal-title":"Insect Sci."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/4\/389\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,6]],"date-time":"2026-04-06T03:30:12Z","timestamp":1775446212000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/4\/389"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,3]]},"references-count":73,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2026,4]]}},"alternative-id":["insects17040389"],"URL":"https:\/\/doi.org\/10.3390\/insects17040389","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,3]]}}}