Targeting and functional mechanisms of the cytokinesis-related F-BAR protein Hof1 during the cell cycle

Molecular Biology of the Cell

Volumn 24, Issue 9, 2013, Pages 1305-1320

  Oh, Younghoon ^a   Schreiter, Jennifer ^a   Nishihama, Ryuichi ^b,d   Wloka, Carsten ^a,c   Bi, Erfei ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CDC10 PROTEIN; CHITIN SYNTHASE; CHS2 PROTEIN; F BAR PROTEIN; HOF1 PROTEIN; MEMBRANE PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN I; PLASMA PROTEIN; PROTEIN SH3; SEPTIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL DIVISION; CELL GROWTH; CELL POLARITY; COILED BODY; CONTROLLED STUDY; CYTOKINESIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ACTOMYOSIN; CELL CYCLE; CHITIN SYNTHASE; CYTOKINESIS; GTP PHOSPHOHYDROLASES; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MYOSIN HEAVY CHAINS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEPTINS; SRC HOMOLOGY DOMAINS; TIME-LAPSE IMAGING;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84877111824     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-11-0804     Document Type: Article

References (74)

1. Angers-Loustau A, Cote JF, Charest A, Dowbenko D, Spencer S, Lasky LA, Tremblay ML (1999). Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144, 1019-1031.
2. Ayscough KR, Stryker J, Pokala N, Sanders M, Crews P, Drubin DG (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 137, 399-416.
3. Balasubramanian MK, Bi E, Glotzer M (2004). Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr Biol 14, R806-818.
4. Barr FA, Gruneberg U (2007). Cytokinesis: placing and making the final cut. Cell 131, 847-860.
5. Bi E (2001). Cytokinesis in budding yeast: the relationship between actomyosin ring function and septum formation. Cell Struct Funct 26, 529-537.
6. Bi E, Maddox P, Lew DJ, Salmon ED, McMillan JN, Yeh E, Pringle JR (1998). Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J Cell Biol 142, 1301-1312.
7. Bi E, Pringle JR (1996). ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol Cell Biol 16, 5264-5275.
8. Blondel M, Bach S, Bamps S, Dobbelaere J, Wiget P, Longaretti C, Barral Y, Meijer L, Peter M (2005). Degradation of Hof1 by SCF(Grr1) is important for actomyosin contraction during cytokinesis in yeast. EMBO J 24, 1440-1452.
9. Boyne JR, Yosuf HM, Bieganowski P, Brenner C, Price C (2000). Yeast myosin light chain, Mlc1p, interacts with both IQGAP and class II myosin to effect cytokinesis. J Cell Sci 113, 4533-4543.
10. Carnahan RH, Gould KL (2003). The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J Cell Biol 162, 851-862.
11. Chin CF, Bennett AM, Ma WK, Hall MC, Yeong FM (2011). Dependence of Chs2 ER export on dephosphorylation by cytoplasmic Cdc14 ensures that septum formation follows mitosis. Mol Biol Cell 23, 45-58.
12. Chuang JS, Schekman RW (1996). Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J Cell Biol 135, 597-610.
13. Dobbelaere J, Barral Y (2004). Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305, 393-396.
14. Epp JA, Chant J (1997). An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr Biol 7, 921-929.
15. Fang X, Luo J, Nishihama R, Wloka C, Dravis C, Travaglia M, Iwase M, Vallen EA, Bi E (2010). Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin-II. J Cell Biol 191, 1333-1350.
16. Ford RA, Shaw JA, Cabib E (1996). Yeast chitin synthases 1 and 2 consist of a non-homologous and dispensable N-terminal region and of a homologous moiety essential for function. Mol Gen Genet 252, 420-428.
17. Frazier JA, Wong ML, Longtine MS, Pringle JR, Mann M, Mitchison TJ, Field C (1998). Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J Cell Biol 143, 737-749.
18. Gao XD, Sperber LM, Kane SA, Tong Z, Hin Yan Tong A, Boone C, Bi E (2007). Sequential and distinct roles of the cadherin domain-containing protein Axl2p in cell polarization in yeast cell cycle. Mol Biol Cell 18, 2542-2560.
19. Garcia G 3rd, Bertin A, Li Z, Song Y, McMurray MA, Thorner J, Nogales E (2011). Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J Cell Biol 195, 993-1004.
20. Gladfelter AS, Pringle JR, Lew DJ (2001). The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol 4, 681-689.
21. Guthrie C, Fink GR (1991). Guide to Yeast Genetics and Molecular Biology, San Diego, CA: Academic Press.
22. Hartwell LH (1971). Genetic control of the cell division cycle in yeast. I V. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69, 265-276.
23. Heath RJ, Insall RH (2008). F-BAR domains: multifunctional regulators of membrane curvature. J Cell Sci 121, 1951-1954.
24. Hu CD, Chinenov Y, Kerppola TK (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9, 789-798.
25. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P (2005). Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9, 791-804.
26. Kamei T, Tanaka K, Hihara T, Umikawa M, Imamura H, Kikyo M, Ozaki K, Takai Y (1998). Interaction of Bnr1p with a novel Src Homology 3 domain-containing Hof1p implication in cytokinesis in Saccharomyces cerevisiae. J Biol Chem 273, 28341-28345.
27. Kerppola TK (2008). Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu Rev Biophys 37, 465-487.
28. Korinek WS, Bi E, Epp JA, Wang L, Ho J, Chant J (2000). Cyk3, a novel SH3-domain protein, affects cytokinesis in yeast. Curr Biol 10, 947-950.
29. Labedzka K, Tian C, Nussbaumer U, Timmermann S, Walther P, Muller J, Johnsson N (2012). Sho1p connects the plasma membrane with proteins of the cytokinesis network via multiple isomeric interaction states. J Cell Sci 125, 4103-4113.
30. Li R (1997). Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J Cell Biol 136, 649-658.
31. Lillie SH, Pringle JR (1980). Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143, 1384-1394.
32. Lippincott J, Li R (1998a). Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J Cell Biol 140, 355-366.
33. Lippincott J, Li R (1998b). Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J Cell Biol 143, 1947-1960.
34. Lippincott J, Shannon KB, Shou W, Deshaies RJ, Li R (2001). The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J Cell Sci 114, 1379-1386.
35. Longtine MS, McKenzie A III, DeMarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
36. Luo J, Vallen EA, Dravis C, Tcheperegine SE, Drees BL, Bi E (2004). Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J Cell Biol 165, 843-855.
37. Madania A, Dumoulin P, Grava S, Kitamoto H, Scharer-Brodbeck C, Soulard A, Moreau V, Winsor B (1999). The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol Biol Cell 10, 3521-3538.
38. McMurray MA, Bertin A, Garcia G 3rd, Lam L, Nogales E, Thorner J (2011). Septin filament formation is essential in budding yeast. Dev Cell 20, 540-549.
39. McMurray MA, Thorner J (2009). Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div 4, 18.
40. Meitinger F, Boehm ME, Hofmann A, Hub B, Zentgraf H, Lehmann WD, Pereira G (2011). Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev 25, 875-888.
41. Meitinger F, Palani S, Hub B, Pereira G (2013). Dual function of the NDR-kinase Dbf2 in the regulation of the F-BAR protein Hof1 during cytokinesis. Mol Biol Cell 24, 1290-1304.
42. Meitinger F, Petrova B, Mancini Lombardi I, Bertazzi DT, Hub B, Zentgraf H, Pereira G (2010). Targeted localization of Inn1, Cyk3 and Chs2 by the mitotic-exit network regulates cytokinesis in budding yeast. J Cell Sci 123, 1851-1861.
43. Munn AL, Stevenson BJ, Geli MI, Riezman H (1995). end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol Biol Cell 6, 1721-1742.
44. Nishihama R et al. (2009). Role of Inn1 and its interactions with Hof1 and Cyk3 in promoting cleavage furrow and septum formation in S. cerevisiae. J Cell Biol 185, 995-1012.
45. Oh Y, Bi E (2011). Septin structure and function in yeast and beyond. Trends Cell Biol 21, 141-148.
46. Oh Y, Chang K-J, Orlean P, Wloka C, Deshaies R, Bi E (2012). Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast. Mol Biol Cell 23, 2445-2456.
47. Pollard TD (2010). Mechanics of cytokinesis in eukaryotes. Curr Opin Cell Biol 22, 50-56.
48. Ren G, Wang J, Brinkworth R, Winsor B, Kobe B, Munn AL (2005). Verprolin cytokinesis function mediated by the Hof one trap domain. Traffic 6, 575-593.
49. Roberts-Galbraith RH, Chen JS, Wang J, Gould KL (2009). The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccha-romyces pombe contractile ring. J Cell Biol 184, 113-127.
50. Roberts-Galbraith RH, Gould KL (2010). Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9, 4091-4097.
51. Roberts-Galbraith RH, Ohi MD, Ballif BA, Chen JS, McLeod I, McDonald WH, Gygi SP, Yates JR 3rd, Gould KL (2010). Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaf-folding activity at the cell division site. Mol Cell 39, 86-99.
52. Rodriguez JR, Paterson BM (1990). Yeast myosin heavy chain mutant: maintenance of the cell type specific budding pattern and the normal deposition of chitin and cell wall components requires an intact myosin heavy chain gene. Cell Motil Cytoskeleton 17, 301-308.
53. Sanchez-Diaz A, Marchesi V, Murray S, Jones R, Pereira G, Edmondson R, Allen T, Labib K (2008). Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat Cell Biol 10, 395-406.
54. Schmidt M, Bowers B, Varma A, Roh D-H, Cabib E (2002). In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J Cell Sci 115, 293-302.
55. Shannon KB, Li R (2000). A myosin light chain mediates the localization of the budding yeast IQGAP-like protein during contractile ring formation. Curr Biol 10, 727-730.
56. Shimada A et al. (2007). Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772.
57. Sikorski RS, Hieter P (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
58. Spencer S, Dowbenko D, Cheng J, Li W, Brush J, Utzig S, Simanis V, Lasky LA (1997). PSTPIP: a tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J Cell Biol 138, 845-860.
59. Stevens RC, Davis TN (1998). Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae. J Cell Biol 142, 711-722.
60. Suetsugu S, Toyooka K, Senju Y (2010). Subcellular membrane curvature mediated by the BAR domain superfamily proteins. Semin Cell Dev Biol 21, 340-349.
61. Sung MK, Huh WK (2007). Bimolecular fluorescence complementation analysis system for in vivo detection of protein-protein interaction in Saccharomyces cerevisiae. Yeast 24, 767-775.
62. Teh EM, Chai CC, Yeong FM (2009). Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 8, 2964-2974.
63. Tsujita K, Suetsugu S, Sasaki N, Furutani M, Oikawa T, Takenawa T (2006). Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol 172, 269-279.
64. Tully GH, Nishihama R, Pringle JR, Morgan DO (2009). The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol Biol Cell 20, 1201-1212.
65. Vallen EA, Caviston J, Bi E (2000). Roles of Hof1p, Bni1p, Bnr1p, and Myo1p in cytokinesis in Saccharomyces cerevisiae. Mol Biol Cell 11, 593-611.
66. VerPlank L, Li R (2005). Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. Mol Biol Cell 16, 2529-2543.
67. Versele M, Gullbrand B, Shulewitz MJ, Cid VJ, Bahmanyar S, Chen RE, Barth P, Alber T, Thorner J (2004). Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae. Mol Biol Cell 15, 4568-4583.
68. Watts FZ, Shiels G, Orr E (1987). The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J 6, 3499-3505.
69. Weirich CS, Erzberger J P, Barral Y (2008). The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 9, 478-489.
70. Wloka C, Bi E (2012). Mechanisms of cytokinesis in budding yeast. Cytoskeleton (Hoboken) 69, 710-726.
71. Wloka C, Nishihama R, Onishi M, Oh Y, Hanna J, Pringle JR, Krauss M, Bi E (2011). Evidence that a septin diffusion barrier is dispensable for cytokinesis in budding yeast. Biol Chem 392, 813-829.
72. Wloka C, Vallen EA, Thé L, Fang X, Oh Y, Bi E (2013). Immobile myosin-II plays a scaffolding role during cytokinesis in budding yeast. J Cell Biol 200, 271-286.
73. Wu Y, Spencer SD, Lasky LA (1998). Tyrosine phosphorylation regulates the SH3-mediated binding of the Wiskott-Aldrich syndrome protein to PST-PIP, a cytoskeletal-associated protein. J Biol Chem 273, 5765-5770.
74. Zhang G, Kashimshetty R, Ng KE, Tan HB, Yeong FM (2006). Exit from mitosis triggers Chs2p transport from the endoplasmic reticulum to mother-daughter neck via the secretory pathway in budding yeast. J Cell Biol 174, 207-220.