小非编码RNA在雄性生殖发育和代际遗传中研究进展

doi:10.16288/j.yczz.24-335

遗传 ›› 2025, Vol. 47 ›› Issue (8): 861-875.doi: 10.16288/j.yczz.24-335

小非编码RNA在雄性生殖发育和代际遗传中研究进展

师愉倩¹^,²^,³(), 马剑峰¹^,²^,³, 陈思宇¹^,²^,³, 周立新⁴, 薛佳⁴, 沈林園¹^,²^,³, 朱砺¹^,²^,³(), 甘麦邻¹^,²^,³()

1.四川农业大学，猪禽种业全国重点实验室，成都 611130
2.四川农业大学，畜禽遗传资源发掘与创新利用四川省重点实验室，成都 611130
3.四川农业大学动物科技学院，农业农村部畜禽生物组学重点实验室，成都 611130
4.成都市动物疫病预防控制中心，成都 610041

收稿日期:2024-11-24 修回日期:2025-03-10 出版日期:2025-05-12 发布日期:2025-05-12
通讯作者: 朱砺，教授，博士生导师，研究方向：动物遗传育种与繁殖。E-mail: zhuli@sicau.edu.cn;
甘麦邻，博士，教授，研究方向：动物遗传育种与繁殖。E-mail: ganmailin@sicau.edu.cn
作者简介:师愉倩，硕士研究生，专业方向：动物遗传育种与繁殖。E-mail: 2023302150@stu.sicau.edu.cn
基金资助:
国家自然科学基金项目(32302689);四川省科技计划项目(2021YFYZ0007);四川省科技计划项目(2021ZDZX0008);四川省科技计划项目(2024NSFSC1176);国家现代农业产业技术体系四川生猪创新团队项目(SCCXTD-2024-8);国家生猪产业体系(CARS-35)

Progress on small non-coding RNAs in male reproductive development and intergenerational inheritance

Yuqian Shi¹^,²^,³(), Jianfeng Ma¹^,²^,³, Siyu Chen¹^,²^,³, Lixin Zhou⁴, Jia Xue⁴, Linyuan Shen¹^,²^,³, Li Zhu¹^,²^,³(), Mailin Gan¹^,²^,³()

1. National Key Laboratory of Pig and Poultry Seed Industry, Sichuan Agricultural University, Chengdu 611130, China
2. Sichuan Provincial Key Laboratory of Exploration and Innovative Utilization of Livestock and Poultry Genetic Resources, Sichuan Agricultural University, Chengdu 611130, China
3. Key Laboratory of Livestock and Poultry Biomics, Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
4. Chengdu City Animal Disease Prevention and Control Center, Chengdu 610041, China

Received:2024-11-24 Revised:2025-03-10 Published:2025-05-12 Online:2025-05-12
Supported by:
National Natural Science Foundation of China(32302689);Sichuan Province Science and Technology Plan Project(2021YFYZ0007);Sichuan Province Science and Technology Plan Project(2021ZDZX0008);Sichuan Province Science and Technology Plan Project(2024NSFSC1176);National Modern Agricultural Industry Technology System Sichuan Pig Innovation Team Project(SCCXTD-2024-8);National Pig Industry System(CARS-35)

摘要/Abstract

摘要：

作为表观遗传的重要研究内容，小非编码RNA (small non-coding RNAs，sncRNAs)在雄性生殖正常发育和代际遗传中发挥着重要的调控作用。研究表明，哺乳动物雄性生殖细胞中高度表达的小非编码RNA包括miRNA、piRNA和tsRNA等，在维持雄性生殖细胞发育和精子发生等过程中发挥重要作用。sncRNAs通过调控基因表达、影响蛋白翻译、改变精子表观遗传修饰等方式参与维持不同阶段的雄性生殖发育过程，其表达异常与雄性不育密切相关。此外，越来越多的证据表明，环境暴露影响精子的表观遗传修饰，这种表观遗传修饰的变化常导致后代表型发生改变。本文系统总结了雄性生殖细胞中sncRNAs的种类及其发挥的功能，介绍了各种因素环境暴露引起的代际遗传中sncRNAs的作用，以期为雄性生殖健康的研究提供新的视角和理论依据，为预防和治疗雄性不育及相关生殖疾病提供潜在的靶点和策略。

关键词: sncRNA, 雄性生殖, 精子发生, 代际遗传

Abstract:

Small non-coding RNAs (sncRNAs) are crucial in epigenetics, playing a significant regulatory role in the normal development and intergenerational inheritance of male reproduction. Research has shown that highly expressed sncRNAs, including miRNAs, piRNAs, and tsRNAs, are vital in maintaining male germ cell development and spermatogenesis. sncRNAs regulate gene expression, influence protein translation, and modify sperm epigenetics, contributing to male reproductive development at various stages. Abnormal expression of sncRNAs is closely linked to male infertility. Furthermore, growing evidence suggests that environmental exposures affect sperm epigenetic modifications, often leading to phenotypic changes in future generations. In this review, we summarize the types and functions of sncRNAs in male germ cells and examine their role in intergenerational inheritance due to environmental factors. It aims to provide new insights into male reproductive health and potential targets for preventing and treating male infertility and related diseases.

Key words: sncRNA, male reproduction, spermatogenesis, intergenerational inheritance

师愉倩, 马剑峰, 陈思宇, 周立新, 薛佳, 沈林園, 朱砺, 甘麦邻. 小非编码RNA在雄性生殖发育和代际遗传中研究进展[J]. 遗传, 2025, 47(8): 861-875.

Yuqian Shi, Jianfeng Ma, Siyu Chen, Lixin Zhou, Jia Xue, Linyuan Shen, Li Zhu, Mailin Gan. Progress on small non-coding RNAs in male reproductive development and intergenerational inheritance[J]. Hereditas(Beijing), 2025, 47(8): 861-875.

图/表 2

图1

表1

雄性生殖相关疾病sncRNAs生物标志物"

表型	物种	样本类型	小非编码RNA	可能作用靶标和机理	参考文献
非梗阻性无精子症	人	睾丸	miR-370-3p、miR-10b-3p、miR-539-5p和miR-22-5p上调；miR-34b-5p、miR-516b-5p和miR-122-5p下调	通过靶向与精子生成相关的基因，并调控这些基因表达，影响精子发生过程中细胞分化和发育	[55]
弱精子症	人	精子	let-7a、miR-7-1-3p、miR-141、miR-200a和miR-429与精液浓度负相关，miR-15b、miR-34b和miR-122与精液浓度正相关	miR-141通过靶向SPAG9的3′-UTR，抑制其表达，进而影响精子活力；miR-429通过靶向HSPA4L的3′-UTR抑制其表达，从而影响精子的活力和存活率；miR-15b通过靶向CDC25A的3′-UTR，调节细胞周期进程，促进精子发生	[56]
不育	人	精子	hsa-mir-9-3p、hsa-mir-30b-5p和hsa-mir-122-5p上调	hsa-miR-122-5p通过靶向ADAM10，阻断Notch信号通路，进而影响细胞的增殖和迁移；在精子发生中，其上调可能通过抑制TNP2的表达，影响精子形成过程中的染色质压缩	[57]
非梗阻性无精子症	人	睾丸、精液	piR-31704、piR-31843、piR-36659、piR-45048、piR-46102、piR-55522、piR-60351和piR-61927与精液浓度正相关	通过靶向调控生殖细胞发育、细胞周期、代谢过程和精子成熟，影响精子生成和精液质量	[58]
不育	人	精浆	hsa-mir-7110、hsa-mir-4800、hsa-mir-4488、hsa-mir-3916和hsa-mir-4508上调	hsa-mir-7110通过靶向IGF2BP2的3′-UTR，抑制其表达；IGF2BP2在细胞增殖和代谢中起重要作用，其抑制可能导致生殖细胞发育受阻，进而影响精子发生；hsa-mir-4508通过靶向RFX1，抑制其表达，进而影响细胞内的信号传导和基因调控	[59]
不育	人	精子	15种miRNA的表达上调，5种miRNA表达下调	miR-130a通过下调AR表达，干扰精子发生；miR-29b-3p下调通过调节TRPV4表达，影响生精细胞凋亡	[60]
高原生质滴精子	猪	精浆	ssc-miR-101、ssc-miR-148a-5p和ssc-miR-184等13种miRNA上调；ssc-miR-1249、ssc-mir-155-5p和ssc-miR-296-5p下调	ssc-miR-101通过抑制PI3K-AKT信号通路，可能影响细胞凋亡和存活，进而调节精子发生；miR-155-5p通过靶向多种与细胞凋亡和炎症相关的基因，在精子发生中，可能通过类似机制影响生殖细胞的存活和功能	[61]
精液质量	猪	精浆	miR-205和miR-378b-3p在低质量组中上调	miR-205-5p通过靶向ANGPT2抑制细胞增殖和迁移；在精液中，miR-205-5p的上调可能通过抑制ANGPT2，影响精子发生过程中的细胞功能	[62]
精液质量	猪	精浆	ssc-miR-122-p、ssc-miR-486、ssc-miR-345-p、ssc-miR-362和ssc-miR-500-5p作为预测精子活力的潜在标志物	miR-122-p可能通过靶向CBL(casitas B-lineage lymphoma)基因，调节精子干细胞(SSCs)的增殖和DNA合成，同时抑制早期凋亡，对精子发生过程中的细胞存活和功能发挥重要作用	[63]
低繁殖力	牛	睾丸、精子	miR-19a、miR-142和miR-143上调；miR-7d、miR-23a和miR-23b下调	miR-19a通过靶向CLCA4抑制其表达，在生殖细胞中影响精子发生过程中的细胞功能；miR-23a通过靶向NID2和PPP2R5E，促进细胞增殖和抑制凋亡，进而影响精子发生	[64]
低繁殖力	牛	精子	miR-2385-5p(下调)和miR-98(上调)与牛生育能力显著相关	miR-98可能通过靶向调控细胞凋亡和信号传导相关基因，影响精子的存活和功能	[65]
弱精子症	人	精子	piR-1207和piR-2107下调	piR-1207和piR-2107可以共同靶向SEMG1基因的编码序列(CDS区)，通过结合SEMG1 mRNA抑制其表达	[66]
弱精子症	人	精子	piR-hsa-32694、piR-hsa-26591、piR-hs-18725和piR-hsa-18586的表达显著上调	piR-hsa-26591可能靶向CFAP45和BRD2；CFAP45在低活力精子中的表达显著增加，而BRD2在弱精子症患者中的表达显著降低，piR-hsa-26591可能通过沉默这些基因的表达，导致精子活力下降	[67]
不育	人	精浆	piR-28478和piR-1077上调	piR-1077可能通过靶向与精子成熟或运动相关的基因，影响精子的最终功能	[68]
非梗阻性无精子症	人	睾丸	1,328个piRNAs差异表达，其中1,322个下调，6个上调	piRNA的失调通过转座子沉默，破坏基因组稳定性；靶向mRNA调控基因表达导致精子发生过程中关键基因表达异常	[69]
精液质量	猪	精子	piR-ssc-120840、piR-ssc-120840、piR-ssc-117286、piR-ssc-127298、piR-ssc-114575、piR-ssc- 1272746、piR-ssc-887100和piR-ssc-1133701与精子质量显著负相关	piR-ssc-120840的异常表达可能通过干扰精子发生过程中的基因表达模式，导致精子发生受阻或异常，进而影响精子的质量和数量	[70]
低繁殖力	羊	睾丸	206个piRNA簇在高繁殖力品种中上调	piRNA簇在生殖干细胞的维持和分化中发挥重要作用	[71]
非梗阻性无精子症	人	精浆	tRF-Val-AAC-010和tRF-Pro-AGG-003上调	通过调控精子发生过程中的基因表达，影响生殖细胞的增殖、分化和成熟，并作为诊断非梗阻性无精子症的潜在生物标志物	[72]
非梗阻性无精子症	人	血液	tRF-Gly-GCC-002与tRF-Glu-CC-005是NOA患者进行睾丸显微提取精子手术的生物标志物	通过调控神经内分泌蛋白代谢和发育相关通路中的靶基因，影响精子发生过程	[73]
低繁殖力	牛	精子	tRX-Glu-NNN-3811是预测奶牛生育力的标志物	通过调节非编码RNA加工来影响胚胎基因组激活	[65]

表1

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小非编码RNA在雄性生殖发育和代际遗传中研究进展

Progress on small non-coding RNAs in male reproductive development and intergenerational inheritance

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