{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T06:56:38Z","timestamp":1782888998550,"version":"3.54.5"},"reference-count":83,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,6,11]],"date-time":"2024-06-11T00:00:00Z","timestamp":1718064000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,6,11]],"date-time":"2024-06-11T00:00:00Z","timestamp":1718064000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Amol University of Special Modern Technologies Grant","award":["14\/20\/14696"],"award-info":[{"award-number":["14\/20\/14696"]}]},{"name":"DFG Grant","award":["SK 49\/10-1"],"award-info":[{"award-number":["SK 49\/10-1"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Genomics"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>The issue of male fertility is becoming increasingly common due to genetic differences inherited over generations. Gene expression and evaluation of non-coding RNA (ncRNA), crucial for sperm development, are significant factors. This gene expression can affect sperm motility and, consequently, fertility. Understanding the intricate protein interactions that play essential roles in sperm differentiation and development is vital. This knowledge could lead to more effective treatments and interventions for male infertility.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Materials and methods<\/jats:title>\n                <jats:p>Our research aim to identify new and key genes and ncRNA involved in non-obstructive azoospermia (NOA), improving genetic diagnosis and offering more accurate estimates for successful sperm extraction based on an individual\u2019s genotype.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We analyzed the transcript of three NOA patients who tested negative for genetic sperm issues, employing comprehensive genome-wide analysis of approximately 50,000 transcript sequences using microarray technology. This compared gene expression profiles between NOA sperm and normal sperm. We found significant gene expression differences: 150 genes were up-regulated, and 78 genes were down-regulated, along with 24 ncRNAs up-regulated and 13 ncRNAs down-regulated compared to normal conditions. By cross-referencing our results with a single-cell genomics database, we identified overexpressed biological process terms in differentially expressed genes, such as \u201cprotein localization to endosomes\u201d and \u201cxenobiotic transport.\u201d Overrepresented molecular function terms in up-regulated genes included \u201cvoltage-gated calcium channel activity,\u201d \u201cgrowth hormone-releasing hormone receptor activity,\u201d and \u201csialic acid transmembrane transporter activity.\u201d Analysis revealed nine hub genes associated with NOA sperm: <jats:italic>RPL34, CYB5B, GOL6A6, LSM1, ARL4A, DHX57, STARD9, HSP90B1<\/jats:italic>, and <jats:italic>VPS36<\/jats:italic>.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>These genes and their interacting proteins may play a role in the pathophysiology of germ cell abnormalities and infertility.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12864-024-10506-9","type":"journal-article","created":{"date-parts":[[2024,6,11]],"date-time":"2024-06-11T03:45:49Z","timestamp":1718077549000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Whole transcriptome analysis to identify non-coding RNA regulators and hub genes in sperm of non-obstructive azoospermia by microarray, single-cell RNA sequencing, weighted gene co-expression network analysis, and mRNA-miRNA-lncRNA interaction analysis"],"prefix":"10.1186","volume":"25","author":[{"given":"Danial Hashemi","family":"Karoii","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hossein","family":"Azizi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Skutella","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,6,11]]},"reference":[{"issue":"5","key":"10506_CR1","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1016\/j.fertnstert.2019.03.036","volume":"111","author":"N Thirumavalavan","year":"2019","unstructured":"Thirumavalavan N, Gabrielsen JS, Lamb DJ. Where are we going with gene screening for male infertility? Fertil Steril. 2019;111(5):842\u201350.","journal-title":"Fertil Steril"},{"issue":"2","key":"10506_CR2","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1093\/molehr\/gat073","volume":"20","author":"E Fragouli","year":"2014","unstructured":"Fragouli E, et al. Morphological and cytogenetic assessment of cleavage and blastocyst stage embryos. Mol Hum Reprod. 2014;20(2):117\u201326.","journal-title":"Mol Hum Reprod"},{"issue":"15","key":"10506_CR3","doi-asserted-by":"publisher","first-page":"5274","DOI":"10.3390\/ijms21155274","volume":"21","author":"P Kami\u0144ski","year":"2020","unstructured":"Kami\u0144ski P, et al. External and genetic conditions determining male infertility. Int J Mol Sci. 2020;21(15):5274.","journal-title":"Int J Mol Sci"},{"issue":"1","key":"10506_CR4","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1093\/tas\/txz174","volume":"4","author":"ML Butler","year":"2020","unstructured":"Butler ML, et al. Selection for bull fertility: a review. Translational Anim Sci. 2020;4(1):423\u201341.","journal-title":"Translational Anim Sci"},{"key":"10506_CR5","doi-asserted-by":"publisher","first-page":"106355","DOI":"10.1016\/j.anireprosci.2020.106355","volume":"220","author":"E Memili","year":"2020","unstructured":"Memili E, Moura AA, Kaya A. Metabolomes of sperm and seminal plasma associated with bull fertility. Anim Reprod Sci. 2020;220:106355.","journal-title":"Anim Reprod Sci"},{"issue":"4","key":"10506_CR6","doi-asserted-by":"publisher","first-page":"554","DOI":"10.4103\/1008-682X.153847","volume":"17","author":"P Sutovsky","year":"2015","unstructured":"Sutovsky P, et al. Negative biomarker-based male fertility evaluation: sperm phenotypes associated with molecular-level anomalies. Asian J Androl. 2015;17(4):554.","journal-title":"Asian J Androl"},{"issue":"3","key":"10506_CR7","doi-asserted-by":"publisher","first-page":"100377","DOI":"10.1016\/j.esxm.2021.100377","volume":"9","author":"P Capogrosso","year":"2021","unstructured":"Capogrosso P, et al. Male sexual dysfunctions in the infertile couple\u2013recommendations from the European Society of Sexual Medicine (ESSM). Sex Med. 2021;9(3):100377.","journal-title":"Sex Med"},{"issue":"2","key":"10506_CR8","doi-asserted-by":"publisher","first-page":"238","DOI":"10.3390\/ijms18020238","volume":"18","author":"Z Zhang","year":"2017","unstructured":"Zhang Z, et al. Serum metabolomic profiling identifies characterization of non-obstructive azoospermic men. Int J Mol Sci. 2017;18(2):238.","journal-title":"Int J Mol Sci"},{"key":"10506_CR9","doi-asserted-by":"publisher","first-page":"608629","DOI":"10.3389\/fgene.2021.608629","volume":"12","author":"H He","year":"2021","unstructured":"He H, et al. The novel key genes of non-obstructive azoospermia affect spermatogenesis: transcriptomic analysis based on RNA-Seq and scRNA-Seq data. Front Genet. 2021;12:608629.","journal-title":"Front Genet"},{"issue":"6","key":"10506_CR10","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1080\/19396368.2021.1958094","volume":"67","author":"Y Kuyucu","year":"2021","unstructured":"Kuyucu Y, et al. Immunohistochemical examination of androgen receptor and estrogen receptor alpha expressions in obstructive and non-obstructive azoospermia. Syst Biology Reproductive Med. 2021;67(6):463\u201370.","journal-title":"Syst Biology Reproductive Med"},{"key":"10506_CR11","doi-asserted-by":"publisher","first-page":"29","DOI":"10.2147\/IJGM.S241099","volume":"13","author":"E Babakhanzadeh","year":"2020","unstructured":"Babakhanzadeh E, et al. Some of the factors involved in male infertility: a prospective review. Int J Gen Med. 2020;13:29.","journal-title":"Int J Gen Med"},{"issue":"3","key":"10506_CR12","doi-asserted-by":"publisher","first-page":"459","DOI":"10.4103\/1008-682X.148719","volume":"17","author":"SC Esteves","year":"2015","unstructured":"Esteves SC. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl. 2015;17(3):459.","journal-title":"Asian J Androl"},{"key":"10506_CR13","doi-asserted-by":"crossref","unstructured":"Babakhanzadeh E et al. Some of the factors involved in male infertility: a prospective review. Int J Gen Med, 2020: p. 29\u201341.","DOI":"10.2147\/IJGM.S241099"},{"issue":"11","key":"10506_CR14","doi-asserted-by":"publisher","first-page":"2193","DOI":"10.1007\/s11255-021-02979-4","volume":"53","author":"APP Achermann","year":"2021","unstructured":"Achermann APP, Pereira TA, Esteves SC. Microdissection testicular sperm extraction (micro-TESE) in men with infertility due to nonobstructive azoospermia: summary of current literature. Int Urol Nephrol. 2021;53(11):2193\u2013210.","journal-title":"Int Urol Nephrol"},{"key":"10506_CR15","doi-asserted-by":"crossref","unstructured":"Krausz C, Cioppi F. Genetic Factors of Non-Obstructive Azoospermia: Consequences on Patients\u2019 and Offspring Health. J Clin Med, 2021. 10(17).","DOI":"10.3390\/jcm10174009"},{"issue":"9","key":"10506_CR16","first-page":"14634","volume":"8","author":"XW Yu","year":"2015","unstructured":"Yu XW, et al. Y chromosome azoospermia factor region microdeletions and transmission characteristics in azoospermic and severe oligozoospermic patients. Int J Clin Exp Med. 2015;8(9):14634\u201346.","journal-title":"Int J Clin Exp Med"},{"key":"10506_CR17","doi-asserted-by":"publisher","first-page":"775123","DOI":"10.3389\/fgene.2022.775123","volume":"13","author":"Z Cai","year":"2022","unstructured":"Cai Z, Li H. Congenital bilateral absence of the Vas Deferens. Front Genet. 2022;13:775123.","journal-title":"Front Genet"},{"issue":"14","key":"10506_CR18","doi-asserted-by":"publisher","first-page":"3144","DOI":"10.3390\/jcm10143144","volume":"10","author":"DL Andrade","year":"2021","unstructured":"Andrade DL, Viana MC, Esteves SC. Differential diagnosis of azoospermia in men with infertility. J Clin Med. 2021;10(14):3144.","journal-title":"J Clin Med"},{"issue":"18","key":"10506_CR19","doi-asserted-by":"publisher","first-page":"S35","DOI":"10.12968\/bjon.2016.25.18.S35","volume":"25","author":"RB Leaver","year":"2016","unstructured":"Leaver RB. Male infertility: an overview of causes and treatment options. Br J Nurs. 2016;25(18):S35\u201340.","journal-title":"Br J Nurs"},{"issue":"9","key":"10506_CR20","first-page":"998","volume":"19","author":"M Gershoni","year":"2017","unstructured":"Gershoni M, et al. A familial study of azoospermic men identifies three novel causative mutations in three new human azoospermia genes. Genet Sci. 2017;19(9):998\u20131006.","journal-title":"Genet Sci"},{"issue":"2","key":"10506_CR21","doi-asserted-by":"publisher","first-page":"e1009306","DOI":"10.1371\/journal.pgen.1009306","volume":"17","author":"I Aprea","year":"2021","unstructured":"Aprea I, et al. Defects in the cytoplasmic assembly of axonemal dynein arms cause morphological abnormalities and dysmotility in sperm cells leading to male infertility. PLoS Genet. 2021;17(2):e1009306.","journal-title":"PLoS Genet"},{"key":"10506_CR22","doi-asserted-by":"crossref","unstructured":"Garcia M-I, Fernandez-Vallone V, Vassart G. Discovery and characterization of leucine-rich repeat-containing G protein-coupled receptors. G protein-coupled receptor Genetics. Springer; 2014. pp. 365\u201388.","DOI":"10.1007\/978-1-62703-779-2_20"},{"issue":"4","key":"10506_CR23","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1007\/s10815-020-01735-4","volume":"37","author":"Y Wang","year":"2020","unstructured":"Wang Y, et al. Novel DNAAF6 variants identified by whole-exome sequencing cause male infertility and primary ciliary dyskinesia. J Assist Reprod Genet. 2020;37(4):811\u201320.","journal-title":"J Assist Reprod Genet"},{"issue":"3","key":"10506_CR24","doi-asserted-by":"publisher","first-page":"236","DOI":"10.4103\/aja.aja_53_19","volume":"22","author":"W-L Wang","year":"2020","unstructured":"Wang W-L, Tu C-F, Tan Y-Q. Insight on multiple morphological abnormalities of sperm flagella in male infertility: what is new? Asian J Androl. 2020;22(3):236.","journal-title":"Asian J Androl"},{"issue":"3","key":"10506_CR25","doi-asserted-by":"publisher","first-page":"e1006631","DOI":"10.1371\/journal.pgen.1006631","volume":"13","author":"Y-R Shen","year":"2017","unstructured":"Shen Y-R, et al. SEPT12 phosphorylation results in loss of the septin ring\/sperm annulus, defective sperm motility and poor male fertility. PLoS Genet. 2017;13(3):e1006631.","journal-title":"PLoS Genet"},{"issue":"2","key":"10506_CR26","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1111\/cge.12905","volume":"91","author":"P Ray","year":"2017","unstructured":"Ray P, et al. Genetic abnormalities leading to qualitative defects of sperm morphology or function. Clin Genet. 2017;91(2):217\u201332.","journal-title":"Clin Genet"},{"issue":"1","key":"10506_CR27","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1007\/s10815-019-01622-7","volume":"37","author":"J Bedenk","year":"2020","unstructured":"Bedenk J, Vrta\u010dnik-Bokal E, Virant-Klun I. The role of anti-M\u00fcllerian hormone (AMH) in ovarian disease and infertility. J Assist Reprod Genet. 2020;37(1):89\u2013100.","journal-title":"J Assist Reprod Genet"},{"issue":"1","key":"10506_CR28","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1186\/s13048-021-00880-3","volume":"14","author":"D Bhartiya","year":"2021","unstructured":"Bhartiya D, Patel H. An overview of FSH-FSHR biology and explaining the existing conundrums. J Ovarian Res. 2021;14(1):144.","journal-title":"J Ovarian Res"},{"issue":"1","key":"10506_CR29","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1095\/biolreprod.113.109132","volume":"89","author":"C Chang","year":"2013","unstructured":"Chang C, et al. Androgen receptor (AR) physiological roles in male and female reproductive systems: lessons learned from AR-knockout mice lacking AR in selective cells. Biol Reprod. 2013;89(1):21.","journal-title":"Biol Reprod"},{"key":"10506_CR30","doi-asserted-by":"publisher","first-page":"905324","DOI":"10.3389\/fendo.2022.905324","volume":"13","author":"RL Cate","year":"2022","unstructured":"Cate RL. Anti-M\u00fcllerian Hormone Signal Transduction involved in M\u00fcllerian Duct Regression. Front Endocrinol (Lausanne). 2022;13:905324.","journal-title":"Front Endocrinol (Lausanne)"},{"key":"10506_CR31","doi-asserted-by":"crossref","unstructured":"Tang ZR et al. Estrogen-receptor expression and function in Female Reproductive Disease. Cells, 2019. 8(10).","DOI":"10.3390\/cells8101123"},{"issue":"10","key":"10506_CR32","doi-asserted-by":"publisher","first-page":"e74596","DOI":"10.1371\/journal.pone.0074596","volume":"8","author":"L Han","year":"2013","unstructured":"Han L, et al. Characterization of the mechanism of Inhibin \u03b1-Subunit gene in mouse anterior pituitary cells by RNA interference. PLoS ONE. 2013;8(10):e74596.","journal-title":"PLoS ONE"},{"issue":"6","key":"10506_CR33","doi-asserted-by":"publisher","first-page":"660","DOI":"10.4103\/aja2021131","volume":"24","author":"Z Zhang","year":"2022","unstructured":"Zhang Z, et al. Identification and characterization of circular RNAs in the testicular tissue of patients with non-obstructive azoospermia. Asian J Androl. 2022;24(6):660\u20135.","journal-title":"Asian J Androl"},{"issue":"10","key":"10506_CR34","doi-asserted-by":"publisher","first-page":"2649","DOI":"10.1093\/humrep\/deab196","volume":"36","author":"C Ji","year":"2021","unstructured":"Ji C, et al. Potential of testis-derived circular RNAs in seminal plasma to predict the outcome of microdissection testicular sperm extraction in patients with idiopathic non-obstructive azoospermia. Hum Reprod. 2021;36(10):2649\u201360.","journal-title":"Hum Reprod"},{"key":"10506_CR35","doi-asserted-by":"publisher","first-page":"541777","DOI":"10.3389\/fendo.2020.00395","volume":"11","author":"F Manfrevola","year":"2020","unstructured":"Manfrevola F, et al. CircRNA role and circRNA-dependent network (ceRNET) in asthenozoospermia. Front Endocrinol. 2020;11:541777.","journal-title":"Front Endocrinol"},{"issue":"13","key":"10506_CR36","doi-asserted-by":"publisher","first-page":"5956","DOI":"10.1080\/07391102.2021.1875879","volume":"40","author":"S Sabetian","year":"2022","unstructured":"Sabetian S, et al. Exploring the dysregulated mRNAs\u2013miRNAs\u2013lncRNAs interactions associated to idiopathic non-obstructive azoospermia. J Biomol Struct Dynamics. 2022;40(13):5956\u201364.","journal-title":"J Biomol Struct Dynamics"},{"issue":"8","key":"10506_CR37","doi-asserted-by":"publisher","first-page":"673","DOI":"10.2217\/epi-2020-0008","volume":"12","author":"H Bo","year":"2020","unstructured":"Bo H, et al. Long noncoding RNAs expression profile and long noncoding RNA-mediated competing endogenous RNA network in nonobstructive azoospermia patients. Epigenomics. 2020;12(8):673\u201384.","journal-title":"Epigenomics"},{"issue":"1","key":"10506_CR38","doi-asserted-by":"publisher","first-page":"e12297","DOI":"10.1111\/cpr.12297","volume":"50","author":"WY Song","year":"2017","unstructured":"Song WY, et al. Reduced micro RNA-188\u20103p expression contributes to apoptosis of spermatogenic cells in patients with azoospermia. Cell Prolif. 2017;50(1):e12297.","journal-title":"Cell Prolif"},{"key":"10506_CR39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1477-7827-7-13","volume":"7","author":"J Lian","year":"2009","unstructured":"Lian J, et al. Altered microRNA expression in patients with non-obstructive azoospermia. Reproductive Biology Endocrinol. 2009;7:1\u201310.","journal-title":"Reproductive Biology Endocrinol"},{"issue":"3","key":"10506_CR40","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.bbagrm.2013.08.004","volume":"1839","author":"C Rathke","year":"2014","unstructured":"Rathke C, et al. Chromatin dynamics during spermiogenesis. Biochim et Biophys Acta (BBA)-Gene Regul Mech. 2014;1839(3):155\u201368.","journal-title":"Biochim et Biophys Acta (BBA)-Gene Regul Mech"},{"issue":"10","key":"10506_CR41","doi-asserted-by":"publisher","first-page":"2487","DOI":"10.7150\/ijbs.60384","volume":"17","author":"M Azhar","year":"2021","unstructured":"Azhar M, et al. Towards post-meiotic sperm production: genetic insight into human infertility from mouse models. Int J Biol Sci. 2021;17(10):2487.","journal-title":"Int J Biol Sci"},{"key":"10506_CR42","doi-asserted-by":"crossref","unstructured":"Patankar A, Parte P. Sperm chromatin compaction and male infertility Male Infertility: Understanding, Causes and Treatment, 2017: pp. 295\u2013315.","DOI":"10.1007\/978-981-10-4017-7_17"},{"issue":"10","key":"10506_CR43","doi-asserted-by":"publisher","first-page":"3702","DOI":"10.3390\/ijms21103702","volume":"21","author":"ME Teves","year":"2020","unstructured":"Teves ME, et al. Sperm differentiation: the role of trafficking of proteins. Int J Mol Sci. 2020;21(10):3702.","journal-title":"Int J Mol Sci"},{"key":"10506_CR44","unstructured":"Shang P. Testis-specific Protein Kinases TSSK1 and TSSK2 in Mouse Spermiogenesis 2014."},{"key":"10506_CR45","doi-asserted-by":"crossref","unstructured":"Danial Hashemi K, Hossein A. Undifferentiated and differentiated spermatogonial stem cells. Advances in pluripotent stem cells. Z. Prof. Leisheng, Editor.; 2023. IntechOpen: Rijeka. p. Ch. 10.","DOI":"10.5772\/intechopen.112964"},{"issue":"7","key":"10506_CR46","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1002\/cbf.3838","volume":"41","author":"D Hashemi Karoii","year":"2023","unstructured":"Hashemi Karoii D, Azizi H. Functions and mechanism of noncoding RNA in regulation and differentiation of male mammalian reproduction. Cell Biochem Funct. 2023;41(7):767\u201378.","journal-title":"Cell Biochem Funct"},{"key":"10506_CR47","doi-asserted-by":"crossref","unstructured":"Hashemi Karoii D, Azizi H, Skutella T. Altered G-Protein transduction protein gene expression in the Testis of Infertile patients with Nonobstructive Azoospermia. DNA and Cell Biology; 2023.","DOI":"10.1089\/dna.2023.0189"},{"key":"10506_CR48","doi-asserted-by":"crossref","unstructured":"Hashemi Karoii D, Azizi H. A review of protein-protein interaction and signaling pathway of Vimentin in cell regulation, morphology and cell differentiation in normal cells. J Recept Signal Transduction, 2022: p. 1\u20139.","DOI":"10.1080\/10799893.2022.2047199"},{"key":"10506_CR49","doi-asserted-by":"crossref","unstructured":"Karoii DH, Azizi H, Amirian M. Signaling pathways and protein\u2013protein Interaction of Vimentin in Invasive and Migration cells: a review. Cellular Reprogramming; 2022.","DOI":"10.1089\/cell.2022.0025"},{"issue":"3","key":"10506_CR50","doi-asserted-by":"publisher","first-page":"268","DOI":"10.3390\/ani12030268","volume":"12","author":"A Niazi Tabar","year":"2022","unstructured":"Niazi Tabar A, et al. Testicular localization and potential function of Vimentin Positive Cells during Spermatogonial differentiation stages. Animals. 2022;12(3):268.","journal-title":"Animals"},{"key":"10506_CR51","doi-asserted-by":"publisher","first-page":"p8582526","DOI":"10.1155\/2016\/8582526","volume":"2016","author":"S Conrad","year":"2016","unstructured":"Conrad S, et al. Expression of genes related to germ cell lineage and pluripotency in single cells and colonies of human adult germ stem cells. Stem Cells Int. 2016;2016:p8582526.","journal-title":"Stem Cells Int"},{"issue":"3","key":"10506_CR52","first-page":"281","volume":"21","author":"H Azizi","year":"2019","unstructured":"Azizi H, Asgari B, Skutella T. Pluripotency potential of embryonic stem cell-like cells derived from mouse testis. Cell J (Yakhteh). 2019;21(3):281.","journal-title":"Cell J (Yakhteh)"},{"key":"10506_CR53","doi-asserted-by":"crossref","unstructured":"Azizi H et al. Derivation of pluripotent cells from mouse SSCs seems to be age dependent Stem cells international, 2016. 2016.","DOI":"10.1155\/2016\/8216312"},{"issue":"1","key":"10506_CR54","doi-asserted-by":"publisher","first-page":"17259","DOI":"10.1038\/s41598-022-22137-9","volume":"12","author":"M Amirian","year":"2022","unstructured":"Amirian M, et al. VASA protein and gene expression analysis of human non-obstructive azoospermia and normal by immunohistochemistry, immunocytochemistry, and bioinformatics analysis. Sci Rep. 2022;12(1):17259.","journal-title":"Sci Rep"},{"issue":"20","key":"10506_CR55","doi-asserted-by":"publisher","first-page":"12570","DOI":"10.3390\/ijms232012570","volume":"23","author":"H Azizi","year":"2022","unstructured":"Azizi H, Hashemi Karoii D, Skutella T. Whole exome sequencing and in Silico Analysis of Human sertoli in patients with Non-obstructive Azoospermia. Int J Mol Sci. 2022;23(20):12570.","journal-title":"Int J Mol Sci"},{"issue":"2","key":"10506_CR56","doi-asserted-by":"publisher","first-page":"359","DOI":"10.21037\/tau-23-485","volume":"13","author":"H Azizi","year":"2024","unstructured":"Azizi H, Hashemi Karoii D, Skutella T. Clinical management, differential diagnosis, follow-up and biomarkers of infertile men with nonobstructive azoospermia. Translational Androl Urol. 2024;13(2):359\u201362.","journal-title":"Translational Androl Urol"},{"key":"10506_CR57","doi-asserted-by":"crossref","unstructured":"Hashemi Karoii D, Azizi H. OCT4 protein and gene expression analysis in the differentiation of spermatogonia stem cells into neurons by immunohistochemistry, immunocytochemistry, and bioinformatics analysis. Stem Cell Reviews Rep, 2023: p. 1\u201317.","DOI":"10.1007\/s12015-023-10548-8"},{"key":"10506_CR58","first-page":"511","volume-title":"Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays","author":"J Sha","year":"2002","unstructured":"Sha J, et al. Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays. Volume 8. MHR: Basic science of reproductive medicine; 2002. pp. 511\u20137. 6."},{"issue":"1","key":"10506_CR59","doi-asserted-by":"publisher","first-page":"btad031","DOI":"10.1093\/bioinformatics\/btad031","volume":"39","author":"M Franz","year":"2023","unstructured":"Franz M, et al. Cytoscape. Js 2023 update: a graph theory library for visualization and analysis. Bioinformatics. 2023;39(1):btad031.","journal-title":"Bioinformatics"},{"issue":"2","key":"10506_CR60","doi-asserted-by":"publisher","first-page":"757","DOI":"10.3892\/or.2015.4415","volume":"35","author":"L Cao","year":"2016","unstructured":"Cao L, et al. Microarray profiling of bone marrow long non-coding RNA expression in Chinese pediatric acute myeloid leukemia patients. Oncol Rep. 2016;35(2):757\u201370.","journal-title":"Oncol Rep"},{"issue":"1","key":"10506_CR61","doi-asserted-by":"publisher","first-page":"3460","DOI":"10.1038\/s41467-022-31160-3","volume":"13","author":"PF C\u00e9spedes","year":"2022","unstructured":"C\u00e9spedes PF, et al. T-cell trans-synaptic vesicles are distinct and carry greater effector content than constitutive extracellular vesicles. Nat Commun. 2022;13(1):3460.","journal-title":"Nat Commun"},{"issue":"1","key":"10506_CR62","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1186\/1471-2105-9-559","volume":"9","author":"P Langfelder","year":"2008","unstructured":"Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9(1):559.","journal-title":"BMC Bioinformatics"},{"key":"10506_CR63","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.reprotox.2020.05.017","volume":"96","author":"L Wang","year":"2020","unstructured":"Wang L, et al. Actin binding proteins, actin cytoskeleton and spermatogenesis\u2013lesson from toxicant models. Reprod Toxicol. 2020;96:76\u201389.","journal-title":"Reprod Toxicol"},{"issue":"4","key":"10506_CR64","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1002\/rmb2.12407","volume":"20","author":"Y Inagaki","year":"2021","unstructured":"Inagaki Y, et al. The expression of human testis-specific actin capping protein predicts in vitro fertilization outcomes: a novel biomarker of sperm function for assisted reproductive technology. Reproductive Med Biology. 2021;20(4):537\u201342.","journal-title":"Reproductive Med Biology"},{"issue":"2","key":"10506_CR65","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1002\/rmb2.12316","volume":"19","author":"T Soda","year":"2020","unstructured":"Soda T, et al. Physiological role of actin regulation in male fertility: insight into actin capping proteins in spermatogenic cells. Reproductive Med Biology. 2020;19(2):120\u20137.","journal-title":"Reproductive Med Biology"},{"issue":"2","key":"10506_CR66","doi-asserted-by":"publisher","first-page":"R53","DOI":"10.1530\/REP-18-0457","volume":"157","author":"JE Dunleavy","year":"2019","unstructured":"Dunleavy JE, et al. The cytoskeleton in spermatogenesis. Reproduction. 2019;157(2):R53\u201372.","journal-title":"Reproduction"},{"issue":"4","key":"10506_CR67","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1111\/brv.12498","volume":"94","author":"CD Pereira","year":"2019","unstructured":"Pereira CD, et al. Nuclear envelope dynamics during mammalian spermatogenesis: new insights on male fertility. Biol Rev. 2019;94(4):1195\u2013219.","journal-title":"Biol Rev"},{"issue":"4","key":"10506_CR68","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1152\/physrev.00009.2002","volume":"82","author":"CY Cheng","year":"2002","unstructured":"Cheng CY, Mruk DD. Cell junction dynamics in the testis: sertoli-germ cell interactions and male contraceptive development. Physiol Rev. 2002;82(4):825\u201374.","journal-title":"Physiol Rev"},{"issue":"13","key":"10506_CR69","doi-asserted-by":"publisher","first-page":"1145","DOI":"10.1016\/S0960-9822(02)00922-3","volume":"12","author":"K Ozaki-Kuroda","year":"2002","unstructured":"Ozaki-Kuroda K, et al. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol. 2002;12(13):1145\u201350.","journal-title":"Curr Biol"},{"issue":"3","key":"10506_CR70","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.mrrev.2011.04.002","volume":"727","author":"S Rajender","year":"2011","unstructured":"Rajender S, Avery K, Agarwal A. Epigenetics, spermatogenesis and male infertility. Mutat Research\/Reviews Mutat Res. 2011;727(3):62\u201371.","journal-title":"Mutat Research\/Reviews Mutat Res"},{"issue":"3","key":"10506_CR71","doi-asserted-by":"publisher","first-page":"181","DOI":"10.5152\/tud.2013.037","volume":"39","author":"S G\u00fcne\u015f","year":"2013","unstructured":"G\u00fcne\u015f S, Kula\u00e7 T. The role of epigenetics in spermatogenesis. Turkish J Urol. 2013;39(3):181.","journal-title":"Turkish J Urol"},{"issue":"10","key":"10506_CR72","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.2217\/epi-2016-0056","volume":"8","author":"KR Stewart","year":"2016","unstructured":"Stewart KR, Veselovska L, Kelsey G. Establishment and functions of DNA methylation in the germline. Epigenomics. 2016;8(10):1399\u2013413.","journal-title":"Epigenomics"},{"issue":"1","key":"10506_CR73","first-page":"48","volume":"36","author":"K Khambata","year":"2021","unstructured":"Khambata K, et al. DNA methylation defects in spermatozoa of male partners from couples experiencing recurrent pregnancy loss. Hum Reprod. 2021;36(1):48\u201360.","journal-title":"Hum Reprod"},{"issue":"4","key":"10506_CR74","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1111\/andr.12379","volume":"5","author":"D Santi","year":"2017","unstructured":"Santi D, et al. Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology. 2017;5(4):695\u2013703.","journal-title":"Andrology"},{"issue":"6","key":"10506_CR75","doi-asserted-by":"publisher","first-page":"3259","DOI":"10.3390\/ijms22063259","volume":"22","author":"K Nowicka-Bauer","year":"2021","unstructured":"Nowicka-Bauer K, Szymczak-Cendlak M. Structure and function of Ion channels regulating sperm Motility\u2014An overview. Int J Mol Sci. 2021;22(6):3259.","journal-title":"Int J Mol Sci"},{"issue":"1","key":"10506_CR76","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.jmb.2014.08.010","volume":"427","author":"J Payandeh","year":"2015","unstructured":"Payandeh J, Minor DL Jr. Bacterial voltage-gated sodium channels (BacNaVs) from the soil, sea, and salt lakes enlighten molecular mechanisms of electrical signaling and pharmacology in the brain and heart. J Mol Biol. 2015;427(1):3\u201330.","journal-title":"J Mol Biol"},{"issue":"4","key":"10506_CR77","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1242\/jeb.110270","volume":"218","author":"Y Moran","year":"2015","unstructured":"Moran Y, et al. Evolution of voltage-gated ion channels at the emergence of Metazoa. J Exp Biol. 2015;218(4):515\u201325.","journal-title":"J Exp Biol"},{"key":"10506_CR78","doi-asserted-by":"crossref","unstructured":"Beltr\u00e1n C et al. Role of ion channels in the sperm acrosome reaction. Sperm Acrosome Biogenesis Function Dur Fertilization, 2016: p. 35\u201369.","DOI":"10.1007\/978-3-319-30567-7_3"},{"issue":"1","key":"10506_CR79","doi-asserted-by":"publisher","first-page":"31","DOI":"10.17305\/bjbms.2018.3477","volume":"19","author":"MB Khawar","year":"2019","unstructured":"Khawar MB, Mehmood R, Roohi N. MicroRNAs: recent insights towards their role in male infertility and reproductive cancers. Bosnian J Basic Med Sci. 2019;19(1):31.","journal-title":"Bosnian J Basic Med Sci"},{"key":"10506_CR80","doi-asserted-by":"crossref","unstructured":"Holt JE et al. Non-coding RNA in spermatogenesis and epididymal maturation Non-coding RNA and the Reproductive System, 2016: pp. 95\u2013120.","DOI":"10.1007\/978-94-017-7417-8_6"},{"issue":"20","key":"10506_CR81","doi-asserted-by":"publisher","first-page":"4071","DOI":"10.1007\/s00018-019-03201-6","volume":"76","author":"HM La","year":"2019","unstructured":"La HM, Hobbs RM. Mechanisms regulating mammalian spermatogenesis and fertility recovery following germ cell depletion. Cell Mol Life Sci. 2019;76(20):4071\u2013102.","journal-title":"Cell Mol Life Sci"},{"issue":"6","key":"10506_CR82","doi-asserted-by":"publisher","first-page":"1383","DOI":"10.1093\/humrep\/deq081","volume":"25","author":"KI Aston","year":"2010","unstructured":"Aston KI, et al. Evaluation of 172 candidate polymorphisms for association with oligozoospermia or azoospermia in a large cohort of men of European descent. Hum Reprod. 2010;25(6):1383\u201397.","journal-title":"Hum Reprod"},{"key":"10506_CR83","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1038\/s41525-020-0117-4","volume":"5","author":"D Tomoiaga","year":"2020","unstructured":"Tomoiaga D, et al. Single-cell sperm transcriptomes and variants from fathers of children with and without autism spectrum disorder. NPJ Genom Med. 2020;5:14.","journal-title":"NPJ Genom Med"}],"container-title":["BMC Genomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-024-10506-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12864-024-10506-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-024-10506-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,11]],"date-time":"2024-06-11T03:46:17Z","timestamp":1718077577000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcgenomics.biomedcentral.com\/articles\/10.1186\/s12864-024-10506-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,11]]},"references-count":83,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["10506"],"URL":"https:\/\/doi.org\/10.1186\/s12864-024-10506-9","relation":{},"ISSN":["1471-2164"],"issn-type":[{"value":"1471-2164","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,11]]},"assertion":[{"value":"19 March 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 June 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 June 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All the gene expression data and clinical information used in this study have been approved by the local ethical committees Heidelberg (Ethics Committee of the Medical Faculty of Heidelberg University) and Amol University of Special Modern Technologies (Iran National Committee for Ethics in Biomedical Research: approved number: Ir.ausmt.rec.1402.05).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"It is declared by the remaining authors that there are no commercial or financial relationships that might conflict with the research.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}],"article-number":"583"}}