Characterization of Mid1 domains for targeting and scaffolding in fission yeast cytokinesis

Journal of Cell Science

Volumn 125, Issue 12, 2012, Pages 2973-2985

  Lee, I Ju ^a   Wu, Jian Qiu ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Anillin; Cdr2; Contractile ring; Mid1; Node; PH domain; Pom1

Indexed keywords

PROTEIN; PROTEIN MID1; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL DIVISION; CYTOKINESIS; INTERPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE; YEAST;

CYTOKINESIS; NUCLEAR MATRIX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCETACEAE;

EID: 84859409970     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.102574     Document Type: Article

References (60)

1. Almonacid, M., Moseley, J. B., Janvore, J., Mayeux, A., Fraisier, V., Nurse, P. and Paoletti, A. (2009). Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr. Biol. 19, 961-966.
2. Almonacid, M., Celton-Morizur, S., Jakubowski, J. L., Dingli, F., Loew, D., Mayeux, A., Chen, J. S., Gould, K. L., Clifford, D. M. and Paoletti, A. (2011). Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin. Curr. Biol. 21, 473-479.
3. Bähler, J. and Pringle, J. R. (1998). Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes Dev. 12, 1356-1370.
4. Bähler, J., Steever, A. B., Wheatley, S., Wang, Y., Pringle, J. R., Gould, K. L. and McCollum, D. (1998a). Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J. Cell Biol. 143, 1603-1616.
5. 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. (1998b). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
6. Balasubramanian, M. K., Bi, E. and Glotzer, M. (2004). Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14, R806-R818.
7. Barr, F. A. and Gruneberg, U. (2007). Cytokinesis: placing and making the final cut. Cell 131, 847-860.
8. Bathe, M. and Chang, F. (2010). Cytokinesis and the contractile ring in fission yeast: towards a systems-level understanding. Trends Microbiol. 18, 38-45.
9. Berlin, A., Paoletti, A. and Chang, F. (2003). Mid2p stabilizes septin rings during cytokinesis in fission yeast. J. Cell Biol. 160, 1083-1092.
10. Celton-Morizur, S., Bordes, N., Fraisier, V., Tran, P. T. and Paoletti, A. (2004). Cterminal anchoring of mid1p to membranes stabilizes cytokinetic ring position in early mitosis in fission yeast. Mol. Cell. Biol. 24, 10621-10635.
11. Celton-Morizur, S., Racine, V., Sibarita, J. B. and Paoletti, A. (2006). Pom1 kinase links division plane position to cell polarity by regulating Mid1p cortical distribution. J. Cell Sci. 119, 4710-4718.
12. Clifford, D. M., Wolfe, B. A., Roberts-Galbraith, R. H., McDonald, W. H., Yates, J. R., 3rd, and Gould, K. L. (2008). The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J. Cell Biol. 181, 79-88.
13. Coffman, V. C., Nile, A. H., Lee, I-J., Liu, H. and Wu, J.-Q. (2009). Roles of formin nodes and myosin motor activity in Mid1p-dependent contractile-ring assembly during fission yeast cytokinesis. Mol. Biol. Cell 20, 5195-5210.
14. Coffman, V. C., Wu, P., Parthun, M. R. and Wu, J.-Q. (2011). CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J. Cell Biol. 195, 563-572.
15. D'Avino, P. P. (2009). How to scaffold the contractile ring for a safe cytokinesis -lessons from Anillin-related proteins. J. Cell Sci. 122, 1071-1079.
16. D'Avino, P. P., Takeda, T., Capalbo, L., Zhang, W., Lilley, K. S., Laue, E. D. and Glover, D. M. (2008). Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J. Cell Sci. 121, 1151-1158.
17. Daga, R. R. and Chang, F. (2005). Dynamic positioning of the fission yeast cell division plane. Proc. Natl. Acad. Sci. USA 102, 8228-8232.
18. Field, C. M. and Alberts, B. M. (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165-178.
19. Field, C. M., Coughlin, M., Doberstein, S., Marty, T. and Sullivan, W. (2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 132, 2849-2860.
20. Goldbach, P., Wong, R., Beise, N., Sarpal, R., Trimble, W. S. and Brill, J. A. (2010). Stabilization of the actomyosin ring enables spermatocyte cytokinesis in Drosophila. Mol. Biol. Cell 21, 1482-1493.
21. Goyal, A., Takaine, M., Simanis, V. and Nakano, K. (2011). Dividing the spoils of growth and the cell cycle: The fission yeast as a model for the study of cytokinesis. Cytoskeleton (Hoboken) 68, 69-88.
22. Gregory, S. L., Ebrahimi, S., Milverton, J., Jones, W. M., Bejsovec, A. and Saint, R. (2008). Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr. Biol. 18, 25-29.
23. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. and Tsien, R. Y. (2001). Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194.
24. Haglund, K., Nezis, I. P., Lemus, D., Grabbe, C., Wesche, J., Liestøl, K., Dikic, I., Palmer, R. and Stenmark, H. (2010). Cindr interacts with anillin to control cytokinesis in Drosophila melanogaster. Curr. Biol. 20, 944-950.
25. Hickson, G. R. and O'Farrell, P. H. (2008). Anillin: a pivotal organizer of the cytokinetic machinery. Biochem. Soc. Trans. 36, 439-441.
26. Jin, Q.-W., Ray, S., Choi, S. H. and McCollum, D. (2007). The nucleolar Net1/Cfi1-related protein Dnt1 antagonizes the septation initiation network in fission yeast. Mol. Biol. Cell 18, 2924-2934.
27. Kavran, J. M., Klein, D. E., Lee, A., Falasca, M., Isakoff, S. J., Skolnik, E. Y. and Lemmon, M. A. (1998). Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273, 30497-30508.
28. Kinoshita, M., Field, C. M., Coughlin, M. L., Straight, A. F. and Mitchison, T. J. (2002). Self- and actin-templated assembly of Mammalian septins. Dev. Cell 3, 791-802.
29. Laporte, D., Zhao, R. and Wu, J.-Q. (2010). Mechanisms of contractile-ring assembly in fission yeast and beyond. Semin. Cell Dev. Biol. 21, 892-898.
30. Laporte, D., Coffman, V. C., Lee, I-J. and Wu, J.-Q. (2011). Assembly and architecture of precursor nodes during fission yeast cytokinesis. J. Cell Biol. 192, 1005-1021.
31. Macia, E., Paris, S. and Chabre, M. (2000). Binding of the PH and polybasic Cterminal domains of ARNO to phosphoinositides and to acidic lipids. Biochemistry 39, 5893-5901.
32. Maddox, A. S., Habermann, B., Desai, A. and Oegema, K. (2005). Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132, 2837-2848.
33. Martin, S. G. and Berthelot-Grosjean, M. (2009). Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459, 852-856.
34. Miller, K. G., Field, C. M. and Alberts, B. M. (1989). Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatography. J. Cell Biol. 109, 2963-2975.
35. Mitra, P., Zhang, Y., Rameh, L. E., Ivshina, M. P., McCollum, D., Nunnari, J. J., Hendricks, G. M., Kerr, M. L., Field, S. J., Cantley, L. C. et al. (2004). A novel phosphatidylinositol(3,4,5)P3 pathway in fission yeast. J. Cell Biol. 166, 205-211.
36. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
37. Moseley, J. B., Mayeux, A., Paoletti, A. and Nurse, P. (2009). A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459, 857-860.
38. 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.
39. Oegema, K., Savoian, M. S., Mitchison, T. J. and Field, C. M. (2000). Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J. Cell Biol. 150, 539-552.
40. Padmanabhan, A., Bakka, K., Sevugan, M., Naqvi, N. I., D'souza, V., Tang, X., Mishra, M. and Balasubramanian, M. K. (2011). IQGAP-related Rng2p organizes cortical nodes and ensures position of cell division in fission yeast. Curr. Biol. 21, 467-472.
41. Padte, N. N., Martin, S. G., Howard, M. and Chang, F. (2006). The cell-end factor pom1p inhibits mid1p in specification of the cell division plane in fission yeast. Curr. Biol. 16, 2480-2487.
42. Paoletti, A. and Chang, F. (2000). Analysis of mid1p, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast. Mol. Biol. Cell 11, 2757-2773.
43. Piekny, A. J. and Glotzer, M. (2008). Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 18, 30-36.
44. Piekny, A. J. and Maddox, A. S. (2010). The myriad roles of Anillin during cytokinesis. Semin. Cell Dev. Biol. 21, 881-891.
45. Pollard, T. D. and Wu, J.-Q. (2010). Understanding cytokinesis: lessons from fission yeast. Nat. Rev. Mol. Cell Biol. 11, 149-155.
46. Silverman-Gavrila, R. V., Hales, K. G. and Wilde, A. (2008). Anillin-mediated targeting of peanut to pseudocleavage furrows is regulated by the GTPase Ran. Mol. Biol. Cell 19, 3735-3744.
47. Sohrmann, M., Fankhauser, C., Brodbeck, C. and Simanis, V. (1996). The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev. 10, 2707-2719.
48. Straight, A. F., Field, C. M. and Mitchison, T. J. (2005). Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol. Biol. Cell 16, 193-201.
49. Tasto, J. J., Morrell, J. L. and Gould, K. L. (2003). An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J. Cell Biol. 160, 1093-1103.
50. Watanabe, S., Okawa, K., Miki, T., Sakamoto, S., Morinaga, T., Segawa, K., Arakawa, T., Kinoshita, M., Ishizaki, T. and Narumiya, S. (2010). Rho and anillindependent control of mDia2 localization and function in cytokinesis. Mol. Biol. Cell 21, 3193-3204.
51. Watt, S., Mata, J., López-Maury, L., Marguerat, S., Burns, G. and Bähler, J. (2008). urg1: a uracil-regulatable promoter system for fission yeast with short induction and repression times. PLoS ONE 3, e1428.
52. Woods, A., Sherwin, T., Sasse, R., MacRae, T. H., Baines, A. J. and Gull, K. (1989). Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93, 491-500.
53. Wu, J.-Q. and Pollard, T. D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
54. 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. Dev. Cell 5, 723-734.
55. Wu, J.-Q., Sirotkin, V., Kovar, D. R., Lord, M., Beltzner, C. 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.
56. Wu, J.-Q., McCormick, C. D. and Pollard, T. D. (2008). Counting proteins in living cells by quantitative fluorescence microscopy with internal standards. In Biophysical Tools for Biologists, Volume Two. In Vivo Techniques (Methods in Cell Biology. Vol. 89) (ed J. J. Correia and H. W. Detrich, 3rd), pp. 253-273. Maryland Heights, MO, USA: Elsevier.
57. Wu, P., Zhao, R., Ye, Y. and Wu, J.-Q. (2011). Roles of the DYRK kinase Pom2 in cytokinesis, mitochondrial morphology, and sporulation in fission yeast. PLoS ONE 6, e28000.
58. Ye, Y., Lee, I-J., Runge, K. W. and Wu, J.-Q. (2012). Roles of putative Rho-GEF Gef2 in division-site positioning and contractile-ring function in fission yeast cytokinesis. Mol. Biol. Cell 23, 1181-1195.
59. Yu, J. W., Mendrola, J. M., Audhya, A., Singh, S., Keleti, D., DeWald, D. B., Murray, D., Emr, S. D. and Lemmon, M. A. (2004). Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol. Cell 13, 677-688.
60. Zhang, D., Vjestica, A. and Oliferenko, S. (2010). The cortical ER network limits the permissive zone for actomyosin ring assembly. Curr. Biol. 20, 1029-1034.