Characterization, identification and functional analysis of miRNA in seminal plasma exosomes of Yorkshire boar

SUN Yanmei; SUN Jingshuai; QIN Jiali; YUAN Renqiang; ZHU Xiaoping; ZHAO Yunxiang

doi:10.7671/j.issn.1001-411X.202205004

Journal of South China Agricultural University > 2023 > 44(3): 340-347. > DOI: 10.7671/j.issn.1001-411X.202205004

SUN Yanmei, SUN Jingshuai, QIN Jiali, et al. Characterization, identification and functional analysis of miRNA in seminal plasma exosomes of Yorkshire boar[J]. Journal of South China Agricultural University, 2023, 44(3): 340-347. DOI: 10.7671/j.issn.1001-411X.202205004

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Characterization, identification and functional analysis of miRNA in seminal plasma exosomes of Yorkshire boar

1.
School of Life Science and Engineering, Foshan University, Foshan 528231, China
2.
Guangxi Yangxiang Agriculture and Animal Husbandry Co., Ltd., Guigang 537000, China
3.
Guangxi Guigang Xiubo Gene Technology Co., Ltd., Guigang 537000, China

More Information

Received Date: December 31, 2022
Available Online: May 17, 2023

Graphical Abstract

Abstract

Abstract

Objective
Seminal plasma exosomes (spEXs) play a crucial role in sperm maturation, apoptosis and fertilization. This study was aimed to explore the miRNA expression of boar spEXs and the potential regulatory role of miRNA in sperm maturation and functional maintenance.

Method
The spEXs from Yorkshire boar semen were isolated and the exosomes were identified through transmission electron microscopy, nanoparticle tracking analysis, marker protein expression analysis and high-throughput miRNA sequencing.

Result
The spEXs were successfully isolated. A total of 329 spEX miRNAs were identified by miRNA sequencing. Through target gene prediction and functional enrichment analysis of highly expressed miRNAs, it was concluded that spEX miRNAs played potential regulatory roles in sperm ejaculation, P53 signaling pathway, prostate cancer, cell response to DNA damage stimuli, negative regulation of apoptosis, acrosome membrane binding, fertilization, etc.

Conclusion
This study provides basic data for spEX miRNAs regulating sperm motility and sperm fertilization, and provides references for studying the regulation mechanism of semen preservation.
- Seminal plasma exosome,
- Yorkshire boar,
- miRNA,
- Target gene,
- Sperm motility,
- Sperm apoptosis

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References (42)

References

[1]	SHAO H, IM H, CASTRO C M, et al. New technologies for analysis of extracellular vesicles[J]. Chemical Reviews, 2018, 118(4): 1917-1950. doi: 10.1021/acs.chemrev.7b00534
[2]	SUN J, ZHAO Y, HE J, et al. Small RNA expression patterns in seminal plasma exosomes isolated from semen containing spermatozoa with cytoplasmic droplets versus regular exosomes in boar semen[J]. Theriogenology, 2021, 176: 233-243. doi: 10.1016/j.theriogenology.2021.09.031
[3]	杜冠潮, 王福, 张继伟, 等. 精浆外泌体在精子成熟过程中的调节机制研究进展[J]. 山东医药, 2020, 60(36): 105-107. doi: 10.3969/j.issn.1002-266X.2020.36.028
[4]	THERY C, OSTROWSKI M, SEGURA E. Membrane vesicles as conveyors of immune responses[J]. Nature Reviews Immunology, 2009, 9(8): 581-593. doi: 10.1038/nri2567
[5]	SAINT-DIZIER M, MAHE C, REYNAUD K, et al. Sperm interactions with the female reproductive tract: A key for successful fertilization in mammals[J]. Molecular and Cellular Endocrinology, 2020, 516: 110956. doi: 10.1016/j.mce.2020.110956
[6]	秦佳丽, 孙敬帅, 曹婷婷, 等. 精浆外泌体的转运机制及生物学功能研究进展[J]. 中国畜牧杂志, 2022, 58(2): 52-58.
[7]	GUO H, CHANG Z, ZHANG Z, et al. Extracellular ATPs produced in seminal plasma exosomes regulate boar sperm motility and mitochondrial metabolism[J]. Theriogenology, 2019, 139: 113-120. doi: 10.1016/j.theriogenology.2019.08.003
[8]	杨秀芹, 万洪宇, 王金奎, 等. 猪miR-101表达特性分析[J]. 东北农业大学学报, 2016, 47(6): 74-80.
[9]	曲波, 甄贞, 仇有文, 等. 基于生物信息学方法挖掘奶山羊miRNAs研究[J]. 东北农业大学学报, 2015, 46(1): 86-93. doi: 10.3969/j.issn.1005-9369.2015.01.014
[10]	TWENTER H, KLOHONATZ K, DAVIS K, et al. Transfer of MicroRNAs from epididymal epithelium to equine spermatozoa[J]. Journal of Equine Veterinary Science, 2020, 87: 102841. doi: 10.1016/j.jevs.2019.102841
[11]	FOSHAY K M, GALLICANO G I. miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation[J]. Developmental Biology, 2009, 326(2): 431-443. doi: 10.1016/j.ydbio.2008.11.016
[12]	BOUHALLIER F, ALLIOLI N, LAVIAL F, et al. Role of miR-34c microRNA in the late steps of spermatogenesis[J]. RNA, 2010, 16(4): 720-731. doi: 10.1261/rna.1963810
[13]	薛林涛, 黄悦悦, 施文. 精浆外泌体在精子发生与功能调控中的研究进展[J]. 右江医学, 2021, 49(9): 706-709.
[14]	吴志胜, 陈慧芳, 刘俊杰, 等. 长白猪精浆外泌体miRNAs的鉴定与功能分析[J]. 农业生物技术学报, 2021, 29(2): 279-287.
[15]	白绪祥, 韩帅琪, 胡建宏. 猪精液常温保存研究进展[J]. 畜牧兽医杂志, 2021, 40(1): 28-30.
[16]	舒密. 外泌体miRNAs在结直肠癌中的研究进展[J]. 医学信息, 2021, 34(15): 15-18.
[17]	卞玉莹. 精浆外泌体miRNA作为男性不育症新型分子标志物的临床研究[D]. 镇江: 江苏大学, 2020.
[18]	MCGRAW L A, SUAREZ S S, WOLFNER M F. On a matter of seminal importance[J]. BioEssays, 2015, 37(2): 142-147. doi: 10.1002/bies.201400117
[19]	TEOW S, LIEW K, KHOO A S, et al. Pathogenic role of exosomes in Epstein-Barr virus (EBV)-associated cancers[J]. International Journal of Biological Sciences, 2017, 13(10): 1276-1286. doi: 10.7150/ijbs.19531
[20]	陈慧芳, 杨镁楹, 吴志胜, 等. 外泌体miRNA在配子发育和受精中的调控作用[J]. 中国畜牧杂志, 2021, 57(1): 17-24. doi: 10.19556/j.0258-7033.20200304-01
[21]	SANTONOCITO M, VENTO M, GUGLIELMINO M R, et al. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation[J]. Fertility and Sterility, 2014, 102(6): 1751-1761. doi: 10.1016/j.fertnstert.2014.08.005
[22]	ROUSH S, SLACK F J. The let-7 family of microRNAs[J]. Trends in Cell Biology, 2008, 18(10): 505-516. doi: 10.1016/j.tcb.2008.07.007
[23]	LUO Z, DAI X, RAN X, et al. Identification and profile of microRNAs in Xiang pig testes in four different ages detected by Solexa sequencing[J]. Theriogenology, 2018, 117: 61-71. doi: 10.1016/j.theriogenology.2017.06.023
[24]	CURRY E, SAFRANSKI T J, PRATT S L. Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility[J]. Theriogenology, 2011, 76(8): 1532-1539. doi: 10.1016/j.theriogenology.2011.06.025
[25]	LUO M, HAO L, HU F, et al. MicroRNA profiles and potential regulatory pattern during the early stage of spermatogenesis in mice[J]. Science China Life Sciences, 2015, 58(5): 442-450. doi: 10.1007/s11427-014-4737-8
[26]	WU W, HU Z, QIN Y, et al. Seminal plasma microRNAs: Potential biomarkers for spermatogenesis status[J]. Molecular Human Reproduction, 2012, 18(10): 489-497. doi: 10.1093/molehr/gas022
[27]	HOSSEINI S, HOSSEINI S, SALEHI M. Upregulation of Toll-like receptor 4 through anti-miR-Let-7a enhances blastocyst attachment to endometrial cells in mice[J]. Journal of Cellular Physiology, 2020, 235(12): 9752-9762. doi: 10.1002/jcp.29787
[28]	BISSONNETTE N, LÉVESQUE-SERGERIE J, THIBAULT C, et al. Spermatozoal transcriptome profiling for bull sperm motility: A potential tool to evaluate semen quality[J]. Reproduction (Cambridge, England), 2009, 138(1): 65-80. doi: 10.1530/REP-08-0503
[29]	WANG W, LIANG K, CHANG Y, et al. miR-26a is Involved in glycometabolism and affects boar sperm viability by targeting PDHX[J]. Cells, 2020, 9(1): 146. doi: 10.3390/cells9010146
[30]	范宇. 睾酮缺乏诱导miR-26a-5p和let-7g-5p作为信号递质靶向作用于PTEN和PMAIP1调控公猪精子细胞凋亡[D]. 雅安: 四川农业大学, 2018.
[31]	GODIA M, CASTELLÓ A, ROCCO M, et al. Identification of circular RNAs in porcine sperm and evaluation of their relation to sperm motility[J]. Scientific Reports, 2020, 10(1): 1-11. doi: 10.1038/s41598-019-56847-4
[32]	GONZALEZ-GONZALEZ E, LOPEZ-CASAS P P, DEL MAZO J. Gene silencing by RNAi in mouse Sertoli cells[J]. Reproductive Biology and Endocrinology, 2008, 6: 29. doi: 10.1186/1477-7827-6-29
[33]	KOTAJA N, BHATTACHARYYA S N, JASKIEWICZ L, et al. The chromatoid body of male germ cells: Similarity with processing bodies and presence of Dicer and microRNA pathway components[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(8): 2647-2652. doi: 10.1073/pnas.0509333103
[34]	HUNTER M P, ISMAIL N, ZHANG X, et al. Detection of microRNA expression in human peripheral blood microvesicles[J]. PLoS One, 2008, 3(11): e3694. doi: 10.1371/journal.pone.0003694
[35]	梅星星, 李小勇, 吴际. 一组miRNAs在睾丸发育中的表达及miR-125a对精原干细胞发育的调节作用[J]. 上海交通大学学报(医学版), 2015, 35(5): 625-630.
[36]	LI J, LIU X, HU X, et al. MicroRNA-10b regulates the renewal of spermatogonial stem cells through Kruppel-like factor 4[J]. Cell Biochemistry and Function, 2017, 35(3): 184-191. doi: 10.1002/cbf.3263
[37]	王道光. p53蛋白介导的细胞DNA损伤响应的动力学机制研究[D]. 南京: 南京大学, 2017.
[38]	SANTO G D, FRASCA M, BERTOLI G, et al. Identification of key miRNAs in prostate cancer progression based on miRNA-mRNA network construction[J]. Computational and Structural Biotechnology Journal, 2022, 20: 864-873. doi: 10.1016/j.csbj.2022.02.002
[39]	RAUHALA H E, JALAVA S E, ISOTALO J, et al. miR-193b is an epigenetically regulated putative tumor suppressor in prostate cancer[J]. International Journal of Cancer, 2010, 127(6): 1363-1372. doi: 10.1002/ijc.25162
[40]	MERKULOVA M, PĂUNESCU T G, AZROYAN A, et al. Mapping the H+ (V)-ATPase interactome: Identification of proteins involved in trafficking, folding, assembly and phosphorylation[J]. Scientific Reports, 2015, 5: 14827. doi: 10.1038/srep14827
[41]	SILVA J V, SANTIAGO J, SOUSA M, et al. New evidences of ubiquitin-proteasome system activity in human sperm[J]. Biochimica et Biophysica Acta-Molecular Cell Research, 2021, 1868(3): 118932. doi: 10.1016/j.bbamcr.2020.118932
[42]	IJIRI T W, MERDIUSHEV T, CAO W, et al. Identification and validation of mouse sperm proteins correlated with epididymal maturation[J]. Proteomics, 2011, 11(20): 4047-4062. doi: 10.1002/pmic.201100075

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