A role for F-BAR protein Rga7p during cytokinesis in S. pombe

Journal of Cell Science

Volumn 128, Issue 13, 2015, Pages 2259-2268

  Arasada, Rajesh ^a   Pollard, Thomas D ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bgs4; Cell wall; Cytokinesis; F BAR proteins; Golgi complex; S. pombe

Indexed keywords

CLATHRIN LIGHT CHAIN; FUNGAL PROTEIN; GLUCAN SYNTHASE; PROTEIN RGA7P; UNCLASSIFIED DRUG; GLUCOSYLTRANSFERASE; HYBRID PROTEIN; MUTANT PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ACTIN FILAMENT; AMNION BAND; ARTICLE; CELL DIVISION; CELL MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINESIS; FLUORESCENCE MICROSCOPY; FUNGAL CELL; FUNGAL CELL WALL; FUNGAL GENE; GENE DELETION; GENE INTERACTION; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RGA7 GENE; RHOGAP DOMAIN; SCHIZOSACCHAROMYCES POMBE; CHEMISTRY; CYTOLOGY; EPISTASIS; GENETIC COMPLEMENTATION; METABOLISM; PROTEIN TERTIARY STRUCTURE; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCES POMBE;

CYTOKINESIS; EPISTASIS, GENETIC; GENETIC COMPLEMENTATION TEST; GLUCOSYLTRANSFERASES; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84935516383     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.162974     Document Type: Article

References (47)

1. Antebi, A. and Fink, G. R. (1992). The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell 3, 633-654.
2. Arasada, R. and Pollard, T. D. (2011). Distinct roles for F-BAR proteins Cdc15p and Bzz1p in actin polymerization at sites of endocytosis in fission yeast. Curr. Biol. 21, 1450-1459.
3. Arasada, R. and Pollard, T. D. (2014). Contractile ring stability in S. pombe depends on F-BAR protein Cdc15p and Bgs1p transport from the Golgi complex. Cell Rep. 8, 1533-1544.
4. Bahler, J., Wu, J.-Q., Longtine, M. S., Shah, N. G., McKenzie, A., III, Steever, A. B.,Wach, A., Philippsen, P. and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
5. Balasubramanian, M. K.,McCollum, D.,Chang, L.,Wong,K.C.,Naqvi,N. I., He, X., Sazer, S. and Gould, K. L. (1998). Isolation and characterization of new fission yeast cytokinesis mutants. Genetics 149, 1265-1275.
6. Barrowman, J., Bhandari, D., Reinisch, K. and Ferro-Novick, S. (2010). TRAPP complexes in membrane traffic: convergence through a common Rab. Nat. Rev. Mol. Cell Biol. 11, 759-763.
7. Chang, F., Drubin, D. and Nurse, P. (1997). cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137, 169-182.
8. Coffman, V. C., Sees, J. A., Kovar, D. R. and Wu, J.-Q. (2013). The formins Cdc12 and For3 cooperate during contractile ring assembly in cytokinesis. J. Cell Biol. 203, 101-114.
9. Cortes, J. C. G., Ishiguro, J., Duran, A. and Ribas, J. C. (2002). Localization of the (1,3)beta-D-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J. Cell Sci. 115, 4081-4096.
10. Cortes, J. C. G., Carnero, E., Ishiguro, J., Sanchez, Y., Duran, A. and Ribas, J. C. (2005). The novel fission yeast (1,3)beta-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J. Cell Sci. 118, 157-174.
11. Cortes, J. C. G., Konomi, M., Martins, I. M., Muñoz, J., Moreno, M. B., Osumi, M., Durán, A. and Ribas, J. C. (2007). The (1,3)beta-D-glucan synthase subunit Bgs1p is responsible for the fission yeast primary septum formation. Mol. Microbiol. 65, 201-217.
12. Cortes, J. C. G., Sato, M., Munoz, J., Moreno, M. B., Clemente-Ramos, J. A., Ramos, M., Okada, H., Osumi, M., Duran, A. and Ribas, J. C. (2012). Fission yeast Ags1 confers the essential septum strength needed for safe gradual cell abscission. J. Cell Biol. 198, 637-656.
13. de Leon, N., Sharifmoghadam, M. R., Hoya, M., Curto, M.-A., Doncel, C. and Valdivieso, M.-H. (2013). Regulation of cell wall synthesis by the clathrin light chain is essential for viability in Schizosaccharomyces pombe. PLoS ONE 8, e71510.
14. Demeter, J. and Sazer, S. (1998). imp2, a new component of the actin ring in the fission yeast Schizosaccharomyces pombe. J. Cell. Biol. 143, 415-427.
15. Estravis, M., Rincon, S. A., Santos, B. and Perez, P. (2011). Cdc42 regulates multiple membrane traffic events in fission yeast. Traffic 12, 1744-1758.
16. Feierbach, B. and Chang, F. (2001). Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11, 1656-1665.
17. Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E. H., De Camilli, P. and Unger, V. M. (2008). Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817.
18. Gautier, R., Douguet, D., Antonny, B. and Drin, G. (2008). HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24, 2101-2102.
19. Glotzer, M. (2005). The molecular requirements for cytokinesis. Science 307, 1735-1739.
20. Henne, W. M., Kent, H. M., Ford, M. G. J., Hegde, B. G., Daumke, O., Butler, P. J. G., Mittal, R., Langen, R., Evans, P. R. and McMahon, H. T. (2007). Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852.
21. Humbel, B. M., Konomi, M., Takagi, T., Kamasawa, N., Ishijima, S. A. and Osumi, M. (2001). In situ localization of beta-glucans in the cell wall of Schizosaccharomyces pombe. Yeast 18, 433-444.
22. Ishiguro, J., Saitou, A., Duran, A. and Ribas, J. C. (1997). cps1+, a Schizosaccharomyces pombe gene homolog of Saccharomyces cerevisiae FKS genes whose mutation confers hypersensitivity to cyclosporin A and papulacandin B. J. Bacteriol. 179, 7653-7662.
23. Liu, J., Wang, H., McCollum, D. and Balasubramanian, M. K. (1999). Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. Genetics 153, 1193-1203.
24. Liu, J., Tang, X., Wang, H. and Balasubramanian, M. (2000). Bgs2p, a 1,3-beta-glucan synthase subunit, is essential for maturation of ascospore wall in Schizosaccharomyces pombe. FEBS Lett. 478, 105-108.
25. Liu, J., Tang, X., Wang, H., Oliferenko, S. and Balasubramanian, M. K. (2002). The localization of the integral membrane protein Cps1p to the cell division site is dependent on the actomyosin ring and the septation-inducing network in Schizosaccharomyces pombe. Mol. Biol. Cell 13, 989-1000.
26. Lord, M. and Pollard, T. D. (2004). UCS protein Rng3p activates actin filament gliding by fission yeast myosin-II. J. Cell Biol. 167, 315-325.
27. Martin, S. G. and Chang, F. (2006). Dynamics of the formin for3p in actin cable assembly. Curr. Biol. 16, 1161-1170.
28. Martin, V., Ribas, J. C., Carnero, E., Duran, A. and Sanchez, Y. (2000). bgs2+, a sporulation-specific glucan synthase homologue is required for proper ascospore wall maturation in fission yeast. Mol. Microbiol. 38, 308-321.
29. Martin, V., Garcia, B., Carnero, E., Duran, A. and Sanchez, Y. (2003). Bgs3p, a putative 1,3-beta-glucan synthase subunit, is required for cell wall assembly in Schizosaccharomyces pombe. Eukaryot. Cell 2, 159-169.
30. Martin, S. G., Rincon, S. A., Basu, R., Perez, P. and Chang, F. (2007). Regulation of the formin for3p by cdc42p and bud6p. Mol. Biol. Cell 18, 4155-4167.
31. Martin-Garcia, R., Coll, P. M. and Perez, P. (2014). F-BAR domain protein Rga7 collaborates with Cdc15 and Imp2 to ensure proper cytokinesis in fission yeast. J. Cell Sci. 127, 4146-4158.
32. Martins, I. M., Cortes, J. C. G., Munoz, J., Moreno, M. B., Ramos, M., Clemente-Ramos, J. A., Duran, A. and Ribas, J. C. (2011). Differential activities of three families of specific beta(1,3)glucan synthase inhibitors in wild-type and resistant strains of fission yeast. J. Biol. Chem. 286, 3484-3496.
33. Munoz, J., Cortes, J. C. G., Sipiczki, M., Ramos, M., Clemente-Ramos, J. A., Moreno, M. B., Martins, I. M., Perez, P. and Ribas, J. C. (2013). Extracellular cell wall beta(1,3)glucan is required to couple septation to actomyosin ring contraction. J. Cell Biol. 203, 265-282.
34. Nakano, K., Imai, J., Arai, R., Toh-e, A., Matsui, Y. and Mabuchi, I. (2002). The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. J. Cell Sci. 115, 4629-4639.
35. Pollard, T. D. (2010). Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50-56.
36. Proctor, S. A., Minc, N., Boudaoud, A. and Chang, F. (2012). Contributions of turgor pressure, the contractile ring, and septum assembly to forces in cytokinesis in fission yeast. Curr. Biol. 22, 1601-1608.
37. Roberts-Galbraith, R. H., Chen, J.-S.,Wang, J. and Gould, K. L. (2009). The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 184, 113-127.
38. Shimada, A., Niwa, H., Tsujita, K., Suetsugu, S., Nitta, K., Hanawa-Suetsugu, K., Akasaka, R., Nishino, Y., Toyama, M., Chen, L. 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.
39. Simanis, V. (2015). Pombe's thirteen - control of fission yeast cell division by the septation initiation network. J. Cell Sci. 128, 1465-1474.
40. Sipiczki, M. and Bozsik, A. (2000). The use of morphomutants to investigate septum formation and cell separation in Schizosaccharomyces pombe. Arch. Microbiol. 174, 386-392.
41. Soto, T., Villar-Tajadura, M. A., Madrid, M., Vicente, J., Gacto, M., Perez, P. and Cansado, J. (2010). Rga4 modulates the activity of the fission yeast cell integrity MAPK pathway by acting as a Rho2 GTPase-activating protein. J. Biol. Chem. 285, 11516-11525.
42. Vjestica, A., Tang, X.-Z. and Oliferenko, S. (2008). The actomyosin ring recruits early secretory compartments to the division site in fission yeast. Mol. Biol. Cell 19, 1125-1138.
43. Wu, J.-Q. and Pollard, T. D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
44. Wu, J.-Q., Sirotkin, V., Kovar, D., Lord, M., Beltzner, C., Kuhn, J. R. and Pollard, T. D. (2006). Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 174, 391-402.
45. Xu, X. and Vogel, B. E. (2011). A secreted protein promotes cleavage furrow maturation during cytokinesis. Curr. Biol. 21, 114-119.
46. Yang, P., Qyang, Y., Bartholomeusz, G., Zhou, X. and Marcus, S. (2003). The novel Rho GTPase-activating protein family protein, Rga8, provides a potential link between Cdc42/p21-activated kinase and Rho signaling pathways in the fission yeast, Schizosaccharomyces pombe. J. Biol. Chem. 278, 48821-48830.
47. Yu, Y., Li, C., Kita, A., Katayama, Y., Kubouchi, K., Udo, M., Imanaka, Y., Ueda, S., Masuko, T. and Sugiura, R. (2013). Sip1, an AP-1 accessory protein in fission yeast, is required for localization of Rho3 GTPase. PLoS ONE 8, e68488.