Mechanistic Insights into the Anchorage of the Contractile Ring by Anillin and Mid1

Developmental Cell

Volumn 33, Issue 4, 2015, Pages 413-426

  Sun, Lingfei ^a   Guan, Ruifang ^a   Lee, I Ju ^b   Liu, Yajun ^b   Chen, Mengran ^a   Wang, Jiawei ^a   Wu, Jian Qiu ^b   Chen, Zhucheng ^a  

^a TSINGHUA UNIVERSITY   (China)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANILLIN; MID1 PROTEIN; PHOSPHOLIPID; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; ACTIN-BINDING PROTEIN ANILLIN, HUMAN; MID1 PROTEIN, S POMBE;

ANILLIN HOMOLOGY DOMAIN; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINESIS; DIMERIZATION; FEMALE; HUMAN; HUMAN CELL; MEMBRANE BINDING; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; ACTIN FILAMENT; AMINO ACID SEQUENCE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANIMALIA; FUNGI;

ACTIN CYTOSKELETON; AMINO ACID SEQUENCE; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; CYTOKINESIS; HUMANS; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; PROTEIN STRUCTURE, TERTIARY; RHOA GTP-BINDING PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84929963996     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.03.003     Document Type: Article

References (58)

1. Akamatsu M., Berro J., Pu K.M., Tebbs I.R., Pollard T.D. Cytokinetic nodes in fission yeast arise from two distinct types of nodes that merge during interphase. J.Cell Biol. 2014, 204:977-988.
2. Almonacid M., Moseley J.B., Janvore J., Mayeux A., Fraisier V., Nurse P., Paoletti A. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr. Biol. 2009, 19:961-966.
3. Almonacid M., Celton-Morizur S., Jakubowski J.L., Dingli F., Loew D., Mayeux A., Chen J.S., Gould K.L., Clifford D.M., Paoletti A. Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin. Curr. Biol. 2011, 21:473-479.
4. Arasada R., Pollard T.D. Contractile ring stability in S. pombe depends on F-BAR protein Cdc15p and Bgs1p transport from the Golgi complex. Cell Rep. 2014, 8:1533-1544.
5. Barr F.A., Gruneberg U. Cytokinesis: placing and making the final cut. Cell 2007, 131:847-860.
6. Celton-Morizur S., Bordes N., Fraisier V., Tran P.T., Paoletti A. C-terminal anchoring of mid1p to membranes stabilizes cytokinetic ring position in early mitosis in fission yeast. Mol. Cell. Biol. 2004, 24:10621-10635.
7. Chang F., Woollard A., Nurse P. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J.Cell Sci. 1996, 109:131-142.
8. Chant J., Herskowitz I. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 1991, 65:1203-1212.
9. Cho W., Stahelin R.V. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 2006, 1761:838-849.
10. D'Avino P.P. How to scaffold the contractile ring for a safe cytokinesis - lessons from Anillin-related proteins. J.Cell Sci. 2009, 122:1071-1079.
11. D'Avino P.P., Takeda T., Capalbo L., Zhang W., Lilley K.S., Laue E.D., Glover D.M. Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J.Cell Sci. 2008, 121:1151-1158.
12. El Amine N., Kechad A., Jananji S., Hickson G.R. Opposing actions of septins and Sticky on Anillin promote the transition from contractile to midbody ring. J.Cell Biol. 2013, 203:487-504.
13. Field C.M., Alberts B.M. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J.Cell Biol. 1995, 131:165-178.
14. Field S.J., Madson N., Kerr M.L., Galbraith K.A., Kennedy C.E., Tahiliani M., Wilkins A., Cantley L.C. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr. Biol. 2005, 15:1407-1412.
15. Fotopoulos N., Wernike D., Chen Y., Makil N., Marte A., Piekny A. Caenorhabditis elegans anillin (ani-1) regulates neuroblast cytokinesis and epidermal morphogenesis during embryonic development. Dev. Biol. 2013, 383:61-74.
16. Gbadegesin R.A., Hall G., Adeyemo A., Hanke N., Tossidou I., Burchette J., Wu G., Homstad A., Sparks M.A., Gomez J., et al. Mutations in the gene that encodes the F-actin binding protein anillin cause FSGS. J.Am. Soc. Nephrol. 2014, 25:1991-2002.
17. Glotzer M. The molecular requirements for cytokinesis. Science 2005, 307:1735-1739.
18. Hickson G.R., O'Farrell P.H. Rho-dependent control of anillin behavior during cytokinesis. J.Cell Biol. 2008, 180:285-294.
19. Holm L., Kaariainen S., Rosenstrom P., Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 2008, 24:2780-2781.
20. Justa-Schuch D., Heilig Y., Richthammer C., Seiler S. Septum formation is regulated by the RHO4-specific exchange factors BUD3 and RGF3 and by the landmark protein BUD4 in Neurospora crassa. Mol. Microbiol. 2010, 76:220-235.
21. Kechad A., Jananji S., Ruella Y., Hickson G.R. Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr. Biol. 2012, 22:197-203.
22. Kinoshita M., Field C.M., Coughlin M.L., Straight A.F., Mitchison T.J. Self- and actin-templated assembly of Mammalian septins. Dev. Cell 2002, 3:791-802.
23. Laporte D., Zhao R., Wu J.-Q. Mechanisms of contractile-ring assembly in fission yeast and beyond. Semin. Cell Dev. Biol. 2010, 21:892-898.
24. Laporte D., Coffman V.C., Lee I.-J., Wu J.-Q. Assembly and architecture of precursor nodes during fission yeast cytokinesis. J.Cell Biol. 2011, 192:1005-1021.
25. Lee I.-J., Wu J.-Q. Characterization of Mid1 domains for targeting and scaffolding in fission yeast cytokinesis. J.Cell Sci. 2012, 125:2973-2985.
26. Lee J.O., Yang H., Georgescu M.M., Di Cristofano A., Maehama T., Shi Y., Dixon J.E., Pandolfi P., Pavletich N.P. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999, 99:323-334.
27. Lee I.-J., Coffman V.C., Wu J.-Q. Contractile-ring assembly infission yeast cytokinesis: Recent advances and new perspectives. Cytoskeleton 2012, 69:751-763.
28. Liu J., Fairn G.D., Ceccarelli D.F., Sicheri F., Wilde A. Cleavage furrow organization requires PIP(2)-mediated recruitment of anillin. Curr. Biol. 2012, 22:64-69.
29. Martin S.G., Berthelot-Grosjean M. Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 2009, 459:852-856.
30. Moseley J.B., Mayeux A., Paoletti A., Nurse P. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 2009, 459:857-860.
31. Nalefski E.A., Falke J.J. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 1996, 5:2375-2390.
32. Oegema K., Savoian M.S., Mitchison T.J., Field C.M. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J.Cell Biol. 2000, 150:539-552.
33. Padmanabhan A., Bakka K., Sevugan M., Naqvi N.I., D'souza V., Tang X., Mishra M., Balasubramanian M.K. IQGAP-related Rng2p organizes cortical nodes and ensures position of cell division in fission yeast. Curr. Biol. 2011, 21:467-472.
34. Paoletti A., Chang F. 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 2000, 11:2757-2773.
35. Piekny A.J., Glotzer M. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 2008, 18:30-36.
36. Piekny A.J., Maddox A.S. The myriad roles of Anillin during cytokinesis. Semin. Cell Dev. Biol. 2010, 21:881-891.
37. Pollard T.D., Wu J.-Q. Understanding cytokinesis: lessons from fission yeast. Nat. Rev. Mol. Cell Biol. 2010, 11:149-155.
38. Reyes C.C., Jin M., Breznau E.B., Espino R., Delgado-Gonzalo R., Goryachev A.B., Miller A.L. Anillin regulates cell-cell junction integrity by organizing junctional accumulation of Rho-GTP and actomyosin. Curr. Biol. 2014, 24:1263-1270.
39. Rincon S.A., Paoletti A. Mid1/anillin and the spatial regulation of cytokinesis in fission yeast. Cytoskeleton 2012, 69:764-777.
40. Rincon S.A., Bhatia P., Bicho C., Guzman-Vendrell M., Fraisier V., Borek W.E., Alves Fde.L., Dingli F., Loew D., Rappsilber J., et al. Pom1 regulates the assembly of Cdr2-Mid1 cortical nodes for robust spatial control of cytokinesis. J.Cell Biol. 2014, 206:61-77.
41. Saha S., Pollard T.D. Anillin-related protein Mid1p coordinates the assembly of the cytokinetic contractile ring in fission yeast. Mol. Biol. Cell 2012, 23:3982-3992.
42. Saha S., Pollard T.D. Characterization of structural and functional domains of the anillin-related protein Mid1p that contribute to cytokinesis in fission yeast. Mol. Biol. Cell 2012, 23:3993-4007.
43. Sawyer G.M., Clark A.R., Robertson S.P., Sutherland-Smith A.J. Disease-associated substitutions in the filamin B actin binding domain confer enhanced actin binding affinity in the absence of major structural disturbance: Insights from the crystal structures of filamin B actin binding domains. J.Mol. Biol. 2009, 390:1030-1047.
44. Sedzinski J., Biro M., Oswald A., Tinevez J.Y., Salbreux G., Paluch E. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 2011, 476:462-466.
45. Shannon K.B. IQGAP family members in yeast, dictyostelium, and mammalian cells. Int. J. Cell Biol. 2012, 2012:894817.
46. Si H., Rittenour W.R., Xu K., Nicksarlian M., Calvo A.M., Harris S.D. Morphogenetic and developmental functions of the Aspergillus nidulans homologues of the yeast bud site selection proteins Bud4 and Axl2. Mol. Microbiol. 2012, 85:252-270.
47. Sohrmann M., Fankhauser C., Brodbeck C., Simanis V. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev. 1996, 10:2707-2719.
48. Straight A.F., Field C.M., Mitchison T.J. Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol. Biol. Cell 2005, 16:193-201.
49. Su K.C., Takaki T., Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell 2011, 21:1104-1115.
50. Suzuki C., Daigo Y., Ishikawa N., Kato T., Hayama S., Ito T., Tsuchiya E., Nakamura Y. ANLN plays a critical role in human lung carcinogenesis through the activation of RHOA and by involvement in the phosphoinositide 3-kinase/AKT pathway. Cancer Res. 2005, 65:11314-11325.
51. Tatsumoto T., Xie X., Blumenthal R., Okamoto I., Miki T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J.Cell Biol. 1999, 147:921-928.
52. Watanabe S., Okawa K., Miki T., Sakamoto S., Morinaga T., Segawa K., Arakawa T., Kinoshita M., Ishizaki T., Narumiya S. Rho and anillin-dependent control of mDia2 localization and function in cytokinesis. Mol. Biol. Cell 2010, 21:3193-3204.
53. White E.A., Glotzer M. Centralspindlin: at the heart of cytokinesis. Cytoskeleton 2012, 69:882-892.
54. Ye Y., Lee I.-J., Runge K.W., Wu J.-Q. Roles of putative Rho-GEF Gef2 in division-site positioning and contractile-ring function in fission yeast cytokinesis. Mol. Biol. Cell 2012, 23:1181-1195.
55. Yüce O., Piekny A., Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J.Cell Biol. 2005, 170:571-582.
56. Zhang Y., Sugiura R., Lu Y., Asami M., Maeda T., Itoh T., Takenawa T., Shuntoh H., Kuno T. Phosphatidylinositol 4-phosphate 5-kinase Its3 and calcineurin Ppb1 coordinately regulate cytokinesis in fission yeast. J.Biol. Chem. 2000, 275:35600-35606.
57. Zhao W.M., Fang G. Anillin is a substrate of anaphase-promoting complex/cyclosome (APC/C) that controls spatial contractility of myosin during late cytokinesis. J.Biol. Chem. 2005, 280:33516-33524.
58. Zhu Y.H., Ye Y., Wu Z., Wu J.-Q. Cooperation between Rho-GEF Gef2 and its binding partner Nod1 in the regulation of fission yeast cytokinesis. Mol. Biol. Cell 2013, 24:3187-3204.