The mitosis-to-interphase transition is coordinated by cross talk between the SIN and MOR pathways in Schizosaccharomyces pombe

Journal of Cell Biology

Volumn 190, Issue 5, 2010, Pages 793-805

  Ray, Samriddha ^a   Kume, Kazunori ^b   Gupta, Sneha ^a   Ge, Wanzhong ^c   Balasubramanian, Mohan ^c   Hirata, Dai ^b   McCollum, Dannel ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN NAK1 KINASE; PROTEIN ORB6; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CYTOKINESIS; CYTOSKELETON; INTERPHASE; MITOSIS; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; SCHIZOSACCHAROMYCES POMBE;

ACTINS; CELL DIVISION; CYTOKINESIS; GREEN FLUORESCENT PROTEINS; INTERPHASE; MITOSIS; RECOMBINANT FUSION PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 77956356651     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201002055     Document Type: Article

References (51)

1. Balasubramanian, M.K., B.R. Hirani, J.D. Burke, and K.L. Gould. 1994. The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125:1289-1301. doi:10.1083/jcb.125.6.1289
2. Balasubramanian, M.K., D. McCollum, and K.L. Gould. 1997. Cytokinesis in fission yeast Schizosaccharomyces pombe. Methods Enzymol. 283:494-506. doi:10.1016/S0076-6879(97)83039-X
3. Balasubramanian, M.K., D. McCollum, L. Chang, K.C. Wong, N.I. Naqvi, X. He, S. Sazer, and K.L. Gould. 1998. Isolation and characterization of new fission yeast cytokinesis mutants. Genetics. 149:1265-1275.
4. Bothos, J., R.L. Tuttle, M. Ottey, F.C. Luca, and T.D. Halazonetis. 2005. Human LATS1 is a mitotic exit network kinase. Cancer Res. 65:6568-6575. doi:10.1158/0008-5472.CAN-05-0862
5. Chan, E.H., M. Nousiainen, R.B. Chalamalasetty, A. Schäfer, E.A. Nigg, and H.H. Silljé. 2005. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene. 24:2076-2086. doi:10.1038/sj.onc.1208445
6. Cong, J., W. Geng, B. He, J. Liu, J. Charlton, and P.N. Adler. 2001. The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis. Development. 128:2793-2802.
7. Craven, R.A., D.J. Griffiths, K.S. Sheldrick, R.E. Randall, I.M. Hagan, and A.M. Carr. 1998. Vectors for the expression of tagged proteins in Schizosaccharomyces pombe. Gene. 221:59-68. doi:10.1016/S0378-1119(98)00434-X
8. Das, M., D.J. Wiley, X. Chen, K. Shah, and F. Verde. 2009. The conserved NDR kinase Orb6 controls polarized cell growth by spatial regulation of the small GTPase Cdc42. Curr. Biol. 19:1314-1319. doi:10.1016/j.cub.2009.06.057
9. Emoto, K., J.Z. Parrish, L.Y. Jan, and Y.N. Jan. 2006. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature. 443:210-213. doi:10.1038/nature05090
10. Fankhauser, C., J. Marks, A. Reymond, and V. Simanis. 1993. The S. pombe cdc16 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis? EMBO J. 12:2697-2704.
11. Fankhauser, C., A. Reymond, L. Cerutti, S. Utzig, K. Hofmann, and V. Simanis. 1995. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell. 82:435-444. doi:10.1016/0092-8674(95)90432-8
12. Forsburg, S.L., and N. Rhind. 2006. Basic methods for fission yeast. Yeast. 23:173-183. doi:10.1002/yea.1347
13. García-Cortés, J.C., and D. McCollum. 2009. Proper timing of cytokinesis is regulated by Schizosaccharomyces pombe Etd1. J. Cell Biol. 186:739-753. doi:10.1083/jcb.200902116
14. Guertin, D.A., L. Chang, F. Irshad, K.L. Gould, and D. McCollum. 2000. The role of the sid1p kinase and cdc14p in regulating the onset of cytokinesis in fission yeast. EMBO J. 19:1803-1815. doi:10.1093/emboj/19.8.1803
15. Guo, C., S. Tommasi, L. Liu, J.K. Yee, R. Dammann, and G.P. Pfeifer. 2007. RASSF1A is part of a complex similar to the Drosophila Hippo/Salvador/Lats tumor-suppressor network. Curr. Biol. 17:700-705. doi:10.1016/j.cub.2007.02.055
16. Hachet, O., and V. Simanis. 2008. Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev. 22:3205-3216. doi:10.1101/gad.1697208
17. Hao, Y., A. Chun, K. Cheung, B. Rashidi, and X. Yang. 2008. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J. Biol. Chem. 283:5496-5509. doi:10.1074/jbc.M709037200
18. Hergovich, A., S.J. Bichsel, and B.A. Hemmings. 2005. Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. Mol. Cell. Biol. 25:8259-8272. doi:10.1128/MCB.25.18.8259- 8272.2005
19. Hergovich, A., M.R. Stegert, D. Schmitz, and B.A. Hemmings. 2006. NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 7:253-264. doi:10.1038/nrm1891
20. Hergovich, A., H. Cornils, and B.A. Hemmings. 2008. Mammalian NDR protein kinases: from regulation to a role in centrosome duplication. Biochim. Biophys. Acta. 1784:3-15.
21. Hirata, D., N. Kishimoto, M. Suda, Y. Sogabe, S. Nakagawa, Y. Yoshida, K. Sakai, M. Mizunuma, T. Miyakawa, J. Ishiguro, and T. Toda. 2002. Fission yeast Mor2/Cps12, a protein similar to Drosophila Furry, is essential for cell morphogenesis and its mutation induces Wee1-dependent G(2) delay. EMBO J. 21:4863-4874. doi:10.1093/emboj/cdf495
22. Huang, T.Y., N.A. Markley, and D. Young. 2003. Nak1, an essential germinal center (GC) kinase regulates cell morphology and growth in Schizosaccharomyces pombe. J. Biol. Chem. 278:991-997. doi:10.1074/jbc. M208993200
23. Huang, Y., H. Yan, and M.K. Balasubramanian. 2008. Assembly of normal actomyosin rings in the absence of Mid1p and cortical nodes in fission yeast. J. Cell Biol. 183:979-988. doi:10.1083/jcb.200806151
24. Imai, T., S. Shimamura, A. Kurosaka, H. Yamagishi, and T. Terachi. 2004. Cloning and characterization of a novel radish protein kinase which is homologous to fungal cot-I like and animal Ndr protein kinases. Genes Genet. Syst. 79:283-291. doi:10.1266/ggs.79.283
25. Kanai, M., K. Kume, K. Miyahara, K. Sakai, K. Nakamura, K. Leonhard, D.J. Wiley, F. Verde, T. Toda, and D. Hirata. 2005. Fission yeast MO25 protein is localized at SPB and septum and is essential for cell morphogenesis. EMBO J. 24:3012-3025. doi:10.1038/sj.emboj.7600782
26. Krapp, A., and V. Simanis. 2008. An overview of the fission yeast septation initiation network (SIN). Biochem. Soc. Trans. 36:411-415. doi:10.1042/BST0360411
27. Kume, K., T. Goshima, K. Miyahara, T. Toda, and D. Hirata. 2007. A method for Pmo25-associated kinase assay in fission yeast: the activity is dependent on two gC kinases Nak1 and Sid1. Biosci. Biotechnol. Biochem. 71:615-617. doi:10.1271/bbb.60574
28. Le Goff, X., F. Motegi, E. Salimova, I. Mabuchi, and V. Simanis. 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.
29. Leonhard, K., and P. Nurse. 2005. Ste20/GCK kinase Nak1/Orb3 polarizes the actin cytoskeleton in fission yeast during the cell cycle. J. Cell Sci. 118:1033-1044. doi:10.1242/jcs.01690
30. Liu, J., H. Wang, and M.K. Balasubramanian. 2000. A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe. J. Cell Sci. 113:1223-1230.
31. Martin, S.G. 2009. Microtubule-dependent cell morphogenesis in the fission yeast. Trends Cell Biol. 19:447-454. doi:10.1016/j.tcb.2009.06.003
32. Mendoza, M., S. Redemann, and D. Brunner. 2005. The fission yeast MO25 protein functions in polar growth and cell separation. Eur. J. Cell Biol. 84:915-926. doi:10.1016/j.ejcb.2005.09.013
33. Minet, M., P. Nurse, P. Thuriaux, and J.M. Mitchison. 1979. Uncontrolled septation in a cell division cycle mutant of the fission yeast Schizosaccharomyces pombe. J. Bacteriol. 137:440-446.
34. Mishra, M., J. Karagiannis, S. Trautmann, H. Wang, D. McCollum, and M.K. Balasubramanian. 2004. The Clp1p/Flp1p phosphatase ensures completion of cytokinesis in response to minor perturbation of the cell division machinery in Schizosaccharomyces pombe. J. Cell Sci. 117:3897-3910. doi:10.1242/jcs.01244
35. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823. doi:10.1016/0076-6879(91)94059-L
36. Naqvi, N.I., K.C. Wong, X. Tang, and M.K. Balasubramanian. 2000. Type II myosin regulatory light chain relieves auto-inhibition of myosin-heavy-chain function. Nat. Cell Biol. 2:855-858. doi:10.1038/35041107
37. Preisinger, C., B. Short, V. De Corte, E. Bruyneel, A. Haas, R. Kopajtich, J. Gettemans, and F.A. Barr. 2004. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta. J. Cell Biol. 164:1009-1020. doi:10.1083/jcb.200310061
38. Roberts-Galbraith, R.H., and K.L. Gould. 2008. Stepping into the ring: the SIN takes on contractile ring assembly. Genes Dev. 22:3082-3088. doi:10.1101/gad.1748908
39. Schmidt, S., M. Sohrmann, K. Hofmann, A. Woollard, and V. Simanis. 1997. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes Dev. 11:1519-1534. doi:10.1101/gad.11.12. 1519
40. Seidel, C., U. Schagdarsurengin, K. Blümke, P. Würl, G.P. Pfeifer, S. Hauptmann, H. Taubert, and R. Dammann. 2007. Frequent hypermethylation of MST1 and MST2 in soft tissue sarcoma. Mol. Carcinog. 46:865-871. doi:10.1002/mc.20317
41. Simanis, V. 2003. Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116:4263-4275. doi:10.1242/jcs.00807
42. Snell, V., and P. Nurse. 1993. Investigations into the control of cell form and polarity: the use of morphological mutants in fission yeast. Dev. Suppl. 1993:289-299.
43. Sparks, C.A., M. Morphew, and D. McCollum. 1999. Sid2p, a spindle pole body kinase that regulates the onset of cytokinesis. J. Cell Biol. 146:777-790. doi:10.1083/jcb.146.4.777
44. Takahashi, Y., Y. Miyoshi, C. Takahata, N. Irahara, T. Taguchi, Y. Tamaki, and S. Noguchi. 2005. Down-regulation of LATS1 and LATS2 mRNA expression by promoter hypermethylation and its association with biologically aggressive phenotype in human breast cancers. Clin. Cancer Res. 11:1380-1385. doi:10.1158/1078-0432.CCR-04-1773
45. Tamaskovic, R., S.J. Bichsel, and B.A. Hemmings. 2003. NDR family of AGC kinases - essential regulators of the cell cycle and morphogenesis. FEBS Lett. 546:73-80. doi:10.1016/S0014-5793(03)00474-5
46. ten Klooster, J.P., M. Jansen, J. Yuan, V. Oorschot, H. Begthel, V. Di Giacomo, F. Colland, J. de Koning, M.M. Maurice, P. Hornbeck, and H. Clevers. 2009. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell. 16:551-562. doi:10.1016/j.devcel.2009.01.016
47. Trautmann, S., and D. McCollum. 2005. Distinct nuclear and cytoplasmic functions of the S. pombe Cdc14-like phosphatase Clp1p/Flp1p and a role for nuclear shuttling in its regulation. Curr. Biol. 15:1384-1389. doi:10.1016/j.cub.2005.06.039
48. Trautmann, S., B.A. Wolfe, P. Jorgensen, M. Tyers, K.L. Gould, and D. McCollum. 2001. Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression. Curr. Biol. 11:931-940. doi:10.1016/S0960-9822(01)00268-8
49. Verde, F., D.J. Wiley, and P. Nurse. 1998. Fission yeast orb6, a ser/thr protein kinase related to mammalian rho kinase and myotonic dystrophy kinase, is required for maintenance of cell polarity and coordinates cell morphogenesis with the cell cycle. Proc. Natl. Acad. Sci. USA. 95:7526-7531. doi:10.1073/pnas.95.13.7526
50. Vichalkovski, A., E. Gresko, H. Cornils, A. Hergovich, D. Schmitz, and B.A. Hemmings. 2008. NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 18:1889-1895. doi:10.1016/j.cub.2008.10.060
51. Zhang, J., G.A. Smolen, and D.A. Haber. 2008. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res. 68:2789-2794. doi:10.1158/0008-5472.CAN-07-6205