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Molecular mechanism of APC/C activation by mitotic phosphorylation.

Zhang S, Chang L, Alfieri C, Zhang Z, Yang J, Maslen S, Skehel M, Barford D
Nature 533 260-264 (2016)
Cited: 111 times
EuropePMC logo PMID: 27120157

Abstract

In eukaryotes, the anaphase-promoting complex (APC/C, also known as the cyclosome) regulates the ubiquitin-dependent proteolysis of specific cell-cycle proteins to coordinate chromosome segregation in mitosis and entry into the G1 phase. The catalytic activity of the APC/C and its ability to specify the destruction of particular proteins at different phases of the cell cycle are controlled by its interaction with two structurally related coactivator subunits, Cdc20 and Cdh1. Coactivators recognize substrate degrons, and enhance the affinity of the APC/C for its cognate E2 (refs 4-6). During mitosis, cyclin-dependent kinase (Cdk) and polo-like kinase (Plk) control Cdc20- and Cdh1-mediated activation of the APC/C. Hyperphosphorylation of APC/C subunits, notably Apc1 and Apc3, is required for Cdc20 to activate the APC/C, whereas phosphorylation of Cdh1 prevents its association with the APC/C. Since both coactivators associate with the APC/C through their common C-box and Ile-Arg tail motifs, the mechanism underlying this differential regulation is unclear, as is the role of specific APC/C phosphorylation sites. Here, using cryo-electron microscopy and biochemical analysis, we define the molecular basis of how phosphorylation of human APC/C allows for its control by Cdc20. An auto-inhibitory segment of Apc1 acts as a molecular switch that in apo unphosphorylated APC/C interacts with the C-box binding site and obstructs engagement of Cdc20. Phosphorylation of the auto-inhibitory segment displaces it from the C-box-binding site. Efficient phosphorylation of the auto-inhibitory segment, and thus relief of auto-inhibition, requires the recruitment of Cdk-cyclin in complex with a Cdk regulatory subunit (Cks) to a hyperphosphorylated loop of Apc3. We also find that the small-molecule inhibitor, tosyl-l-arginine methyl ester, preferentially suppresses APC/C(Cdc20) rather than APC/C(Cdh1), and interacts with the binding sites of both the C-box and Ile-Arg tail motifs. Our results reveal the mechanism for the regulation of mitotic APC/C by phosphorylation and provide a rationale for the development of selective inhibitors of this state.

Reviews - 5g05 mentioned but not cited (1)

  1. Visualizing the complex functions and mechanisms of the anaphase promoting complex/cyclosome (APC/C). Alfieri C, Zhang S, Barford D. Open Biol 7 (2017)

Articles - 5g05 mentioned but not cited (7)

  1. Molecular mechanism of APC/C activation by mitotic phosphorylation. Zhang S, Chang L, Alfieri C, Zhang Z, Yang J, Maslen S, Skehel M, Barford D. Nature 533 260-264 (2016)
  2. Identification of cancer driver genes based on nucleotide context. Dietlein F, Weghorn D, Taylor-Weiner A, Richters A, Reardon B, Liu D, Lander ES, Van Allen EM, Sunyaev SR. Nat Genet 52 208-218 (2020)
  3. Structure of the super-elongation complex subunit AFF4 C-terminal homology domain reveals requirements for AFF homo- and heterodimerization. Chen Y, Cramer P. J Biol Chem 294 10663-10673 (2019)
  4. Integrative modeling reveals the molecular architecture of the intraflagellar transport A (IFT-A) complex. McCafferty CL, Papoulas O, Jordan MA, Hoogerbrugge G, Nichols C, Pigino G, Taylor DW, Wallingford JB, Marcotte EM. Elife 11 e81977 (2022)
  5. WD40 domain of Apc1 is critical for the coactivator-induced allosteric transition that stimulates APC/C catalytic activity. Li Q, Chang L, Aibara S, Yang J, Zhang Z, Barford D. Proc. Natl. Acad. Sci. U.S.A. 113 10547-10552 (2016)
  6. research-article 3D structural human interactome reveals proteome-wide perturbations by disease mutations. Xiong D, Zhao J, Qiu Y, Zhou Y, Lee D, Gupta S, Lu W, Liang S, Kang JJ, Eng C, Loscalzo J, Cheng F, Yu H. bioRxiv 2023.04.24.538110 (2023)
  7. Analysis of Secondary Structure Biases in Naturally Presented HLA-I Ligands. Perez MAS, Bassani-Sternberg M, Coukos G, Gfeller D, Zoete V. Front Immunol 10 2731 (2019)


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  1. Ubiquitin Ligases: Structure, Function, and Regulation. Zheng N, Shabek N. Annu. Rev. Biochem. 86 129-157 (2017)
  2. Unravelling biological macromolecules with cryo-electron microscopy. Fernandez-Leiro R, Scheres SH. Nature 537 339-346 (2016)
  3. Posing the APC/C E3 Ubiquitin Ligase to Orchestrate Cell Division. Watson ER, Brown NG, Peters JM, Stark H, Schulman BA. Trends Cell Biol 29 117-134 (2019)
  4. Building a Regulatory Network with Short Linear Sequence Motifs: Lessons from the Degrons of the Anaphase-Promoting Complex. Davey NE, Morgan DO. Mol. Cell 64 12-23 (2016)
  5. Cdc20: At the Crossroads between Chromosome Segregation and Mitotic Exit. Kapanidou M, Curtis NL, Bolanos-Garcia VM. Trends Biochem. Sci. 42 193-205 (2017)
  6. Evolving Therapeutic Strategies to Exploit Chromosome Instability in Cancer. Thompson LL, Jeusset LM, Lepage CC, McManus KJ. Cancers (Basel) 9 (2017)
  7. APC/C ubiquitin ligase: Functions and mechanisms in tumorigenesis. Schrock MS, Stromberg BR, Scarberry L, Summers MK. Semin Cancer Biol 67 80-91 (2020)
  8. Kinase and Phosphatase Cross-Talk at the Kinetochore. Saurin AT. Front Cell Dev Biol 6 62 (2018)
  9. Recent advances in understanding the role of Cdk1 in the Spindle Assembly Checkpoint. Serpico AF, Grieco D. F1000Res 9 (2020)
  10. The unconventional kinetoplastid kinetochore: from discovery toward functional understanding. Akiyoshi B. Biochem. Soc. Trans. 44 1201-1217 (2016)
  11. Activating the Anaphase Promoting Complex to Enhance Genomic Stability and Prolong Lifespan. Harkness TAA. Int J Mol Sci 19 (2018)
  12. Ubiquitin signaling in cell cycle control and tumorigenesis. Dang F, Nie L, Wei W. Cell Death Differ 28 427-438 (2021)
  13. Intricate Regulatory Mechanisms of the Anaphase-Promoting Complex/Cyclosome and Its Role in Chromatin Regulation. Bodrug T, Welsh KA, Hinkle M, Emanuele MJ, Brown NG. Front Cell Dev Biol 9 687515 (2021)
  14. Protein phosphatases in the regulation of mitosis. Nilsson J. J. Cell Biol. 218 395-409 (2019)
  15. The diverging role of CDC14B: from mitotic exit in yeast to cell fate control in humans. Partscht P, Schiebel E. EMBO J 42 e114364 (2023)
  16. Who guards the guardian? Mechanisms that restrain APC/C during the cell cycle. Kernan J, Bonacci T, Emanuele MJ. Biochim Biophys Acta Mol Cell Res 1865 1924-1933 (2018)
  17. APC/C: current understanding and future perspectives. Yamano H. F1000Res 8 (2019)
  18. Interplay between Phosphatases and the Anaphase-Promoting Complex/Cyclosome in Mitosis. Kataria M, Yamano H. Cells 8 (2019)
  19. Mechanisms for the temporal regulation of substrate ubiquitination by the anaphase-promoting complex/cyclosome. Bansal S, Tiwari S. Cell Div 14 14 (2019)
  20. Mitotic Cell Division in Caenorhabditis elegans. Pintard L, Bowerman B. Genetics 211 35-73 (2019)
  21. Multiple Roles of PLK1 in Mitosis and Meiosis. Kalous J, Aleshkina D. Cells 12 187 (2023)
  22. Structural, enzymatic and spatiotemporal regulation of PP2A-B55 phosphatase in the control of mitosis. Lacroix B, Lorca T, Castro A. Front Cell Dev Biol 10 967909 (2022)
  23. The Centrosome and the Primary Cilium: The Yin and Yang of a Hybrid Organelle. Joukov V, De Nicolo A. Cells 8 (2019)
  24. The Hunt for Degrons of the 26S Proteasome. Ella H, Reiss Y, Ravid T. Biomolecules 9 (2019)
  25. The Nuclear Lamina: Protein Accumulation and Disease. Almendáriz-Palacios C, Gillespie ZE, Janzen M, Martinez V, Bridger JM, Harkness TAA, Mousseau DD, Eskiw CH. Biomedicines 8 (2020)

Articles citing this publication (78)

  1. Molecular basis of APC/C regulation by the spindle assembly checkpoint. Alfieri C, Chang L, Zhang Z, Yang J, Maslen S, Skehel M, Barford D. Nature 536 431-436 (2016)
  2. Cryo-EM of Mitotic Checkpoint Complex-Bound APC/C Reveals Reciprocal and Conformational Regulation of Ubiquitin Ligation. Yamaguchi M, VanderLinden R, Weissmann F, Qiao R, Dube P, Brown NG, Haselbach D, Zhang W, Sidhu SS, Peters JM, Stark H, Schulman BA. Mol. Cell 63 593-607 (2016)
  3. The G2-to-M Transition Is Ensured by a Dual Mechanism that Protects Cyclin B from Degradation by Cdc20-Activated APC/C. Lara-Gonzalez P, Moyle MW, Budrewicz J, Mendoza-Lopez J, Oegema K, Desai A. Dev Cell 51 313-325.e10 (2019)
  4. APC/C Dysfunction Limits Excessive Cancer Chromosomal Instability. Sansregret L, Patterson JO, Dewhurst S, López-García C, Koch A, McGranahan N, Chao WCH, Barry DJ, Rowan A, Instrell R, Horswell S, Way M, Howell M, Singleton MR, Medema RH, Nurse P, Petronczki M, Swanton C. Cancer Discov 7 218-233 (2017)
  5. Distinct kinetics of serine and threonine dephosphorylation are essential for mitosis. Hein JB, Hertz EPT, Garvanska DH, Kruse T, Nilsson J. Nat. Cell Biol. 19 1433-1440 (2017)
  6. Molecular mechanism for the regulation of yeast separase by securin. Luo S, Tong L. Nature 542 255-259 (2017)
  7. Rottlerin inhibits cell growth and invasion via down-regulation of Cdc20 in glioma cells. Wang L, Hou Y, Yin X, Su J, Zhao Z, Ye X, Zhou X, Zhou L, Wang Z. Oncotarget 7 69770-69782 (2016)
  8. Calibrated mitotic oscillator drives motile ciliogenesis. Al Jord A, Shihavuddin A, Servignat d'Aout R, Faucourt M, Genovesio A, Karaiskou A, Sobczak-Thépot J, Spassky N, Meunier A. Science 358 803-806 (2017)
  9. Kinetochores accelerate or delay APC/C activation by directing Cdc20 to opposing fates. Kim T, Lara-Gonzalez P, Prevo B, Meitinger F, Cheerambathur DK, Oegema K, Desai A. Genes Dev. 31 1089-1094 (2017)
  10. The PP2AB56 phosphatase promotes the association of Cdc20 with APC/C in mitosis. Lee SJ, Rodriguez-Bravo V, Kim H, Datta S, Foley EA. J. Cell. Sci. 130 1760-1771 (2017)
  11. Cyclin B3 activates the Anaphase-Promoting Complex/Cyclosome in meiosis and mitosis. Garrido D, Bourouh M, Bonneil É, Thibault P, Swan A, Archambault V. PLoS Genet 16 e1009184 (2020)
  12. The mitotic checkpoint complex (MCC): looking back and forth after 15 years. Liu ST, Zhang H. AIMS Mol Sci 3 597-634 (2016)
  13. Bistable, Biphasic Regulation of PP2A-B55 Accounts for the Dynamics of Mitotic Substrate Phosphorylation. Kamenz J, Gelens L, Ferrell JE. Curr Biol 31 794-808.e6 (2021)
  14. EMBuilder: A Template Matching-based Automatic Model-building Program for High-resolution Cryo-Electron Microscopy Maps. Zhou N, Wang H, Wang J. Sci Rep 7 2664 (2017)
  15. Different Functionality of Cdc20 Binding Sites within the Mitotic Checkpoint Complex. Sewart K, Hauf S. Curr. Biol. 27 1213-1220 (2017)
  16. Dissecting ribosomal particles throughout the kingdoms of life using advanced hybrid mass spectrometry methods. van de Waterbeemd M, Tamara S, Fort KL, Damoc E, Franc V, Bieri P, Itten M, Makarov A, Ban N, Heck AJR. Nat Commun 9 2493 (2018)
  17. Gene expression and cell identity controlled by anaphase-promoting complex. Oh E, Mark KG, Mocciaro A, Watson ER, Prabu JR, Cha DD, Kampmann M, Gamarra N, Zhou CY, Rape M. Nature 579 136-140 (2020)
  18. Polyubiquitylation of α-tubulin at K304 is required for flagellar disassembly in Chlamydomonas. Wang Q, Peng Z, Long H, Deng X, Huang K. J Cell Sci 132 (2019)
  19. Structural basis of human separase regulation by securin and CDK1-cyclin B1. Yu J, Raia P, Ghent CM, Raisch T, Sadian Y, Cavadini S, Sabale PM, Barford D, Raunser S, Morgan DO, Boland A. Nature 596 138-142 (2021)
  20. Sumoylation promotes optimal APC/C Activation and Timely Anaphase. Lee CC, Li B, Yu H, Matunis MJ. Elife 7 (2018)
  21. Cyclin B1-Cdk1 facilitates MAD1 release from the nuclear pore to ensure a robust spindle checkpoint. Jackman M, Marcozzi C, Barbiero M, Pardo M, Yu L, Tyson AL, Choudhary JS, Pines J. J Cell Biol 219 (2020)
  22. APC/CCdh1 Enables Removal of Shugoshin-2 from the Arms of Bivalent Chromosomes by Moderating Cyclin-Dependent Kinase Activity. Rattani A, Ballesteros Mejia R, Roberts K, Roig MB, Godwin J, Hopkins M, Eguren M, Sanchez-Pulido L, Okaz E, Ogushi S, Wolna M, Metson J, Pendás AM, Malumbres M, Novák B, Herbert M, Nasmyth K. Curr. Biol. 27 1462-1476.e5 (2017)
  23. BubR1 Promotes Bub3-Dependent APC/C Inhibition during Spindle Assembly Checkpoint Signaling. Overlack K, Bange T, Weissmann F, Faesen AC, Maffini S, Primorac I, Müller F, Peters JM, Musacchio A. Curr. Biol. 27 2915-2927.e7 (2017)
  24. Cancer-derived UTX TPR mutations G137V and D336G impair interaction with MLL3/4 complexes and affect UTX subcellular localization. Kato H, Asamitsu K, Sun W, Kitajima S, Yoshizawa-Sugata N, Okamoto T, Masai H, Poellinger L. Oncogene 39 3322-3335 (2020)
  25. Cdk1 phosphorylation of Esp1/Separase functions with PP2A and Slk19 to regulate pericentric Cohesin and anaphase onset. Lianga N, Doré C, Kennedy EK, Yeh E, Williams EC, Fortinez CM, Wang A, Bloom KS, Rudner AD. PLoS Genet. 14 e1007029 (2018)
  26. Cell division: Mitotic regulation comes into focus. Morgan DO. Nature 536 407-408 (2016)
  27. Comprehensive Discovery of Cell-Cycle-Essential Pathways in Chlamydomonas reinhardtii. Breker M, Lieberman K, Cross FR. Plant Cell 30 1178-1198 (2018)
  28. Global gene expression analysis combined with a genomics approach for the identification of signal transduction networks involved in postnatal mouse myocardial proliferation and development. Wang R, Su C, Wang X, Fu Q, Gao X, Zhang C, Yang J, Yang X, Wei M. Int. J. Mol. Med. 41 311-321 (2018)
  29. Kinetochore-catalyzed MCC formation: A structural perspective. Fischer ES. IUBMB Life 75 289-310 (2023)
  30. SUMO targets the APC/C to regulate transition from metaphase to anaphase. Eifler K, Cuijpers SAG, Willemstein E, Raaijmakers JA, El Atmioui D, Ovaa H, Medema RH, Vertegaal ACO. Nat Commun 9 1119 (2018)
  31. Tank Binding Kinase 1 modulates spindle assembly checkpoint components to regulate mitosis in breast and lung cancer cells. Maan M, Agrawal NJ, Padmanabhan J, Leitzinger CC, Rivera-Rivera Y, Saavedra HI, Chellappan SP. Biochim Biophys Acta Mol Cell Res 1868 118929 (2021)
  32. USP11 deubiquitinates RAE1 and plays a key role in bipolar spindle formation. Stockum A, Snijders AP, Maertens GN. PLoS ONE 13 e0190513 (2018)
  33. A cell based, high throughput assay for quantitative analysis of Hedgehog pathway activation using a Smoothened activation sensor. Albert EA, Bökel C. Sci Rep 7 14341 (2017)
  34. A proteomics approach for the identification of cullin-9 (CUL9) related signaling pathways in induced pluripotent stem cell models. Ortolano NA, Romero-Morales AI, Rasmussen ML, Bodnya C, Kline LA, Joshi P, Connelly JP, Rose KL, Pruett-Miller SM, Gama V. PLoS One 16 e0248000 (2021)
  35. A unique binding mode of Nek2A to the APC/C allows its ubiquitination during prometaphase. Alfieri C, Tischer T, Barford D. EMBO Rep 21 e49831 (2020)
  36. APC/CFZR-1 Controls SAS-5 Levels To Regulate Centrosome Duplication in Caenorhabditis elegans. Medley JC, DeMeyer LE, Kabara MM, Song MH. G3 (Bethesda) 7 3937-3946 (2017)
  37. CDC20 and PTTG1 are Important Biomarkers and Potential Therapeutic Targets for Metastatic Prostate Cancer. Dai L, Song ZX, Wei DP, Zhang JD, Liang JQ, Wang BB, Ma WT, Li LY, Dang YL, Zhao L, Zhang LM, Zhao YM. Adv Ther 38 2973-2989 (2021)
  38. Cell Cycle Control by Nuclear Sequestration of CDC20 and CDH1 mRNA in Plant Stem Cells. Yang W, Wightman R, Meyerowitz EM. Mol. Cell 68 1108-1119.e3 (2017)
  39. Delayed APC/C activation extends the first mitosis of mouse embryos. Ajduk A, Strauss B, Pines J, Zernicka-Goetz M. Sci Rep 7 9682 (2017)
  40. Dynamic regulation of mitotic ubiquitin ligase APC/C by coordinated Plx1 kinase and PP2A phosphatase action on a flexible Apc1 loop. Fujimitsu K, Yamano H. EMBO J 40 e107516 (2021)
  41. Molecular mechanisms of APC/C release from spindle assembly checkpoint inhibition by APC/C SUMOylation. Yatskevich S, Kroonen JS, Alfieri C, Tischer T, Howes AC, Clijsters L, Yang J, Zhang Z, Yan K, Vertegaal ACO, Barford D. Cell Rep 34 108929 (2021)
  42. Network mechanisms and dysfunction within an integrated computational model of progression through mitosis in the human cell cycle. Terhune SS, Jung Y, Cataldo KM, Dash RK. PLoS Comput Biol 16 e1007733 (2020)
  43. Ordered dephosphorylation initiated by the selective proteolysis of cyclin B drives mitotic exit. Holder J, Mohammed S, Barr FA. Elife 9 (2020)
  44. PP1 promotes cyclin B destruction and the metaphase-anaphase transition by dephosphorylating CDC20. Bancroft J, Holder J, Geraghty Z, Alfonso-Pérez T, Murphy D, Barr FA, Gruneberg U. Mol Biol Cell 31 2315-2330 (2020)
  45. Paradoxical mitotic exit induced by a small molecule inhibitor of APC/CCdc20. Richeson KV, Bodrug T, Sackton KL, Yamaguchi M, Paulo JA, Gygi SP, Schulman BA, Brown NG, King RW. Nat Chem Biol 16 546-555 (2020)
  46. Reconstitution and use of highly active human CDK1:Cyclin-B:CKS1 complexes. Huis In 't Veld PJ, Wohlgemuth S, Koerner C, Müller F, Janning P, Musacchio A. Protein Sci 31 528-537 (2022)
  47. Ubiquitin chain-elongating enzyme UBE2S activates the RING E3 ligase APC/C for substrate priming. Martinez-Chacin RC, Bodrug T, Bolhuis DL, Kedziora KM, Bonacci T, Ordureau A, Gibbs ME, Weissmann F, Qiao R, Grant GD, Cook JG, Peters JM, Wade Harper J, Emanuele MJ, Brown NG. Nat Struct Mol Biol 27 550-560 (2020)
  48. APC7 mediates ubiquitin signaling in constitutive heterochromatin in the developing mammalian brain. Ferguson CJ, Urso O, Bodrug T, Gassaway BM, Watson ER, Prabu JR, Lara-Gonzalez P, Martinez-Chacin RC, Wu DY, Brigatti KW, Puffenberger EG, Taylor CM, Haas-Givler B, Jinks RN, Strauss KA, Desai A, Gabel HW, Gygi SP, Schulman BA, Brown NG, Bonni A. Mol Cell 82 90-105.e13 (2022)
  49. Alternative CDC20 translational isoforms tune mitotic arrest duration. Tsang MJ, Cheeseman IM. Nature 617 154-161 (2023)
  50. Boolean model of growth signaling, cell cycle and apoptosis predicts the molecular mechanism of aberrant cell cycle progression driven by hyperactive PI3K. Sizek H, Hamel A, Deritei D, Campbell S, Ravasz Regan E. PLoS Comput. Biol. 15 e1006402 (2019)
  51. Calcineurin promotes APC/C activation at meiotic exit by acting on both XErp1 and Cdc20. Heim A, Tischer T, Mayer TU. EMBO Rep. 19 (2018)
  52. Comparative analysis of transcriptomes revealed the molecular mechanism of development of Tricholoma matsutake at different stages of fruiting bodies. Tang X, Ding X, Hou YL. Food Sci Biotechnol 29 939-951 (2020)
  53. Control of division in Chlamydomonas by cyclin B/CDKB1 and the anaphase-promoting complex. Pecani K, Lieberman K, Tajima-Shirasaki N, Onishi M, Cross FR. PLoS Genet 18 e1009997 (2022)
  54. Cyclin A2 degradation during the spindle assembly checkpoint requires multiple binding modes to the APC/C. Zhang S, Tischer T, Barford D. Nat Commun 10 3863 (2019)
  55. Deficiency of GPI Glycan Modification by Ethanolamine Phosphate Results in Increased Adhesion and Immune Resistance of Aspergillus fumigatus. Ouyang H, Zhang Y, Zhou H, Ma Y, Li R, Yang J, Wang X, Jin C. Front Cell Infect Microbiol 11 780959 (2021)
  56. Hematopoietic PBX-interacting protein is a substrate and an inhibitor of the APC/C-Cdc20 complex and regulates mitosis by stabilizing cyclin B1. Khumukcham SS, Samanthapudi VSK, Penugurti V, Kumari A, Kesavan PS, Velatooru LR, Kotla SR, Mazumder A, Manavathi B. J Biol Chem 294 10236-10252 (2019)
  57. High levels of histones promote whole-genome-duplications and trigger a Swe1WEE1-dependent phosphorylation of Cdc28CDK1. Maya Miles D, Peñate X, Sanmartín Olmo T, Jourquin F, Muñoz Centeno MC, Mendoza M, Simon MN, Chavez S, Geli V. Elife 7 (2018)
  58. Identification of novel microtubule inhibitors effective in fission yeast and human cells and their effects on breast cancer cell lines. Morishita J, Nurse P. Open Biol 11 210161 (2021)
  59. Identification, characterization and expression profiles of E2 and E3 gene superfamilies during the development of tetrasporophytes in Gracilariopsis lemaneiformis (Rhodophyta). Wu Q, Yin J, Jiang M, Zhang J, Sui Z. BMC Genomics 24 549 (2023)
  60. Mitotic Exit Dysfunction through the Deregulation of APC/C Characterizes Cisplatin-Resistant State in Epithelial Ovarian Cancer. Belur Nagaraj A, Kovalenko O, Avelar R, Joseph P, Brown A, Surti A, Mantilla S, DiFeo A. Clin. Cancer Res. 24 4588-4601 (2018)
  61. Noisy Cell-Size-Correlated Expression of Cyclin B Drives Probabilistic Cell-Size Homeostasis in Fission Yeast. Patterson JO, Rees P, Nurse P. Curr. Biol. 29 1379-1386.e4 (2019)
  62. PP2A-B56 binds to Apc1 and promotes Cdc20 association with the APC/C ubiquitin ligase in mitosis. Fujimitsu K, Yamano H. EMBO Rep. 21 e48503 (2020)
  63. Peptide inhibitors of the anaphase promoting-complex that cause sensitivity to microtubule poison. Schuyler SC, Wu YO, Chen HY, Ding YS, Lin CJ, Chu YT, Chen TC, Liao L, Tsai WW, Huang A, Wang LI, Liao TW, Jhuo JH, Cheng V. PLoS ONE 13 e0198930 (2018)
  64. Polyanions provide selective control of APC/C interactions with the activator subunit. Mizrak A, Morgan DO. Nat Commun 10 5807 (2019)
  65. Real-Time Monitoring of APC /C-Mediated Substrate Degradation Using Xenopus laevis Egg Extracts. Kamenz J, Qiao R, Yang Q, Ferrell JE. Methods Mol Biol 2329 29-38 (2021)
  66. Recovery from spindle checkpoint-mediated arrest requires a novel Dnt1-dependent APC/C activation mechanism. Bai S, Sun L, Wang X, Wang SM, Luo ZQ, Wang Y, Jin QW. PLoS Genet 18 e1010397 (2022)
  67. Regulation of OLC1 protein expression by the anaphase-promoting complex. Zhang X, Chen W, Yin N, Dong L, Fu M, Zhan Q, Tong T. Oncol Lett 17 2639-2646 (2019)
  68. Role of phosphorylation of Cdc20 in the regulation of the action of APC/C in mitosis. Shevah-Sitry D, Miniowitz-Shemtov S, Teichner A, Kaisari S, Hershko A. Proc Natl Acad Sci U S A 119 e2210367119 (2022)
  69. Short-term starvation stress at young adult stages enhances meiotic activity of germ cells to maintain spermatogenesis in aged male Caenorhabditis elegans. Chou WY, Lin YC, Lee YH. Aging Cell 18 e12930 (2019)
  70. Single-molecule analysis of specificity and multivalency in binding of short linear substrate motifs to the APC/C. Hartooni N, Sung J, Jain A, Morgan DO. Nat Commun 13 341 (2022)
  71. Spatiotemporal control of mitotic exit during anaphase by an aurora B-Cdk1 crosstalk. Afonso O, Castellani CM, Cheeseman LP, Ferreira JG, Orr B, Ferreira LT, Chambers JJ, Morais-de-Sá E, Maresca TJ, Maiato H. Elife 8 (2019)
  72. Structural and functional insight into the effect of AFF4 dimerization on activation of HIV-1 proviral transcription. Tang D, Chen C, Liao G, Liu J, Liao B, Huang Q, Chen Q, Zhao J, Jiang H, Duan J, Huang J, Wang K, Wang J, Zhou C, Chu W, Li W, Sun B, Li Z, Dai L, Fu X, Cheng W, Xue Y, Qi S. Cell Discov 6 7 (2020)
  73. Taming the Beast: Control of APC/CCdc20-Dependent Destruction. Lara-Gonzalez P, Kim T, Desai A. Cold Spring Harb. Symp. Quant. Biol. 82 111-121 (2017)
  74. The APC/C targets the Cep152-Cep63 complex at the centrosome to regulate mitotic spindle assembly. Tischer T, Yang J, Barford D. J Cell Sci 135 jcs259273 (2022)
  75. The RepID-CRL4 ubiquitin ligase complex regulates metaphase to anaphase transition via BUB3 degradation. Jang SM, Nathans JF, Fu H, Redon CE, Jenkins LM, Thakur BL, Pongor LS, Baris AM, Gross JM, OʹNeill MJ, Indig FE, Cappell SD, Aladjem MI. Nat Commun 11 24 (2020)
  76. The spindle assembly checkpoint and the spatial activation of Polo kinase determine the duration of cell division and prevent tumor formation. Gallaud E, Richard-Parpaillon L, Bataillé L, Pascal A, Métivier M, Archambault V, Giet R. PLoS Genet 18 e1010145 (2022)
  77. Transcriptome sequencing and screening of genes related to glucose availability in Schizosaccharomyces pombe by RNA-seq analysis. Tarhan Ç, Çakır Ö. Genet Mol Biol 44 e20200245 (2021)
  78. USP39-mediated deubiquitination of Cyclin B1 promotes tumor cell proliferation and glioma progression. Xiao Y, Chen X, Hu W, Ma W, Di Q, Tang H, Zhao X, Huang G, Chen W. Transl Oncol 34 101713 (2023)


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