DCAF2 regulates the proliferation and differentiation of mouse progenitor spermatogonia by targeting p21 and thymine DNA glycosylase.


Journal

Cell proliferation
ISSN: 1365-2184
Titre abrégé: Cell Prolif
Pays: England
ID NLM: 9105195

Informations de publication

Date de publication:
04 Jun 2024
Historique:
revised: 24 04 2024
received: 05 03 2024
accepted: 11 05 2024
medline: 5 6 2024
pubmed: 5 6 2024
entrez: 5 6 2024
Statut: aheadofprint

Résumé

DDB1-Cullin-4-associated factor-2 (DCAF2, also known as DTL or CDT2), a conserved substrate recognition protein of Cullin-RING E3 ligase 4 (CRL4), recognizes and degrades several substrate proteins during the S phase to maintain cell cycle progression and genome stability. Dcaf2 mainly expressed in germ cells of human and mouse. Our study found that Dcaf2 was expressed in mouse spermatogonia and spermatocyte. The depletion of Dcaf2 in germ cells by crossing Dcaf2

Identifiants

pubmed: 38837535
doi: 10.1111/cpr.13676
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13676

Subventions

Organisme : National Key Research and Development Program of China
ID : 2022YFC2703000
Organisme : National Natural Science Foundation of China
ID : 32270900

Informations de copyright

© 2024 The Authors. Cell Proliferation published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd.

Références

Umehara T, Tsujita N, Shimada M. Activation of Toll‐like receptor 7/8 encoded by the X chromosome alters sperm motility and provides a novel simple technology for sexing sperm. PLoS Biol. 2019;17(8):e3000398.
Wang Z, Xu X, Li J‐L, Palmer C, Maric D, Dean J. Sertoli cell‐only phenotype and scRNA‐seq define PRAMEF12 as a factor essential for spermatogenesis in mice. Nat Commun. 2019;10(1):5196.
Liu W, Lu X, Zhao Z‐H, et al. SRSF10 is essential for progenitor spermatogonia expansion by regulating alternative splicing. eLife. 2022;11:11.
Teletin M, Vernet N, Yu J, et al. Two functionally redundant sources of retinoic acid secure spermatogonia differentiation in the seminiferous epithelium. Development (Cambridge, England). 2019;146(1):dev170225.
Bae MJ, Kang MK, Kye YU, et al. Differential effects of low and high radiation dose rates on mouse spermatogenesis. Int J Mol Sci. 2021;22(23):12834.
Yin H, Kang Z, Zhang Y, et al. HDAC3 controls male fertility through enzyme‐independent transcriptional regulation at the meiotic exit of spermatogenesis. Nucleic Acids Res. 2021;49(9):5106‐5123.
Huang Q, Liu Y, Zhang S, et al. Autophagy core protein ATG5 is required for elongating spermatid development, sperm individualization and normal fertility in male mice. Autophagy. 2021;17(7):1753‐1767.
Qin J, Huang T, Wang J, et al. RAD51 is essential for spermatogenesis and male fertility in mice. Cell Death Discov. 2022;8(1):118.
Lu C, Zhang D, Zhang J, et al. Casein kinase 1α regulates murine spermatogenesis via p53‐Sox3 signaling. Development (Cambridge, England). 2022;149(13):dev200205.
Alpaugh WF, Voigt AL, Dardari R, et al. Loss of ubiquitin carboxy‐terminal hydrolase L1 impairs long‐term differentiation competence and metabolic regulation in murine spermatogonial stem cells. Cells. 2021;10(9):2265.
Heinrich A, Potter SJ, Guo L, Ratner N, DeFalco T. Distinct roles for Rac1 in sertoli cell function during testicular development and spermatogenesis. Cell Rep. 2020;31(2):107513.
Wang W, Jiang Z, Zhang D, Fu L, Wan R, Hong K. Comparative transcriptional analysis of pulmonary arterial hypertension associated with three different diseases. Front Cell Dev Biol. 2021;9:672159.
Paul D, Kales SC, Cornwell JA, et al. Revealing β‐TrCP activity dynamics in live cells with a genetically encoded biosensor. Nat Commun. 2022;13(1):6364.
Seaayfan E, Nasrah S, Quell L, et al. Reciprocal regulation of MAGED2 and HIF‐1α augments their expression under hypoxia: role of cAMP and PKA type II. Cells. 2022;11(21):3424.
Niu C, Guo J, Shen X, et al. Meiotic gatekeeper STRA8 regulates cell cycle by interacting with SETD8 during spermatogenesis. J Cell Mol Med. 2020;24(7):4194‐4211.
Lin H, Yan Y, Luo Y, et al. IP6‐assisted CSN‐COP1 competition regulates a CRL4‐ETV5 proteolytic checkpoint to safeguard glucose‐induced insulin secretion. Nat Commun. 2021;12(1):2461.
Jang S‐M, Redon CE, Aladjem MI. Switching DCAFs: beyond substrate receptors. BioEssays. 2021;43(7):e2100057.
Wang X, Arceci A, Bird K, et al. VprBP/DCAF1 regulates the degradation and nonproteolytic activation of the cell cycle transcription factor FoxM1. Mol Cell Biol. 2017;37(13):e00609‐16.
Simoneschi D, Rona G, Zhou N, et al. CRL4AMBRA1 is a master regulator of D‐type cyclins. Nature. 2021;592(7856):789‐793.
Wu Y, Zhou L, Wang X, et al. A genome‐scale CRISPR‐Cas9 screening method for protein stability reveals novel regulators of Cdc25A. Cell Discov. 2016;2:16014.
Chen Z, Wang K, Hou C, et al. CRL4BDCAF11 E3 ligase targets p21 for degradation to control cell cycle progression in human osteosarcoma cells. Sci Rep. 2017;7(1):1175.
Djakbarova U, Marzluff WF, Köseoğlu MM. DDB1 and CUL4 associated factor 11 (DCAF11) mediates degradation of stem‐loop binding protein at the end of S phase. Cell Cycle. 2016;15(15):1986‐1996.
Wang K, Liu Y, Yu Z, et al. Phosphorylation at Ser68 facilitates DCAF11‐mediated ubiquitination and degradation of CENP‐A during the cell cycle. Cell Rep. 2021;37(6):109987.
Jo U, Murai Y, Chakka S, et al. SLFN11 promotes CDT1 degradation by CUL4 in response to replicative DNA damage, while its absence leads to synthetic lethality with ATR/CHK1 inhibitors. Proc Natl Acad Sci U S A. 2021;118(6):e2015654118.
Huh J, Piwnica‐Worms H. CRL4(CDT2) targets CHK1 for PCNA‐independent destruction. Mol Cell Biol. 2013;33(2):213‐226.
Zielke N, Kim KJ, Tran V, et al. Control of Drosophila endocycles by E2F and CRL4(CDT2). Nature. 2011;480(7375):123‐127.
Tirado‐Class N, Hathaway C, Nelligan A, Nguyen T, Dungrawala H. DCAF14 regulates CDT2 to promote SET8‐dependent replication fork protection. Life Sci Alliance. 2024;7(1):e202302230.
Kim Y, Starostina NG, Kipreos ET. The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev. 2008;22(18):2507‐2519.
Huang Y, Zhu Y, Yang J, et al. CMTM6 inhibits tumor growth and reverses chemoresistance by preventing ubiquitination of p21 in hepatocellular carcinoma. Cell Death Dis. 2022;13(3):251.
Jo U, Cai W, Wang J, Kwon Y, D'Andrea AD, Kim H. PCNA‐dependent cleavage and degradation of SDE2 regulates response to replication stress. PLoS Genet. 2016;12(12):e1006465.
Shibata E, Dar A, Dutta A. CRL4Cdt2 E3 ubiquitin ligase and proliferating cell nuclear antigen (PCNA) cooperate to degrade thymine DNA glycosylase in S phase. J Biol Chem. 2014;289(33):23056‐23064.
Mistry BV, Alanazi M, Fitwi H, et al. Expression profiling of WD40 family genes including DDB1‐ and CUL4‐associated factor (DCAF) genes in mice and human suggests important regulatory roles in testicular development and spermatogenesis. BMC Genomics. 2020;21(1):602.
Xu Y‐W, Cao L‐R, Wang M, et al. Maternal DCAF2 is crucial for maintenance of genome stability during the first cell cycle in mice. J Cell Sci. 2017;130(19):3297‐3307.
Choi Y, Lee EG, Lee G, et al. Amodiaquine promotes testosterone production and de novo synthesis of cholesterol and triglycerides in Leydig cells. J Lipid Res. 2021;62:100152.
Endo T, Freinkman E, de Rooij DG, Page DC. Periodic production of retinoic acid by meiotic and somatic cells coordinates four transitions in mouse spermatogenesis. Proc Natl Acad Sci U S A. 2017;114(47):E10132‐E10141.
Feng Y, Chen D, Wang T, et al. Sertoli cell survival and barrier function are regulated by miR‐181c/d‐Pafah1b1 axis during mammalian spermatogenesis. Cell Mol Life Sci. 2022;79(9):498.
Ma D, Zou Y, Chu Y, et al. A cell‐permeable peptide‐based PROTAC against the oncoprotein CREPT proficiently inhibits pancreatic cancer. Theranostics. 2020;10(8):3708‐3721.
Ernst C, Eling N, Martinez‐Jimenez CP, Marioni JC, Odom DT. Staged developmental mapping and X chromosome transcriptional dynamics during mouse spermatogenesis. Nat Commun. 2019;10(1):1251.
Zhou S, Dong J, Xiong M, et al. UHRF1 interacts with snRNAs and regulates alternative splicing in mouse spermatogonial stem cells. Stem Cell Rep. 2022;17(8):1859‐1873.
Panagopoulos A, Taraviras S, Nishitani H, Lygerou Z. CRL4Cdt2: coupling genome stability to ubiquitination. Trends Cell Biol. 2020;30(4):290‐302.
Ratnayeke N, Baris Y, Chung M, Yeeles JTP, Meyer T. CDT1 inhibits CMG helicase in early S phase to separate origin licensing from DNA synthesis. Mol Cell. 2023;83(1):26‐42.
Liu B, Liu C, Ma B, et al. PA1 participates in the maintenance of blood‐testis barrier integrity via cooperation with JUN in the Sertoli cells of mice. Cell Biosci. 2022;12(1):41.
Ciccarelli M, Giassetti MI, Miao D, et al. Donor‐derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Proc Natl Acad Sci U S A. 2020;117(39):24195‐24204.
Feng M, Bai Y, Chen Y, Wang K. Knockout of the transducin‐like enhancer of split 6 gene affects the proliferation and cell cycle process of mouse spermatogonia. Int J Mol Sci. 2020;21(16):5827.
Hayashi A, Giakoumakis NN, Heidebrecht T, et al. Direct binding of Cdt2 to PCNA is important for targeting the CRL4Cdt2 E3 ligase activity to Cdt1. Life Sci Alliance. 2018;1(6):e201800238.
Xue Z, Guo J, Ma R, et al. The DDB1‐DCAF2 complex is essential for B cell development because it regulates cell cycle progression. Cell Mol Immunol. 2021;18(3):758‐760.
Zhang Y, Wang C, Wu L, et al. Epithelial CRL4DCAF2 is critical for maintaining intestinal homeostasis against DSS‐induced colitis by regulating the proliferation and repair of intestinal epithelial cells. Dig Dis Sci. 2024;69(1):66‐80.
Qi R, Wang J, Jiang Y, et al. Snai1‐induced partial epithelial‐mesenchymal transition orchestrates p53‐p21‐mediated G2/M arrest in the progression of renal fibrosis via NF‐κB‐mediated inflammation. Cell Death Dis. 2021;12(1):44.
Yu J‐B, Lee D‐S, Padanilam BJ, Kim J. Repeated administration of cisplatin transforms kidney fibroblasts through G2/M arrest and cellular senescence. Cells. 2022;11(21):3472.
He P, Li Z, Xu F, et al. AMPK activity contributes to G2 arrest and DNA damage decrease via p53/p21 pathways in oxidatively damaged mouse zygotes. Front Cell Dev Biol. 2020;8:539485.
Ma J‐Y, Zhao K, OuYang Y‐C, et al. Exogenous thymine DNA glycosylase regulates epigenetic modifications and meiotic cell cycle progression of mouse oocytes. Mol Hum Reprod. 2015;21(2):186‐194.
Yadav K, Ali SA, Mohanty AK, Muthusamy E, Subaharan K, Kaul G. MSN, MWCNT and ZnO nanoparticle‐induced CHO‐K1 cell polarisation is linked to cytoskeleton ablation. J Nanobiotechnol. 2021;19(1):45.
Wu Y, Wang H, Zhu J, Shen H, Liu H. Licochalcone A activation of glycolysis pathway has an anti‐aging effect on human adipose stem cells. Aging. 2021;13(23):25180‐25194.
Hwang B‐J, Madabushi A, Jin J, Lin S‐YS, Lu AL. Histone/protein deacetylase SIRT1 is an anticancer therapeutic target. Am J Cancer Res. 2014;4(3):211‐221.
Sjolund A, Nemec AA, Paquet N, et al. A germline polymorphism of thymine DNA glycosylase induces genomic instability and cellular transformation. PLoS Genet. 2014;10(11):e1004753.
Ueki T, Nishidate T, Park JH, et al. Involvement of elevated expression of multiple cell‐cycle regulator, DTL/RAMP (denticleless/RA‐regulated nuclear matrix associated protein), in the growth of breast cancer cells. Oncogene. 2008;27(43):5672‐5683.
Pan W‐W, Zhou J‐J, Yu C, et al. Ubiquitin E3 ligase CRL4(CDT2/DCAF2) as a potential chemotherapeutic target for ovarian surface epithelial cancer. J Biol Chem. 2013;288(41):29680‐29691.
Huang F, Wang M, Liu R, et al. CDT2‐controlled cell cycle reentry regulates the pathogenesis of Alzheimer's disease. Alzheimers Dement. 2019;15(2):217‐231.
Singh G, Sharma SK, Singh SK. miR‐34a negatively regulates cell cycle factor Cdt2/DTL in HPV infected cervical cancer cells. BMC Cancer. 2022;22(1):777.

Auteurs

Hongwei Wei (H)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Zhijuan Wang (Z)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Yating Huang (Y)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Longwei Gao (L)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Weiyong Wang (W)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Shuang Liu (S)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Yan-Li Sun (YL)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Huiyu Liu (H)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Yashuang Weng (Y)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Heng-Yu Fan (HY)

MOE Key Laboratory for Biosystems Homeostasis and Protection and Innovation Center for Cell Signaling Network, Life Sciences Institute, Zhejiang University, Hangzhou, China.

Meijia Zhang (M)

The Innovation Centre of Ministry of Education for Development and Diseases, The second Affiliated Hospital, School of Medicine, South China University of Technology, Guangzhou, China.

Classifications MeSH