Journal of Shanghai Jiao Tong University (Medical Science) >
Role of SUMOylation in spermatogenesis
Received date: 2022-02-11
Accepted date: 2022-07-01
Online published: 2022-09-04
Supported by
Medical Innovation Research Project of Shanghai Scientific and Technological Project(20Y11907600);National Natural Science Foundation of China(82171586)
SUMOylation is a reversible post-translational modification of proteins, which is involved in many important biological processes, such as transcriptional regulation, signal transduction, and DNA damage repair. It is found that the overall expressions and localizations of SUMOylation change dynamically in spermatogenesis, suggesting that it may be involved in key events in the process. Spermatogenesis is a series of processes regulated by complex biological crosstalk. In the seminiferous tubules, spermatogenic cells undergo three stages, that is, the proliferation and differentiation of spermatogonial stem cells, the meiosis of spermatocytes and spermiogenesis, and eventually form highly specialized spermatozoa. In this process, the effects and mechanisms of SUMOylation in spermatogenesis have not been clear. Therefore, this review summarizes the effect of the SUMOylation enzyme system, SUMO family and SUMO-specific proteases family in spermatogenesis.
Key words: spermatogenesis; SUMOylation; post-translational modification
Jiayan LUAN , Peng LI , Bangmin HAN . Role of SUMOylation in spermatogenesis[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2022 , 42(7) : 925 -930 . DOI: 10.3969/j.issn.1674-8115.2022.07.012
1 | SANTIAGO J, SILVA J V, HOWL J, et al. All you need to know about sperm RNAs[J]. Hum Reprod Update, 2021, 28(1): 67-91. |
2 | GAO H H, WEN H, CAO C C, et al. Overexpression of microRNA-10a in germ cells causes male infertility by targeting Rad51 in mouse and human[J]. Front Physiol, 2019, 10: 765. |
3 | CHEN X X, ZHENG Y, LEI A M, et al. Early cleavage of preimplantation embryos is regulated by tRNAGln-TTG-derived small RNAs present in mature spermatozoa[J]. J Biol Chem, 2020, 295(32): 10885-10900. |
4 | TYEBJI S, HANNAN A J, TONKIN C J. Pathogenic infection in male mice changes sperm small RNA profiles and transgenerationally alters offspring behavior[J]. Cell Rep, 2020, 31(4): 107573. |
5 | SHARMA U. Paternal contributions to offspring health: role of sperm small RNAs in intergenerational transmission of epigenetic information[J]. Front Cell Dev Biol, 2019, 7: 215. |
6 | VIGODNER M. Roles of small ubiquitin-related modifiers in male reproductive function[J]. Int Rev Cell Mol Biol, 2011, 288: 227-259. |
7 | OKURA T, GONG L, KAMITANI T, et al. Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin[J]. J Immunol, 1996, 157(10): 4277-4281. |
8 | WILSON V G. SUMO Regulation of Cellular Processes[M]. 2nd ed. Switzerland: Springer, 2017. |
9 | VIGODNER M. Sumoylation precedes accumulation of phosphorylated H2AX on sex chromosomes during their meiotic inactivation[J]. Chromosome Res, 2009, 17(1): 37-45. |
10 | FEITOSA W B, MORRIS P L. SUMOylation regulates germinal vesicle breakdown and the Akt/PKB pathway during mouse oocyte maturation[J]. Am J Physiol Cell Physiol, 2018, 315(1): C115-C121. |
11 | DEL PRIORE L, PIGOZZI M I. DNA organization along pachytene chromosome axes and its relationship with crossover frequencies[J]. Int J Mol Sci, 2021, 22(5): 2414. |
12 | SONG S H, CHIBA K, RAMASAMY R, et al. Recent advances in the genetics of testicular failure[J]. Asian J Androl, 2016, 18(3): 350-355. |
13 | GRAY S, COHEN P E. Control of meiotic crossovers: from double-strand break formation to designation[J]. Annu Rev Genet, 2016, 50: 175-210. |
14 | SHRIVASTAVA V, PEKAR M, GROSSER E, et al. SUMO proteins are involved in the stress response during spermatogenesis and are localized to DNA double-strand breaks in germ cells[J]. Reproduction, 2010, 139(6): 999-1010. |
15 | CHANG H M, YEH E T H. SUMO: from bench to bedside[J]. Physiol Rev, 2020, 100(4): 1599-1619. |
16 | RAO H P, QIAO H Y, BHATT S K, et al. A SUMO-ubiquitin relay recruits proteasomes to chromosome axes to regulate meiotic recombination[J]. Science, 2016, 355: 403-407. |
17 | VIGODNER M, ISHIKAWA T, SCHLEGEL P N, et al. SUMO-1, human male germ cell development, and the androgen receptor in the testis of men with normal and abnormal spermatogenesis[J]. Am J Physiol Endocrinol Metab, 2006, 290(5): E1022-E1033. |
18 | PANICKER N, GE P, DAWSON V L, et al. The cell biology of Parkinson's disease[J]. J Cell Biol, 2021, 220(4): e202012095. |
19 | RICHARD M A, SOK P, CANON S, et al. Altered mechanisms of genital development identified through integration of DNA methylation and genomic measures in hypospadias[J]. Sci Rep, 2020, 10(1): 12715. |
20 | SENGUPTA A, NANDA M, TARIQ S B, et al. Sumoylation and its regulation in testicular Sertoli cells[J]. Biochem Biophys Res Commun, 2021, 580: 56-62. |
21 | SEELER J S, DEJEAN A. Nuclear and unclear functions of SUMO[J]. Nat Rev Mol Cell Biol, 2003, 4(9): 690-699. |
22 | BROWN P W, HWANG K, SCHLEGEL P N, et al. Small ubiquitin-related modifier (SUMO)-1, SUMO-2/3 and SUMOylation are involved with centromeric heterochromatin of chromosomes 9 and 1 and proteins of the synaptonemal complex during meiosis in men[J]. Hum Reprod, 2008, 23(12): 2850-2857. |
23 | YANG W L, ROBICHAUX W G 3rd, MEI F C, et al. Epac1 activation by cAMP regulates cellular SUMOylation and promotes the formation of biomolecular condensates[J]. Sci Adv, 2022, 8(16): eabm2960. |
24 | SHRIVASTAVA V, MARMOR H, CHERNYAK S, et al. Cigarette smoke affects posttranslational modifications and inhibits capacitation-induced changes in human sperm proteins[J]. Reprod Toxicol, 2014, 43: 125-129. |
25 | VIGODNER M, SHRIVASTAVA V, GUTSTEIN L E, et al. Localization and identification of sumoylated proteins in human sperm: excessive sumoylation is a marker of defective spermatozoa[J]. Hum Reprod, 2013, 28(1): 210-223. |
26 | GONG L, KAMITANI T, FUJISE K, et al. Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9[J]. J Biol Chem, 1997, 272(45): 28198-28201. |
27 | LA SALLE S, SUN F Y, ZHANG X D, et al. Developmental control of sumoylation pathway proteins in mouse male germ cells[J]. Dev Biol, 2008, 321(1): 227-237. |
28 | VIGODNER M, LUCAS B, KEMENY S, et al. Identification of sumoylated targets in proliferating mouse spermatogonia and human testicular seminomas[J]. Asian J Androl, 2020, 22(6): 569-577. |
29 | NACERDDINE K, LEHEMBRE F, BHAUMIK M, et al. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice[J]. Dev Cell, 2005, 9(6): 769-779. |
30 | MAGALHAES J, TRESSE E, EJLERSKOV P, et al. PIAS2-mediated blockade of IFN-β signaling: a basis for sporadic Parkinson disease dementia[J]. Mol Psychiatry, 2021, 26(10): 6083-6099. |
31 | BEGITT A, CAVEY J, DROESCHER M, et al. On the role of STAT1 and STAT6 ADP-ribosylation in the regulation of macrophage activation[J]. Nat Commun, 2018, 9(1): 2144. |
32 | PAAKINAHO V, LEMPI?INEN J K, SIGISMONDO G, et al. SUMOylation regulates the protein network and chromatin accessibility at glucocorticoid receptor-binding sites[J]. Nucleic Acids Res, 2021, 49(4): 1951-1971. |
33 | WANG R H, HUANG S F, FU X N, et al. The conserved ancient role of chordate PIAS as a multilevel repressor of the NF-κB pathway[J]. Sci Rep, 2017, 7(1): 17063. |
34 | YAN W, SANTTI H, J?NNE O A, et al. Expression of the E3 SUMO-1 ligases PIASx and PIAS1 during spermatogenesis in the rat[J]. Gene Expr Patterns, 2003, 3(3): 301-308. |
35 | SANTTI H, MIKKONEN L, ANAND A, et al. Disruption of the murine PIASx gene results in reduced testis weight[J]. J Mol Endocrinol, 2005, 34(3): 645-654. |
36 | SAJEEV T K, JOSHI G, ARYA P, et al. SUMO and SUMOylation pathway at the forefront of host immune response[J]. Front Cell Dev Biol, 2021, 9: 681057. |
37 | WEN S M, NIU Y J, HUANG H J. Posttranslational regulation of androgen dependent and independent androgen receptor activities in prostate cancer[J]. Asian J Urol, 2020, 7(3): 203-218. |
38 | TAKAHASHI M, INAGUMA Y, HIAI H, et al. Developmentally regulated expression of a human "finger"-containing gene encoded by the 5' half of the ret transforming gene[J]. Mol Cell Biol, 1988, 8(4): 1853-1856. |
39 | ZHUANG X J, TANG W H, FENG X, et al. Trim27 interacts with Slx2, is associated with meiotic processes during spermatogenesis[J]. Cell Cycle, 2016, 15(19): 2576-2584. |
40 | MATSUURA T, SHIMONO Y, KAWAI K M, et al. PIAS proteins are involved in the SUMO-1 modification, intracellular translocation and transcriptional repressive activity of RET finger protein[J]. Exp Cell Res, 2005, 308(1): 65-77. |
41 | LONG X J, ZHAO B Y, LU W B, et al. The critical roles of the SUMO-specific protease SENP3 in human diseases and clinical implications[J]. Front Physiol, 2020, 11: 558220. |
42 | JANSEN N S, VERTEGAAL A C O. A chain of events: regulating target proteins by SUMO polymers[J]. Trends Biochem Sci, 2021, 46(2): 113-123. |
43 | HAN Z J, FENG Y H, GU B H, et al. The post-translational modification, SUMOylation, and cancer (Review)[J]. Int J Oncol, 2018, 52(4): 1081-1094. |
44 | KUNZ K, PILLER T, MüLLER S. SUMO-specific proteases and isopeptidases of the SENP family at a glance[J]. J Cell Sci, 2018, 131(6): jcs211904. |
45 | DEYRIEUX A F, WILSON V G. Sumoylation in development and differentiation[J]. Adv Exp Med Biol, 2017, 963: 197-214. |
46 | WU D, HUANG C J, KHAN F A, et al. SENP3 grants tight junction integrity and cytoskeleton architecture in mouse Sertoli cells[J]. Oncotarget, 2017, 8(35): 58430-58442. |
47 | MRUK D D, CHENG C Y. The mammalian blood-testis barrier: its biology and regulation[J]. Endocr Rev, 2015, 36(5): 564-591. |
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