Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast

PLoS Genetics

Volumn 11, Issue 7, 2015, Pages

  G Cortés, Juan C ^a   Pujol, Nuria ^b   Sato, Mamiko ^c   Pinar, Mario ^d   Ramos, Mariona ^a   Moreno, Belén ^a   Osumi, Masako ^c   Ribas, Juan Carlos ^a   Pérez, Pilar ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF LLEIDA   (Spain)

^c and Department of Chemical and Biological Sciences Women’s University ^*  (Japan)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; GLUCAN SYNTHASE; MYOSIN ADENOSINE TRIPHOSPHATASE; PAXILLIN; PROTEIN BGS1; PROTEIN CDC15; PROTEIN PXL1; UNCLASSIFIED DRUG; 1,3-BETA-GLUCAN SYNTHASE; BETA GLUCAN; BETA-1,2-GLUCAN; CDC15 PROTEIN; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; GLUCOSYLTRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; PXL1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ALLELE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SCHIZOSACCHAROMYCES; ACTIN FILAMENT; CELL SURFACE; CELL WALL; CHEMISTRY; CYTOKINESIS; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

SCHIZOSACCHAROMYCETACEAE;

ACTIN CYTOSKELETON; ACTOMYOSIN; BETA-GLUCANS; CELL CYCLE PROTEINS; CELL MEMBRANE; CELL SURFACE EXTENSIONS; CELL WALL; CYTOKINESIS; CYTOSKELETAL PROTEINS; GLUCOSYLTRANSFERASES; GTP-BINDING PROTEINS; MEMBRANE PROTEINS; PAXILLIN; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84938768274     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005358     Document Type: Article

References (50)

1. Pollard TD, Wu JQ, (2010) Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 11: 149–155. doi: 10.1038/nrm2834 20094054
2. Balasubramanian MK, Srinivasan R, Huang Y, Ng KH, (2012) Comparing contractile apparatus-driven cytokinesis mechanisms across kingdoms. Cytoskeleton (Hoboken) 69: 942–956.
3. Proctor SA, Minc N, Boudaoud A, 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. doi: 10.1016/j.cub.2012.06.042 22840513
4. Muñoz J, Cortés JCG, Sipiczki M, Ramos M, Clemente-Ramos JA, et al. (2013) Extracellular cell wall β(1,3)glucan is required to couple septation to actomyosin ring contraction. J Cell Biol 203: 265–282. doi: 10.1083/jcb.201304132 24165938
5. Wu JQ, Kuhn JR, Kovar DR, Pollard TD, (2003) Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 5: 723–734. 14602073
6. Balasubramanian MK, Bi E, Glotzer M, (2004) Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr Biol 14: R806–818. 15380095
7. Rincon SA, Paoletti A, (2012) Mid1/anillin and the spatial regulation of cytokinesis in fission yeast. Cytoskeleton (Hoboken) 69: 764–777.
8. Lee IJ, Coffman VC, Wu JQ, (2012) Contractile-ring assembly in fission yeast cytokinesis: Recent advances and new perspectives. Cytoskeleton (Hoboken) 69: 751–763.
9. Arellano M, Durán A, Pérez P, (1996) Rho 1 GTPase activates the (1–3)beta-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15: 4584–4591. 8887550
10. Drgonova J, Drgon T, Tanaka K, Kollar R, Chen GC, et al. (1996) Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272: 277–279. 8602514
11. Cortés JCG, Konomi M, Martins IM, Muñoz J, Moreno MB, et al. (2007) The (1,3)β-D-glucan synthase subunit Bgs1p is responsible for the fission yeast primary septum formation. Mol Microbiol 65: 201–217. 17581129
12. Cortés JCG, Carnero E, Ishiguro J, Sanchez Y, Durán A, et al. (2005) The novel fission yeast (1,3)β-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J Cell Sci 118: 157–174. 15615781
13. Hochstenbach F, Klis FM, van den Ende H, van Donselaar E, Peters PJ, et al. (1998) Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc Natl Acad Sci U S A 95: 9161–9166. 9689051
14. Katayama S, Hirata D, Arellano M, Pérez P, Toda T, (1999) Fission yeast α-glucan synthase Mok1 requires the actin cytoskeleton to localize the sites of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function. J Cell Biol 144: 1173–1186. 10087262
15. Cortés JCG, Sato M, Muñoz J, Moreno MB, Clemente-Ramos JA, et al. (2012) Fission yeast Ags1 confers the essential septum strength needed for safe gradual cell abscission. J Cell Biol 198: 637–656. doi: 10.1083/jcb.201202015 22891259
16. Wolfe BA, Gould KL, (2005) Split decisions: coordinating cytokinesis in yeast. Trends Cell Biol 15: 10–18. 15653073
17. 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. 12939254
18. Roberts-Galbraith RH, Ohi MD, Ballif BA, Chen JS, McLeod I, et al. (2010) Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol Cell 39: 86–99. doi: 10.1016/j.molcel.2010.06.012 20603077
19. Arasada R, Pollard TD, (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. doi: 10.1016/j.cub.2011.07.046 21885283
20. Arasada R, Pollard TD, (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. doi: 10.1016/j.celrep.2014.07.048 25159149
21. Demeter J, Sazer S, (1998) imp2, a new component of the actin ring in the fission yeast Schizosaccharomyces pombe. J Cell Biol 143: 415–427. 9786952
22. Roberts-Galbraith RH, Chen JS, Wang J, Gould KL, (2009) The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J Cell Biol 184: 113–127. doi: 10.1083/jcb.200806044 19139265
23. Martín-Garcia R, Coll PM, Pérez P, (2014) F-BAR domain protein Rga7 collaborates with Cdc15 and Imp2 to ensure proper cytokinesis in fission yeast. J Cell Sci.
24. Kume K, Kubota S, Koyano T, Kanai M, Mizunuma M, et al. (2013) Fission yeast leucine-rich repeat protein Lrp1 is essential for cell morphogenesis as a component of the morphogenesis Orb6 network (MOR). Biosci Biotechnol Biochem 77: 1086–1091. 23649273
25. Ge W, Balasubramanian MK, (2008) Pxl1p, a paxillin-related protein, stabilizes the actomyosin ring during cytokinesis in fission yeast. Mol Biol Cell 19: 1680–1692. doi: 10.1091/mbc.E07-07-0715 18272786
26. Pinar M, Coll PM, Rincón SA, Pérez P, (2008) Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol Biol Cell 19: 1727–1738. doi: 10.1091/mbc.E07-07-0718 18256290
27. Cortés JCG, Ishiguro J, Durán A, Ribas JC, (2002) Localization of the (1,3)β-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. 12356913
28. Tebbs IR, Pollard TD, (2013) Separate roles of IQGAP Rng2p in forming and constricting the Schizosaccharomyces pombe cytokinetic contractile ring. Mol Biol Cell 24: 1904–1917. doi: 10.1091/mbc.E12-10-0775 23615450
29. Nakamura T, Nakamura-Kubo M, Hirata A, Shimoda C, (2001) The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1(+)-encoding syntaxin-like protein. Mol Biol Cell 12: 3955–3972. 11739793
30. Forsburg SL, (1993) Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res 21: 2955–2956. 8332516
31. Moreno MB, Durán A, Ribas JC, (2000) A family of multifunctional thiamine-repressible expression vectors for fission yeast. Yeast 16: 861–872. 10861909
32. Onishi M, Ko N, Nishihama R, Pringle JR, (2013) Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis. J Cell Biol 202: 311–329. doi: 10.1083/jcb.201302001 23878277
33. Calonge TM, Arellano M, Coll PM, Pérez P, (2003) Rga5p is a specific Rho1p GTPase-activating protein that regulates cell integrity in Schizosaccharomyces pombe. Mol Microbiol 47: 507–518. 12519200
34. Ren L, Willet AH, Roberts-Galbraith RH, McDonald NA, Feoktistova A, et al. (2015) The Cdc15 and Imp2 SH3 domains cooperatively scaffold a network of proteins that redundantly ensure efficient cell division in fission yeast. Mol Biol Cell 26: 256–269. doi: 10.1091/mbc.E14-10-1451 25428987
35. Rustici G, Mata J, Kivinen K, Lio P, Penkett CJ, et al. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat Genet 36: 809–817. 15195092
36. Huang Y, Chew TG, Ge W, Balasubramanian MK, (2007) Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev Cell 12: 987–996. 17543869
37. Liu J, Wang H, Balasubramanian MK, (2000) A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe. J Cell Sci 113: 1223–1230. 10704373
38. Schmidt M, Bowers B, Varma A, Roh DH, 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. 11839781
39. Zhou Z, Munteanu EL, He J, Ursell T, Bathe M, et al. (2014) The contractile ring coordinates curvature dependent septum assembly during fission yeast cytokinesis. Mol Biol Cell.
40. Sánchez-Díaz A, Marchesi V, Murray S, Jones R, Pereira G, et al. (2008) Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat Cell Biol 10: 395–406. doi: 10.1038/ncb1701 18344988
41. Nishihama R, Schreiter JH, Onishi M, Vallen EA, Hanna J, 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. doi: 10.1083/jcb.200903125 19528296
42. Martín-García R, Valdivieso MH, (2006) The fission yeast Chs2 protein interacts with the type-II myosin Myo3p and is required for the integrity of the actomyosin ring. J Cell Sci 119: 2768–2779. 16772338
43. Pollard LW, Onishi M, Pringle JR, Lord M, (2012) Fission yeast Cyk3p is a transglutaminase-like protein that participates in cytokinesis and cell morphogenesis. Mol Biol Cell 23: 2433–2444. doi: 10.1091/mbc.E11-07-0656 22573890
44. Bähler J, Wu J-Q, Longtine MS, Shah NG, McKenzie IIIA, et al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943–951. 9717240
45. Shaner NC, Steinbach PA, Tsien RY, (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905–909. 16299475
46. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795–823. 2005825
47. Kunkel TA, (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci USA 82: 488–492. 3881765
48. Sambrook J, Russell DW, (2001) Molecular cloning: A laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.
49. Gietz RD, Schiestl RH, Willems AR, Woods RA, (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355–360. 7785336
50. Konomi M, Fujimoto K, Toda T, Osumi M, (2003) Characterization and behaviour of alpha-glucan synthase in Schizosaccharomyces pombe as revealed by electron microscopy. Yeast 20: 427–438. 12673626