1,402
Views
11
CrossRef citations to date
0
Altmetric
Reports

Polo-like kinase 1 (PLK1)-dependent phosphorylation of methylenetetrahydrofolate reductase (MTHFR) regulates replication via histone methylation

, , , , , , , , , & ORCID Icon show all
Pages 1933-1942 | Received 06 Jul 2017, Accepted 30 Jul 2017, Published online: 13 Sep 2017

References

  • Locasale JW. Serine, glycine and one-carbon units: cancer metabolism in full circle. Nat Rev Cancer. 2013;13:572-83. doi:10.1038/nrc3557. PMID:23822983
  • Mentch SJ, Locasale JW. One-carbon metabolism and epigenetics: understanding the specificity. Ann N Y Acad Sci. 2016;1363:91-8. doi:10.1111/nyas.12956. PMID:26647078
  • Jorgensen S, Schotta G, Sorensen CS. Histone H4 lysine 20 methylation: key player in epigenetic regulation of genomic integrity. Nucleic Acids Res. 2013;41:2797-806. doi:10.1093/nar/gkt012. PMID:23345616
  • Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, Jenuwein T. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 2005;24:800-12. doi:10.1038/sj.emboj.7600545. PMID:15678104
  • Benetti R, Garcia-Cao M, Blasco MA. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet. 2007;39:243-50. doi:10.1038/ng1952. PMID:17237781
  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 2004;18:1251-62. doi:10.1101/gad.300704. PMID:15145825
  • van Nuland R, Gozani O. Histone H4 Lysine 20 (H4K20) Methylation, Expanding the Signaling Potential of the Proteome One Methyl Moiety at a Time. Mol Cell Proteomics. 2016;15:755-64. doi:10.1074/mcp.R115.054742. PMID:26598646
  • Houston SI, McManus KJ, Adams MM, Sims JK, Carpenter PB, Hendzel MJ, Rice JC. Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J Biol Chem. 2008;283:19478-88. doi:10.1074/jbc.M710579200. PMID:18480059
  • Tardat M, Murr R, Herceg Z, Sardet C, Julien E. PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J Cell Biol. 2007;179:1413-26. doi:10.1083/jcb.200706179. PMID:18158331
  • Jorgensen S, Elvers I, Trelle MB, Menzel T, Eskildsen M, Jensen ON, Helleday T, Helin K, Sorensen CS. The histone methyltransferase SET8 is required for S-phase progression. J Cell Biol. 2007;179:1337-45. doi:10.1083/jcb.200706150. PMID:18166648
  • Centore RC, Havens CG, Manning AL, Li JM, Flynn RL, Tse A, Jin J, Dyson NJ, Walter JC, Zou L. CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol Cell. 2010;40:22-33. doi:10.1016/j.molcel.2010.09.015. PMID:20932472
  • Beck DB, Burton A, Oda H, Ziegler-Birling C, Torres-Padilla ME, Reinberg D. The role of PR-Set7 in replication licensing depends on Suv4-20h. Genes Dev. 2012;26:2580-9. doi:10.1101/gad.195636.112. PMID:23152447
  • Evertts AG, Manning AL, Wang X, Dyson NJ, Garcia BA, Coller HA. H4K20 methylation regulates quiescence and chromatin compaction. Mol Biol Cell. 2013;24:3025-37. doi:10.1091/mbc.E12-07-0529. PMID:23924899
  • Arias EE, Walter JC. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 2007;21:497-518. doi:10.1101/gad.1508907. PMID:17344412
  • Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ, Gozani O. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature. 2012; 484:115-9. doi:10.1038/nature10956. PMID:22398447
  • Shen Z, Sathyan KM, Geng Y, Zheng R, Chakraborty A, Freeman B, Wang F, Prasanth KV, Prasanth SG. A WD-repeat protein stabilizes ORC binding to chromatin. Mol Cell. 2010;40:99-111. doi:10.1016/j.molcel.2010.09.021. PMID:20932478
  • Schotta G, Sengupta R, Kubicek S, Malin S, Kauer M, Callen E, Celeste A, Pagani M, Opravil S, De La Rosa-Velazquez IA, et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev 2008; 22:2048-61. doi:10.1101/gad.476008. PMID:18676810
  • Wang Y, Khan A, Marks AB, Smith OK, Giri S, Lin YC, Creager R, MacAlpine DM, Prasanth KV, Aladjem MI, et al. Temporal association of ORCA/LRWD1 to late-firing origins during G1 dictates heterochromatin replication and organization. Nucleic Acids Res. 2017; 45:2490-502. doi:10.1093/nar/gkw1211. PMID:27924004
  • Zhu B, Xiahou Z, Zhao H, Peng B, Xu X. MTHFR promotes heterochromatin maintenance. Biochem Biophys Res Commun. 2014;447:702-6. doi:10.1016/j.bbrc.2014.04.082. PMID:24769206
  • Chabner BA, Roberts TG, Jr. Timeline: Chemotherapy and the war on cancer. Nat Rev Cancer. 2005;5:65-72. doi:10.1038/nrc1529. PMID:15630416
  • Yeh CC, Lai CY, Chang SN, Hsieh LL, Tang R, Sung FC, Lin YK. Polymorphisms of MTHFR C677T and A1298C associated with survival in patients with colorectal cancer treated with 5-fluorouracil-based chemotherapy. Int J Clin Oncol. 2017;22(3):484-493. doi:10.1007/s10147-016-1080-z. PMID:28044213.
  • Yamada K, Strahler JR, Andrews PC, Matthews RG. Regulation of human methylenetetrahydrofolate reductase by phosphorylation. Proc Natl Acad Sci U S A. 2005;102:10454-9. doi:10.1073/pnas.0504786102. PMID:16024724
  • Archambault V, Glover DM. Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol. 2009;10:265-75. doi:10.1038/nrm2653. PMID:19305416
  • Elia AE, Cantley LC, Yaffe MB. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science. 2003;299:1228-31. doi:10.1126/science.1079079. PMID:12595692
  • Zitouni S, Nabais C, Jana SC, Guerrero A, Bettencourt-Dias M. Polo-like kinases: structural variations lead to multiple functions. Nat Rev Mol Cell Biol. 2014;15:433-52. doi:10.1038/nrm3819. PMID:24954208
  • Guenther BD, Sheppard CA, Tran P, Rozen R, Matthews RG, Ludwig ML. The structure and properties of methylenetetrahydrofolate reductase from Escherichia coli suggest how folate ameliorates human hyperhomocysteinemia. Nat Struct Biol. 1999;6:359-65. doi:10.1038/7594. PMID:10201405
  • Bao ZS, Chen HM, Yang MY, Zhang CB, Yu K, Ye WL, Hu BQ, Yan W, Zhang W, Akers J, et al. RNA-seq of 272 gliomas revealed a novel, recurrent PTPRZ1-MET fusion transcript in secondary glioblastomas. Genome Res. 2014;24:1765-73. doi:10.1101/gr.165126.113. PMID:25135958
  • Archambault V, Lepine G, Kachaner D. Understanding the Polo Kinase machine. Oncogene. 2015;34:4799-807. doi:10.1038/onc.2014.451. PMID:25619835
  • Hardy CF, Pautz A. A novel role for Cdc5p in DNA replication. Mol Cell Biol. 1996;16:6775-82. doi:10.1128/MCB.16.12.6775. PMID:8943332
  • Tsvetkov L, Stern DF. Interaction of chromatin-associated Plk1 and Mcm7. J Biol Chem. 2005;280:11943-7. doi:10.1074/jbc.M413514200. PMID:15654075
  • Stuermer A, Hoehn K, Faul T, Auth T, Brand N, Kneissl M, Putter V, Grummt F. Mouse pre-replicative complex proteins colocalise and interact with the centrosome. Eur J Cell Biol. 2007;86:37-50. doi:10.1016/j.ejcb.2006.09.002. PMID:17157410
  • Song B, Liu XS, Davis K, Liu X. Plk1 phosphorylation of Orc2 promotes DNA replication under conditions of stress. Mol Cell Biol. 2011;31:4844-56. doi:10.1128/MCB.06110-11. PMID:21947279
  • Wu ZQ, Liu X. Role for Plk1 phosphorylation of Hbo1 in regulation of replication licensing. Proc Natl Acad Sci U S A. 2008;105:1919-24. doi:10.1073/pnas.0712063105. PMID:18250300
  • Lei M, Erikson RL. Plk1 depletion in nontransformed diploid cells activates the DNA-damage checkpoint. Oncogene. 2008;27:3935-43. doi:10.1038/onc.2008.36. PMID:18297112
  • Park SH, Yu SE, Chai YG, Jang YK. CDK2-dependent phosphorylation of Suv39H1 is involved in control of heterochromatin replication during cell cycle progression. Nucleic Acids Res. 2014;42:6196-207. doi:10.1093/nar/gku263. PMID:24728993
  • Wu S, Wang W, Kong X, Congdon LM, Yokomori K, Kirschner MW, Rice JC. Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 2010;24:2531-42. doi:10.1101/gad.1984210. PMID:20966048
  • Zhou L, Tian X, Zhu C, Wang F, Higgins JM. Polo-like kinase-1 triggers histone phosphorylation by Haspin in mitosis. EMBO Rep. 2014;15:273-81. PMID:24413556
  • Ghenoiu C, Wheelock MS, Funabiki H. Autoinhibition and Polo-dependent multisite phosphorylation restrict activity of the histone H3 kinase Haspin to mitosis. Mol Cell. 2013;52:734-45. doi:10.1016/j.molcel.2013.10.002. PMID:24184212
  • Prioleau MN, MacAlpine DM. DNA replication origins-where do we begin? Genes Dev. 2016; 30:1683-97. doi:10.1101/gad.285114.116. PMID:27542827
  • Gonzalo S, Garcia-Cao M, Fraga MF, Schotta G, Peters AH, Cotter SE, Eguia R, Dean DC, Esteller M, Jenuwein T, et al. Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin. Nat Cell Biol. 2005;7:420-8. doi:10.1038/ncb1235. PMID:15750587
  • Manning AL, Yazinski SA, Nicolay B, Bryll A, Zou L, Dyson NJ. Suppression of genome instability in pRB-deficient cells by enhancement of chromosome cohesion. Mol Cell. 2014;53:993-1004. doi:10.1016/j.molcel.2014.01.032. PMID:24613344
  • Zheng G, Yu H. Regulation of sister chromatid cohesion during the mitotic cell cycle. Sci China Life Sci. 2015;58:1089-98. doi:10.1007/s11427-015-4956-7. PMID:26511516
  • Wu R, Wang Z, Zhang H, Gan H, Zhang Z. H3K9me3 demethylase Kdm4d facilitates the formation of pre-initiative complex and regulates DNA replication. Nucleic Acids Res. 2017;45:169-80. doi:10.1093/nar/gkw848. PMID:27679476
  • Huang C, Cheng J, Bawa-Khalfe T, Yao X, Chin YE, Yeh ET. SUMOylated ORC2 Recruits a Histone Demethylase to Regulate Centromeric Histone Modification and Genomic Stability. Cell Rep. 2016;15:147-57. doi:10.1016/j.celrep.2016.02.091. PMID:27052177
  • Li S, Swanson SK, Gogol M, Florens L, Washburn MP, Workman JL, Suganuma T. Serine and SAM Responsive Complex SESAME Regulates Histone Modification Crosstalk by Sensing Cellular Metabolism. Mol Cell. 2015;60:408-21. doi:10.1016/j.molcel.2015.09.024. PMID:26527276
  • Suganuma T, Workman JL. Histone modification as a reflection of metabolism. Cell Cycle. 2016;15:481-2. doi:10.1080/15384101.2015.1128190. PMID:26726751
  • Shyh-Chang N, Locasale JW, Lyssiotis CA, Zheng Y, Teo RY, Ratanasirintrawoot S, Zhang J, Onder T, Unternaehrer JJ, Zhu H, et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science. 2013;339:222-6. doi:10.1126/science.1226603. PMID:23118012
  • Shiraki N, Shiraki Y, Tsuyama T, Obata F, Miura M, Nagae G, Aburatani H, Kume K, Endo F, Kume S. Methionine metabolism regulates maintenance and differentiation of human pluripotent stem cells. Cell Metab. 2014;19:780-94. doi:10.1016/j.cmet.2014.03.017. PMID:24746804
  • Milutinovic S, Zhuang Q, Niveleau A, Szyf M. Epigenomic stress response. Knockdown of DNA methyltransferase 1 triggers an intra-S-phase arrest of DNA replication and induction of stress response genes. J Biol Chem. 2003;278:14985-95.
  • Unterberger A, Andrews SD, Weaver IC, Szyf M. DNA methyltransferase 1 knockdown activates a replication stress checkpoint. Mol Cell Biol. 2006; 26:7575-86. doi:10.1128/MCB.01887-05. PMID:17015478
  • Strickland M, Stoll EA. Metabolic Reprogramming in Glioma. Front Cell Dev Biol. 2017;5:43. doi:10.3389/fcell.2017.00043. PMID:28491867
  • Lewis PW, Muller MM, Koletsky MS, Cordero F, Lin S, Banaszynski LA, Garcia BA, Muir TW, Becher OJ, Allis CD. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science. 2013; 340:857-61. doi:10.1126/science.1232245. PMID:23539183
  • Sharma V, Malgulwar PB, Purkait S, Patil V, Pathak P, Agrawal R, Kulshreshtha R, Mallick S, Julka PK, Suri A, et al. Genome-wide ChIP-seq analysis of EZH2-mediated H3K27me3 target gene profile highlights differences between low- and high-grade astrocytic tumors. Carcinogenesis 2017;38:152-61. PMID:27993893
  • Mohammad F, Weissmann S, Leblanc B, Pandey DP, Hojfeldt JW, Comet I, Zheng C, Johansen JV, Rapin N, Porse BT, et al. EZH2 is a potential therapeutic target for H3K27M-mutant pediatric gliomas. Nat Med. 2017;23:483-92. doi:10.1038/nm.4293. PMID:28263309
  • Li J, Wang J, Hou W, Jing Z, Tian C, Han Y, Liao J, Dong MQ, Xu X. Phosphorylation of Ataxin-10 by polo-like kinase 1 is required for cytokinesis. Cell Cycle. 2011;10:2946-58. doi:10.4161/cc.10.17.15922. PMID:21857149
  • Tian J, Tian C, Ding Y, Li Z, Geng Q, Xiahou Z, Wang J, Hou W, Liao J, Dong MQ, et al. Aurora B-dependent phosphorylation of Ataxin-10 promotes the interaction between Ataxin-10 and Plk1 in cytokinesis. Sci Rep. 2015;5:8360. doi:10.1038/srep08360. PMID:25666058
  • Li J, Liu X, Liao J, Tian J, Wang J, Wang X, Zhang J, Xu X. MYPT1 sustains centromeric cohesion and the spindle-assembly checkpoint. J Genet Genomics. 2013;40:575-8. doi:10.1016/j.jgg.2013.08.005. PMID:24238611

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.