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We report (i) the relative abundance of the ssc-miR-1285, miR-16, miR-4332, miR-92a, miR-671-5p, miR-4334-5p, miR-425-5p, miR-191, miR-92b-5p and miR-15b miRNAs, and (ii) the presence of 347 up-regulated and 174 down-regulated RNA transcripts in high-fertility breeding boars, based on differences of farrowing rate (FS) and litter size (LS), relative to low-fertility boars in the (Artificial Insemination) AI program. An overrepresentation analysis of the protein class (PANTHER) identified significant fold-increases for C-C chemokine binding (GO:0019957): CCR7, which activates B- and T-lymphocytes, 8-fold increase), XCR1 and CXCR4 (with ubiquitin as a natural ligand, 1.24-fold increase), cytokine receptor activity (GO:0005126): IL23R receptor of the IL23 protein, associated to JAK2 and STAT3, 3.4-fold increase), the TGF-receptor (PC00035) genes ACVR1C and ACVR2B (12-fold increase). Moreover, two micro-RNAs (miR-221 and mir-621) were down- and up-regulated, respectively, in high-fertility males. In conclusion, boars with different fertility performance possess a wide variety of differentially expressed RNA present in spermatozoa that would be attractive targets as non-invasive molecular markers for predicting fertility.<\/jats:p>","DOI":"10.3390\/ijms21051572","type":"journal-article","created":{"date-parts":[[2020,2,26]],"date-time":"2020-02-26T04:18:29Z","timestamp":1582690709000},"page":"1572","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":50,"title":["The Transcriptome of Pig Spermatozoa, and Its Role in Fertility"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0120-354X","authenticated-orcid":false,"given":"Manuel","family":"Alvarez-Rodriguez","sequence":"first","affiliation":[{"name":"Department of Biomedical &amp; Clinical Sciences (BKV), BKH\/Obstetrics &amp; Gynaecology, Faculty of Medicine and Health Sciences, Link\u00f6ping University, SE-58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cristina","family":"Martinez","sequence":"additional","affiliation":[{"name":"Department of Biomedical &amp; Clinical Sciences (BKV), BKH\/Obstetrics &amp; Gynaecology, Faculty of Medicine and Health Sciences, Link\u00f6ping University, SE-58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominic","family":"Wright","sequence":"additional","affiliation":[{"name":"Department of Physics, Chemistry and Biology, Faculty of Science and Engineering, Link\u00f6ping University, SE-58183 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9873-814X","authenticated-orcid":false,"given":"Isabel","family":"Barranco","sequence":"additional","affiliation":[{"name":"Biotechnology of Animal and Human Reproduction (TechnoSperm), Department of Biology, Institute of Food and Agricultural Technology, University of Girona, 17003 Girona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4213-3093","authenticated-orcid":false,"given":"Jordi","family":"Roca","sequence":"additional","affiliation":[{"name":"Department of Medicine and Animal Surgery, Faculty of Veterinary Medicine, International Campus for Higher Education and Research \u201cCampus Mare Nostrum\u201d, University of Murcia, 30100 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5194-2124","authenticated-orcid":false,"given":"Heriberto","family":"Rodriguez-Martinez","sequence":"additional","affiliation":[{"name":"Department of Biomedical &amp; Clinical Sciences (BKV), BKH\/Obstetrics &amp; Gynaecology, Faculty of Medicine and Health Sciences, Link\u00f6ping University, SE-58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1530\/jrf.0.0280369","article-title":"Transport of live and dead boar spermatozoa within the reproductive tract of gilts","volume":"28","author":"Baker","year":"1972","journal-title":"J. Reprod. Fertil."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.theriogenology.2004.09.027","article-title":"Uterine activity, sperm transport, and the role of boar stimuli around insemination in sows","volume":"63","author":"Langendijk","year":"2005","journal-title":"Theriogenology"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Alminana, C., Caballero, I., Heath, P.R., Maleki-Dizaji, S., Parrilla, I., Cuello, C., Gil, M.A., Vazquez, J.L., Vazquez, J.M., and Roca, J. (2014). The battle of the sexes starts in the oviduct: Modulation of oviductal transcriptome by X and Y-bearing spermatozoa. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-293"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Alvarez-Rodriguez, M., Atikuzzaman, M., Venhoranta, H., Wright, D., and Rodriguez-Martinez, H. (2019). Expression of Immune Regulatory Genes in the Porcine Internal Genital Tract Is Differentially Triggered by Spermatozoa and Seminal Plasma. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20030513"},{"key":"ref_5","first-page":"1","article-title":"The physiological roles of the boar ejaculate","volume":"66","author":"Kvist","year":"2009","journal-title":"Soc. Reprod. Fertil. Suppl."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1006\/smim.2000.0320","article-title":"The role of semen in induction of maternal immune tolerance to pregnancy","volume":"13","author":"Robertson","year":"2001","journal-title":"Semin. Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1530\/jrf.0.0890591","article-title":"Immunocytochemical localization of nuclear protamine in boar spermatozoa during epididymal transit","volume":"89","author":"Courtens","year":"1990","journal-title":"J. Reprod. Fertil."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1111\/j.1439-0272.2005.00656.x","article-title":"Mature human spermatozoa do not transcribe novel RNA","volume":"37","author":"Grunewald","year":"2005","journal-title":"Andrologia"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.anireprosci.2008.08.012","article-title":"Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa","volume":"113","author":"Yang","year":"2009","journal-title":"Anim. Reprod. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Dai, D.-H., Qazi, I.H., Ran, M.-X., Liang, K., Zhang, Y., Zhang, M., Zhou, G.-B., Angel, C., and Zeng, C.-J. (2019). Exploration of miRNA and mRNA Profiles in Fresh and Frozen-Thawed Boar Sperm by Transcriptome and Small RNA Sequencing. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20040802"},{"key":"ref_11","first-page":"641","article-title":"Novel functions for small RNA molecules","volume":"11","author":"Zhang","year":"2009","journal-title":"Curr. Opin. Mol. Ther."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1002\/(SICI)1098-2795(200006)56:2+<259::AID-MRD10>3.0.CO;2-R","article-title":"Analysis and Significance of Messenger RNA in Human Ejaculated Spermatozoa","volume":"56","author":"Miller","year":"2000","journal-title":"Mol. Reprod. Dev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2011","DOI":"10.1126\/science.1094637","article-title":"Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase","volume":"303","author":"Brunet","year":"2004","journal-title":"Science"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1007\/s10815-014-0406-x","article-title":"microRNA profiling in three main stages during porcine spermatogenesis","volume":"32","author":"Luo","year":"2015","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Luo, L., Ye, L., Liu, G., Shao, G., Zheng, R., Ren, Z., Zuo, B., Xu, D., Lei, M., and Jiang, S. (2010). Microarray-Based approach identifies differentially expressed MicroRNAs in porcine sexually immature and mature testes. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0011744"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1532","DOI":"10.1016\/j.theriogenology.2011.06.025","article-title":"Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility","volume":"76","author":"Curry","year":"2011","journal-title":"Theriogenology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e257","DOI":"10.1016\/j.fsigss.2017.09.092","article-title":"Expression difference of miR-10b and miR-135b between the fertile and infertile semen samples (p)","volume":"6","author":"Tian","year":"2017","journal-title":"Forensic Sci. Int. Genet. Suppl. Ser."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/j.fertnstert.2015.06.015","article-title":"Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile","volume":"104","author":"Blanco","year":"2015","journal-title":"Fertil. Steril."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1177\/0300985811402846","article-title":"Swine as Models in Biomedical Research and Toxicology Testing","volume":"49","author":"Swindle","year":"2012","journal-title":"Vet. Pathol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.theriogenology.2015.11.026","article-title":"Will AI in pigs become more efficient?","volume":"86","author":"Roca","year":"2016","journal-title":"Theriogenology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/0012-1606(89)90178-4","article-title":"Mitochondrial gene expression in male germ cells of the mouse","volume":"135","author":"Alcivar","year":"1989","journal-title":"Dev. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1101\/gad.367606","article-title":"Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes","volume":"20","author":"Gur","year":"2006","journal-title":"Genes Dev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"299","DOI":"10.3389\/fgene.2019.00299","article-title":"A RNA-seq analysis to describe the boar sperm transcriptome and its seasonal changes","volume":"10","author":"Estill","year":"2019","journal-title":"Front. Genet."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2199-11-74","article-title":"MIQE pr\u00e9cis: Practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments","volume":"11","author":"Bustin","year":"2010","journal-title":"BMC Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4059","DOI":"10.1210\/en.2014-1982","article-title":"MicroRNA-1285 regulates 17\u03b2-estradiol-inhibited immature boar sertoli cell proliferation via adenosine monophosphate-Activated protein kinase activation","volume":"156","author":"Jiao","year":"2015","journal-title":"Endocrinology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1080\/15569527.2017.1355314","article-title":"Evaluation of microRNA responses in ARPE-19 cells against the oxidative stress","volume":"37","author":"Ayaz","year":"2018","journal-title":"Cutan. Ocul. Toxicol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1016\/j.biopha.2018.05.041","article-title":"miR-15a\/miR-16 cluster inhibits invasion of prostate cancer cells by suppressing TGF-\u03b2 signaling pathway","volume":"104","author":"Jin","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Wang, Z., Li, Q., Chamba, Y., Zhang, B., Shang, P., Zhang, H., and Wu, C. (2015). Identification of Genes Related to Growth and Lipid Deposition from Transcriptome Profiles of Pig Muscle Tissue. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0141138"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.ejogrb.2016.01.007","article-title":"MicroRNA-92 expression may be associated with reduced estrogen receptor \u03b21 mRNA levels in cervical portion of uterosacral ligaments in women with pelvic organ prolapse","volume":"198","author":"He","year":"2016","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"24209","DOI":"10.18632\/oncotarget.24819","article-title":"MiR-92 suppresses proliferation and induces apoptosis by targeting EP4\/Notch1 axis in gastric cancer","volume":"9","author":"Shin","year":"2018","journal-title":"Oncotarget"},{"key":"ref_31","first-page":"4753","article-title":"MiR-671-5p inhibits gastric cancer cell proliferatioand promotes cell apoptosis by targeting URGCP","volume":"16","author":"Qiu","year":"2018","journal-title":"Exp. Ther. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1892","DOI":"10.7150\/ijbs.32429","article-title":"MiR-671-5p blocks the progression of human esophageal squamous cell carcinoma by suppressing FGFR2","volume":"15","author":"Li","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_33","first-page":"122","article-title":"Role of postnatal expression of fgfr1 and fgfr2 in testicular germ cells on spermatogenesis and fertility in mice","volume":"15","author":"Li","year":"2014","journal-title":"J. Reprod. Infertil."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"9477","DOI":"10.1021\/acs.jafc.9b02925","article-title":"Porcine Milk Exosome MiRNAs Attenuate LPS-Induced Apoptosis through Inhibiting TLR4\/NF-\u03baB and p53 Pathways in Intestinal Epithelial Cells","volume":"67","author":"Xie","year":"2019","journal-title":"J. Agric. Food Chem."},{"key":"ref_35","first-page":"6300","article-title":"MiR-425 Involves in the Development and Progression of Renal Cell Carcinoma by Inhibiting E2F6","volume":"22","author":"Cai","year":"2018","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Chen, F.F., Xiong, Y., Peng, Y., Gao, Y., Qin, J., Chu, G.Y., Pang, W.J., and Yang, G.S. (2017). MiR-425-5p inhibits differentiation and proliferation in porcine intramuscular preadipocytes. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18102101"},{"key":"ref_37","first-page":"4595","article-title":"Correlation of miR-425-5p and IL-23 with pancreatic cancer","volume":"17","author":"Lu","year":"2019","journal-title":"Oncol. Lett."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1146\/annurev.immunol.22.012703.104758","article-title":"Discovery and Biology of IL-23 and IL-27: Related but Functionally Distinct Regulators of Inflammation","volume":"25","author":"Kastelein","year":"2007","journal-title":"Annu. Rev. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.1093\/carcin\/bgy102","article-title":"Amplification of hsa-miR-191\/425 locus promotes breast cancer proliferation and metastasis by targeting DICER1","volume":"39","author":"Zhang","year":"2018","journal-title":"Carcinogenesis"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3321","DOI":"10.1096\/fj.201601263R","article-title":"MIR-191 suppresses angiogenesis by activation of NF-kB signaling","volume":"31","author":"Gu","year":"2017","journal-title":"FASEB J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1002\/iub.1705","article-title":"miR-191\/DAB2 axis regulates the tumorigenicity of estrogen receptor-positive breast cancer","volume":"70","author":"Tian","year":"2018","journal-title":"IUBMB Life"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e1043","DOI":"10.1002\/mgg3.1043","article-title":"MiR-191-5p inhibits lung adenocarcinoma by repressing SATB1 to inhibit Wnt pathway","volume":"8","author":"Zhou","year":"2020","journal-title":"Mol. Genet. Genomic Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.1016\/j.theriogenology.2011.11.016","article-title":"The value of microscopic semen motility assessment at collection for a commercial artificial insemination center, a retrospective study on factors explaining variation in pig fertility","volume":"77","author":"Broekhuijse","year":"2012","journal-title":"Theriogenology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"11192","DOI":"10.1038\/s41598-019-47702-7","article-title":"Effect of low sperm quality on progeny: A study on zebrafish as model species","volume":"9","author":"Riesco","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_45","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_46","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.ydbio.2014.10.009","article-title":"Zn2+-stimulation of sperm capacitation and of the acrosome reaction is mediated by EGFR activation","volume":"396","author":"Michailov","year":"2014","journal-title":"Dev. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2745","DOI":"10.1080\/15384101.2018.1556060","article-title":"MiR-221 is involved in depression by regulating Wnt2\/CREB\/BDNF axis in hippocampal neurons","volume":"17","author":"Lian","year":"2018","journal-title":"Cell Cycle"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1093\/molehr\/6.4.303","article-title":"Molecular characterization of a voltage-gated potassium channel expressed in rat testis","volume":"6","author":"Jacob","year":"2000","journal-title":"Mol. Hum. Reprod."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.repbio.2017.01.001","article-title":"The CatSper channel modulates boar sperm motility during capacitation","volume":"17","year":"2017","journal-title":"Reprod. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1095\/biolreprod.109.077107","article-title":"A Novel, Single, Transmembrane Protein CATSPERG Is Associated with CATSPER1 Channel Protein1","volume":"81","author":"Wang","year":"2009","journal-title":"Biol. Reprod."},{"key":"ref_51","first-page":"127","article-title":"Inhibition of CatSper and Hv1 Channels and NOX5 Enzyme Affect Progesterone-Induced Increase of Intracellular Calcium Concentration and ROS Generation in Human Sperm","volume":"44","author":"Ghanbari","year":"2019","journal-title":"Iran. J. Med. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1152\/physiol.00049.2009","article-title":"Calcium signaling through CatSper channels in mammalian fertilization","volume":"25","author":"Ren","year":"2010","journal-title":"Physiology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/cddiscovery.2017.71","article-title":"Zinc-finger proteins in health and disease","volume":"3","author":"Cassandri","year":"2017","journal-title":"Cell Death Discov."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"15901","DOI":"10.1074\/jbc.RA118.004167","article-title":"Palmitoylation of caveolin-1 is regulated by the same DHHC acyltransferases that modify steroid hormone receptors","volume":"293","author":"Woolfrey","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1210\/jc.2003-031681","article-title":"Estrogen Receptor (ER)\u03b1 and ER\u03b2 Are Both Expressed in Human Ejaculated Spermatozoa: Evidence of Their Direct Interaction with Phosphatidylinositol-3-OH Kinase\/Akt Pathway","volume":"89","author":"Aquila","year":"2004","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/S0167-4781(01)00194-4","article-title":"Cloning and characterization of a novel Kr\u00fcppel-like zinc finger gene, ZNF268, expressed in early human embryo","volume":"1518","author":"Gou","year":"2001","journal-title":"Biochim. Biophys. Acta-Gene Struct. Expr."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1095\/biolreprod65.6.1663","article-title":"GLI1 Localization in the Germinal Epithelial Cells Alternates Between Cytoplasm and Nucleus: Upregulation in Transgenic Mice Blocks Spermatogenesis in Pachytene1","volume":"65","author":"Kroft","year":"2001","journal-title":"Biol. Reprod."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"225","DOI":"10.2164\/jandrol.05114","article-title":"Sonic hedgehog pathway inhibition alters epididymal function as assessed by the development of sperm motility","volume":"27","author":"Turner","year":"2006","journal-title":"J. Androl."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1016\/j.mam.2008.08.001","article-title":"The ADAM metalloproteinases","volume":"29","author":"Edwards","year":"2009","journal-title":"Mol. Asp. Med."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Atikuzzaman, M., Alvarez-Rodriguez, M., Vicente-Carrillo, A., Johnsson, M., Wright, D., and Rodriguez-Martinez, H. (2017). Conserved gene expression in sperm reservoirs between birds and mammals in response to mating. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3488-x"},{"key":"ref_61","first-page":"44","article-title":"Spermatozoa rather than seminal fluid drives immune-modulation in the sperm storage tubuli of Red Jungle Fowl hens","volume":"50","author":"Atikuzzaman","year":"2015","journal-title":"Reprod. Domest. Anim."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1095\/biolreprod.115.130252","article-title":"Reduced Fertility and Altered Epididymal and Sperm Integrity in Mice Lacking ADAM71","volume":"93","author":"Choi","year":"2015","journal-title":"Biol. Reprod."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"E2148","DOI":"10.1002\/humu.21477","article-title":"Analysis of the disintegrin-metalloproteinases family reveals ADAM29 and ADAM7 are often mutated in melanoma","volume":"32","author":"Wei","year":"2011","journal-title":"Hum. Mutat."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1002\/gcc.22447","article-title":"Alterations of type II classical cadherin, cadherin-10 (CDH10), is associated with pancreatic ductal adenocarcinomas","volume":"56","author":"Jinawath","year":"2017","journal-title":"Genes Chromosom. Cancer"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1007\/s00438-018-1435-4","article-title":"HLA-C*06:02-independent, gender-related association of PSORS1C3 and PSORS1C1\/CDSN single-nucleotide polymorphisms with risk and severity of psoriasis","volume":"293","author":"Matusiak","year":"2018","journal-title":"Mol. Genet. Genom."},{"key":"ref_66","first-page":"1","article-title":"Integrin beta8 (ITGB8) activates VAV-RAC1 signaling via FAK in the acquisition of endometrial epithelial cell receptivity for blastocyst implantation","volume":"7","author":"Kumar","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fendo.2014.00004","article-title":"Angiopoietin-like proteins: A comprehensive look","volume":"5","author":"Santulli","year":"2014","journal-title":"Front. Endocrinol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.modgep.2004.06.006","article-title":"Differential downregulation of \u03b1T-catenin expression in placenta: Trophoblast cell type-dependent imprinting of the CTNNA3 gene","volume":"5","author":"Mulders","year":"2004","journal-title":"Gene Expr. Patterns"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-019-09829-z","article-title":"A conserved CCM complex promotes apoptosis non-autonomously by regulating zinc homeostasis","volume":"10","author":"Chapman","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1016\/j.jmb.2016.04.028","article-title":"Functional and Structural Insights of the Zinc-Finger HIT protein family members Involved in Box C\/D snoRNP Biogenesis","volume":"428","author":"Bragantini","year":"2016","journal-title":"J. Mol. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1016\/j.celrep.2015.04.060","article-title":"The CPEB3 Protein Is a Functional Prion that Interacts with the Actin Cytoskeleton","volume":"11","author":"Stephan","year":"2015","journal-title":"Cell Rep."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1694","DOI":"10.1016\/j.celrep.2015.04.061","article-title":"SUMOylation Is an Inhibitory Constraint that Regulates the Prion-like Aggregation and Activity of CPEB3","volume":"11","author":"Drisaldi","year":"2015","journal-title":"Cell Rep."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"12618","DOI":"10.1002\/jcb.28528","article-title":"miRNA-301b-3p accelerates migration and invasion of high-grade ovarian serous tumor via targeting CPEB3\/EGFR axis","volume":"120","author":"Liu","year":"2019","journal-title":"J. Cell. Biochem."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-3-319-50044-7_1","article-title":"Introduction to sumoylation","volume":"Volume 963","author":"Wilson","year":"2017","journal-title":"Advances in Experimental Medicine and Biology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1530\/REP-18-0417","article-title":"CXCL16\/CXCR6 interaction promotes endometrial decidualization via the PI3K\/AKT pathway","volume":"157","author":"Mei","year":"2019","journal-title":"Reproduction"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1095\/biolreprod.110.088591","article-title":"Seminal Fluid Regulates Accumulation of FOXP3+ Regulatory T Cells in the Preimplantation Mouse Uterus Through Expanding the FOXP3+ Cell Pool and CCL19-Mediated Recruitment1","volume":"85","author":"Guerin","year":"2011","journal-title":"Biol. Reprod."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e13028","DOI":"10.1111\/aji.13028","article-title":"The CXL12\/CXCR4\/CXCR7 axis in female reproductive tract disease: Review","volume":"80","author":"Krikun","year":"2018","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1095\/biolreprod.110.086231","article-title":"Activin A Balances Sertoli and Germ Cell Proliferation in the Fetal Mouse Testis","volume":"84","author":"Mendis","year":"2011","journal-title":"Biol. Reprod."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"D155","DOI":"10.1093\/nar\/gky1141","article-title":"miRBase: From microRNA sequences to function","volume":"47","author":"Kozomara","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1002\/mrd.22504","article-title":"A testis-specific gene, Ubqlnl, is dispensable for mouse embryonic development and spermatogenesis","volume":"82","author":"Yuan","year":"2015","journal-title":"Mol. Reprod. Dev."},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Mar\u00edn, I. (2014). The ubiquilin gene family: Evolutionary patterns and functional insights. BMC Evol. Biol., 14.","DOI":"10.1186\/1471-2148-14-63"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"4321","DOI":"10.1242\/dev.081869","article-title":"SUMO1-activating enzyme subunit 1 is essential for the survival of hematopoietic stem\/progenitor cells in zebrafish","volume":"139","author":"Li","year":"2012","journal-title":"Development"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/embor.2012.3","article-title":"DeSUMOylating isopeptidase: A second class of SUMO protease","volume":"13","author":"Shin","year":"2012","journal-title":"EMBO Rep."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1634","DOI":"10.1083\/jcb.201901115","article-title":"ATG9A shapes the forming autophagosome through Arfaptin 2 and phosphatidylinositol 4-kinase III\u03b2","volume":"218","author":"Judith","year":"2019","journal-title":"J. Cell Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"43549","DOI":"10.1074\/jbc.C200502200","article-title":"Neuronal leucine-rich repeat protein-3 amplifies MAPK activation by epidermal growth factor through a carboxyl-terminal region containing endocytosis motifs","volume":"277","author":"Fukamachi","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1603","DOI":"10.2147\/OTT.S118151","article-title":"TCF21 functions as a tumor suppressor in colorectal cancer through inactivation of PI3K\/AKT signaling","volume":"10","author":"Dai","year":"2017","journal-title":"Onco Targets Ther."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1111\/rda.13426","article-title":"Comparative proteomic analysis of high- and low-fertile buffalo bull spermatozoa for identification of fertility-associated proteins","volume":"54","author":"Kumaresan","year":"2019","journal-title":"Reprod. Domest. Anim."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.biopha.2015.06.005","article-title":"Annexin A7 modulates BAG4 and BAG4-binding proteins in mitochondrial apoptosis","volume":"74","author":"Du","year":"2015","journal-title":"Biomed. Pharmacother."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1101\/gr.772403","article-title":"PANTHER: A library of protein families and subfamilies indexed by function","volume":"13","author":"Thomas","year":"2003","journal-title":"Genome Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/5\/1572\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:01:40Z","timestamp":1760173300000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/5\/1572"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,25]]},"references-count":89,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,3]]}},"alternative-id":["ijms21051572"],"URL":"https:\/\/doi.org\/10.3390\/ijms21051572","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,25]]}}}