ULK3 regulates cytokinetic abscission by phosphorylating ESCRT-III proteins

eLife

Volumn 4, Issue MAY, 2015, Pages 1-70

  Caballe, Anna ^a   Wenzel, Dawn M ^b   Agromayor, Monica ^a   Alam, Steven L ^b   Skalicky, Jack J ^b   Kloc, Magdalena ^a   Carlton, Jeremy G ^a   Labrador, Leticia ^a   Sundquist, Wesley I ^b   Martin Serrano, Juan ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA KINASE INHIBITOR; BETA GALACTOSIDASE; BIOTIN; ESCRT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NUCLEOPORIN; PEPTIDES AND PROTEINS; SMALL INTERFERING RNA; TUBULIN; UNC 51 LIKE KINASE 3; UNCLASSIFIED DRUG; VIRUS PROTEIN; OLC1 PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SNF7-3 PROTEIN, HUMAN; ULK3 PROTEIN, HUMAN;

ABSCISSION; ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; CRYSTALLIZATION; CYTOKINETIC ABSCISSION; DOWN REGULATION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE POLARIZATION; GENE MUTATION; GENE SEQUENCE; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; ION EXCHANGE CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR PORE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA EDITING; WESTERN BLOTTING; CELL LINE; CYTOKINESIS; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING;

CELL LINE; CYTOKINESIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES;

EID: 84930631701     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06547     Document Type: Article

References (63)

1. Caballe, A. & Martin-Serrano, J. ESCRT machinery and cytokinesis: the road to daughter cell separation. Traffic 12, 1318-26 (2011).
2. Mierzwa, B. & Gerlich, D.W. Cytokinetic Abscission: Molecular Mechanisms and Temporal Control. Developmental cell 31, 525-538 (2014).
3. Carlton, J.G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-12 (2007).
4. Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. Embo J 26, 4215-27 (2007).
5. Henne, W.M., Buchkovich, N.J. & Emr, S.D. The ESCRT pathway. Developmental cell 21, 77-91 (2011).
6. McCullough, J., Colf, L.A. & Sundquist, W.I. Membrane Fission Reactions of the Mammalian ESCRT Pathway. Annual review of biochemistry 82, 663-92 (2013).
7. Hurley, J.H. & Yang, D. MIT domainia. Dev Cell 14, 6-8 (2008).
8. Jimenez, A.J. et al. ESCRT machinery is required for plasma membrane repair. Science 343, 1247136 (2014).
9. Carlton, J.G., Agromayor, M. & Martin-Serrano, J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci U S A 105, 10541-6 (2008).
10. Guizetti, J. et al. Cortical Constriction During Abscission Involves Helices of ESCRT-III-Dependent Filaments. Science (2011).
11. Elia, N., Sougrat, R., Spurlin, T.A., Hurley, J.H. & Lippincott-Schwartz, J. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A (2011).
12. Babst, M., Wendland, B., Estepa, E.J. & Emr, S.D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. The EMBO journal 17, 2982-93 (1998).
13. Lata, S. et al. Helical structures of ESCRT-III are disassembled by VPS4. Science 321, 1354-7 (2008).
14. Yang, D. et al. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15, 1278-86 (2008).
15. Connell, J.W., Lindon, C., Luzio, J.P. & Reid, E. Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 10, 42-56 (2009).
16. Skalicky, J.J. et al. Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. The Journal of biological chemistry 287, 43910-26 (2012).
17. Hadders, M.A. et al. ESCRT-III binding protein MITD1 is involved in cytokinesis and has an unanticipated PLD fold that binds membranes. Proceedings of the National Academy of Sciences of the United States of America 109, 17424-9 (2012).
18. Azmi, I. et al. Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. The Journal of cell biology 172, 705-17 (2006).
19. Agromayor, M. & Martin-Serrano, J. Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends in cell biology (2013).
20. Steigemann, P. et al. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-84 (2009).
21. Norden, C. et al. The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125, 85-98 (2006).
22. Mendoza, M. et al. A mechanism for chromosome segregation sensing by the NoCut checkpoint. Nat Cell Biol 11, 477-83 (2009).
23. Carlton, J.G., Caballe, A., Agromayor, M., Kloc, M. & Martin-Serrano, J. ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336, 220-5 (2012).
24. Capalbo, L. et al. The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis. Open biology 2, 120070 (2012).
25. Mackay, D.R., Makise, M. & Ullman, K.S. Defects in nuclear pore assembly lead to activation of an Aurora B-mediated abscission checkpoint. J Cell Biol 191, 923-31 (2010).
26. Webster, B.M., Colombi, P., Jager, J. & Lusk, C.P. Surveillance of Nuclear Pore Complex Assembly by ESCRT-III/Vps4. Cell 159, 388-401 (2014).
27. Lafaurie-Janvore, J. et al. ESCRT-III assembly and cytokinetic abscission are induced by tension release in the intercellular bridge. Science 339, 1625-9 (2013).
28. Row, P.E. et al. The MIT domain of UBPY constitutes a CHMP binding and endosomal localization signal required for efficient epidermal growth factor receptor degradation. J Biol Chem 282, 30929-37 (2007).
29. Bajorek, M. et al. Biochemical analyses of human IST1 and its function in cytokinesis. Mol Biol Cell 20, 1360-73 (2009).
30. Agromayor, M. et al. Essential role of hIST1 in cytokinesis. Mol Biol Cell 20, 1374- 87 (2009).
31. Roux, K.J., Kim, D.I., Raida, M. & Burke, B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. The Journal of cell biology 196, 801-10 (2012).
32. Stuchell-Brereton, M.D. et al. ESCRT-III recognition by VPS4 ATPases. Nature 449, 740-4 (2007).
33. Obita, T. et al. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-9 (2007).
34. Guo, E.Z. & Xu, Z. Distinct Mechanisms of Recognizing Endosomal Sorting Complex Required for Transport III (ESCRT-III) Protein IST1 by Different Microtubule Interacting and Trafficking (MIT) Domains. The Journal of biological chemistry 290, 8396-408 (2015).
35. Hewitt, E.W. et al. Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. The EMBO journal 21, 2418-29 (2002).
36. Agromayor, M. et al. The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain. Structure 20, 414-28 (2012).
37. Ran, F.A. et al. Genome engineering using the CRISPR-Cas9 system. Nature protocols 8, 2281-308 (2013).
38. Chan, E.Y., Longatti, A., McKnight, N.C. & Tooze, S.A. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13- independent mechanism. Molecular and cellular biology 29, 157-71 (2009).
39. Jouvenet, N., Zhadina, M., Bieniasz, P.D. & Simon, S.M. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat Cell Biol 13, 394-401 (2011).
40. Maloverjan, A., Piirsoo, M., Michelson, P., Kogerman, P. & Osterlund, T. Identification of a novel serine/threonine kinase ULK3 as a positive regulator of Hedgehog pathway. Experimental cell research 316, 627-37 (2010).
41. Bajorek, M. et al. Structural basis for ESCRT-III protein autoinhibition. Nat Struct Mol Biol 16, 754-62 (2009).
42. Muziol, T. et al. Structural basis for budding by the ESCRT-III factor CHMP3. Developmental cell 10, 821-30 (2006).
43. Hendzel, M.J. et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348- 60 (1997).
44. Ditchfield, C. et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. The Journal of cell biology 161, 267-80 (2003).
45. McCullough, J., Fisher, R.D., Whitby, F.G., Sundquist, W.I. & Hill, C.P. ALIX- CHMP4 interactions in the human ESCRT pathway. Proc Natl Acad Sci U S A 105, 7687-91 (2008).
46. Thoresen, S.B. et al. ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nature cell biology 16, 550-60 (2014).
47. Dimaano, C., Jones, C.B., Hanono, A., Curtiss, M. & Babst, M. Ist1 regulates Vps4 localization and assembly. Molecular biology of the cell 19, 465-74 (2008).
48. Pharoah, P.D. et al. GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer. Nature genetics 45, 362-70, 370e1-2 (2013).
49. Sanjana, N.E., Shalem, O. & Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nature methods 11, 783-4 (2014).
50. Studier, F.W. Protein production by auto-induction in high density shaking cultures. Protein expression and purification 41, 207-34 (2005).
51. Goddard, T.D., and Kneller, D. G. . SPARKY 3. (University of California, San Francisco, 2001).
52. Zimmerman, D.E. et al. Automated analysis of protein NMR assignments using methods from artificial intelligence. Journal of molecular biology 269, 592-610 (1997).
53. Cavanagh, J.F., W. J.; Palmer, A. G.; 3rd, Rance, M.; Skelton, N. J. . Protein NMR Spectroscopy: Principles and Practice, (Elsevier Academic Press, San Diego, 2007).
54. Soltis, S.M. et al. New paradigm for macromolecular crystallography experiments at SSRL: automated crystal screening and remote data collection. Acta crystallographica. Section D, Biological crystallography 64, 1210-21 (2008).
55. Kabsch, W. Xds. Acta crystallographica. Section D, Biological crystallography 66, 125-32 (2010).
56. Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta crystallographica. Section D, Biological crystallography 66, 133-44 (2010).
57. Gonzalez , A., and Tsai, Y. http://smb.slac.stanford.edu/facilities/software/xds/ -autoxds script. (2010)
58. Afonine, P.V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta crystallographica. Section D, Biological crystallography 68, 352- 67 (2012)
59. Ciccarelli, F.D. et al. The identification of a conserved domain in both spartin and spastin, mutated in hereditary spastic paraplegia. Genomics 81, 437-41 (2003)
60. Jouvenet, N., Bieniasz, P.D. & Simon, S.M. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454, 236-40 (2008)
61. Hurley, J.H. & Hanson, P.I. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol 11, 556-66 (2010)
62. Pardieu, C. et al. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV 1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS pathogens 6, e1000843 (2010)
63. Pettersen, E.F. et al. UCSF Chimera--a visualization system for exploratory research and analysis. Journal of computational chemistry 25, 1605-12 (2004)