930
Views
0
CrossRef citations to date
0
Altmetric
Epigenetics

ANP32e Binds Histone H2A.Z in a Cell Cycle-Dependent Manner and Regulates Its Protein Stability in the Cytoplasm

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 72-85 | Received 07 Sep 2023, Accepted 13 Feb 2024, Published online: 14 Mar 2024

References

  • Xiong Z, Ye L, Zhenyu H, Li F, Xiong Y, Lin C, Wu X, Deng G, Shi W, Song L, et al. ANP32E induces tumorigenesis of triple-negative breast cancer cells by upregulating E2F1. Mol Oncol. 2018;12:896–912. doi:10.1002/1878-0261.12202.
  • Zhang N, Chen Y, Shen Y, Lou S, Deng J. Comprehensive analysis the potential biomarkers for the high-risk of childhood acute myeloid leukemia based on a competing endogenous RNA network. Blood Cells Mol Dis. 2019;79:102352. doi:10.1016/j.bcmd.2019.102352.
  • Pippa R, Boffo S, Odero MD, Giordano A. Data mining analysis of the PP2A cell cycle axis in mesothelioma patients. J Cell Physiol. 2020;235:5284–5292. doi:10.1002/jcp.29414.
  • Huang J, Gao W, Liu H, Yin G, Duan H, Huang Z, Zhang Y. Up-regulated ANP32E promotes the thyroid carcinoma cell proliferation and migration via activating AKT/mTOR/HK2-mediated glycolysis. Gene. 2020;750:144681. doi:10.1016/j.gene.2020.144681.
  • Hupfer A, Brichkina A, Adhikary T, Lauth M. The mammalian Hedgehog pathway is modulated by ANP32 proteins. Biochem Biophys Res Commun. 2021;553:78–84. doi:10.1016/j.bbrc.2021.03.027.
  • Wang L, Li J, Li Y, Pang LB. Hsa-let-7c exerts an anti-tumor function by negatively regulating ANP32E in lung adenocarcinoma. Tissue Cell. 2020;65:101372. doi:10.1016/j.tice.2020.101372.
  • Zhang J, Lan Z, Qiu G, Ren H, Zhao Y, Gu Z, Li Z, Feng L, He J, Wang C. Over-expression of ANP32E is associated with poor prognosis of pancreatic cancer and promotes cell proliferation and migration through regulating beta-catenin. BMC Cancer. 2020;20:1065. doi:10.1186/s12885-020-07556-z.
  • Reilly PT, Yu Y, Hamiche A, Wang L. Cracking the ANP32 whips: important functions, unequal requirement, and hints at disease implications. Bioessays. 2014;36:1062–1071. doi:10.1002/bies.201400058.
  • Costanzo RV, Vilá-Ortíz GJ, Perandones C, Carminatti H, Matilla A, Radrizzani M. Anp32e/Cpd1 regulates protein phosphatase 2A activity at synapses during synaptogenesis. Eur J Neurosci. 2006;23:309–324. doi:10.1111/j.1460-9568.2005.04555.x.
  • Jiang M, Ma Y, Ni X, Cao G, Ji C, Cheng H, Tang R, Xie Y, Mao Y. Molecular cloning and characterization of a novel human gene (ANP32E alias LANPL) from human fetal brain. Cytogenet Genome Res. 2002;97:68–71. doi:10.1159/000064058.
  • Sardiu ME, Cai Y, Jin J, Swanson SK, Conaway RC, Conaway JW, Florens L, Washburn MP. Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc Natl Acad Sci USA. 2008;105:1454–1459. doi:10.1073/pnas.0706983105.
  • Obri A, Ouararhni K, Papin C, Diebold ML, Padmanabhan K, Marek M, Stoll I, Roy L, Reilly PT, Mak TW, et al. ANP32E is a histone chaperone that removes H2A.Z from chromatin. Nature. 2014;505:648–653. doi:10.1038/nature12922.
  • Shin H, He M, Yang Z, Jeon YH, Pfleger J, Sayed D, Abdellatif M. Transcriptional regulation mediated by H2A.Z via ANP32e-dependent inhibition of protein phosphatase 2A. Biochim Biophys Acta Gene Regul Mech. 2018;1861:481–496. doi:10.1016/j.bbagrm.2018.03.002.
  • Mao Z, Pan L, Wang W, Sun J, Shan S, Dong Q, Liang X, Dai L, Ding X, Chen S, et al. Anp32e, a higher eukaryotic histone chaperone directs preferential recognition for H2A.Z. Cell Res. 2014;24:389–399. doi:10.1038/cr.2014.30.
  • Murphy PJ, Wu SF, James CR, Wike CL, Cairns BR. Placeholder nucleosomes underlie germline-to-embryo DNA methylation reprogramming. Cell. 2018;172:993–1006.e1013. doi:10.1016/j.cell.2018.01.022.
  • Murphy KE, Meng FW, Makowski CE, Murphy PJ. Genome-wide chromatin accessibility is restricted by ANP32E. Nat Commun. 2020;11:5063. doi:10.1038/s41467-020-18821-x.
  • Stefanelli G, Makowski CE, Brimble MA, Hall M, Reda A, Creighton SD, Leonetti AM, McLean TAB, Zakaria JM, Baumbach J, et al. The histone chaperone Anp32e regulates memory formation, transcription, and dendritic morphology by regulating steady-state H2A.Z binding in neurons. Cell Rep. 2021;36:109551. doi:10.1016/j.celrep.2021.109551.
  • Alatwi HE, Downs JA. Removal of H2A.Z by INO80 promotes homologous recombination. EMBO Rep. 2015;16:986–994. doi:10.15252/embr.201540330.
  • Gursoy-Yuzugullu O, Ayrapetov MK, Price BD. Histone chaperone Anp32e removes H2A.Z from DNA double-strand breaks and promotes nucleosome reorganization and DNA repair. Proc Natl Acad Sci USA. 2015;112:7507–7512. doi:10.1073/pnas.1504868112.
  • Latrick CM, Marek M, Ouararhni K, Papin C, Stoll I, Ignatyeva M, Obri A, Ennifar E, Dimitrov S, Romier C, et al. Molecular basis and specificity of H2A.Z-H2B recognition and deposition by the histone chaperone YL1. Nat Struct Mol Biol. 2016;23:309–316. doi:10.1038/nsmb.3189.
  • Piquet S, Le Parc F, Bai SK, Chevallier O, Adam S, Polo SE. The histone chaperone FACT coordinates H2A.X-dependent signaling and repair of DNA damage. Mol Cell. 2018;72:888–901.e7. doi:10.1016/j.molcel.2018.09.010.
  • Giaimo BD, Ferrante F, Herchenröther A, Hake SB, Borggrefe T. The histone variant H2A.Z in gene regulation. Epigenetics Chromatin. 2019;12:37. doi:10.1186/s13072-019-0274-9.
  • Greaves IK, Rangasamy D, Ridgway P, Tremethick DJ. H2A.Z contributes to the unique 3D structure of the centromere. Proc Natl Acad Sci USA. 2007;104:525–530. doi:10.1073/pnas.0607870104.
  • Guillemette B, Bataille AR, Gévry N, Adam M, Blanchette M, Robert F, Gaudreau L. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 2005;3:e384. doi:10.1371/journal.pbio.0030384.
  • Krogan NJ, Baetz K, Keogh MC, Datta N, Sawa C, Kwok TC, Thompson NJ, Davey MG, Pootoolal J, Hughes TR, et al. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc Natl Acad Sci USA. 2004;101:13513–13518. doi:10.1073/pnas.0405753101.
  • Rangasamy D, Berven L, Ridgway P, Tremethick DJ. Pericentric heterochromatin becomes enriches with H2A.Z during early mammalian development. EMBO J. 2003;22:1599–1607. doi:10.1093/emboj/cdg160.
  • Subramanian V, Mazumder A, Surface LE, Butty VL, Fields PA, Alwan A, Torrey L, Thai KK, Levine SS, Bathe M, et al. H2A.Z acidic patch couples chromatin dynamics to regulation of gene expression programs during ESC differentiation. PLoS Genet. 2013;9:e1003725. doi:10.1371/journal.pgen.1003725.
  • Zhang H, Roberts DN, Cairns BR. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell. 2005;123:219–231. doi:10.1016/j.cell.2005.08.036.
  • Nekrasov M, Amrichova J, Parker BJ, Soboleva TA, Jack C, Williams R, Huttley GA, Tremethick DJ. Histone H2A.Z inheritance during the cell cycle and its impact on promoter organization and dynamics. Nat Struct Mol Biol. 2012;19:1076–1083. doi:10.1038/nsmb.2424.
  • Dijkwel Y, Tremethick DJ. The Role of the Histone Variant H2A.Z in Metazoan Development. JDB. 2022;10:28 10.3390/jdb10030028.
  • Baptista T, Graça I, Sousa EJ, Oliveira AI, Costa NR, Costa-Pinheiro P, Amado F, Henrique R, Jerónimo C. Regulation of histone H2A.Z expression is mediated by sirtuin 1 in prostate cancer. Oncotarget. 2013;4:1673–1685. doi:10.18632/oncotarget.1237.
  • Hua S, Kallen CB, Dhar R, Baquero MT, Mason CE, Russell BA, Shah PK, Liu J, Khramtsov A, Tretiakova MS, et al. Genomic analysis of estrogen cascade reveals histone variant H2A.Z associated with breast cancer progression. Mol Syst Biol. 2008;4:188. doi:10.1038/msb.2008.25.
  • Yang B, Tong R, Liu H, Wu J, Chen D, Xue Z, Ding C, Zhou L, Xie H, Wu J, et al. H2A.Z regulates tumorigenesis, metastasis and sensitivity to cisplatin in intrahepatic cholangiocarcinoma. Int J Oncol. 2018;52:1235–1245. doi:10.3892/ijo.2018.4292.
  • Svotelis A, Gévry N, Grondin G, Gaudreau L. H2A.Z overexpression promotes cellular proliferation of breast cancer cells. Cell Cycle. 2010;9:364–370. doi:10.4161/cc.9.2.10465.
  • Vardabasso C, Gaspar-Maia A, Hasson D, Pünzeler S, Valle-Garcia D, Straub T, Keilhauer EC, Strub T, Dong J, Panda T, et al. Histone variant H2A.Z.2 mediates proliferation and drug sensitivity of malignant melanoma. Mol Cell. 2015;59:75–88. doi:10.1016/j.molcel.2015.05.009.
  • Li P, Xu T, Zhou X, Liao L, Pang G, Luo W, Han L, Zhang J, Luo X, Xie X, et al. Downregulation of miRNA-141 in breast cancer cells is associated with cell migration and invasion: involvement of ANP32E targeting. Cancer Med. 2017;6:662–672. doi:10.1002/cam4.1024.
  • Diller L, Kassel J, Nelson CE, Gryka MA, Litwak G, Gebhardt M, Bressac B, Ozturk M, Bakter SJ, Vogelstein B, et al. p53 functions as a cell cycle control protein in osteosarcomas. Mol Cell Biol. 1990;10:5772–5781. doi:10.1128/MCB.10.11.5772.
  • Cai Y, Jin J, Florens L, Swanson SK, Kusch T, Li B, Workman JL, Washburn MP, Conaway RC, Conaway JW. The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem. 2005;280:13665–13670. doi:10.1074/jbc.M500001200.
  • Fu H, Subramanian RR, Masters SC. 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol. 2000;40:617–647. doi:10.1146/annurev.pharmtox.40.1.617.
  • Santa-Coloma TA. Anp32e (Cpd1) and related protein phosphatase 2 inhibitors. Cerebellum. 2003;2:310–320. doi:10.1080/14734220310017212.
  • Matsubae M, Kurihara T, Tachibana T, Imamoto N, Yoneda Y. Characterization of the nuclear transport of a novel leucine-rich acidic nuclear protein-like protein. FEBS Lett. 2000;468:171–175. doi:10.1016/s0014-5793(00)01218-7.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408. doi:10.1006/meth.2001.1262.
  • Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11:36–42.
  • Hart-Smith G, Raftery MJ. Detection and characterization of low abundance glycopeptides via higher-energy C-trap dissociation and Orbitrap mass analysis. J Am Soc Mass Spectrom. 2012;23:124–140. doi:10.1007/s13361-011-0273-y).
  • Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26:1367–1372. doi:10.1038/nbt.1511.
  • Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794–1805. doi:10.1021/pr101065j.
  • Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014;13:2513–2526. doi:10.1074/mcp.M113.031591.
  • Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods. 2016;13:731–740. doi:10.1038/nmeth.3901.
  • Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i890. doi:10.1093/bioinformatics/bty560.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359. doi:10.1038/nmeth.1923.
  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi:10.1093/bioinformatics/btp352.
  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9:R137. doi:10.1186/gb-2008-9-9-r137.
  • Perez-Riverol Y, Bai J, Bandla C, García-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M, et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 2022;50:D543–D552. doi:10.1093/nar/gkab1038.