Dephosphorylation of F-BAR Protein Cdc15 Modulates Its Conformation and Stimulates Its Scaffolding Activity at the Cell Division Site

Molecular Cell

Volumn 39, Issue 1, 2010, Pages 86-99

  Roberts Galbraith, Rachel H ^a   Ohi, Melanie D ^a   Ballif, Bryan A ^b   Chen, Jun Song ^a   McLeod, Ian ^c   McDonald, W Hayes ^c   Gygi, Steven P ^b   Yates, John R ^c   Gould, Kathleen L ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cellcycle

Indexed keywords

PROTEIN CDC15; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; INTERPHASE; MITOSIS; NONHUMAN; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SCHIZOSACCHAROMYCES POMBE;

ALANINE; CELL CYCLE PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; GTP-BINDING PROTEINS; MODELS, BIOLOGICAL; MUTANT PROTEINS; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

SCHIZOSACCHAROMYCES POMBE;

EID: 77954261508     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.06.012     Document Type: Article

References (60)

1. Albuquerque C.P., Smolka M.B., Payne S.H., Bafna V., Eng J., Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell. Proteomics 2008, 7:1389-1396.
2. Bähler J., Wu J.Q., Longtine M.S., Shah N.G., McKenzie A., Steever A.B., Wach A., Philippsen P., Pringle J.R. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 1998, 14:943-951.
3. Balasubramanian M.K., Bi E., Glotzer M. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 2004, 14:R806-R818.
4. Bauerfeind R., Takei K., De Camilli P. Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 1997, 272:30984-30992.
5. Carnahan R.H., Gould K.L. The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J. Cell Biol. 2003, 162:851-862.
6. Chang F., Drubin D., Nurse P. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 1997, 137:169-182.
7. Chi A., Huttenhower C., Geer L.Y., Coon J.J., Syka J.E., Bai D.L., Shabanowitz J., Burke D.J., Troyanskaya O.G., Hunt D.F. Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc. Natl. Acad. Sci. USA 2007, 104:2193-2198.
8. Chitu V., Stanley E.R. Pombe Cdc15 homology (PCH) proteins: coordinators of membrane-cytoskeletal interactions. Trends Cell Biol. 2007, 17:145-156.
9. Clifford D.M., Wolfe B.A., Roberts-Galbraith R.H., McDonald W.H., Yates J.R., Gould K.L. The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J. Cell Biol. 2008, 181:79-88.
10. Dosztányi Z., Csizmok V., Tompa P., Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 2005, 21:3433-3434.
11. Fankhauser C., Reymond A., Cerutti L., Utzig S., Hofmann K., Simanis V. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 1995, 82:435-444.
12. Floyd S.R., Porro E.B., Slepnev V.I., Ochoa G.C., Tsai L.H., De Camilli P. Amphiphysin 1 binds the cyclin-dependent kinase (cdk) 5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 2001, 276:8104-8110.
13. Frost A., Perera R., Roux A., Spasov K., Destaing O., Egelman E.H., De Camilli P., Unger V.M. Structural basis of membrane invagination by F-BAR domains. Cell 2008, 132:807-817.
14. Fujiwara T., Bandi M., Nitta M., Ivanova E.V., Bronson R.T., Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005, 437:1043-1047.
15. Gould K.L., Moreno S., Owen D.J., Sazer S., Nurse P. Phosphorylation at Thr167 is required for Schizosaccharomyces pombe p34cdc2 function. EMBO J. 1991, 10:3297-3309.
16. Gray C.H., Good V.M., Tonks N.K., Barford D. The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase. EMBO J. 2003, 22:3524-3535.
17. Gsponer J., Futschik M.E., Teichmann S.A., Babu M.M. Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 2008, 322:1365-1368.
18. Hachet O., Simanis V. Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev. 2008, 22:3205-3216.
19. Halbach A., Mörgelin M., Baumgarten M., Milbrandt M., Paulsson M., Plomann M. PACSIN 1 forms tetramers via its N-terminal F-BAR domain. FEBS J. 2007, 274:773-782.
20. Huang Y., Yan H., Balasubramanian M.K. Assembly of normal actomyosin rings in the absence of Mid1p and cortical nodes in fission yeast. J. Cell Biol. 2008, 183:979-988.
21. Huckaba T.M., Gay A.C., Pantalena L.F., Yang H.C., Pon L.A. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 2004, 167:519-530.
22. Itoh T., Erdmann K.S., Roux A., Habermann B., Werner H., De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 2005, 9:791-804.
23. Keeney J.B., Boeke J.D. Efficient targeted integration at leu1-32 and ura4-294 in Schizosaccharomyces pombe. Genetics 1994, 136:849-856.
24. Larocca M.C., Shanks R.A., Tian L., Nelson D.L., Stewart D.M., Goldenring J.R. AKAP350 interaction with cdc42 interacting protein 4 at the Golgi apparatus. Mol. Biol. Cell 2004, 15:2771-2781.
25. Lee J., Colwill K., Aneliunas V., Tennyson C., Moore L., Ho Y., Andrews B. Interaction of yeast Rvs167 and Pho85 cyclin-dependent kinase complexes may link the cell cycle to the actin cytoskeleton. Curr. Biol. 1998, 8:1310-1321.
26. Li X., Gerber S.A., Rudner A.D., Beausoleil S.A., Haas W., Villén J., Elias J.E., Gygi S.P. Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae. J. Proteome Res. 2007, 6:1190-1197.
27. Lippincott J., Li R. Involvement of PCH family proteins in cytokinesis and actin distribution. Microsc. Res. Tech. 2000, 49:168-172.
28. Montagnac G., Echard A., Chavrier P. Endocytic traffic in animal cell cytokinesis. Curr. Opin. Cell Biol. 2008, 20:454-461.
29. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991, 194:795-823.
30. Moses A.M., Hériché J.K., Durbin R. Clustering of phosphorylation site recognition motifs can be exploited to predict the targets of cyclin-dependent kinase. Genome Biol. 2007, 8:R23.
31. Motegi F., Mishra M., Balasubramanian M.K., Mabuchi I. Myosin-II reorganization during mitosis is controlled temporally by its dephosphorylation and spatially by Mid1 in fission yeast. J. Cell Biol. 2004, 165:685-695.
32. Mulvihill D.P., Barretto C., Hyams J.S. Localization of fission yeast type II myosin, Myo2, to the cytokinetic actin ring is regulated by phosphorylation of a C-terminal coiled-coil domain and requires a functional septation initiation network. Mol. Biol. Cell 2001, 12:4044-4053.
33. Ohi M., Li Y., Cheng Y., Walz T. Negative staining and image classification - powerful tools in modern electron microscopy. Biol. Proced. Online 2004, 6:23-34.
34. Pelham R.J., Chang F. Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nat. Cell Biol. 2001, 3:235-244.
35. Pinar M., Coll P.M., Rincon S.A., Pérez P. Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol. Biol. Cell 2008, 19:1727-1738.
36. Plomann M., Lange R., Vopper G., Cremer H., Heinlein U.A., Scheff S., Baldwin S.A., Leitges M., Cramer M., Paulsson M., Barthels D. PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells. Eur. J. Biochem. 1998, 256:201-211.
37. Ren G., Vajjhala P., Lee J.S., Winsor B., Munn A.L. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 2006, 70:37-120.
38. Riedl J., Crevenna A.H., Kessenbrock K., Yu J.H., Neukirchen D., Bista M., Bradke F., Jenne D., Holak T.A., Werb Z., et al. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 2008, 5:605-607.
39. Roberts-Galbraith R.H., Gould K.L. Stepping into the ring: the SIN takes on contractile ring assembly. Genes Dev. 2008, 22:3082-3088.
40. Roberts-Galbraith R.H., Chen J.S., Wang J., Gould K.L. The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 2009, 184:113-127.
41. Schmidt S., Sohrmann M., Hofmann K., Woollard A., Simanis V. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes Dev. 1997, 11:1519-1534.
42. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 2000, 78:1606-1619.
43. Shimada A., Niwa H., Tsujita K., Suetsugu S., Nitta K., Hanawa-Suetsugu K., Akasaka R., Nishino Y., Toyama M., Chen L., et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 2007, 129:761-772.
44. Smolka M.B., Albuquerque C.P., Chen S.H., Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. USA 2007, 104:10364-10369.
45. Spencer S., Dowbenko D., Cheng J., Li W., Brush J., Utzig S., Simanis V., Lasky L.A. PSTPIP: a tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 1997, 138:845-860.
46. Takeda T., Kawate T., Chang F. Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 2004, 6:1142-1144.
47. Tasto J.J., Carnahan R.H., McDonald W.H., Gould K.L. Vectors and gene targeting modules for tandem affinity purification in Schizosaccharomyces pombe. Yeast 2001, 18:657-662.
48. Tsujita K., Suetsugu S., Sasaki N., Furutani M., Oikawa T., Takenawa T. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 2006, 172:269-279.
49. Vallen E.A., Caviston J., Bi E. Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell 2000, 11:593-611.
50. Vavylonis D., Wu J.Q., Hao S., O'Shaughnessy B., Pollard T.D. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 2008, 319:97-100.
51. Wachtler V., Huang Y., Karagiannis J., Balasubramanian M.K. Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. Mol. Biol. Cell 2006, 17:3254-3266.
52. Wang Q., Navarro M.V., Peng G., Molinelli E., Goh S.L., Judson B.L., Rajashankar K.R., Sondermann H. Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc. Natl. Acad. Sci. USA 2009, 106:12700-12705.
53. Wolfe B.A., Gould K.L. Split decisions: coordinating cytokinesis in yeast. Trends Cell Biol. 2005, 15:10-18.
54. Wu J.Q., Pollard T.D. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005, 310:310-314.
55. Wu Y., Spencer S.D., Lasky L.A. Tyrosine phosphorylation regulates the SH3-mediated binding of the Wiskott-Aldrich syndrome protein to PSTPIP, a cytoskeletal-associated protein. J. Biol. Chem. 1998, 273:5765-5770.
56. Wu J.Q., Kuhn J.R., Kovar D.R., Pollard T.D. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 2003, 5:723-734.
57. Wu X., Gan B., Yoo Y., Guan J.L. FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell 2005, 9:185-196.
58. Wu J.Q., Sirotkin V., Kovar D.R., Lord M., Beltzner C.C., Kuhn J.R., Pollard T.D. Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 2006, 174:391-402.
59. Yaffe M.B., Rittinger K., Volinia S., Caron P.R., Aitken A., Leffers H., Gamblin S.J., Smerdon S.J., Cantley L.C. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 1997, 91:961-971.
60. Yonetani A., Lustig R.J., Moseley J.B., Takeda T., Goode B.L., Chang F. Regulation and targeting of the fission yeast formin cdc12p in cytokinesis. Mol. Biol. Cell 2008, 19:2208-2219.