调节性小非编码RNA在精子发生过程中的作用研究进展

刘永珍, 戚新明, 宫丽崑, 任进, 邓中平

中国药学杂志 ›› 2019, Vol. 54 ›› Issue (6) : 429-436.

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中国药学杂志
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中国药学杂志 ›› 2019, Vol. 54 ›› Issue (6) : 429-436. DOI: 10.11669/cpj.2019.06.001
综述

调节性小非编码RNA在精子发生过程中的作用研究进展

  • 刘永珍1,2, 戚新明2, 宫丽崑2, 任进2*, 邓中平1*
作者信息 +

Roles of Regulatory Small Non-coding RNAs in the Spermatogenesis

  • LIU Yong-zhen1,2, QI Xin-ming2, GONG Li-kun2, REN Jin2*, DENG Zhong-ping1*
Author information +
文章历史 +

摘要

非编码RNA(non-coding RNA,ncRNA)在生物体内大量存在,组成复杂的生物调控网络,是目前生物医学领域的研究热点之一。调节性小非编码RNA(small ncRNA,sncRNA),如微小RNA(microRNA)、内源性小干扰RNA(siRNA)和PIWI相互作用RNA(piRNA)是基因表达调控的关键成员,调控着细胞内的多种生理和病理过程。男性不育已经成为一个全球性的健康问题,主要与已知或未知原因引起的精子发生障碍从而导致的无精子症、少精子症或弱精子症有关。近十年来的研究表明,调节性sncRNA通过沉默活性转座子元件和调控编码基因等方式在雄性生殖细胞发育、分化、成熟以及功能发挥等过程中发挥重要作用,这些sncRNA,尤其是在雄性生殖细胞富集表达的piRNA,在生精细胞发育的不同阶段的异常表达与雄性不育密切相关。笔者对调节性sncRNA(尤其是piRNA)在精子发生过程中的作用及其研究进展进行总结,以期为后续相关研究以及男性不育的诊断、干预和治疗提供参考。

Abstract

Non-coding RNA (ncRNA), expressed widely in organisms and comprised of a complex, regulatory and controlling biologically network, is an emerging theme in the biomedicine field at present. Regulatory sncRNAs, for example, microRNA (miRNA), endogenous small interfering RNA (siRNA) and PIWI-interacting RNA (piRNA), are the key members of the gene regulatory network and play important roles in the regulation of multiple pathophysiological activities in cells. Male infertility, a serious social problem all over the world, is mainly related the malfunctions of the spermatogenesis caused by known or unknown factors; and finally result in azoospermia, oligozoospermia or asthenospermia. Recent research indicated that regulatory sncRNAs play important roles in the development, differentiation and mature of the germ cells and their functions at different stages by silencing the transposable elements and regulating the expression of coding gene; and their abnormal expression in germ cells at different stage is closely related to male infertility. In this review, the roles and recent progresses of regulatory sncRNA focusing on piRNA to provide insight for future research in this field and for the diagnoses, interventions and treatments of male infertility are briefly summarized.

关键词

小非编码RNA / 非编码RNA / 微小RNA / 小干扰RNA / PIWI相互作用RNA / 精子发生

Key words

sncRNA / ncRNA / miRNA / siRNA / piRNA / spermatogenesis

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刘永珍, 戚新明, 宫丽崑, 任进, 邓中平. 调节性小非编码RNA在精子发生过程中的作用研究进展[J]. 中国药学杂志, 2019, 54(6): 429-436 https://doi.org/10.11669/cpj.2019.06.001
LIU Yong-zhen , QI Xin-ming , GONG Li-kun , REN Jin , DENG Zhong-ping. Roles of Regulatory Small Non-coding RNAs in the Spermatogenesis[J]. Chinese Pharmaceutical Journal, 2019, 54(6): 429-436 https://doi.org/10.11669/cpj.2019.06.001
中图分类号： R965   

参考文献

[1] QI L, LI X M, ZHANG S G, et al. Genetic regulation by non-coding RNAs. Sci China Ser C(中国科学C辑), 2006, 49 (3):201-217.
[2] SOICHIRO Y, MITSUHO I S, YUICHIRO T, et al. Interaction and crosstalk between noncoding RNAs. Cell Mol Life Sci, 2018,75(3):467-484.
[3] SAXE J P, LIN H. Small noncoding RNAs in the germline. Cold Spring Harb Perspect Biol, 2011, 3(9):a002717.
[4] SALAS H A, BLANCO J, VIDAL F, et al. Spermatozoa from normozoospermic fertile and infertile individuals convey a distinct miRNA cargo. Andrology, 2016, 4(6):1028-1036.
[5] L M, TIAN H, CAO Y X, et al. Downregulation of miR-320a/383-sponge-like long non-coding RNA NLC1-C (narcolepsy candidateregion 1 genes) is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation. Cell Death Dis, 2015, 6(11):e1960-1966.
[6] HAN X D, ZHOU H. Updated relationship of microRNA with male reproduction. Natl J Androl(中华男科学杂志), 2015, 21(11):963-966.
[7] RAJENDER S, MEADOR C, AGARWAL A. Small RNA in spermatogenesis and male infertility. Front Biosci (Schol Ed), 2012, 4:1266-1274.
[8] LEE T L, PANG A L Y, RENNERT O M, et al. Genomic landscape of developing male germ cells. Birth Defects Res C Embryo Today, 2009, 87(1):43-63.
[9] CHRISTINA E, DUNCAN T O, CLAUDIA K, et al. The emergence of piRNAs against transposon invasion to preserve mammalian genome integrity. Nat Commun, 2017, 8:1411.
[10] LEGRAND J M D, HOBBS R M. RNA processing in the male germline:mechanisms and implications for fertility. Semin Cell Dev Biol, 2018, 79:80-91.
[11] BAEK D, VILLEN J, SHIN C, et al. The impact of microRNAs on protein output. Nature, 2008(7209),455:64-71.
[12] CHI S W, ZANG J B, MELE A, et al. Argonaute HITSCLIP decodes microRNA-mRNA interaction maps. Nature, 2009, 460:479-486.
[13] SOOD P, KREK A, ZAVOLAN M, et al. Cell-type-specific signatures of microRNAs on target mRNA expression. PNAS, 2006, 103(8):2746-2751.
[14] DENLI A M, TOPS B B, PLAATERK R H, et al. Processing of primary microRNAs by the microprocessor complex. Nature, 2004, 432(7014):231-235.
[15] GREGORY R I, YAN K P, AMUTHAN G, et al. The microprocessor complex mediates the genesis of microRNAs. Nature, 2004, 432(7014):235-240.
[16] LEE Y, AHN C, HAN J J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature, 2003, 425(6956):415-419.
[17] LUND E, GUTTINGER S, CALADO A, et al. Nuclear export of microRNA precursors. Science, 2004, 303(5654):95-98.
[18] YI R, QIN Y, MACARA I G, et al. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Deve, 2003, 17(24):3011-3016.
[19] RUBY J G, JAN C H, BARTEL D P. Intronic microRNA precursors that bypass Drosha processing. Nature, 2007, 448(7149):83-86.
[20] NAQVI A R, ISLAM M N, CHOUDHURY N R, et al. The fascinating world of RNA interference. Int J Biol Sci, 2009, 5(2):97-117.
[21] NILSEN T W. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet, 2007, 23(5):243-249.
[22] BARTEL D P. MicroRNAs:genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2):281-297.
[23] WINTER J, JUNG S, KELLER S, et al. Many roads to maturity:microRNA biogenesis pathways and their regulation. Nat Cell Biol, 2009, 11(3):228-234.
[24] LEE R C, FEINBAUM R L, AMBROS V, et al. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5):843-854.
[25] REINHART B J, SLACK F J, BASSON M, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 2000, 403(6772):901-906.
[26] HAYASHI K, DE SONSA M C, KANEDA M, et al. MicroRNA bogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One, 2008, 3( 3):e1738.
[27] OLIVE V, BENNETT M J, WALKER J C, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev, 2009, 23(24):2839-2849.
[28] NIU Z Y, GOODYEAR S M, RAO S, et al. MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. PNAS, 2011, 108(31):12740-12745.
[29] HE Z, JIANG J, KOKKINAKI M, et al. miRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells, 2013, 31(10):2205-2217.
[30] CHEN J, CAI T X, ZHENG C W, et al. MicroRNA-202 maintains spermatogonial stem cells by inhibiting cell cycle regulators and RNA binding proteins. Nucleic Acids Res, 2017, 45(7):4142-4157.
[31] VAN DEN DRIESCHE S, SHARPE R M, SAUNDERS P K, et al. Regulation of the germ stem cell niche as the foundation for adult spermatogenesis: a role for miRNAs. Semin Cell Dev Biol, 2014, 29:76-83.
[32] CUI N, HAO G M, ZHAO Z M, et al. MicroRNA-224 regulates self-renewal of mouse spermatogonial stem cells via targeting DMRT1. J Cell Mol Med, 2016, 20(8):1503-1512.
[33] MORITOKI Y, HAYASHI Y, MIZUNO K, et al. Expression profiling of microRNA in cryptorchid testes:miR-135a contributes to the maintenance of spermatogonial stem cells by regulating Foxo1. J Urol, 2014, 191(4):1174-1180.
[34] TONG M H, MITCHELL D A, MCGOWAN S D, et al. Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice. Biol Reprod, 2012, 86 (3):72.
[35] ZHOU Y, XIANG Z, LI D, et al. Regulation of microcystin-LR-induced toxicity in mouse spermatogonia by miR-96. Environ Sci Technol, 2014, 48 (11):6383-6390.
[36] SHEN G, WU R, LIU B, et al. Upstream and downstream mechanisms for the promoting effects of IGF-1 on differentiation of spermatogonia to primary spermatocytes. Life Sci, 2014, 101 (1):49-55.
[37] BOUHALLIER F, ALLIOLI N, LAVIAL F, et al. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA, 2010, 16(4):720-731.
[38] LIANG X X, ZHOU D D, WEI C, et al. MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS One, 2012, 7 (3): e33861.
[39] CORNEY D C, FLESKEN-NIKITIN A, GODWIN A K, et al. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res, 2007, 67 (8):8433-8438.
[40] BAO J, LI D, WANG L, et al. MicroRNA-449 and microRNA-34b /c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. J Biol Chem, 2012, 287(26):21686-21698.
[41] CHEN X X, LI X L, GUO J Y, et al. The roles of microRNAs in regulation of mammalian spermatogenesis. J Anim Sci Biotechnol, 2017, 8:35.
[42] LIU T, HUANG Y, LIU J, et al. MicroRNA-122 influences the development of sperm abnormalities from human induced pluripotent stem cells by regulating TNP2 expression. Stem Cells Dev, 2013, 22 (12):1839-1850.
[43] KOTAJA N. MicroRNAs and spermatogenesis. Fertil Steril, 2014, 101 (6):1552-1562.
[44] WU J W, BAO J Q, WANG L, et al. MicroRNA-184 down regulates nuclear receptor corepressor 2 in mouse spermatogenesis. BMC Dev Biol, 2011, 11 (1):64.
[45] WATANABE T, TOTOKI Y, TOYODA A, et al. Endogenous siRNAs from naturally formed dsRNA regulate transcripts in mouse oocytes. Nature, 2008, 453(7194):539-543.
[46] TAM O, ARAVIN A, STEIN P, et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature, 2008, 453(7194):534-538.
[47] KIM V N, HAN J, SIOMI M C. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol, 2009, 10:126-139.
[48] TOMARI Y, MATRANGA C, HALEY B, et al. A protein sensor for siRNA asymmetry. Science, 2004, 306 (5700):1377-1380.
[49] VALENCIA-SANCHEZ M A, LIU J, HANNON G J, et al. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev, 2006, 20(5):515-524.
[50] OHRT T, MTZE J, STAROSKE W, et al. Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC in vivo in human cells. Nucleic Acids Res, 2008, 36(20):6439-6449.
[51] DING S W, VOINNET O. Antiviral immunity directed by small RNAs. Cell, 2007, 130:413-426.
[52] BORSANI O, ZHU J, VERSLUES P E, et al. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell, 2005, 123(7):1279-1291.
[53] LEE R C, HAMMELL C M, AMBROS V, et al. Interacting endogenous and exogenous RNAi pathways in Caenorhabditis elegans. RNA, 2006, 12 (4):589-597.
[54] ARAVIN A A, KLENOV M S, VAGIN V V, et al. Dissection of a natural RNA silencing process in the Drosophila melanogaster germline. Mol Cell Biol, 2004 (24):6742-6750.
[55] BAULCOMBE D. Viruses and gene silencing in plants. Arch Virol, 1999, 15(suppl):189-201.
[56] HE L, HANNON G J. MicroRNAs:small RNAs with a big role in gene regulation. Nat Rev Genet, 2004, 5(7):522-531.
[57] BABIARZ J, RUBY J G, WANG Y, et al. Mouse ES cells express endogenous shRNA, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev, 2008, 22(27):2773-2785.
[58] SONG R, HENNIG G, WU Q, et al. Male germ cells express abundant endogenous siRNAs. PNAS, 2011,108 (32):13159-13164.
[59] ZHANG H, LIU J L, TAI Y R, et al. Identification and characterization of L1-specific endo-siRNAs essential for early embryonic development in pig. Oncotarget, 2017, 8(14):23167-23176.
[60] TAN T, ZHANG Y, JI W, et al. miRNA signature in mouse spermatogonial stem cells revealed by high-throughput sequencing. Biomed Res Int, 2014,2014:154251.
[61] COCQUET J, ELLIS P J, YAMAUCHI Y, et al. Deficiency in the multicopy Sycp3-like X-linked genes Slx and Slxl1 causes major defects in spermatid differentiation. Mol Biol Cell, 2010, 21 (20):3497-3505.
[62] WONG E W, MRUK D D, LEE W M, et al. Par3 /Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. PNAS, 2008, 105 (28):9657-9662.
[63] YAN H H, MRUK D D, WONG E W, et al. An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA, 2008, 105 (26):8950-8955.
[64] OATLEY J M, AVARBOCK M R, BRINSTER R L. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem, 2007, 282(35):25842-25851.
[65] CARISSIMI C, LAUDADIO I, CIPOLLETTA E, et al. ARGONAUTE2 cooperates with SWI/SNF complex to determine nucleosome occupancy at human transcription start sites. Nucleic Acids Res, 2015, 43(3):1498-1512.
[66] ARAVIN A, GAIDATZIS D, PFEFFER S, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 2006, 442(7099):203-207.
[67] GIRARD A, SACHIDANANDAM R, HANNON G J, et al. A germline specific class of small RNAs binds mammalian Piwi proteins. Nature, 2006, 442(7099):199-202.
[68] GRIVNA S T, BEYRET E, WANG Z, et al. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev, 2006, 20(13):1709-1714.
[69] LAU N C, SETO A G, KIM J, et al. Characterization of the piRNA complex from rat testes. Science, 2006, 313 (5785):363-367.
[70] YUKA W, IWASAKI, MIKIKO C, et al. Siomi and haruhiko siomi. PIWI-interacting RNA:its biogenesis and functions. Annu Rev Biochem, 2015, 84:405-433.
[71] HIROTSUGU I, HARUHIKO S, MIKIKO C S. Biology of PIWI-interacting RNAs:new insights into biogenesis and function inside and outside of germlines. Gents Dev, 2012, 26(21):2361-2373.
[72] THOMSON T, LIN H. The biogenesis and function of PIWI proteins and piRNAs:progress and prospect. Annu Rev Cell Dev Biol, 2009, 25(1):355-376.
[73] ZAMORE P D. Somatic piRNA biogenesis. EMBO J, 2010, 29(19):3219-3221.
[74] WEICK E M, MISKA E A. piRNAs:from biogenesis to function. Development, 2014, 141(18):3458-3471.
[75] ASSUMPCAO C B, CALCAGNO D Q, ARAUJO T M, et al. The role of piRNA and its potential clinical implications in cancer. Epigenomics, 2015, 7 (6):975-984.
[76] YANG Z, CHEN K M, PANDEY R R, et al. PIWI slicing and EXD1 drive biogenesis of nuclear piRNAs from cytosolic targets of the mouse piRNA pathway. Mol Cell, 2016, 61(1):138-152.
[77] HANDLER D, OLIVIERI D, NOVATCHKOVA M, et al. A systematic analysis of droso phila TUDOR domain-containing proteins identifies vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J, 2011, 30(19):3977-3993.
[78] CHUMA S,NAKANO T. piRNAs and their involvement in male germline development in mice. Dev Growth Differ, 2012, 54(1):78-92.
[79] WENDA J M, HOMOLKA D, YANG Z, et al. Distinct roles of RNA helicases MVH and TDRD9 in PIWI slicing-triggered mamalianpiRNA biogenesis and function. Dev Cell, 2017, 41(6):623-637.
[80] PANDEY R R, PILLAI R S. Primary piRNA biogenesis:caught up in a maelstrom. EMBO J, 2014, 33(18):1979-1980.
[81] CASTANEDA J, GENZOR P, VAN DER HEJDEN G W, et al. Reduced pachytene piRNAs and translation underlienspermiogenic arrest in Maelstrom mutant mice. EMBO J, 2014,33(18):1999-2019.
[82] ZHANG P, KANG J Y, GOU L T, et al. MIWI and piRNA mediated cleavage of messenger RNAs in mouse testes. Cell Res, 2015, 25(2):193-207.
[83] GOU L T, KANG J Y, DAI P, et al. Ubiquitination-deficient mutations in human Piwi cause male infertility by impairing histone-to protamine exchange during spermiogenesis. Cell, 2017, 169(6):1090-1104.
[84] CHEN X X, XIA T, HU X W, et al. piTNA derived from GAS5 activating tumor suppressor FOXO4 in breast cancer cell. Chin Arch Gen Surg(Electr Ed) (中华普通外科学文献:电子版), 2017, 11(3):154-158.
[85] PARK Y J, KWON W S, OH S A, et al. Fertility-related proteomic profiling bull spermatozoa separated by Percoll. J Proteome Res, 2012, 11:4162-4168.
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