Next-generation sequencing analysis reveals segmental patterns of microRNA expression in yak epididymis
Wangsheng Zhao
A , Eugene Quansah A , Meng Yuan A , Pengcheng Li A , Chuanping Yi A , Xin Cai B C D and Jiangjiang Zhu B C D
+ Author Affiliations
- Author Affiliations
A School of Life Science and Engineering, Southwest University of Science and Technology, Mianyang, 621010 Sichuan, China.
B Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilisation (Southwest Minzu University), Ministry of Education, Chengdu, Sichuan 610041, China.
C Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilisation Key Laboratory of Sichuan Province, Chengdu, Sichuan 610041, China.
D Corresponding authors. Email: caixin2323@126.com; zhujiang4656@hotmail.com
Reproduction, Fertility and Development 32(12) 1067-1083 https://doi.org/10.1071/RD20113
Submitted: 9 May 2020 Accepted: 16 June 2020 Published: 27 July 2020
Abstract
MicroRNAs (miRNAs) have emerged as potent regulators of gene expression and are widely expressed in biological systems. In reproduction, they have been shown to have a significant role in the acquisition and maintenance of male fertility, whereby deletion of Dicer in mouse germ cells leads to infertility. Evidence indicates that this role of miRNAs extends from the testis into the epididymis, controlling gene expression and contributing to regional variations in gene expression. In this study, RNA sequencing technology was used to investigate miRNA expression patterns in the yak epididymis. Region-specific miRNA expression was found in the yak epididymis. In all, 683 differentially expressed known miRNAs were obtained; 190, 186 and 307 differentially expressed miRNAs were identified for caput versus corpus, corpus versus cauda and caput versus cauda region pairs respectively. Kyoto Encyclopedia of Genes and Genomes results showed endocytosis as the most enriched pathway across region pairs, followed by protein processing in the endoplasmic reticulum, phagosome, spliceosome and biosynthesis of amino acids in region pair-specific hierarchical order. Gene ontology results showed varied enrichment in terms including cell, biogenesis, localisation, binding and locomotion across region pairs. In addition, significantly higher miR-34c expression was seen in the yak caput epididymidis relative to the corpus and cauda epididymidis.
Additional keywords: Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway, miRNA sequencing, sperm maturation.
References
Abu-Halima, M., Hammadeh, M., Schmitt, J., Leidinger, P., Keller, A., Meese, E., and Backes, C. (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril. 99, 1249–1255.e16.| Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments.Crossref | GoogleScholarGoogle Scholar | 23312218PubMed |
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25–29.
| Gene ontology: tool for the unification of biology.Crossref | GoogleScholarGoogle Scholar | 10802651PubMed |
Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.
| MicroRNAs: genomics, biogenesis, mechanism, and function.Crossref | GoogleScholarGoogle Scholar | 14744438PubMed |
Belleannée, C., Belghazi, M., Labas, V., Teixeira‐Gomes, A., Gatti, J. L., Dacheux, J., and Dacheux, F. (2011a). Purification and identification of sperm surface proteins and changes during epididymal maturation. Proteomics 11, 1952–1964.
| Purification and identification of sperm surface proteins and changes during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 21472858PubMed |
Belleannée, C., Labas, V., Teixeira-Gomes, A.-P., Gatti, J. L., Dacheux, J.-L., and Dacheux, F. (2011b). Identification of luminal and secreted proteins in bull epididymis. J. Proteomics 74, 59–78.
| Identification of luminal and secreted proteins in bull epididymis.Crossref | GoogleScholarGoogle Scholar | 20692385PubMed |
Belleannée, C., Calvo, E., Thimon, V., Cyr, D. G., Légaré, C., Garneau, L., and Sullivan, R. (2012). Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One 7, e34996.
| Role of microRNAs in controlling gene expression in different segments of the human epididymis.Crossref | GoogleScholarGoogle Scholar | 22511979PubMed |
Björkgren, I., and Sipilä, P. (2015). The role of Dicer1 in the male reproductive tract. Asian J. Androl. 17, 737–741.
| The role of Dicer1 in the male reproductive tract.Crossref | GoogleScholarGoogle Scholar | 25994652PubMed |
Björkgren, I., Saastamoinen, L., Krutskikh, A., Huhtaniemi, I., Poutanen, M., and Sipilä, P. (2012). Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PLoS One 7, e38457.
| Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling.Crossref | GoogleScholarGoogle Scholar | 22701646PubMed |
Björkgren, I., Gylling, H., Turunen, H., Huhtaniemi, I., Strauss, L., Poutanen, M., and Sipilä, P. (2015). Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane. FASEB J. 29, 433–442.
| Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane.Crossref | GoogleScholarGoogle Scholar | 25366345PubMed |
Bouhallier, F., Allioli, N., Lavial, F., Chalmel, F., Perrard, M.-H., Durand, P., Samarut, J., Pain, B., and Rouault, J.-P. (2010). Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 16, 720–731.
| Role of miR-34c microRNA in the late steps of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 20150330PubMed |
Cannell, I. G., Kong, Y. W., Johnston, S. J., Chen, M. L., Collins, H. M., Dobbyn, H. C., Elia, A., Kress, T. R., Dickens, M., Clemens, M. J., Heery, D. M., Gaestel, M., Eilers, M., Willis, A. E., and Bushell, M. (2010). p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc. Natl Acad. Sci. USA 107, 5375–5380.
| p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication.Crossref | GoogleScholarGoogle Scholar | 20212154PubMed |
Chang, T.-C., Wentzel, E. A., Kent, O. A., Ramachandran, K., Mullendore, M., Lee, K. H., Feldmann, G., Yamakuchi, M., Ferlito, M., Lowenstein, C. J., Arking, D. E., Beer, M. A., Maitra, A., and Mendell, J. T. (2007). Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26, 745–752.
| Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis.Crossref | GoogleScholarGoogle Scholar | 17540599PubMed |
Chaurand, P., Fouchécourt, S., DaGue, B. B., Xu, B. J., Reyzer, M. L., Orgebin-Crist, M., and Caprioli, R. M. (2003). Profiling and imaging proteins in the mouse epididymis by imaging mass spectrometry. Proteomics 3, 2221–2239.
| Profiling and imaging proteins in the mouse epididymis by imaging mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 14595821PubMed |
Chen, C.-Y. A., Zheng, D., Xia, Z., and Shyu, A.-B. (2009). Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat. Struct. Mol. Biol. 16, 1160–1166.
| Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps.Crossref | GoogleScholarGoogle Scholar |
Chen, C., Cheng, P., Xie, H., Zhou, H., Wu, X., Liao, E., and Luo, X. (2014). MiR-503 regulates osteoclastogenesis via targeting RANK. J. Bone Miner. Res. 29, 338–347.
| MiR-503 regulates osteoclastogenesis via targeting RANK.Crossref | GoogleScholarGoogle Scholar | 23821519PubMed |
Cheng, C.-Y., Hwang, C.-I., Corney, D. C., Flesken-Nikitin, A., Jiang, L., Öner, G. M., Munroe, R. J., Schimenti, J. C., Hermeking, H., and Nikitin, A. Y. (2014). miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep. 6, 1000–1007.
| miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment.Crossref | GoogleScholarGoogle Scholar | 24630988PubMed |
Chong, Y., Zhang, J., Guo, X., Li, G., Zhang, S., Li, C., Jiao, Z., and Shao, M. (2014). MicroRNA-503 acts as a tumor suppressor in osteosarcoma by targeting L1CAM. PLoS One 9, e114585.
| MicroRNA-503 acts as a tumor suppressor in osteosarcoma by targeting L1CAM.Crossref | GoogleScholarGoogle Scholar | 25536034PubMed |
Chu, C., Zheng, G., Hu, S., Zhang, J., Xie, S., Ma, W., Ni, M., Tang, C., Zhou, L., Zhou, Y., Liu, M., Li, Y., and Zhang, Y. (2015). Epididymal region-specific miRNA expression and DNA methylation and their roles in controlling gene expression in rats. PLoS One 10, e0124450.
| Epididymal region-specific miRNA expression and DNA methylation and their roles in controlling gene expression in rats.Crossref | GoogleScholarGoogle Scholar | 26657110PubMed |
Concepcion, C. P., Han, Y.-C., Mu, P., Bonetti, C., Yao, E., D’andrea, A., Vidigal, J. A., Maughan, W. P., Ogrodowski, P., and Ventura, A. (2012). Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet. 8, e1002797.
| Intact p53-dependent responses in miR-34-deficient mice.Crossref | GoogleScholarGoogle Scholar | 22844244PubMed |
Corney, D. C., Hwang, C.-I., Matoso, A., Vogt, M., Flesken-Nikitin, A., Godwin, A. K., Kamat, A. A., Sood, A. K., Ellenson, L. H., Hermeking, H., and Nikitin, A. Y. (2010). Frequent downregulation of miR-34 family in human ovarian cancers. Clin. Cancer Res. 16, 1119–1128.
| Frequent downregulation of miR-34 family in human ovarian cancers.Crossref | GoogleScholarGoogle Scholar | 20145172PubMed |
Cornwall, G. A., Vreeburg, J. T., Holland, M. K., and Orgebin-Crist, M.-C. (1990). Interactions of labeled epididymal secretory proteins with spermatozoa after injection of 35S-methionine in the mouse. Biol. Reprod. 43, 121–129.
| Interactions of labeled epididymal secretory proteins with spermatozoa after injection of 35S-methionine in the mouse.Crossref | GoogleScholarGoogle Scholar | 2393685PubMed |
Dacheux, J. L., Belghazi, M., Lanson, Y., and Dacheux, F. (2006). Human epididymal secretome and proteome. Mol. Cell. Endocrinol. 250, 36–42.
| Human epididymal secretome and proteome.Crossref | GoogleScholarGoogle Scholar | 16431015PubMed |
Dacheux, J. L., Belleannée, C., Jones, R., Labas, V., Belghazi, M., Guyonnet, B., Druart, X., Gatti, J. L., and Dacheux, F. (2009). Mammalian epididymal proteome. Mol. Cell. Endocrinol. 306, 45–50.
| Mammalian epididymal proteome.Crossref | GoogleScholarGoogle Scholar | 19464100PubMed |
Donadeu, F. X., Schauer, S. N., and Sontakke, S. D. (2012). Involvement of miRNAs in ovarian follicular and luteal development. J. Endocrinol. 215, 323-334.
| Involvement of miRNAs in ovarian follicular and luteal development.Crossref | GoogleScholarGoogle Scholar | 23038794PubMed |
Frenette, G., Lessard, C., and Sullivan, R. (2002). Selected proteins of ‘prostasome-like particles’ from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol. Reprod. 67, 308–313.
| Selected proteins of ‘prostasome-like particles’ from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull.Crossref | GoogleScholarGoogle Scholar | 12080033PubMed |
Frey, F. P., Urbany, C., Hüttel, B., Reinhardt, R., and Stich, B. (2015). Genome-wide expression profiling and phenotypic evaluation of European maize inbreds at seedling stage in response to heat stress. BMC Genomics 16, 123.
| Genome-wide expression profiling and phenotypic evaluation of European maize inbreds at seedling stage in response to heat stress.Crossref | GoogleScholarGoogle Scholar | 25766122PubMed |
Gillis, A. J. M., Stoop, H. J., Hersmus, R., Oosterhuis, J. W., Sun, Y., Chen, C., Guenther, S., Sherlock, J., Veltman, I., Baeten, J., van der Spek, P. J., de Alarcon, P., and Looijenga, L. H. J. (2007). High-throughput microRNAome analysis in human germ cell tumours. J. Pathol. 213, 319–328.
| High-throughput microRNAome analysis in human germ cell tumours.Crossref | GoogleScholarGoogle Scholar |
Goossens, K., Mestdagh, P., Lefever, S., Van Poucke, M., Van Zeveren, A., Van Soom, A., Vandesompele, J., and Peelman, L. (2013). Regulatory microRNA network identification in bovine blastocyst development. Stem Cells Dev. 22, 1907–1920.
| Regulatory microRNA network identification in bovine blastocyst development.Crossref | GoogleScholarGoogle Scholar | 23398486PubMed |
Guyonnet, B., Marot, G., Dacheux, J. L., Mercat, M. J., Schwob, S., Jaffrézic, F., and Gatti, J. L. (2009). The adult boar testicular and epididymal transcriptomes. BMC Genomics 10, 369.
| The adult boar testicular and epididymal transcriptomes.Crossref | GoogleScholarGoogle Scholar | 19664223PubMed |
Guyonnet, B., Dacheux, F., Dacheux, J.-L., and Gatti, J.-L. (2011). The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J. Androl. 32, 651–664.
| The epididymal transcriptome and proteome provide some insights into new epididymal regulations.Crossref | GoogleScholarGoogle Scholar | 21764898PubMed |
Hagman, Z., Haflidadottir, B. S., Ansari, M., Persson, M., Bjartell, A., Edsjö, A., and Ceder, Y. (2013). The tumour suppressor miR-34c targets MET in prostate cancer cells. Br. J. Cancer 109, 1271–1278.
| The tumour suppressor miR-34c targets MET in prostate cancer cells.Crossref | GoogleScholarGoogle Scholar | 23922103PubMed |
He, L., He, X., Lim, L. P., De Stanchina, E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D., Jackson, A. L., Linsley, P. S., Chen, C., Lowe, S. W., Cleary, M. A., and Hannon, G. J. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447, 1130–1134.
| A microRNA component of the p53 tumour suppressor network.Crossref | GoogleScholarGoogle Scholar | 17554337PubMed |
He, Z., Kokkinaki, M., Pant, D., Gallicano, G. I., and Dym, M. (2009). Small RNA molecules in the regulation of spermatogenesis. Reproduction 137, 901–911.
| Small RNA molecules in the regulation of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 19318589PubMed |
Henderson, N. A., Cooke, G. M., and Robaire, B. (2006). Region-specific expression of androgen and growth factor pathway genes in the rat epididymis and the effects of dual 5α-reductase inhibition. J. Endocrinol. 190, 779–791.
| Region-specific expression of androgen and growth factor pathway genes in the rat epididymis and the effects of dual 5α-reductase inhibition.Crossref | GoogleScholarGoogle Scholar | 17003279PubMed |
Hinton, B. T., Lan, Z. J., Rudolph, D. B., Labus, J. C., and Lye, R. J. (1998). Testicular regulation of epididymal gene expression. J. Reprod. Fertil. Suppl. 53, 47–57.
| 10645265PubMed |
Jelinsky, S. A., Turner, T. T., Bang, H. J., Finger, J. N., Solarz, M. K., Wilson, E., Brown, E. L., Kopf, G. S., and Johnston, D. S. (2007). The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol. Reprod. 76, 561–570.
| The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides.Crossref | GoogleScholarGoogle Scholar | 17167166PubMed |
Johnston, D. S., Jelinsky, S. A., Bang, H. J., DiCandeloro, P., Wilson, E., Kopf, G. S., and Turner, T. T. (2005). The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol. Reprod. 73, 404–413.
| The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis.Crossref | GoogleScholarGoogle Scholar | 15878890PubMed |
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., and Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic Acids Res. 32, D277–D280.
| The KEGG resource for deciphering the genome.Crossref | GoogleScholarGoogle Scholar | 14681412PubMed |
Kim, Y. J., Bae, S. W., Yu, S. S., Bae, Y. C., and Jung, J. S. (2009). miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J. Bone Miner. Res. 24, 816–825.
| miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue.Crossref | GoogleScholarGoogle Scholar | 19063684PubMed |
Krawetz, S. A., Kruger, A., Lalancette, C., Tagett, R., Anton, E., Draghici, S., and Diamond, M. P. (2011). A survey of small RNAs in human sperm. Hum. Reprod. 26, 3401–3412.
| A survey of small RNAs in human sperm.Crossref | GoogleScholarGoogle Scholar | 21989093PubMed |
Krull, N., Ivell, R., Osterhoff, C., and Kirchhoff, C. (1993). Region-specific variation of gene expression in the human epididymis as revealed by in situ hybridization with tissue-specific cDNAs. Mol. Reprod. Dev. 34, 16–24.
| Region-specific variation of gene expression in the human epididymis as revealed by in situ hybridization with tissue-specific cDNAs.Crossref | GoogleScholarGoogle Scholar | 8418812PubMed |
Li, R., Zhang, C.-L., Liao, X.-X., Chen, D., Wang, W.-Q., Zhu, Y.-H., Geng, X.-H., Ji, D.-J., Mao, Y.-J., Gong, Y.-C., and Yang, Z.-P. (2015). Transcriptome microRNA profiling of bovine mammary glands infected with Staphylococcus aureus. Int. J. Mol. Sci. 16, 4997–5013.
| Transcriptome microRNA profiling of bovine mammary glands infected with Staphylococcus aureus.Crossref | GoogleScholarGoogle Scholar | 25749476PubMed |
Lian, J., Zhang, X., Tian, H., Liang, N., Wang, Y., Liang, C., Li, X., and Sun, F. (2009). Altered microRNA expression in patients with non-obstructive azoospermia. Reprod. Biol. Endocrinol. 7, 13-23.
| Altered microRNA expression in patients with non-obstructive azoospermia.Crossref | GoogleScholarGoogle Scholar |
Liu, D., Li, L., Fu, H., Li, S., and Li, J. (2012a). Inactivation of Dicer1 has a severe cumulative impact on the formation of mature germ cells in mouse testes. Biochem. Biophys. Res. Commun. 422, 114–120.
| Inactivation of Dicer1 has a severe cumulative impact on the formation of mature germ cells in mouse testes.Crossref | GoogleScholarGoogle Scholar | 22564735PubMed |
Liu, W.-M., Pang, R. T. K., Chiu, P. C. N., Wong, B. P. C., Lao, K., Lee, K.-F., and Yeung, W. S. B. (2012b). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc. Natl Acad. Sci. USA 109, 490–494.
| Sperm-borne microRNA-34c is required for the first cleavage division in mouse.Crossref | GoogleScholarGoogle Scholar | 22203953PubMed |
Love, M. I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.
| Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.Crossref | GoogleScholarGoogle Scholar | 25516281PubMed |
Lu, J., Gu, H., Tang, Q., Wu, W., Yuan, B., Guo, D., Wei, Y., Sun, H., Xia, Y., Ding, H., Hu, L., Chen, D., Sha, J., and Wang, X. (2016). Common SNP in hsa-miR-196a-2 increases hsa-miR-196a-5p expression and predisposes to idiopathic male infertility in Chinese Han population. Sci. Rep. 6, 19825.
| Common SNP in hsa-miR-196a-2 increases hsa-miR-196a-5p expression and predisposes to idiopathic male infertility in Chinese Han population.Crossref | GoogleScholarGoogle Scholar | 26805933PubMed |
Makker, A., Goel, M. M., Das, V., and Agarwal, A. (2012). PI3K–Akt–mTOR and MAPK signaling pathways in polycystic ovarian syndrome, uterine leiomyomas and endometriosis: an update. Gynecol. Endocrinol. 28, 175–181.
| PI3K–Akt–mTOR and MAPK signaling pathways in polycystic ovarian syndrome, uterine leiomyomas and endometriosis: an update.Crossref | GoogleScholarGoogle Scholar | 21916800PubMed |
McIver, S. C., Roman, S. D., Nixon, B., and McLaughlin, E. A. (2012a). miRNA and mammalian male germ cells. Hum. Reprod. Update 18, 44–59.
| miRNA and mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar | 21989172PubMed |
McIver, S. C., Stanger, S. J., Santarelli, D. M., Roman, S. D., Nixon, B., and McLaughlin, E. A. (2012b). A unique combination of male germ cell miRNAs coordinates gonocyte differentiation. PLoS One 7, e35553.
| A unique combination of male germ cell miRNAs coordinates gonocyte differentiation.Crossref | GoogleScholarGoogle Scholar | 22536405PubMed |
Mor, E., He, L., Torchinsky, A., and Shomron, N. (2014). MicroRNA-34a is dispensable for p53 function as teratogenesis inducer. Arch. Toxicol. 88, 1749–1763.
| MicroRNA-34a is dispensable for p53 function as teratogenesis inducer.Crossref | GoogleScholarGoogle Scholar | 24623309PubMed |
Mueller, D. W., and Bosserhoff, A. (2011). MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression. Int. J. Cancer 129, 1064–1074.
| MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression.Crossref | GoogleScholarGoogle Scholar | 21077158PubMed |
Nicholls, P. K., Harrison, C. A., Walton, K. L., McLachlan, R. I., O’Donnell, L., and Stanton, P. G. (2011). Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology 152, 1670–1683.
| Hormonal regulation of sertoli cell micro-RNAs at spermiation.Crossref | GoogleScholarGoogle Scholar | 21325043PubMed |
Niinuma, T., Suzuki, H., Nojima, M., Nosho, K., Yamamoto, H., Takamaru, H., Yamamoto, E., Maruyama, R., Nobuoka, R., Miyazaki, Y., Nishida, T., Bamba, T., Kanda, T., Ajioka, Y., Taguchi, T., Okahara, S., Takahashi, H., Nishida, Y., Hosokawa, M., Hasegawa, T., et al. (2012). Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res. 72, 1126–1136.
| Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors.Crossref | GoogleScholarGoogle Scholar | 22258453PubMed |
Novotny, G. W., Belling, K. C., Bramsen, J. B., Nielsen, J. E., Bork-Jensen, J., Almstrup, K., Sonne, S. B., Kjems, J., Rajpert-De Meyts, E., and Leffers, H. (2012). MicroRNA expression profiling of carcinoma in situ cells of the testis. Endocr. Relat. Cancer 19, 365–379.
| MicroRNA expression profiling of carcinoma in situ cells of the testis.Crossref | GoogleScholarGoogle Scholar | 22420006PubMed |
Olson, G. E., and Hinton, B. T. (1985). Regional differences in luminal fluid polypeptides of the rat testis and epididymis revealed by two-dimensional gel electrophoresis. J. Androl. 6, 20–34.
| Regional differences in luminal fluid polypeptides of the rat testis and epididymis revealed by two-dimensional gel electrophoresis.Crossref | GoogleScholarGoogle Scholar | 3972717PubMed |
Pan, Y., Shu, X., Sun, L., Yu, L., Sun, L., Yang, Z., and Ran, Y. (2017). miR-196a-5p modulates gastric cancer stem cell characteristics by targeting Smad4. Int. J. Oncol. 50, 1965–1976.
| miR-196a-5p modulates gastric cancer stem cell characteristics by targeting Smad4.Crossref | GoogleScholarGoogle Scholar | 28440445PubMed |
Papaioannou, M. D., and Nef, S. (2010). microRNAs in the testis: building up male fertility. J. Androl. 31, 26–33.
| microRNAs in the testis: building up male fertility.Crossref | GoogleScholarGoogle Scholar | 19875496PubMed |
Papaioannou, M. D., Pitetti, J.-L., Ro, S., Park, C., Aubry, F., Schaad, O., Vejnar, C. E., Kühne, F., Descombes, P., Zdobnov, E. M., McManus, M. T., Guillou, F., Harfe, B. D., Yan, W., Jégou, B., and Nef, S. (2009). Sertoli cell Dicer is essential for spermatogenesis in mice. Dev. Biol. 326, 250–259.
| Sertoli cell Dicer is essential for spermatogenesis in mice.Crossref | GoogleScholarGoogle Scholar | 19071104PubMed |
Papaioannou, M. D., Lagarrigue, M., Vejnar, C. E., Rolland, A. D., Kühne, F., Aubry, F., Schaad, O., Fort, A., Descombes, P., Neerman-Arbez, M., Guillou, F., Zdobnov, E. M., Pineau, C., and Nef, S. (2011). Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Mol. Cell. Proteomics 10, M900587MCP200.
| Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice.Crossref | GoogleScholarGoogle Scholar | 20467044PubMed |
Peng, Y., Liu, Y., Li, L., Wang, L., and Wu, X. (2014). microRNA-503 inhibits gastric cancer cell growth and epithelial-to-mesenchymal transition. Oncol. Lett. 7, 1233–1238.
| microRNA-503 inhibits gastric cancer cell growth and epithelial-to-mesenchymal transition.Crossref | GoogleScholarGoogle Scholar | 24944699PubMed |
Pera, I., Ivell, R., and Kirchhoff, C. (1994). Regional variation of specific gene expression in the dog epididymis as revealed by in-situ transcript hybridization. Int. J. Androl. 17, 324–330.
| Regional variation of specific gene expression in the dog epididymis as revealed by in-situ transcript hybridization.Crossref | GoogleScholarGoogle Scholar | 7744512PubMed |
Raver-Shapira, N., Marciano, E., Meiri, E., Spector, Y., Rosenfeld, N., Moskovits, N., Bentwich, Z., and Oren, M. (2007). Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 26, 731–743.
| Transcriptional activation of miR-34a contributes to p53-mediated apoptosis.Crossref | GoogleScholarGoogle Scholar | 17540598PubMed |
Reilly, J. N., McLaughlin, E. A., Stanger, S. J., Anderson, A. L., Hutcheon, K., Church, K., Mihalas, B. P., Tyagi, S., Holt, J. E., Eamens, A. L., and Nixon, B. (2016). Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Sci. Rep. 6, 31794.
| Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome.Crossref | GoogleScholarGoogle Scholar | 27549865PubMed |
Robaire, B., and Hamzeh, M. (2011). Androgen action in the epididymis. J. Androl. 32, 592–599.
| Androgen action in the epididymis.Crossref | GoogleScholarGoogle Scholar | 21764895PubMed |
Romero, Y., Meikar, O., Papaioannou, M. D., Conne, B., Grey, C., Weier, M., Pralong, F., De Massy, B., Kaessmann, H., Vassalli, J.-D., Kotaja, N., and Nef, S. (2011). Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS One 6, e25241.
| Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects.Crossref | GoogleScholarGoogle Scholar | 21998645PubMed |
Saez, F., Frenette, G., and Sullivan, R. (2003). Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J. Androl. 24, 149–154.
| Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells.Crossref | GoogleScholarGoogle Scholar | 12634297PubMed |
Schimanski, C. C., Frerichs, K., Rahman, F., Berger, M., Lang, H., Galle, P. R., Moehler, M., and Gockel, I. (2009). High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells. World J. Gastroenterol. 15, 2089.
| High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells.Crossref | GoogleScholarGoogle Scholar | 19418581PubMed |
Siersbæk, M. S., Loft, A., Aagaard, M. M., Nielsen, R., Schmidt, S. F., Petrovic, N., Nedergaard, J., and Mandrup, S. (2012). Genome-wide profiling of peroxisome proliferator-activated receptor γ in primary epididymal, inguinal, and brown adipocytes reveals depot-selective binding correlated with gene expression. Mol. Cell. Biol. 32, 3452–3463.
| Genome-wide profiling of peroxisome proliferator-activated receptor γ in primary epididymal, inguinal, and brown adipocytes reveals depot-selective binding correlated with gene expression.Crossref | GoogleScholarGoogle Scholar | 22733994PubMed |
Song, R., Walentek, P., Sponer, N., Klimke, A., Lee, J. S., Dixon, G., Harland, R., Wan, Y., Lishko, P., Lize, M., Kessel, M., and He, L. (2014). miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature 510, 115–120.
| miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110.Crossref | GoogleScholarGoogle Scholar | 24899310PubMed |
Soni, K., Choudhary, A., Patowary, A., Singh, A. R., Bhatia, S., Sivasubbu, S., Chandrasekaran, S., and Pillai, B. (2013). miR-34 is maternally inherited in Drosophila melanogaster and Danio rerio. Nucleic Acids Res. 41, 4470–4480.
| miR-34 is maternally inherited in Drosophila melanogaster and Danio rerio.Crossref | GoogleScholarGoogle Scholar | 23470996PubMed |
Streicher, K. L., Zhu, W., Lehmann, K. P., Georgantas, R. W., Morehouse, C. A., Brohawn, P., Carrasco, R. A., Xiao, Z., Tice, D. A., Higgs, B. W., Richman, L., Jallal, B., Ranade, K., and Yao, Y. (2012). A novel oncogenic role for the miRNA-506–514 cluster in initiating melanocyte transformation and promoting melanoma growth. Oncogene 31, 1558–1570.
| A novel oncogenic role for the miRNA-506–514 cluster in initiating melanocyte transformation and promoting melanoma growth.Crossref | GoogleScholarGoogle Scholar | 21860416PubMed |
Sullivan, R., Frenette, G., and Girouard, J. (2007). Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J. Androl. 9, 483–491.
| Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit.Crossref | GoogleScholarGoogle Scholar | 17589785PubMed |
Syntin, P., Dacheux, F., Druart, X., Gatti, J. L., Okamura, N., and Dacheux, J.-L. (1996). Characterization and identification of proteins secreted in the various regions of the adult boar epididymis. Biol. Reprod. 55, 956–974.
| Characterization and identification of proteins secreted in the various regions of the adult boar epididymis.Crossref | GoogleScholarGoogle Scholar | 8902205PubMed |
Tarasov, V., Jung, P., Verdoodt, B., Lodygin, D., Epanchintsev, A., Menssen, A., Meister, G., and Hermeking, H. (2007). Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6, 1586–1593.
| Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest.Crossref | GoogleScholarGoogle Scholar | 17554199PubMed |
Tazawa, H., Tsuchiya, N., Izumiya, M., and Nakagama, H. (2007). Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl Acad. Sci. USA 104, 15472–15477.
| Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells.Crossref | GoogleScholarGoogle Scholar | 17875987PubMed |
Tong, J. L., Zhang, C. P., Nie, F., Xu, X. T., Zhu, M. M., Xiao, S. D., and Ran, Z. H. (2011). MicroRNA 506 regulates expression of PPAR alpha in hydroxycamptothecin-resistant human colon cancer cells. FEBS Lett. 585, 3560–3568.
| MicroRNA 506 regulates expression of PPAR alpha in hydroxycamptothecin-resistant human colon cancer cells.Crossref | GoogleScholarGoogle Scholar | 22036718PubMed |
Tripurani, S. K., Lee, K.-B., Wee, G., Smith, G. W., and Yao, J. (2011). MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis. BMC Dev. Biol. 11, 25.
| MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 21548929PubMed |
Tscherner, A., Gilchrist, G., Smith, N., Blondin, P., Gillis, D., and LaMarre, J. (2014). MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reprod. Biol. Endocrinol. 12, 85.
| MicroRNA-34 family expression in bovine gametes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 25179211PubMed |
Wang, T., Ge, G., Ding, Y., Zhou, X., Huang, Z., Zhu, W., Shu, Y., and Liu, P. (2014). MiR-503 regulates cisplatin resistance of human gastric cancer cell lines by targeting IGF1R and BCL2. Chin. Med. J. (Engl.) 127, 2357–2362.
| 24931256PubMed |
Welch, C., Chen, Y., and Stallings, R. L. (2007). MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26, 5017–5022.
| MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells.Crossref | GoogleScholarGoogle Scholar | 17297439PubMed |
Wu, J., Mao, X., Cai, T., Luo, J., and Wei, L. (2006). KOBAS server: a web-based platform for automated annotation and pathway identification. Nucleic Acids Res. 34, W720–W724.
| KOBAS server: a web-based platform for automated annotation and pathway identification.Crossref | GoogleScholarGoogle Scholar | 16845106PubMed |
Xie, W., Lu, Q., Wang, K., Lu, J., Gu, X., Zhu, D., Liu, F., and Guo, G. (2018). miR-34b-5p inhibition attenuates lung inflammation and apoptosis in an LPS-induced acute lung injury mouse model by targeting progranulin. J. Cell. Physiol. 233, 6615–6631.
| miR-34b-5p inhibition attenuates lung inflammation and apoptosis in an LPS-induced acute lung injury mouse model by targeting progranulin.Crossref | GoogleScholarGoogle Scholar | 29150939PubMed |
Xu, C., Wu, S., Zhao, W., Mipam, T., Liu, J., Liu, W., Yi, C., alih Shah, M., Yu, S., and Cai, X. (2018). Differentially expressed microRNAs between cattleyak and yak testis. Sci. Rep. 8, 592.
| Differentially expressed microRNAs between cattleyak and yak testis.Crossref | GoogleScholarGoogle Scholar | 29330490PubMed |
Yang, D., Sun, Y., Hu, L., Zheng, H., Ji, P., Pecot, C. V., Zhao, Y., Reynolds, S., Cheng, H., Rupaimoole, R., Cogdell, D., Nykter, M., Broaddus, R., Rodriguez-Aguayo, C., Lopez-Berestein, G., Liu, J., Shmulevich, I., Sood, A. K., Chen, K., and Zhang, W. (2013). Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell 23, 186–199.
| Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer.Crossref | GoogleScholarGoogle Scholar | 23410973PubMed |
Yang, Y., Liu, L., Zhang, Y., Guan, H., Wu, J., Zhu, X., Yuan, J., and Li, M. (2014). MiR-503 targets PI3K p85 and IKK-β and suppresses progression of non-small cell lung cancer. Int. J. Cancer 135, 1531–1542.
| MiR-503 targets PI3K p85 and IKK-β and suppresses progression of non-small cell lung cancer.Crossref | GoogleScholarGoogle Scholar | 24550137PubMed |
Yang, X., Zang, J., Pan, X., Yin, J., Xiang, Q., Yu, J., Gan, R., and Lei, X. (2017). miR-503 inhibits proliferation making human hepatocellular carcinoma cells susceptible to 5-fluorouracil by targeting EIF4E. Oncol. Rep. 37, 563–570.
| miR-503 inhibits proliferation making human hepatocellular carcinoma cells susceptible to 5-fluorouracil by targeting EIF4E.Crossref | GoogleScholarGoogle Scholar | 27840964PubMed |
Young, M. D., Wakefield, M. J., Smyth, G. K., and Oshlack, A. (2012). goseq: gene ontology testing for RNA-seq datasets. Available at https://bioconductor.riken.jp/packages/devel/bioc/vignettes/goseq/inst/doc/goseq.pdf [verified 29 June 2020].
Zhang, J., Liu, Q., Zhang, W., Li, J., Li, Z., Tang, Z., Li, Y., Han, C., Hall, S. H., and Zhang, Y. (2010). Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim. Biophys. Sin. (Shanghai) 42, 145–153.
| Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides.Crossref | GoogleScholarGoogle Scholar | 20119626PubMed |
Zhang, Y., Chen, X., Lian, H., Liu, J., Zhou, B., Han, S., Peng, B., Yin, J., Liu, W., and He, X. (2014). MicroRNA-503 acts as a tumor suppressor in glioblastoma for multiple antitumor effects by targeting IGF-1R. Oncology Reports 31, 1445–1452
Zhao, W., Mengal, K., Yuan, M., Quansah, E., Li, P., Wu, S., Xu, C., Yi, C., and Cai, X. (2019a). Comparative RNA-seq analysis of differentially expressed genes in the epididymides of yak and cattleyak. Curr. Genomics 20, 293–305.
| Comparative RNA-seq analysis of differentially expressed genes in the epididymides of yak and cattleyak.Crossref | GoogleScholarGoogle Scholar | 32030088PubMed |
Zhao, W., Quansah, E., Yuan, M., Gou, Q., Mengal, K., Li, P., Wu, S., Xu, C., Yi, C., and Cai, X. (2019b). Region-specific gene expression in the epididymis of yak. Theriogenology 139, 132–146.
| Region-specific gene expression in the epididymis of yak.Crossref | GoogleScholarGoogle Scholar | 31404823PubMed |
Zou, Q., Mao, Y., Hu, L., Wu, Y., and Ji, Z. (2014). miRClassify: an advanced web server for miRNA family classification and annotation. Comput. Biol. Med. 45, 157–160.
| miRClassify: an advanced web server for miRNA family classification and annotation.Crossref | GoogleScholarGoogle Scholar | 24480175PubMed |
