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Research Article

The PHLPP1 N-Terminal Extension Is a Mitotic Cdk1 Substrate and Controls an Interactome Switch

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Article: e00333-20 | Received 07 Jul 2020, Accepted 19 Dec 2020, Published online: 03 Mar 2023

REFERENCES

  • Naylor RM, van Deursen JM. 2016. Aneuploidy in cancer and aging. Annu Rev Genet 50:45–66. https://doi.org/10.1146/annurev-genet-120215-035303.
  • Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA. 2011. Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci Signal 4:rs5. https://doi.org/10.1126/scisignal.2001497.
  • Dephoure N, Zhou C, Villén J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP. 2008. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 105:10762–10767. https://doi.org/10.1073/pnas.0805139105.
  • Wurzenberger C, Gerlich DW. 2011. Phosphatases: providing safe passage through mitotic exit. Nat Rev Mol Cell Biol 12:469–482. https://doi.org/10.1038/nrm3149.
  • King RW, Peters JM, Tugendreich S, Rolfe M, Hieter P, Kirschner MW. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279–288. https://doi.org/10.1016/0092-8674(95)90338-0.
  • Sudakin V, Ganoth D, Dahan A, Heller H, Hershko J, Luca FC, Ruderman JV, Hershko A. 1995. The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol Biol Cell 6:185–197. https://doi.org/10.1091/mbc.6.2.185.
  • Irniger S, Piatti S, Michaelis C, Nasmyth K. 1995. Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81:269–278. https://doi.org/10.1016/0092-8674(95)90337-2.
  • Dou Z, von Schubert C, Körner R, Santamaria A, Elowe S, Nigg EA. 2011. Quantitative mass spectrometry analysis reveals similar substrate consensus motif for human Mps1 kinase and Plk1. PLoS One 6:e18793. https://doi.org/10.1371/journal.pone.0018793.
  • Hayward D, Alfonso-Pérez T, Cundell MJ, Hopkins M, Holder J, Bancroft J, Hutter LH, Novak B, Barr FA, Gruneberg U. 2019. CDK1-CCNB1 creates a spindle checkpoint-permissive state by enabling MPS1 kinetochore localization. J Cell Biol 218:1182–1199. https://doi.org/10.1083/jcb.201808014.
  • Gharbi-Ayachi A, Labbé J-C, Burgess A, Vigneron S, Strub J-M, Brioudes E, Van-Dorsselaer A, Castro A, Lorca T. 2010. The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330:1673–1677. https://doi.org/10.1126/science.1197048.
  • Blake-Hodek KA, Williams BC, Zhao Y, Castilho PV, Chen W, Mao Y, Yamamoto TM, Goldberg ML. 2012. Determinants for activation of the atypical AGC kinase Greatwall during M phase entry. Mol Cell Biol 32:1337–1353. https://doi.org/10.1128/MCB.06525-11.
  • Vigneron S, Gharbi-Ayachi A, Raymond A-A, Burgess A, Labbé J-C, Labesse G, Monsarrat B, Lorca T, Castro A. 2011. Characterization of the mechanisms controlling Greatwall activity. Mol Cell Biol 31:2262–2275. https://doi.org/10.1128/MCB.00753-10.
  • Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J. 2002. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 21:5911–5920. https://doi.org/10.1093/emboj/cdf567.
  • Wu Z, Jiang Q, Clarke PR, Zhang C. 2013. Phosphorylation of Crm1 by CDK1–cyclin-B promotes Ran-dependent mitotic spindle assembly. J Cell Sci 126:3417–3428. https://doi.org/10.1242/jcs.126854.
  • Grzechnik AT, Newton AC. 2016. PHLPPing through history: a decade in the life of PHLPP phosphatases. Biochem Soc Trans 44:1675–1682. https://doi.org/10.1042/BST20160170.
  • Chen MJ, Dixon JE, Manning G. 2017. Genomics and evolution of protein phosphatases. Sci Signal 10:eaag1796. https://doi.org/10.1126/scisignal.aag1796.
  • Gao T, Furnari F, Newton AC. 2005. PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Mol Cell 18:13–24. https://doi.org/10.1016/j.molcel.2005.03.008.
  • Brognard J, Sierecki E, Gao T, Newton AC. 2007. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell 25:917–931. https://doi.org/10.1016/j.molcel.2007.02.017.
  • Goel A, Arnold CN, Niedzwiecki D, Chang DK, Ricciardiello L, Carethers JM, Dowell JM, Wasserman L, Compton C, Mayer RJ, Bertagnolli MM, Boland CR. 2003. Characterization of sporadic colon cancer by patterns of genomic instability. Cancer Res 63:1608–1614.
  • Johnson-Pais TL, Nellissery MJ, Ammerman DG, Pathmanathan D, Bhatia P, Buller CL, Leach RJ, Hansen MF. 2003. Determination of a minimal region of loss of heterozygosity on chromosome 18q21.33 in osteosarcoma. Int J Cancer 105:285–288. https://doi.org/10.1002/ijc.11070.
  • Rakha EA, Green AR, Powe DG, Roylance R, Ellis IO. 2006. Chromosome 16 tumor-suppressor genes in breast cancer. Genes Chromosomes Cancer 45:527–535. https://doi.org/10.1002/gcc.20318.
  • Tørring N, Borre M, Sørensen KD, Andersen CL, Wiuf C, Ørntoft TF. 2007. Genome-wide analysis of allelic imbalance in prostate cancer using the Affymetrix 50K SNP mapping array. Br J Cancer 96:499–506. https://doi.org/10.1038/sj.bjc.6603476.
  • Chen M, Pratt CP, Zeeman ME, Schultz N, Taylor BS, O'Neill A, Castillo-Martin M, Nowak DG, Naguib A, Grace DM, Murn J, Navin N, Atwal GS, Sander C, Gerald WL, Cordon-Cardo C, Newton AC, Carver BS, Trotman LC. 2011. Identification of PHLPP1 as a tumor suppressor reveals the role of feedback activation in PTEN-mutant prostate cancer progression. Cancer Cell 20:173–186. https://doi.org/10.1016/j.ccr.2011.07.013.
  • Li X, Stevens PD, Liu J, Yang H, Wang W, Wang C, Zeng Z, Schmidt MD, Yang M, Lee EY, Gao T. 2014. PHLPP is a negative regulator of RAF1, which reduces colorectal cancer cell motility and prevents tumor progression in mice. Gastroenterology 146:1301–1312.E10. https://doi.org/10.1053/j.gastro.2014.02.003.
  • Liu J, Stevens PD, Li X, Schmidt MD, Gao T. 2011. PHLPP-mediated dephosphorylation of S6K1 inhibits protein translation and cell growth. Mol Cell Biol 31:4917–4927. https://doi.org/10.1128/MCB.05799-11.
  • Baffi TR, Van AN, Zhao W, Mills GB, Newton AC. 2019. Protein kinase C quality control by phosphatase PHLPP1 unveils loss-of-function mechanism in cancer. Mol Cell 74:378–392.E5. https://doi.org/10.1016/j.molcel.2019.02.018.
  • Gao T, Brognard J, Newton AC. 2008. The phosphatase PHLPP controls the cellular levels of protein kinase C. J Biol Chem 283:6300–6311. https://doi.org/10.1074/jbc.M707319200.
  • Cohen Katsenelson K, Stender JD, Kawashima AT, Lordén G, Uchiyama S, Nizet V, Glass CK, Newton AC. 2019. PHLPP1 counter-regulates STAT1-mediated inflammatory signaling. Elife 8:e48609. https://doi.org/10.7554/eLife.48609.
  • Reyes G, Niederst M, Cohen-Katsenelson K, Stender JD, Kunkel MT, Chen M, Brognard J, Sierecki E, Gao T, Nowak DG, Trotman LC, Glass CK, Newton AC. 2014. Pleckstrin homology domain leucine-rich repeat protein phosphatases set the amplitude of receptor tyrosine kinase output. Proc Natl Acad Sci U S A 111:E3957–E3965. https://doi.org/10.1073/pnas.1404221111.
  • Patterson SJ, Han JM, Garcia R, Assi K, Gao T, O'Neill A, Newton AC, Levings MK. 2011. Cutting edge: PHLPP regulates the development, function, and molecular signaling pathways of regulatory T cells. J Immunol 186:5533–5537. https://doi.org/10.4049/jimmunol.1002126.
  • Hwang SM, Feigenson M, Begun DL, Shull LC, Culley KL, Otero M, Goldring MB, Ta LE, Kakar S, Bradley EW, Westendorf JJ. 2018. Phlpp inhibitors block pain and cartilage degradation associated with osteoarthritis. J Orthop Res 36:1487–1497. https://doi.org/10.1002/jor.23781.
  • Bradley EW, Carpio LR, Westendorf JJ. 2013. Histone deacetylase 3 suppression increases PH domain and leucine-rich repeat phosphatase (Phlpp)1 expression in chondrocytes to suppress Akt signaling and matrix secretion. J Biol Chem 288:9572–9582. https://doi.org/10.1074/jbc.M112.423723.
  • Bradley EW, Carpio LR, Newton AC, Westendorf JJ. 2015. Deletion of the PH-domain and leucine-rich repeat protein phosphatase 1 (Phlpp1) increases fibroblast growth factor (Fgf) 18 expression and promotes chondrocyte proliferation. J Biol Chem 290:16272–16280. https://doi.org/10.1074/jbc.M114.612937.
  • Gangula NR, Maddika S. 2017. Interplay between the phosphatase PHLPP1 and E3 ligase RNF41 stimulates proper kinetochore assembly via the outer-kinetochore protein SGT1. J Biol Chem 292:13947–13958. https://doi.org/10.1074/jbc.M117.782896.
  • Li X, Yang H, Liu J, Schmidt MD, Gao T. 2011. Scribble-mediated membrane targeting of PHLPP1 is required for its negative regulation of Akt. EMBO Rep 12:818–824. https://doi.org/10.1038/embor.2011.106.
  • Mészáros B, Erdos G, Dosztányi Z. 2018. IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res 46:W329–W337. https://doi.org/10.1093/nar/gky384.
  • Malumbres M. 2014. Cyclin-dependent kinases. Genome Biol 15:122. https://doi.org/10.1186/gb4184.
  • Songyang Z, Blechner S, Hoagland N, Hoekstra MF, Piwnica-Worms H, Cantley LC. 1994. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 4:973–982. https://doi.org/10.1016/s0960-9822(00)00221-9.
  • Mok J, Kim PM, Lam HYK, Piccirillo S, Zhou X, Jeschke GR, Sheridan DL, Parker SA, Desai V, Jwa M, Cameroni E, Niu H, Good M, Remenyi A, Ma J-LN, Sheu Y-J, Sassi HE, Sopko R, Chan CSM, De Virgilio C, Hollingsworth NM, Lim WA, Stern DF, Stillman B, Andrews BJ, Gerstein MB, Snyder M, Turk BE. 2010. Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci Signal 3:ra12. https://doi.org/10.1126/scisignal.2000482.
  • Shang C, Hazbun TR, Cheeseman IM, Aranda J, Fields S, Drubin DG, Barnes G. 2003. Kinetochore protein interactions and their regulation by the aurora kinase Ipl1p. Mol Biol Cell 14:3342–3355. https://doi.org/10.1091/mbc.e02-11-0765.
  • Roux KJ, Kim DI, Burke B, May DG. 2018. BioID: a screen for protein-protein interactions. Curr Protoc Protein Sci 91:19.23.1–19.23.15. https://doi.org/10.1002/cpps.51.
  • Choi-Rhee E, Schulman H, Cronan JE. 2004. Promiscuous protein biotinylation by Escherichia coli biotin protein ligase. Protein Sci 13:3043–3050. https://doi.org/10.1110/ps.04911804.
  • Teo G, Liu G, Zhang J, Nesvizhskii AI, Gingras AC, Choi H. 2014. SAINTexpress: improvements and additional features in significance analysis of INTeractome software. J Proteomics 100:37–43. https://doi.org/10.1016/j.jprot.2013.10.023.
  • Wan S, Meyer AS, Weiler SME, Rupp C, Tóth M, Sticht C, Singer S, Thomann S, Roessler S, Schorpp-Kistner M, Schmitt J, Gretz N, Angel P, Tschaharganeh DF, Marquardt J, Schirmacher P, Pinna F, Breuhahn K. 2018. Cytoplasmic localization of the cell polarity factor scribble supports liver tumor formation and tumor cell invasiveness. Hepatology 67:1842–1856. https://doi.org/10.1002/hep.29669.
  • Zhiqiang Z, Qinghui Y, Yongqiang Z, Jian Z, Xin Z, Haiying M, Yuepeng G. 2012. USP1 regulates AKT phosphorylation by modulating the stability of PHLPP1 in lung cancer cells. J Cancer Res Clin Oncol 138:1231–1238. https://doi.org/10.1007/s00432-012-1193-3.
  • Goldbraikh D, Neufeld D, Eid-Mutlak Y, Lasry I, Gilda JE, Parnis A, Cohen S. 2020. USP1 deubiquitinates Akt to inhibit PI3K-Akt-FoxO signaling in muscle during prolonged starvation. EMBO Rep 21:e48791. https://doi.org/10.15252/embr.201948791.
  • Zhang X, Lu X, Akhter S, Georgescu MM, Legerski RJ. 2016. FANCI is a negative regulator of Akt activation. Cell Cycle 15:1134–1143. https://doi.org/10.1080/15384101.2016.1158375.
  • Gangula NR, Maddika S. 2013. WD repeat protein WDR48 in complex with deubiquitinase USP12 suppresses Akt-dependent cell survival signaling by stabilizing PH domain leucine-rich repeat protein phosphatase 1 (PHLPP1). J Biol Chem 288:34545–34554. https://doi.org/10.1074/jbc.M113.503383.
  • Gagnon D, Lehoux M, Archambault J. 2015. Artificial recruitment of UAF1-USP complexes by a PHLPP1-E1 chimeric helicase enhances human papillomavirus DNA replication. J Virol 89:6227–6239. https://doi.org/10.1128/JVI.00560-15.
  • McClurg UL, Summerscales EE, Harle VJ, Gaughan L, Robson CN. 2014. Deubiquitinating enzyme Usp12 regulates the interaction between the androgen receptor and the Akt pathway. Oncotarget 5:7081–7092. https://doi.org/10.18632/oncotarget.2162.
  • Gao G, Kun T, Sheng Y, Qian M, Kong F, Liu X, Yu Z, Zhang H, Zhang Q, Gu J, Zhang X. 2013. SGT1 regulates Akt signaling by promoting beta-TrCP-dependent PHLPP1 degradation in gastric cancer cells. Mol Biol Rep 40:2947–2953. https://doi.org/10.1007/s11033-012-2363-8.
  • Reimand J, Kull M, Peterson H, Hansen J, Vilo J. 2007. g:Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 35:W193–W200. https://doi.org/10.1093/nar/gkm226.
  • Kalsbeek D, Golsteyn RM. 2017. G2/M-phase checkpoint adaptation and micronuclei formation as mechanisms that contribute to genomic instability in human cells. Int J Mol Sci 18:2344. https://doi.org/10.3390/ijms18112344.
  • Santamaría D, Barrière C, Cerqueira A, Hunt S, Tardy C, Newton K, Cáceres JF, Dubus P, Malumbres M, Barbacid M. 2007. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448:811–815. https://doi.org/10.1038/nature06046.
  • Szmyd R, Niska-Blakie J, Diril MK, Renck Nunes P, Tzelepis K, Lacroix A, van Hul N, Deng L-W, Matos J, Dreesen O, Bisteau X, Kaldis P. 2019. Premature activation of Cdk1 leads to mitotic events in S phase and embryonic lethality. Oncogene 38:998–1018. https://doi.org/10.1038/s41388-018-0464-0.
  • Piao J, Zhu L, Sun J, Li N, Dong B, Yang Y, Chen L. 2019. High expression of CDK1 and BUB1 predicts poor prognosis of pancreatic ductal adenocarcinoma. Gene 701:15–22. https://doi.org/10.1016/j.gene.2019.02.081.
  • Ravindran Menon D, Luo Y, Arcaroli JJ, Liu S, KrishnanKutty LN, Osborne DG, Li Y, Samson JM, Bagby S, Tan A-C, Robinson WA, Messersmith WA, Fujita M. 2018. CDK1 interacts with Sox2 and promotes tumor initiation in human melanoma. Cancer Res 78:6561–6574. https://doi.org/10.1158/0008-5472.CAN-18-0330.
  • Yasukawa M, Ando Y, Yamashita T, Matsuda Y, Shoji S, Morioka MS, Kawaji H, Shiozawa K, Machitani M, Abe T, Yamada S, Kaneko MK, Kato Y, Furuta Y, Kondo T, Shirouzu M, Hayashizaki Y, Kaneko S, Masutomi K. 2020. CDK1 dependent phosphorylation of hTERT contributes to cancer progression. Nat Commun 11:1557. https://doi.org/10.1038/s41467-020-15289-7.
  • Heo J, Noh B-J, Lee S, Lee H-Y, Kim Y, Lim J, Ju H, Yu HY, Ryu C-M, Lee PCW, Jeong H, Oh Y, Kim K, Kim S-Y, Son J, Hong B, Kim JS, Cho YM, Shin D-M. 2020. Phosphorylation of TFCP2L1 by CDK1 is required for stem cell pluripotency and bladder carcinogenesis. EMBO Mol Med 12:e10880. https://doi.org/10.15252/emmm.201910880.
  • Dong S, Huang F, Zhang H, Chen Q. 2019. Overexpression of BUB1B, CCNA2, CDC20, and CDK1 in tumor tissues predicts poor survival in pancreatic ductal adenocarcinoma. Bioscience Rep 39:BSR20182306. https://doi.org/10.1042/BSR20182306.
  • Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC, Chen L. 2006. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci U S A 103:10660–10665. https://doi.org/10.1073/pnas.0600447103.
  • Voets E, Marsman J, Demmers J, Beijersbergen R, Wolthuis R. 2015. The lethal response to Cdk1 inhibition depends on sister chromatid alignment errors generated by KIF4 and isoform 1 of PRC1. Sci Rep 5:14798. https://doi.org/10.1038/srep14798.
  • McCloy RA, Rogers S, Caldon CE, Lorca T, Castro A, Burgess A. 2014. Partial inhibition of Cdk1 in G2 phase overrides the SAC and decouples mitotic events. Cell Cycle 13:1400–1412. https://doi.org/10.4161/cc.28401.
  • Holt LJ, Tuch BB, Villén J, Johnson AD, Gygi SP, Morgan DO. 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325:1682–1686. https://doi.org/10.1126/science.1172867.
  • Cukier IH, Li Y, Lee JM. 2007. Cyclin B1/Cdk1 binds and phosphorylates Filamin A and regulates its ability to cross-link actin. FEBS Lett 581:1661–1672. https://doi.org/10.1016/j.febslet.2007.03.041.
  • Foisner R, Malecz N, Dressel N, Stadler C, Wiche G. 1996. M-phase-specific phosphorylation and structural rearrangement of the cytoplasmic cross-linking protein plectin involve p34cdc2 kinase. Mol Biol Cell 7:273–288. https://doi.org/10.1091/mbc.7.2.273.
  • Blethrow JD, Glavy JS, Morgan DO, Shokat KM. 2008. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci U S A 105:1442–1447. https://doi.org/10.1073/pnas.0708966105.
  • Koffa MD, Casanova CM, Santarella R, Köcher T, Wilm M, Mattaj IW. 2006. HURP is part of a Ran-dependent complex involved in spindle formation. Curr Biol 16:743–754. https://doi.org/10.1016/j.cub.2006.03.056.
  • Musacchio A, Desai A. 2017. A molecular view of kinetochore assembly and function. Biology 6:5. https://doi.org/10.3390/biology6010005.
  • Levine MS, Holland AJ. 2018. The impact of mitotic errors on cell proliferation and tumorigenesis. Genes Dev 32:620–638. https://doi.org/10.1101/gad.314351.118.
  • Kandel ES, Skeen J, Majewski N, Di Cristofano A, Pandolfi PP, Feliciano CS, Gartel A, Hay N. 2002. Activation of Akt/protein kinase B overcomes a G(2)/m cell cycle checkpoint induced by DNA damage. Mol Cell Biol 22:7831–7841. https://doi.org/10.1128/mcb.22.22.7831-7841.2002.
  • Shtivelman E, Sussman J, Stokoe D. 2002. A role for PI 3-kinase and PKB activity in the G2/M phase of the cell cycle. Curr Biol 12:919–924. https://doi.org/10.1016/s0960-9822(02)00843-6.
  • Dangi S, Cha H, Shapiro P. 2003. Requirement for phosphatidylinositol-3 kinase activity during progression through S-phase and entry into mitosis. Cell Signal 15:667–675. https://doi.org/10.1016/s0898-6568(03)00002-0.
  • Liu X, Shi Y, Woods KW, Hessler P, Kroeger P, Wilsbacher J, Wang J, Wang JY, Li C, Li Q, Rosenberg SH, Giranda VL, Luo Y. 2008. Akt inhibitor a-443654 interferes with mitotic progression by regulating aurora a kinase expression. Neoplasia 10:828–837. https://doi.org/10.1593/neo.08408.
  • Warfel NA, Niederst M, Stevens MW, Brennan PM, Frame MC, Newton AC. 2011. Mislocalization of the E3 ligase, β-transducin repeat-containing protein 1 (β-TrCP1), in glioblastoma uncouples negative feedback between the pleckstrin homology domain leucine-rich repeat protein phosphatase 1 (PHLPP1) and Akt. J Biol Chem 286:19777–19788. https://doi.org/10.1074/jbc.M111.237081.
  • Kean MJ, Couzens AL, Gingras A-C. 2012. Mass spectrometry approaches to study mammalian kinase and phosphatase associated proteins. Methods 57:400–408. https://doi.org/10.1016/j.ymeth.2012.06.002.
  • Uphoff CC, Drexler HG. 2004. Detecting Mycoplasma contamination in cell cultures by polymerase chain reaction. Methods Mol Med 88:319–326. https://doi.org/10.1385/1-59259-406-9:319.
  • Liu G, Knight JD, Zhang JP, Tsou CC, Wang J, Lambert JP, Larsen B, Tyers M, Raught B, Bandeira N, Nesvizhskii AI, Choi H, Gingras AC. 2016. Data independent acquisition analysis in ProHits 4.0. J Proteomics 149:64–68. https://doi.org/10.1016/j.jprot.2016.04.042.
  • Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567. https://doi.org/10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2.
  • Eng JK, Jahan TA, Hoopmann MR. 2013. Comet: an open-source MS/MS sequence database search tool. Proteomics 13:22–24. https://doi.org/10.1002/pmic.201200439.
  • Shteynberg D, Deutsch EW, Lam H, Eng JK, Sun Z, Tasman N, Mendoza L, Moritz RL, Aebersold R, Nesvizhskii AI. 2011. iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates. Mol Cell Proteomics 10:M111.007690. https://doi.org/10.1074/mcp.M111.007690.
  • Knight JDR, Choi H, Gupta GD, Pelletier L, Raught B, Nesvizhskii AI, Gingras AC. 2017. ProHits-viz: a suite of web tools for visualizing interaction proteomics data. Nat Methods 14:645–646. https://doi.org/10.1038/nmeth.4330.
  • Meitinger F, Anzola JV, Kaulich M, Richardson A, Stender JD, Benner C, Glass CK, Dowdy SF, Desai A, Shiau AK, Oegema K. 2016. 53BP1 and USP28 mediate p53 activation and G1 arrest after centrosome loss or extended mitotic duration. J Cell Biol 214:155–166. https://doi.org/10.1083/jcb.201604081.
  • Watson JV, Chambers SH, Smith PJ. 1987. A pragmatic approach to the analysis of DNA histograms with a definable G1 peak. Cytometry 8:1–8. https://doi.org/10.1002/cyto.990080101.

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