{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T03:09:00Z","timestamp":1777432140822,"version":"3.51.4"},"reference-count":78,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:00:00Z","timestamp":1682380800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Hedwig Stalter Foundation"},{"name":"Saarland University Research Prize"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Sperm motility is a prerequisite for achieving pregnancy, and alterations in sperm motility, along with sperm count and morphology, are commonly observed in subfertile men. The aim of the study was to determine whether the expression level of genes annotated with the Gene Ontology (GO) term \u2018sperm motility\u2019 differed in sperm collected from healthy men and men diagnosed with oligoasthenozoospermia. Reverse transcription quantitative real-time PCR (RT-qPCR), quantitative mass spectrometry (LC-MS\/MS), and enrichment analyses were used to validate a set of 132 genes in 198 men present at an infertility clinic. Out of the 132 studied sperm-motility-associated genes, 114 showed differentially expressed levels in oligoasthenozoospermic men compared to those of normozoospermic controls using an RT-qPCR analysis. Of these, 94 genes showed a significantly lower expression level, and 20 genes showed a significantly higher expression level. An MS analysis of sperm from an independent cohort of healthy and subfertile men identified 692 differentially expressed proteins, of which 512 were significantly lower and 180 were significantly higher in oligoasthenozoospermic men compared to those of the normozoospermic controls. Of the 58 gene products quantified with both techniques, 48 (82.75%) showed concordant regulation. Besides the sperm-motility-associated proteins, the unbiased proteomics approach uncovered several novel proteins whose expression levels were specifically altered in abnormal sperm samples. Among these deregulated proteins, there was a clear overrepresentation of annotation terms related to sperm integrity, the cytoskeleton, and energy-related metabolism, as well as human phenotypes related to spermatogenesis and sperm-related abnormalities. These findings suggest that many of these proteins may serve as diagnostic markers of male infertility. Our study reveals an extended number of sperm-motility-associated genes with altered expression levels in the sperm of men with oligoasthenozoospermia. These genes and\/or proteins can be used in the future for better assessments of male factor infertility.<\/jats:p>","DOI":"10.3390\/cells12091239","type":"journal-article","created":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T05:12:53Z","timestamp":1682399573000},"page":"1239","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Sperm Motility Annotated Genes: Are They Associated with Impaired Fecundity?"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9048-4958","authenticated-orcid":false,"given":"Masood","family":"Abu-Halima","sequence":"first","affiliation":[{"name":"Institute of Human Genetics, Saarland University, 66421 Homburg, Germany"},{"name":"Department of Pediatric Cardiology, Saarland University Medical Center, 66421 Homburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3347-9447","authenticated-orcid":false,"given":"Lea Simone","family":"Becker","sequence":"additional","affiliation":[{"name":"Institute of Human Genetics, Saarland University, 66421 Homburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8262-6247","authenticated-orcid":false,"given":"Mohammad A.","family":"Al Smadi","sequence":"additional","affiliation":[{"name":"Reproductive Endocrinology and IVF Unit, King Hussein Medical Centre, Amman 11733, Jordan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hashim","family":"Abdul-Khaliq","sequence":"additional","affiliation":[{"name":"Department of Pediatric Cardiology, Saarland University Medical Center, 66421 Homburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Markus","family":"Raeschle","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, TU Kaiserslautern, 67653 Kaiserslautern, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eckart","family":"Meese","sequence":"additional","affiliation":[{"name":"Institute of Human Genetics, Saarland University, 66421 Homburg, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1186\/s12958-015-0032-1","article-title":"A unique view on male infertility around the globe","volume":"13","author":"Agarwal","year":"2015","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1093\/humrep\/deab099","article-title":"Exome sequencing reveals variants in known and novel candidate genes for severe sperm motility disorders","volume":"36","author":"Oud","year":"2021","journal-title":"Hum. Reprod."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1093\/humrep\/dez022","article-title":"A systematic review and standardized clinical validity assessment of male infertility genes","volume":"34","author":"Oud","year":"2019","journal-title":"Hum. Reprod."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1034951","DOI":"10.3389\/fgene.2022.1034951","article-title":"Clinical detection, diagnosis and treatment of morphological abnormalities of sperm flagella: A review of literature","volume":"13","author":"Wang","year":"2022","journal-title":"Front. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1080\/01485010390219656","article-title":"Asthenozoospermia: Analysis of a large population","volume":"49","author":"Curi","year":"2003","journal-title":"Arch. Androl."},{"key":"ref_6","unstructured":"World Health Organization (2010). WHO Laboratory Manual for the Examination and Processing of Human Semen, WHO. [5th ed.]."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3645","DOI":"10.1038\/s41598-023-30744-3","article-title":"Expression of SPAG7 and its regulatory microRNAs in seminal plasma and seminal plasma-derived extracellular vesicles of patients with subfertility","volume":"13","author":"Becker","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1111\/andr.13004","article-title":"MicroRNA-targeting in spermatogenesis: Over-expressions of microRNA-23a\/b-3p and its affected targeting of the genes ODF2 and UBQLN3 in spermatozoa of patients with oligoasthenozoospermia","volume":"9","author":"Belkacemi","year":"2021","journal-title":"Andrology"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Manfrevola, F., Ferraro, B., Sellitto, C., Rocco, D., Fasano, S., Pierantoni, R., and Chianese, R. (2021). CRISP2, CATSPER1 and PATE1 Expression in Human Asthenozoospermic Semen. Cells, 10.","DOI":"10.3390\/cells10081956"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Silva, C., Viana, P., Barros, A., Sa, R., Sousa, M., and Pereira, R. (2022). Further Insights on RNA Expression and Sperm Motility. Genes, 13.","DOI":"10.3390\/genes13071291"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1016\/j.fertnstert.2019.12.028","article-title":"MicroRNAs in combined spent culture media and sperm are associated with embryo quality and pregnancy outcome","volume":"113","author":"Khaizaran","year":"2020","journal-title":"Fertil. Steril."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1038\/s41422-018-0099-2","article-title":"The adult human testis transcriptional cell atlas","volume":"28","author":"Guo","year":"2018","journal-title":"Cell Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1016\/j.celrep.2018.10.026","article-title":"The Mammalian Spermatogenesis Single-Cell Transcriptome, from Spermatogonial Stem Cells to Spermatids","volume":"25","author":"Hermann","year":"2018","journal-title":"Cell Rep."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1016\/j.fertnstert.2012.11.054","article-title":"Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments","volume":"99","author":"Hammadeh","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1093\/bioinformatics\/btn615","article-title":"AmiGO: Online access to ontology and annotation data","volume":"25","author":"Carbon","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"W305","DOI":"10.1093\/nar\/gkp427","article-title":"ToppGene Suite for gene list enrichment analysis and candidate gene prioritization","volume":"37","author":"Chen","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"973849","DOI":"10.3389\/fcell.2022.973849","article-title":"MicroRNA-targeting in male infertility: Sperm microRNA-19a\/b-3p and its spermatogenesis related transcripts content in men with oligoasthenozoospermia","volume":"10","author":"Becker","year":"2022","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/nmeth.1322","article-title":"Universal sample preparation method for proteome analysis","volume":"6","author":"Wisniewski","year":"2009","journal-title":"Nat. Methods"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1896","DOI":"10.1038\/nprot.2007.261","article-title":"Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips","volume":"2","author":"Rappsilber","year":"2007","journal-title":"Nat. Protoc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1074\/mcp.M113.031591","article-title":"Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ","volume":"13","author":"Cox","year":"2014","journal-title":"Mol. Cell. Proteom."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/nmeth.3901","article-title":"The Perseus computational platform for comprehensive analysis of (prote)omics data","volume":"13","author":"Tyanova","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Becker, L.S., Al Smadi, M.A., Raeschle, M., Rishik, S., Abdul-Khaliq, H., Meese, E., and Abu-Halima, M. (2023). Proteomic Landscape of Human Sperm in Patients with Different Spermatogenic Impairments. Cells, 12.","DOI":"10.3390\/cells12071017"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e13586","DOI":"10.1111\/and.13586","article-title":"Role of genetics and epigenetics in male infertility","volume":"53","author":"Gunes","year":"2021","journal-title":"Andrologia"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1002\/jemt.10320","article-title":"Fibrous sheath of mammalian spermatozoa","volume":"61","author":"Eddy","year":"2003","journal-title":"Microsc. Res. Tech."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1093\/hmg\/ddab234","article-title":"Loss-of-function missense variant of AKAP4 induced male infertility through reduced interaction with QRICH2 during sperm flagella development","volume":"31","author":"Zhang","year":"2021","journal-title":"Hum. Mol. Genet."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1002\/mrd.23442","article-title":"Downregulation of gene expression and the outcome of ICSI in severe oligozoospermic patients: A preliminary study","volume":"87","author":"Patrylak","year":"2020","journal-title":"Mol. Reprod. Dev."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1038\/s41467-017-02792-7","article-title":"Mutations in CFAP43 and CFAP44 cause male infertility and flagellum defects in Trypanosoma and human","volume":"9","author":"Coutton","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.ajhg.2018.03.007","article-title":"Absence of CFAP69 Causes Male Infertility due to Multiple Morphological Abnormalities of the Flagella in Human and Mouse","volume":"102","author":"Dong","year":"2018","journal-title":"Am. J. Hum. Genet."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1038\/s41467-018-08182-x","article-title":"Loss-of-function mutations in QRICH2 cause male infertility with multiple morphological abnormalities of the sperm flagella","volume":"10","author":"Shen","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1016\/j.ajhg.2017.04.012","article-title":"Biallelic Mutations in CFAP43 and CFAP44 Cause Male Infertility with Multiple Morphological Abnormalities of the Sperm Flagella","volume":"100","author":"Tang","year":"2017","journal-title":"Am. J. Hum. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1038\/ng.726","article-title":"CCDC39 is required for assembly of inner dynein arms and the dynein regulatory complex and for normal ciliary motility in humans and dogs","volume":"43","author":"Merveille","year":"2011","journal-title":"Nat. Genet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"236","DOI":"10.4103\/aja.aja_53_19","article-title":"Insight on multiple morphological abnormalities of sperm flagella in male infertility: What is new?","volume":"22","author":"Wang","year":"2020","journal-title":"Asian J. Androl."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"605237","DOI":"10.3389\/fendo.2020.605237","article-title":"Male Infertility Diagnosis: Improvement of Genetic Analysis Performance by the Introduction of Pre-Diagnostic Genes in a Next-Generation Sequencing Custom-Made Panel","volume":"11","author":"Precone","year":"2020","journal-title":"Front. Endocrinol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"4","DOI":"10.23736\/S2724-6507.21.03477-1","article-title":"A simultaneous next-generation sequencing approach to the diagnosis of couple infertility","volume":"47","author":"Precone","year":"2022","journal-title":"Minerva Endocrinol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1093\/humrep\/dey264","article-title":"Whole-exome sequencing identifies mutations in FSIP2 as a recurrent cause of multiple morphological abnormalities of the sperm flagella","volume":"33","author":"Martinez","year":"2018","journal-title":"Hum. Reprod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1007\/s00439-021-02313-z","article-title":"Bi-allelic truncating variants in CFAP206 cause male infertility in human and mouse","volume":"140","author":"Shen","year":"2021","journal-title":"Hum. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1111\/cge.13644","article-title":"A novel homozygous CFAP65 mutation in humans causes male infertility with multiple morphological abnormalities of the sperm flagella","volume":"96","author":"Zhang","year":"2019","journal-title":"Clin. Genet."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2240","DOI":"10.1093\/hmg\/ddab185","article-title":"CFAP65 is required in the acrosome biogenesis and mitochondrial sheath assembly during spermiogenesis","volume":"30","author":"Wang","year":"2021","journal-title":"Hum. Mol. Genet."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"145536","DOI":"10.1016\/j.gene.2021.145536","article-title":"Novel mutations in FSIP2 lead to multiple morphological abnormalities of the sperm flagella and poor ICSI prognosis","volume":"781","author":"Liu","year":"2021","journal-title":"Gene"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"7539","DOI":"10.1038\/s41598-020-64434-1","article-title":"Alterations in seminal plasma proteomic profile in men with primary and secondary infertility","volume":"10","author":"Martins","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1136\/jmedgenet-2019-106011","article-title":"Homozygous mutations in SPEF2 induce multiple morphological abnormalities of the sperm flagella and male infertility","volume":"57","author":"Liu","year":"2020","journal-title":"J. Med. Genet."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1136\/jmedgenet-2018-105952","article-title":"Loss-of-function mutations in SPEF2 cause multiple morphological abnormalities of the sperm flagella (MMAF)","volume":"56","author":"Liu","year":"2019","journal-title":"J. Med. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/s00439-020-02110-0","article-title":"Novel mutations in SPEF2 causing different defects between flagella and cilia bridge: The phenotypic link between MMAF and PCD","volume":"139","author":"Tu","year":"2020","journal-title":"Hum. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/j.ajhg.2018.07.013","article-title":"Loss of Calmodulin- and Radial-Spoke-Associated Complex Protein CFAP251 Leads to Immotile Spermatozoa Lacking Mitochondria and Infertility in Men","volume":"103","author":"Auguste","year":"2018","journal-title":"Am. J. Hum. Genet."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/j.ajhg.2018.07.014","article-title":"A Homozygous Ancestral SVA-Insertion-Mediated Deletion in WDR66 Induces Multiple Morphological Abnormalities of the Sperm Flagellum and Male Infertility","volume":"103","author":"Kherraf","year":"2018","journal-title":"Am. J. Hum. Genet."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1002\/mrd.20025","article-title":"Tektin3 encodes an evolutionarily conserved putative testicular microtubules-related protein expressed preferentially in male germ cells","volume":"67","author":"Roy","year":"2004","journal-title":"Mol. Reprod. Dev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1016\/S1357-2725(01)00089-9","article-title":"Cloning and characterization of a novel human TEKTIN1 gene","volume":"33","author":"Xu","year":"2001","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1093\/humrep\/dem400","article-title":"A possible association of a human tektin-t gene mutation (A229V) with isolated non-syndromic asthenozoospermia: Case report","volume":"23","author":"Zuccarello","year":"2008","journal-title":"Hum. Reprod."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s10735-019-09817-z","article-title":"Distribution of sperm antigen 6 (SPAG6) and 16 (SPAG16) in mouse ciliated and non-ciliated tissues","volume":"50","author":"Alciaturi","year":"2019","journal-title":"J. Mol. Histol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1186\/s12958-022-00916-3","article-title":"Homozygous SPAG6 variants can induce nonsyndromic asthenoteratozoospermia with severe MMAF","volume":"20","author":"Xu","year":"2022","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1093\/biolre\/ioaa217","article-title":"The sperm-specific form of lactate dehydrogenase is required for fertility and is an attractive target for male contraception (a review)","volume":"104","author":"Goldberg","year":"2021","journal-title":"Biol. Reprod."},{"key":"ref_52","first-page":"2471","article-title":"Aberrant expression of spermspecific glycolytic enzymes are associated with poor sperm quality","volume":"19","author":"Liu","year":"2019","journal-title":"Mol. Med. Rep."},{"key":"ref_53","first-page":"273","article-title":"Characteristics of testis-specific phosphoglycerate kinase 2 and its association with human sperm quality","volume":"31","author":"Liu","year":"2016","journal-title":"Hum. Reprod."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1016\/j.ajhg.2013.03.016","article-title":"Missense mutations in SLC26A8, encoding a sperm-specific activator of CFTR, are associated with human asthenozoospermia","volume":"92","author":"Dirami","year":"2013","journal-title":"Am. J. Hum. Genet."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"14246","DOI":"10.1074\/jbc.M111802200","article-title":"Functional characterization of three novel tissue-specific anion exchangers SLC26A7, -A8, and -A9","volume":"277","author":"Lohi","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1002\/humu.24322","article-title":"Novel biallelic mutations in SLC26A8 cause severe asthenozoospermia in humans owing to midpiece defects: Insights into a putative dominant genetic disease","volume":"43","author":"Gao","year":"2022","journal-title":"Hum. Mutat."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2040","DOI":"10.1111\/jcmm.16116","article-title":"PRSS55 plays an important role in the structural differentiation and energy metabolism of sperm and is required for male fertility in mice","volume":"25","author":"Zhu","year":"2021","journal-title":"J. Cell. Mol. Med."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1111\/andr.12528","article-title":"Among seven testis-specific molecular markers, SPEM1 appears to have a significant clinical value for prediction of sperm retrieval in azoospermic men","volume":"6","author":"Hashemi","year":"2018","journal-title":"Andrology"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"212ra160","DOI":"10.1126\/scitranslmed.3006260","article-title":"Differential diagnosis of azoospermia with proteomic biomarkers ECM1 and TEX101 quantified in seminal plasma","volume":"5","author":"Drabovich","year":"2013","journal-title":"Sci. Transl. Med."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Korbakis, D., Schiza, C., Brinc, D., Soosaipillai, A., Karakosta, T.D., Legare, C., Sullivan, R., Mullen, B., Jarvi, K., and Diamandis, E.P. (2017). Preclinical evaluation of a TEX101 protein ELISA test for the differential diagnosis of male infertility. BMC Med., 15.","DOI":"10.1186\/s12916-017-0817-5"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"652809","DOI":"10.3389\/fcell.2021.652809","article-title":"Comparative Proteomics and Phosphoproteomics Analysis Reveal the Possible Breed Difference in Yorkshire and Duroc Boar Spermatozoa","volume":"9","author":"Xu","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2584","DOI":"10.1038\/s41598-022-06476-1","article-title":"Using publicly available transcriptomic data to identify mechanistic and diagnostic biomarkers in azoospermia and overall male infertility","volume":"12","author":"Omolaoye","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1038\/nrm2407","article-title":"The septin family of GTPases: Architecture and dynamics","volume":"9","author":"Weirich","year":"2008","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1002\/humu.22028","article-title":"SEPT12 mutations cause male infertility with defective sperm annulus","volume":"33","author":"Kuo","year":"2012","journal-title":"Hum. Mutat."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1093\/humrep\/deab229","article-title":"Whole-exome sequencing of a cohort of infertile men reveals novel causative genes in teratozoospermia that are chiefly related to sperm head defects","volume":"37","author":"Li","year":"2021","journal-title":"Hum. Reprod."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1007\/s10815-020-01747-0","article-title":"Development of a novel next-generation sequencing panel for diagnosis of quantitative spermatogenic impairment","volume":"37","author":"Rocca","year":"2020","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1857","DOI":"10.2353\/ajpath.2009.080955","article-title":"The expression level of septin12 is critical for spermiogenesis","volume":"174","author":"Lin","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1111\/and.12466","article-title":"Cadmium inhibits motility, activities of plasma membrane Ca(2+)-ATPase and axonemal dynein-ATPase of human spermatozoa","volume":"48","author":"Botana","year":"2016","journal-title":"Andrologia"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1002\/mrd.20383","article-title":"The human Na,K-ATPase alpha 4 isoform is a ouabain-sensitive alpha isoform that is expressed in sperm","volume":"73","author":"Hlivko","year":"2006","journal-title":"Mol. Reprod. Dev."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1093\/molehr\/gal062","article-title":"The Na,K-ATPase alpha4 isoform from humans has distinct enzymatic properties and is important for sperm motility","volume":"12","author":"Sanchez","year":"2006","journal-title":"Mol. Hum. Reprod."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"88","DOI":"10.4103\/aja.aja_17_19","article-title":"Reduced semen quality in patients with testicular cancer seminoma is associated with alterations in the expression of sperm proteins","volume":"22","author":"Dias","year":"2020","journal-title":"Asian J. Androl."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1111\/andr.12620","article-title":"A quantitative global proteomics approach to understanding the functional pathways dysregulated in the spermatozoa of asthenozoospermic testicular cancer patients","volume":"7","author":"Agarwal","year":"2019","journal-title":"Andrology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1093\/humupd\/dmz032","article-title":"Human sperm ion channel (dys)function: Implications for fertilization","volume":"25","author":"Brown","year":"2019","journal-title":"Hum. Reprod. Update"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2822","DOI":"10.7150\/thno.51869","article-title":"Roles of CatSper channels in the pathogenesis of asthenozoospermia and the therapeutic effects of acupuncture-like treatment on asthenozoospermia","volume":"11","author":"Jin","year":"2021","journal-title":"Theranostics"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1073\/pnas.0610286104","article-title":"All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility","volume":"104","author":"Qi","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Li, R.K., Tan, J.L., Chen, L.T., Feng, J.S., Liang, W.X., Guo, X.J., Liu, P., Chen, Z., Sha, J.H., and Wang, Y.F. (2014). Iqcg is essential for sperm flagellum formation in mice. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0098053"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1095\/biolreprod.102.004838","article-title":"Developmental expression of spermatid-specific thioredoxin-1 protein: Transient association to the longitudinal columns of the fibrous sheath during sperm tail formation","volume":"67","author":"Yu","year":"2002","journal-title":"Biol. Reprod."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"13064","DOI":"10.1038\/s41598-021-92603-3","article-title":"TXNDC2 joint molecular marker is associated with testis pathology and is an accurate predictor of sperm retrieval","volume":"11","author":"Javadirad","year":"2021","journal-title":"Sci. Rep."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/9\/1239\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:23:01Z","timestamp":1760124181000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/9\/1239"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,25]]},"references-count":78,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["cells12091239"],"URL":"https:\/\/doi.org\/10.3390\/cells12091239","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,25]]}}}