Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis

Molecular Biology of the Cell

Volumn 19, Issue 4, 2008, Pages 1727-1738

  Pinar, Mario ^a   Coll, Pedro M ^a   Rincón, Sergio A ^a   Pérez, Pilar ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; LIM PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; PAXILLIN; PROTEIN CDC15; PROTEIN PXL1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL ADHESION; CELL DIVISION; CELL MOTILITY; CELL SEPARATION; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; ENZYME ACTIVITY; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE INTERACTION; HEAT SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION;

ACTOMYOSIN; CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; CYTOKINESIS; GENES, FUNGAL; MULTIPROTEIN COMPLEXES; MUTATION; MYOSIN TYPE II; PAXILLIN; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RHO GTP-BINDING PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TEMPERATURE;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 44949140638     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-07-0718     Document Type: Article

References (67)

1. Alonso-Nunez, M. L., An, H., Martin-Cuadrado, A. B., Mehta, S., Petit, C., Sipiczki, M., del Rey, F., Gould, K. L., and de Aldana, C. R. (2005). Ace2p controls the expression of genes required for cell separation in Schizosaccharomyces pombe. Mol. Biol. Cell 16, 2003-2017.
2. An, H., Morrell, J. L., Jennings, J. L., Link, A. J., and Gould, K. L. (2004). Requirements of fission yeast septins for complex formation, localization and function. Mol. Biol. Cell 15, 5551-5564.
3. Arellano, M., Coll, P. M., and Pérez, P. (1999a). Rho GTPases in the control of cell morphology, cell polarity, and actin localization in fission yeast. Microsc. Res. Tech. 47, 51-60.
4. Arellano, M., Duran, A., and Perez, 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.
5. Arellano, M., Duran, A., and Perez, P. (1997). Localization of the Schizosaccharomyces pombe Rho1 GTPase and its involvement in the organization of the actin cytoskeleton. J. Cell Sci. 110, 2547-2555.
6. Arellano, M., Valdivieso, M. H., Calonge, T. M., Coll, P. M., Durán, A., and Pérez, P. (1999b). Schizosaccharomyces pombe protein kinase C homologues, pck1p and pck2p, are targets of rho1p and rho2p and differentially regulate cell integrity. J. Cell Sci. 112, 3569-3578.
7. Bähler, J., Wu, J.-Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, 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.
8. 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.
9. Bezanilla, M., and Pollard, T. D. (2000). Myosin-II tails confer unique functions in Schizosaccharomyces pombe: characterization of a novel myosin-II tail. Mol. Biol. Cell 11, 79-91.
10. Bi, E., Maddox, P., Lew, D. J., Salmon, E. D., McMillan, J. N., Yeh, E., and Pringle, J. R. (1998). Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. The J. Cell Biol. 142, 1301-1312.
11. Brown, M. C., and Turner, C. E. (2004). Paxillin: adapting to change. Physiol. Rev. 84, 1315-1339.
12. Burgess, D. R., and Chang, F. (2005). Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol. 15, 156-162.
13. Calonge, T. M., Arellano, M., Coll, P. M., and Perez, P. (2003). Rga5p is a specific Rho1p GTPase-activating protein that regulates cell integrity in Schizosaccharomyces pombe. Mol. Microbiol. 47, 507-518.
14. Carnahan, R. H., and Gould, K. L. (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.
15. Carragher, N. O., and Frame, M. C. (2004). Focal adhesion and actin dynamics: a place where kinases and proteases meet to promote invasion. Trends Cell Biol. 14, 241-249.
16. Coll, P. M., Rincon, S. A., Izquierdo, R. A., and Perez, P. (2007). Hob3p, the fission yeast ortholog of human BIN3, localizes Cdc42p to the division site and regulates cytokinesis. EMBO J. 26, 1865-1877.
17. Coll, P. M., Trillo, Y., Ametzazurra, A., and Perez, P. (2003). Gef1p, a new guanine nucleotide exchange factor for Cdc42p, regulates polarity in Schizosaccharomyces pombe. Mol. Biol. Cell 14, 313-323.
18. Cortes, J. C., 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.
19. Cortes, J. C., 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.
20. Cortes, J. C., Konomi, M., Martins, I. M., Munoz, J., Moreno, M. B., Osumi, M., Duran, 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.
21. Chang, E. C., Barr, M., Wang, Y., Jung, V., Xu, H. P., and Wigler, M. H. (1994). Cooperative interaction of S. pombe proteins required for mating and morphogenesis. Cell 79, 131-141.
22. 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.
23. Eng, K., Naqvi, N. I., et al. (1998). Rng2p, a protein required for cytokinesis in fission yeast, is a component of the actomyosin ring and the spindle pole body. Curr. Biol. 8, 611-621.
24. Feierbach, B., and Chang, F. (2001). Cytokinesis and the contractile ring in fission yeast. Curr. Opin. Microbiol. 4, 713-719.
25. Forsburg, S. L., and Sherman, D. A. (1997). General purpose tagging vectors for fission yeast. Gene 191, 191-195.
26. Furge, K. A., Wong, K., Armstrong, J., Balasubramanian, M., and Albright, C. F. (1998). Byr4 and Cdc16 form a two-component GTPase-activating protein for the Spg1 GTPase that controls septation in fission yeast. Curr. Biol. 8, 947-954.
27. Gao, X. D., Caviston, J. P., Tcheperegine, S. E., and Bi, E. (2004). Pxl1p, a paxillin-like protein in Saccharomyces cerevisiae, may coordinate Cdc42p and Rho1p functions during polarized growth. Mol. Biol. Cell 15, 3977-3985.
28. Garcia, I., Jimenez, D., Martin, V., Duran, A., and Sanchez, Y. (2005). The alpha-glucanase Agn1p is required for cell separation in Schizosaccharomyces pombe. Biol. Cell 97, 569-576.
29. García, P., Tajadura, V., Garcia, I., and Sanchez, Y. (2006). Role of Rho GTPases and Rho-GEFs in the regulation of cell shape and integrity in fission yeast. Yeast 23, 1031-1043.
30. Hirota, K., Tanaka, K., Ohta, K., and Yamamoto, M. (2003). Gef1p and Scd1p, the two GDP-GTP exchange factors for Cdc42p, form a ring structure that shrinks during cytokinesis in. Mol. Biol. Cell 14, 3617-3627.
31. Johnson, B. F., Yoo, B. Y., Calleja, G. B., and Kozela, C. P. (2005). Second thoughts on septation by the fission yeast, Schizosaccharomyces pombe: pull vs. push mechanisms with an appendix-dimensional modelling of the flat and variable septa. 88, 1-12.
32. Kadrmas, J. L., and Beckerle, M. C. (2004). The LIM domain: from the cytoskeleton to the nucleus. Nat. Rev. Mol. Cell Biol. 5, 920-931.
33. Kitayama, C., Sugimoto, A., and Yamamoto, M. (1997). Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe. J. Cell Biol. 137, 1309-1319.
34. Krapp, A., Gulli, M. P., and Simanis, V. (2004). SIN and the art of splitting the fission yeast cell. Curr. Biol. 14, R722-R730.
35. Le Goff, X., Motegi, F., Salimova, E., Mabuchi, I., and Simanis, V. (2000). The S. pombe rlc1 gene encodes a putative myosin regulatory light chain that binds the type II myosins myo3p and myo2p. J. Cell Sci. 113, 4157-4163.
36. Le Goff, X., Woollard, A., and Simanis, V. (1999). Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe. Mol. Gen. Genet. 262, 163-172.
37. Levin, D. E. (2005). Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 262-291.
38. Mackin, N. A., Sousou, T. J., and Erdman, S. E. (2004). The PXL1 gene of Saccharomyces cerevisiae encodes a paxillin-like protein functioning in polarized cell growth. Mol. Biol. Cell 15, 1904-1917.
39. Martin-Cuadrado, A. B., Duenas, E., Sipiczki, M., Vazquez de Aldana, C. R., and del Rey, F. (2003). The endo-beta-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J. Cell Sci. 116, 1689-1698.
40. 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.
41. Matsumura, F. (2005). Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371-377.
42. McCollum, D., Balasubramanian, M. K., Pelcher, L. E., Hemmingsen, S. M., and Gould, K. L. (1995). Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis. J. Cell Biol. 130, 651-660.
43. Miller, P. J., and Johnson, D. I. (1994). Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Mol. Cell Biol. 14, 1075-1083.
44. Moreno, S., Klar, A., and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
45. Morrell-Falvey, J. L., Ren, L., Feoktistova, A., Haese, G. D., and Gould, K. L. (2005). Cell wall remodeling at the fission yeast cell division site requires the Rho-GEF Rgf3p. J. Cell Sci. 118, 5563-5573.
46. Motegi, F., Mishra, M., Balasubramanian, M. K., and Mabuchi, I. (2004). Myosin-II reorganization during mitosis is controlled temporally by its dephosphorylation and spatially by Mid1 in fission yeast. J. Cell Biol. 165, 685-695.
47. Motegi, F., Nakano, K., and Mabuchi, I. (2000). Molecular mechanism of myosin-II assembly at the division site in Schizosaccharomyces pombe. J. Cell Sci. 113, 1813-1825.
48. Mulvihill, D. P., and Hyams, J. S. (2003). Role of the two type II myosins, Myo2 and Myp2, in cytokinetic actomyosin ring formation and function in fission yeast. Cell Motil. Cytoskeleton 54, 208-216.
49. Mutoh, T., Nakano, K., and Mabuchi, I. (2005). Rho1-GEFs Rgf1 and Rgf2 are involved in formation of cell wall and septum, while Rgf3 is involved in cytokinesis in fission yeast. Genes Cells 10, 1189-1202.
50. Nakano, K., Mutoh, T., and Mabuchi, I. (2001). Characterization of GTPase-activating proteins for the function of the Rho-family small GTPases in the fission yeast Schizosaccharomyces pombe. Genes Cells 6, 1031-1042.
51. Naqvi, N. I., Eng, K., Gould, K. L., and Balasubramanian, M. K. (1999). Evidence for F-actin-dependent and -independent mechanisms involved in assembly and stability of the medial actomyosin ring in fission yeast. EMBO J. 18, 854-862.
52. Naqvi, N. I., Wong, K. C., Tang, X., and Balasubramanian, M. K. (2000). Type II myosin regulatory light chain relieves auto-inhibition of myosin-heavy-chain function. Nat. Cell Biol. 2, 855-858.
53. Nobes, C. D., and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
54. Park, H. O., and Bi, E. (2007). Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71, 48-96.
55. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P., and Narumiya, S. (1996). Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J. Biol. Chem. 271, 13556-13560.
56. Ren, X. D., Kiosses, W. B., and Schwartz, M. A. (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585.
57. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
58. Rustici, G., Mata, J., Kivinen, K., Lio, P., Penkett, C. J., Burns, G., Hayles, J., Brazma, A., Nurse, P., and Bahler, J. (2004). Periodic gene expression program of the fission yeast cell cycle. Nat. Genet. 36, 809-817.
59. Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A., and Collard, J. G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009-1022.
60. Tajadura, V., Garcia, B., Garcia, I., Garcia, P., and Sanchez, Y. (2004). Schizosaccharomyces pombe Rgf3p is a specific Rho1 GEF that regulates cell wall beta-glucan biosynthesis through the GTPase Rho1p. J. Cell Sci. 117, 6163-6174.
61. Turner, C. E. (2000). Paxillin and focal adhesion signalling. Nat. Cell Biol. 2, E231-E236.
62. Urven, L. E., Yabe, T., and Pelegri, F. (2006). A role for non-muscle myosin II function in furrow maturation in the early zebrafish embryo. J. Cell Sci. 119, 4342-4352.
63. Wang, H., Tang, X., Liu, J., Trautmann, S., Balasundaram, D., McCollum, D., and Balasubramanian, M. K. (2002). The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe. Mol. Biol. Cell 13, 515-529.
64. West, R. R., Vaisberg, E. V., Ding, R., Nurse, P., and McIntosh, J. R. (1998). cut11(+): A gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. Mol. Biol. Cell 9, 2839-2855.
65. Wolfe, B. A., and Gould, K. L. (2005). Split decisions: coordinating cytokinesis in yeast. Trends Cell Biol. 15, 10-18.
66. Wu, J. Q., Kuhn, J. R., Kovar, D. R., and Pollard, T. D. (2003). Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Developmental cell 5, 723-734.
67. 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.