ADP-核糖基化调控精子形成的研究进展

doi:10.11843/j.issn.0366-6964.2022.01.002

Abstract

Abstract: ADP-ribosylation is a kind of post-translational modification of proteins catalyzed by ADP-ribosyl transferases (ARTs). It is divided into poly-ADP-ribosylation and mono-ADP-ribosylation, which plays an important role in regulating many biological events during spermatogenesis, such as assembly of centromere and spindle, DNA damage repair and chromatin condensation. Part of the ARTs gene deletion leads to abnormal spermatogenesis, resulting in reduced semen quality and even male infertility. However, the detailed mechanism of spermatogenesis regulated by ADP-ribosylation is still unclear, and the understand on the role of mono-ADP-ribosylation within it is even less. Therefore, this paper reviews the research progress of ADP-ribosylation in spermatogenesis, hoping to provide new ideas for further revealing the regulatory mechanism of spermatogenesis, and promoting breakthrough in the prevention and control of male reproductive disorders and the treatment of male infertility.

Key words: ADP-ribosylation, spermatogenesis, poly-ADP-ribose polymerases, ecto-ADP-ribosyl transferase

CLC Number:

DUAN Chenying, LI Xin, ZHAO Junjin, LI Ruyi, ZHAO Lingjun, GUO Guanhua, YANG Liguo, HUA Guohua, WANG Dong. Research Progress of ADP-ribosylation in Regulating Spermatogenesis[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(1): 11-19.

References 67

[1]	桑润滋,麻柱,李俊杰,等.我国奶牛繁殖技术研究进展[C]//第七届中国奶业大会论文集.青岛:《中国奶牛》编辑部,2016:4.SANG R Z,MA Z,LI J J,et al.Research progress of dairy cow reproduction technology in China[C]//Proceedings of the 7th China Dairy Congress.Qingdao:China Dairy Editorial Department,2016:4.(in Chinese)
[2]	FAIR S,LONERGAN P.Review:understanding the causes of variation in reproductive wastage among bulls[J].Animal,2018,12:s53-s62.
[3]	张金英,刘晓兰,罗晓青.对不孕症患者进行个性化心理护理以提高患者满意度的研究[J].当代临床医刊,2020,33(4):369,365.ZHANG J Y,LIU X L,LUO X Q.Study on individualized psychological nursing for infertility patients to improve patient satisfaction[J].The Medical Journal of the Present Clinical,2020,33(4):369,365.(in Chinese)
[4]	KROPP J,CARRILLO J A,NAMOUS H,et al.Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos[J].BMC Genomics,2017,18(1):280.
[5]	SIMON L,EMERY B R,CARRELL D T.Review:diagnosis and impact of sperm DNA alterations in assisted reproduction[J].Best Pract Res.Clin Obstetr Gynaecol,2017,44:38-56.
[6]	CAO Z,HUANG W Y,SUN Y R,et al.Deoxynivalenol induced spermatogenesis disorder by blood-testis barrier disruption associated with testosterone deficiency and inflammation in mice[J].Environ Pollut,2020,264:114748.
[7]	祝天喻,李妍,刘小飞,等.精子发生过程中翻译后修饰的蛋白质组学研究进展[J].生理学报,2020,72(1):75-83.ZHU T Y,LI Y,LIU X F,et al.Advances in proteomic studies of post-translational modifications during spermatogenesis[J].Acta Physiologica Sinica,2020,72(1):75-83.(in Chinese)
[8]	STAUB C,JOHNSON L.Review:Spermatogenesis in the bull[J].Animal,2018,12(Suppl 1):s27-s35.
[9]	HAO S L,NI F D,YANG W X.The dynamics and regulation of chromatin remodeling during spermiogenesis[J].Gene,2019,706:201-210.
[10]	曹兴午.男性不育症Y染色体研究[J].中国医学研究与临床,2008,6(5):51-55.CAO X W.Studies of Y chromosome in male infertility[J].Chinese Medical Research and Clinic,2008,6(5):51-55.(in Chinese)
[11]	金穗华,王鹏武,马国辉.影响公牛精子形态异常的原因分析[J].畜牧兽医杂志,2015,34(5):19-21.JIN S H,WANG P W,MA G H.The Analysis on the causes of abnormal bulls sperm morphology[J].Journal of Animal Science and Veterinary Medicine,2015,34(5):19-21.(in Chinese)
[12]	DANIS R B,SAMPLASKI M K.Sperm morphology:history,challenges,and impact on natural and assisted fertility[J].Curr Urol Rep,2019,20(8):43.
[13]	HAMZE J G,SÁNCHEZ J M,O’CALLAGHAN E,et al.JUNO protein coated beads:A potential tool to predict bovine sperm fertilizing ability[J].Theriogenology,2020,155:168-175.
[14]	HOTTIGER M O,HASSA P O,LÜSCHER B,et al.Toward a unified nomenclature for mammalian ADP-ribosyltransferases[J].Trends Biochem Sci,2010,35(4):208-219.
[15]	WANG Y J,LUO W B,WANG Y F.PARP-1 and its associated nucleases in DNA damage response[J].DNA Repair,2019,81:102651.
[16]	MEYER-FICCA M L,LONCHAR J D,IHARA M,et al.Alteration of poly(ADP-ribose) metabolism affects murine sperm nuclear architecture by impairing pericentric heterochromatin condensation[J].Chromosoma,2013,122(4):319-335.
[17]	DI GIROLAMO M,FABRIZIO G.Overview of the mammalian ADP-ribosyl-transferases clostridia toxin-like (ARTCs) family[J].Biochem Pharmacol,2019,167:86-96.
[18]	COLLIER R J,PAPPENHEIMER A M Jr.Studies on the mode of action of diphtheria toxin.II.Effect of toxin on amino acid incorporation in cell-free systems[J].J Exp Med,1964,120(6):1019-1039.
[19]	CHAMBON P,WEILL J D,DOLY J,et al.On the formation of a novel adenylic compound by enzymatic extracts of liver nuclei[J].Biochem Biophys Res Commun,1966,25(6):638-643.
[20]	LI X,DUAN C Y,LI R Y,et al.Insights into the mechanism of bovine spermiogenesis based on comparative transcriptomic studies[J].Animals,2021,11:80.
[21]	VAN NOORT G J V D H.Chemical tools to study protein ADP-ribosylation[J].ACS Omega,2020,5(4):1743-1751.
[22]	ALEMASOVA E E,LAVRIK O I.Poly(ADP-ribosyl)ation by PARP1:reaction mechanism and regulatory proteins[J].Nucleic Acids Res,2019,47(8):3811-3827.
[23]	HOU W H,CHEN S H,YU X C.Poly-ADP ribosylation in DNA damage response and cancer therapy[J].Mutat Res Mutat Res,2019,780:82-91.
[24]	LÜSCHER B,BVTEPAGE M,ECKEI L,et al.ADP-ribosylation,a multifaceted posttranslational modification involved in the control of cell physiology in health and disease[J].Chem Rev,2018,118(3):1092-1136.
[25]	MURTHY S,DESANTIS J,VERHEUGD P,et al.4-(Phenoxy) and 4-(benzyloxy)benzamides as potent and selective inhibitors of mono-ADP-ribosyltransferase PARP10/ARTD10[J].Eu J Med Chem,2018,156:93-102.
[26]	RAY CHAUDHURI A,NUSSENZWEIG A.The multifaceted roles of PARP1 in DNA repair and chromatin remodelling[J].Nat Rev Mol Cell Biol,2017,18(10):610-621.
[27]	GLOWACKI G,BRAREN R,FIRNER K,et al.The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse[J].Prot Sci A Publ Prot Soc,2010,11(7):1657-1670.
[28]	王轩.原发性无精子症男性精母细胞减数分裂过程中联会及重组异常研究[D].南京:东南大学,2018.WANG X.Research on genetic recombination through meiosis in spermatocytes of the non-obstructive azoospermic patients[D].Nanjing:Southeast University,2018.(in Chinese)
[29]	MARTINEZ-EXPOSITO M J,KAPLAN K B,COPELAND J,et al.Retention of the Bub3 checkpoint protein on lagging chromosomes[J].Proc Natl Acad Sci U S A,1999,96(15):8493-8498.
[30]	OVERLACK K,BANGE T,WEISSMANN F,et al.BubR1 promotes Bub3-dependent APC/C inhibition during spindle assembly checkpoint signaling[J].Current Biology,2017,27(19):2915-2927.e7.
[31]	YAN K G,YANG J,ZHANG Z G,et al.Structure of the inner kinetochore CCAN complex assembled onto a centromeric nucleosome[J].Nature,2019,574(7777):278-282.
[32]	SAXENA A,SAFFERY R,WONG L H,et al.Centromere proteins Cenpa,Cenpb,and Bub3 interact with poly(ADP-ribose) polymerase-1 protein and are poly(ADP-ribosyl)ated[J].J Biol Chem,2002,277(30):26921-26926.
[33]	吴晋,吴剑维,余智超,等.NuMA蛋白质的生物学作用[J].中国细胞生物学学报,2017,39(7):947-956.WU J,WU J W,YU Z C,et al.The biological functions of NuMA protein[J].Chinese Journal of Cell Biology,2017,39(7):947-956.(in Chinese)
[34]	DANTZER F,MARK M,QUENET D,et al.Poly(ADP-ribose) polymerase-2 contributes to the fidelity of male meiosis I and spermiogenesis[J].Proc Natl Acad Sci U S A,2006,103(40):14854-14859.
[35]	CHANG W,DYNEK J N,SMITH S.NuMA is a major acceptor of poly(ADP-ribosyl)ation by tankyrase 1 in mitosis[J].Biochem J,2005,391(Pt 2):177-184.
[36]	CHANG P,JACOBSON M K,MITCHISON T J.Poly (ADP-ribose) is required for spindle assembly and structure[J].Nature,2004,432(7017):645-649.
[37]	WHITTEMORE K,VERA E,MARTÍNEZ-NEVADO E,et al.Telomere shortening rate predicts species life span[J].Proc Natl Acad Sci U S A,2019,116(30):15122-15127.
[38]	SHOEB M,MUSTAFA G M,JOSEPH P,et al.Initiation of pulmonary fibrosis after silica inhalation in rats is linked with dysfunctional shelterin complex and DNA damage response[J].Sci Rep,2019,9:471.
[39]	COOK B D,DYNEK J N,CHANG W,et al.Role for the related poly(ADP-ribose) polymerases tankyrase 1 and 2 at human telomeres[J].Mol Cell Biol,2002,22:332-342.
[40]	HARVEY A,MIELKE N,GRIMSTEAD J W,et al.PARP1 is required for preserving telomeric integrity but is dispensable for A-NHEJ[J].Oncotarget,2018,9(78):34821-34837.
[41]	DYNEK J N,SMITH S.Resolution of sister telomere association is required for progression through mitosis[J].Science,2004,304(5667):97-100.
[42]	李金重,黄永汉.PARP-1对精子生成影响的研究进展[J].罕少疾病杂志,2020,27(5):110-112.LI J C,HUANG Y H.Research progress on the effect of PARP-1 on spermatogenesis[J].Journal of Rare and Uncommon Diseases,2020,27(5):110-112.(in Chinese)
[43]	KUTUZOV M M,BELOUSOVA E A,ILINA E S,et al.Impact of PARP1,PARP2 & PARP3 on the base excision repair of nucleosomal DNA[M]//ZHARKOV D.Mechanisms of Genome Protection and Repair.Cham:Springer,2020,1241:47-57.
[44]	MATTA E,KIRIBAYEVA A,KHASSENOV B,et al.Insight into DNA substrate specificity of PARP1-catalysed DNA poly(ADP-ribosyl)ation[J].Sci Rep,2020,10(1):3699.
[45]	CELIK-OZENCI C,TASATARGIL A.Role of poly(ADP-ribose) polymerases in male reproduction[J].Spermatogenesis,2013,3(2):e24194.
[46]	SUKHANOVA M V,HAMON L,KUTUZOV M M,et al.A single-molecule atomic force microscopy study of PARP1 and PARP2 recognition of base excision repair DNA intermediates[J].J Mol Biol,2019,431(15):2655-2673.
[47]	GAULLIER G,ROBERTS G,MUTHURAJAN U M,et al.Bridging of nucleosome-proximal DNA double-strand breaks by PARP2 enhances its interaction with HPF1[J].PLoS One,2020,15(11):e0240932.
[48]	PAZZAGLIA S,PIOLI C.Multifaceted Role of PARP-1 in DNA repair and inflammation:pathological and therapeutic implications in cancer and non-cancer diseases[J].Cells,2020,9(1):41.
[49]	BERGER N A.Poly(ADP-ribose) in the cellular response to DNA damage[J].Radiation Research,1985,101(1):4-15.
[50]	MURATA M M,KONG X D,MONCADA E,et al.NAD+ consumption by PARP1 in response to DNA damage triggers metabolic shift critical for damaged cell survival[J].Mol Biol Cell,2019,30(20):2584-2597.
[51]	AGARWAL A,MAHFOUZ R Z,SHARMA R K,et al.Potential biological role of poly (ADP-ribose) polymerase (PARP) in male gametes[J].Reproduct Biol Endocrinol,2009,7:143.
[52]	ANDRABI S A,KIM N S,YU S W,et al.Poly(ADP-ribose)(PAR) polymer is a death signal[J].Proc Natl Acad Sci U S A,2006,103(48):18308-18313.
[53]	FILHO R M,BELETTI M E,DE OLIVEIRA F.Ultrastructure of bovine sperm chromatin[J].Micros Res Techn,2015,78(12):1117-1120.
[54]	LEDUC F,MAQUENNEHAN V,NKOMA G B,et al.DNA damage response during chromatin remodeling in elongating spermatids of mice[J].Biol Rep,2008,78(2):324-332.
[55]	LABERGE R M,BOISSONNEAULT G.On the nature and origin of DNA strand breaks in elongating spermatids[J].Biol Rep,2005,73(2):289-296.
[56]	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[J].Cell,2017,169(6):1090-1104.e13.
[57]	HUBER A,BAI P,DE MURCIA J M,et al.PARP-1,PARP-2 and ATM in the DNA damage response:functional synergy in mouse development[J].DNA Repair,2004,3(8-9):1103-1108.
[58]	POIRIER G G,DE MURCIA G,JONGSTRA-BILEN J,et al.Poly-(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure[J].Proc Natl Acad Sci U S A,1982,79(11):3423-3427.
[59]	DOGAN S,VARGOVIC P,OLIVEIRA R,et al.Sperm protamine-status correlates to the fertility of breeding bulls[J].Biol Reproduct,2015,92(4):92.
[60]	CARRELL D T,EMERY B R,HAMMOUD S.The aetiology of sperm protamine abnormalities and their potential impact on the sperm epigenome[J].Int J Androl,2008,31(6):537-545.
[61]	MUELLER-DIECKMANN C,RITTER H,HAAG F,et al.Structure of the ecto-ADP-ribosyl transferase ART2.2 from rat[J].J Mol Biol,2002,322(4):687-696.
[62]	RISSIEK B,MENZEL S,LEUTERT M,et al.Ecto-ADP-ribosyltransferase ARTC2.1 functionally modulates FcγR1 and FcγR2B on murine microglia[J].Sci Rep,2017,7(1):16477.
[63]	LIN F Y,JIANG L,YANG H Y,et al.Association of polymorphisms in ART3 gene with male infertility in the Chinese population[J].Int J Clin Exp Med,2014,8(5):7944-7950.
[64]	LEUTERT M,MENZEL S,BRAREN R,et al.Proteomic characterization of the heart and skeletal muscle reveals widespread arginine ADP-ribosylation by the ARTC1 ectoenzyme[J].Cell Rep,2018,24(7):1916-1929.e5.
[65]	KHARADIA S V,HUIATT T W,HUANG H Y,et al.Effect of an arginine-specific ADP-ribosyltransferase inhibitor on differentiation of embryonic chick skeletal muscle cells in culture[J].Exp Cell Res,1992,201(1):33-42.
[66]	NORAMBUENA P A,DIBLÍK J,KRENKOVA P,et al.An ADP-ribosyltransferase 3 (ART3) variant is associated with reduced sperm counts in Czech males:case/control association study replicating results from the Japanese population[J].Neuro Endocrinol Lett,2012,33(1):48-52.
[67]	FRIEDRICH M,GRAHNERT A,KLEIN C,et al.Genomic organization and expression of the human mono-ADP-ribosyltransferase ART3 gene[J].Biochim Biophys Acta Gene Struct Expr,2006,1759(6):270-280.

Research Progress of ADP-ribosylation in Regulating Spermatogenesis

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