Actin filament severing by cofilin is more important for assembly than constriction of the cytokinetic contractile ring

Journal of Cell Biology

Volumn 195, Issue 3, 2011, Pages 485-498

  Chen, Qian ^a   Pollard, Thomas D ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; ALPHA ACTININ; COFILIN; MONOMER; MUTANT PROTEIN; ACTIN DEPOLYMERIZING FACTOR; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOKINESIS; FUNGUS MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIMULATION; WILD TYPE; BINDING SITE; CHEMISTRY; COMPUTER SIMULATION; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCETACEAE;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; BINDING SITES; COMPUTER SIMULATION; CYTOKINESIS; MICROSCOPY, FLUORESCENCE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84855751562     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201103067     Document Type: Article

References (54)

1. Abe, H., T. Obinata, L.S. Minamide, and J.R. Bamburg. 1996. Xenopus laevis actin-depolymerizing factor/cofilin: a phosphorylation-regulated protein essential for development. J. Cell Biol. 132:871-885. http://dx.doi.org/10.1083/jcb.132.5.871
2. Andrianantoandro, E., and T.D. Pollard. 2006. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell. 24:13-23. http://dx.doi.org/10.1016/j.molcel.2006.08.006
3. Bähler, J., A.B. Steever, S. Wheatley, Y. Wang, J.R. Pringle, K.L. Gould, and D. McCollum. 1998. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J. Cell Biol. 143:1603-1616. http://dx.doi.org/10.1083/jcb.143.6.1603
4. Bamburg, J.R., H.E. Harris, and A.G. Weeds. 1980. Partial purification and characterization of an actin depolymerizing factor from brain. FEBS Lett. 121:178-182. http://dx.doi.org/10.1016/0014-5793(80)81292-0
5. Bathe, M., and F. Chang. 2010. Cytokinesis and the contractile ring in fission yeast: towards a systems-level understanding. Trends Microbiol. 18:38-45. http://dx.doi.org/10.1016/j.tim.2009.10.002
6. Bryan, J. 1988. Gelsolin has three actin-binding sites. J. Cell Biol. 106:1553-1562. http://dx.doi.org/10.1083/jcb.106.5.1553
7. Carlier, M.F., V. Laurent, J. Santolini, R. Melki, D. Didry, G.X. Xia, Y. Hong, N.H. Chua, and D. Pantaloni. 1997. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136:1307-1322. http://dx.doi.org/10.1083/jcb.136.6.1307
8. Carter, S.B. 1967. Effects of cytochalasins on mammalian cells. Nature. 213: 261-264. http://dx.doi.org/10.1038/213261a0
9. Chan, C., C.C. Beltzner, and T.D. Pollard. 2009. Cofilin dissociates Arp2/3 complex and branches from actin filaments. Curr. Biol. 19:537-545. http://dx.doi.org/10.1016/j.cub.2009.02.060
10. Chang, F., D. Drubin, and P. Nurse. 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. http://dx.doi.org/10.1083/jcb.137.1.169
11. Coffman, V.C., A.H. Nile, I.J. Lee, H. Liu, and J.Q. Wu. 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. http://dx.doi.org/10.1091/mbc.E09-05-0428
12. D'Avino, P.P., M.S. Savoian, and D.M. Glover. 2004. Mutations in sticky lead to defective organization of the contractile ring during cytokinesis and are enhanced by Rho and suppressed by Rac. J. Cell Biol. 166:61-71. http://dx.doi.org/10.1083/jcb.200402157
13. De La Cruz, E.M. 2005. Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. J. Mol. Biol. 346: 557-564. http://dx.doi.org/10.1016/j.jmb.2004.11.065
14. Giansanti, M.G., S. Bonaccorsi, and M. Gatti. 1999. The role of anillin in meiotic cytokinesis of Drosophila males. J. Cell Sci. 112:2323-2334.
15. Gunsalus, K.C., S. Bonaccorsi, E. Williams, F. Verni, M. Gatti, and M.L. Goldberg. 1995. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131:1243-1259. http://dx.doi.org/10.1083/jcb.131.5.1243
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. http://dx.doi.org/10.1101/gad.1697208
17. Hawkins, M., B. Pope, S.K. Maciver, and A.G. Weeds. 1993. Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry. 32:9985-9993. http://dx.doi.org/10.1021/bi00089a014
18. 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. http://dx.doi.org/10.1083/jcb.200806151
19. Jantsch-Plunger, V., P. Gönczy, A. Romano, H. Schnabel, D. Hamill, R. Schnabel, A.A. Hyman, and M. Glotzer. 2000. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149:1391-1404. http://dx.doi.org/10.1083/jcb.149.7.1391
20. Kaji, N., K. Ohashi, M. Shuin, R. Niwa, T. Uemura, and K. Mizuno. 2003. Cell cycle-associated changes in Slingshot phosphatase activity and roles in cytokinesis in animal cells. J. Biol. Chem. 278:33450-33455. http://dx.doi.org/10.1074/jbc.M305802200
21. Kowalczykowski, S.C., L.S. Paul, N. Lonberg, J.W. Newport, J.A. McSwiggen, and P.H. von Hippel. 1986. Cooperative and noncooperative binding of protein ligands to nucleic acid lattices: experimental approaches to the determination of thermodynamic parameters. Biochemistry. 25:1226-1240. http://dx.doi.org/10.1021/bi00354a006
22. Kuhn, J.R., and T.D. Pollard. 2005. Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys. J. 88:1387-1402. http://dx.doi.org/10.1529/biophysj.104.047399
23. Lappalainen, P., and D.G. Drubin. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature. 388:78-82. http://dx.doi.org/10.1038/40418
24. Lappalainen, P., E.V. Fedorov, A.A. Fedorov, S.C. Almo, and D.G. Drubin. 1997. Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J. 16:5520-5530. http://dx.doi.org/10.1093/emboj/16.18.5520
25. Le Goff, X., A. Woollard, and V. Simanis. 1999. Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe. Mol. Gen. Genet. 262:163-172. http://dx.doi.org/10.1007/s004380051071
26. Liu, J., H. Wang, and M.K. Balasubramanian. 2000. A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe. J. Cell Sci. 113:1223-1230.
27. Maciver, S.K., D.H. Wachsstock, W.H. Schwarz, and T.D. Pollard. 1991. The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with alpha-actinin. J. Cell Biol. 115:1621-1628. http://dx.doi.org/10.1083/jcb.115.6.1621
28. Mackay, A.M., A.M. Ainsztein, D.M. Eckley, and W.C. Earnshaw. 1998. A dominant mutant of inner centromere protein (INCENP), a chromosomal protein, disrupts prometaphase congression and cytokinesis. J. Cell Biol. 140:991-1002. http://dx.doi.org/10.1083/jcb.140.5.991
29. MacLean-Fletcher, S.D., and T.D. Pollard. 1980. Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors. J. Cell Biol. 85:414-428. http://dx.doi.org/10.1083/jcb.85.2.414
30. McGhee, J.D., and P.H. von Hippel. 1974. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J. Mol. Biol. 86:469-489. http://dx.doi.org/10.1016/0022-2836(74)90031-X
31. Michelot, A., J. Berro, C. Guérin, R. Boujemaa-Paterski, C.J. Staiger, J.L. Martiel, and L. Blanchoin. 2007. Actin-filament stochastic dynamics mediated by ADF/cofilin. Curr. Biol. 17:825-833. http://dx.doi.org/10.1016/j.cub.2007.04.037
32. Mishra, M., and S. Oliferenko. 2008. Cytokinesis: catch and drag. Curr. Biol. 18:R247-R250. http://dx.doi.org/10.1016/j.cub.2008.01.029
33. Moriyama, K., and I. Yahara. 1999. Two activities of cofilin, severing and accelerating directional depolymerization of actin filaments, are affected differentially by mutations around the actin-binding helix. EMBO J. 18:6752-6761. http://dx.doi.org/10.1093/emboj/18.23.6752
34. Nagaoka, R., H. Abe, K. Kusano, and T. Obinata. 1995. Concentration of cofilin, a small actin-binding protein, at the cleavage furrow during cytokinesis. Cell Motil. Cytoskeleton. 30:1-7. http://dx.doi.org/10.1002/cm.970300102
35. Nakano, K., and I. Mabuchi. 2006. Actin-depolymerizing protein Adf1 is required for formation and maintenance of the contractile ring during cytokinesis in fission yeast. Mol. Biol. Cell. 17:1933-1945. http://dx.doi.org/10.1091/mbc.E05-09-0900
36. Nishida, E., S. Maekawa, and H. Sakai. 1984. Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interactions with myosin and tropomyosin. Biochemistry. 23:5307-5313. http://dx.doi.org/10.1021/bi00317a032
37. Okreglak, V., and D.G. Drubin. 2007. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J. Cell Biol. 178:1251-1264. http://dx.doi.org/10.1083/jcb.200703092
38. Ono, K., M. Parast, C. Alberico, G.M. Benian, and S. Ono. 2003. Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci. 116:2073-2085. http://dx.doi.org/10.1242/jcs.00421
39. Paavilainen, V.O., E. Oksanen, A. Goldman, and P. Lappalainen. 2008. Structure of the actin-depolymerizing factor homology domain in complex with actin. J. Cell Biol. 182:51-59. http://dx.doi.org/10.1083/jcb.200803100
40. Pace, C.N. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:266-280. http://dx.doi.org/10.1016/0076-6879(86)31045-0
41. Pavlov, D., A. Muhlrad, J. Cooper, M. Wear, and E. Reisler. 2007. Actin filament severing by cofilin. J. Mol. Biol. 365:1350-1358. http://dx.doi.org/10.1016/j.jmb.2006.10.102
42. Pelham, R.J., and F. Chang. 2002. Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature. 419:82-86. http://dx.doi.org/10.1038/nature00999
43. Pollard, T.D. 1984. Polymerization of ADP-actin. J. Cell Biol. 99:769-777. http://dx.doi.org/10.1083/jcb.99.3.769
44. Pollard, T.D., and J.Q. Wu. 2010. Understanding cytokinesis: lessons from fission yeast. Nat. Rev. Mol. Cell Biol. 11:149-155. http://dx.doi.org/10.1038/nrm2834
45. Powers, J., O. Bossinger, D. Rose, S. Strome, and W. Saxton. 1998. A nematode kinesin required for cleavage furrow advancement. Curr. Biol. 8:1133-1136. http://dx.doi.org/10.1016/S0960-9822(98)70470-1
46. Rodal, A.A., J.W. Tetreault, P. Lappalainen, D.G. Drubin, and D.C. Amberg. 1999. Aip1p interacts with cofilin to disassemble actin filaments. J. Cell Biol. 145:1251-1264. http://dx.doi.org/10.1083/jcb.145.6.1251
47. Schumacher, J.M., A. Golden, and P.J. Donovan. 1998. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J. Cell Biol. 143:1635-1646. http://dx.doi.org/10.1083/jcb.143.6.1635
48. Somma, M.P., B. Fasulo, G. Cenci, E. Cundari, and M. Gatti. 2002. Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells. Mol. Biol. Cell. 13:2448-2460. http://dx.doi.org/10.1091/mbc.01-12-0589
49. Toda, T., M. Shimanuki, and M. Yanagida. 1993. Two novel protein kinase C-related genes of fission yeast are essential for cell viability and implicated in cell shape control. EMBO J. 12:1987-1995.
50. Toda, T., H. Niwa, T. Nemoto, S. Dhut, M. Eddison, T. Matsusaka, M. Yanagida, and D. Hirata. 1996. The fission yeast sts5+ gene is required for maintenance of growth polarity and functionally interacts with protein kinase C and an osmosensing MAP-kinase pathway. J. Cell Sci. 109:2331-2342.
51. Vavylonis, D., J.Q. Wu, S. Hao, B. O'Shaughnessy, and T.D. Pollard. 2008. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science. 319:97-100. http://dx.doi.org/10.1126/science.1151086
52. Wu, J.Q., J. Bähler, and J.R. Pringle. 2001. Roles of a fimbrin and an alphaactinin-like protein in fission yeast cell polarization and cytokinesis. Mol. Biol. Cell. 12:1061-1077.
53. Wu, J.Q., J.R. Kuhn, D.R. Kovar, and T.D. Pollard. 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell. 5:723-734. http://dx.doi.org/10.1016/S1534-5807(03)00324-1
54. Wu, J.Q., V. Sirotkin, D.R. Kovar, M. Lord, C.C. Beltzner, J.R. Kuhn, and T.D. Pollard. 2006. Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 174:391-402. http://dx.doi.org/10.1083/jcb.200602032