Supervillin binding to myosin II and synergism with anillin are required for cytokinesis

Molecular Biology of the Cell

Volumn 24, Issue 23, 2013, Pages 3603-3619

  Smith, Tara C ^a   Fridy, Peter C ^b   Li, Yinyin ^b   Basil, Shruti ^a,c   Arjun, Sneha ^a,d   Friesen, Ryan M ^a,e   Leszyk, John ^a   Chait, Brian T ^b   Rout, Michael P ^b   Luna, Elizabeth J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF NEW ENGLAND   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e Providence Alaska Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; MYOSIN HEAVY CHAIN; MYOSIN II; MYOSIN LIGHT CHAIN KINASE; NANOBODY; SUPERVILLIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BINDING SITE; CELL DIVISION; CONTROLLED STUDY; CYTOKINESIS; HUMAN; HUMAN CELL; MUTAGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEOMICS; SPINDLE CELL;

AMINO ACID SEQUENCE; BINDING SITES; CONTRACTILE PROTEINS; CYTOKINESIS; CYTOSKELETON; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MUTAGENESIS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN KINASE; POINT MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 84889008473     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-10-0714     Document Type: Article

References (79)

1. Ahmed SM, Theriault BL, Uppalapati M, Chiu CW, Gallie BL, Sidhu SS, Angers S (2012). KIF14 negatively regulates Rap1a-Radil signaling during breast cancer progression. J Cell Biol 199, 951-967.
2. Archer SK, Claudianos C, Campbell HD (2005). Evolution of the gelsolin family of actin-binding proteins as novel transcriptional coactivators. Bioessays 27, 388-396.
3. Arora PD, Wang Y, Bresnick A, Dawson J, Janmey PA, McCulloch CA (2013). Collagen remodeling by phagocytosis is determined by collagen substrate topology and calcium-dependent interactions of gelsolin with nonmuscle myosin IIA in cell adhesions. Mol Biol Cell 24, 734-747.
4. Avanzi MP, Chen A, He W, Mitchell WB (2012). Optimizing megakaryocyte polyploidization by targeting multiple pathways of cytokinesis. Transfusion 52, 2406-2413.
5. Bhuwania R, Cornfine S, Fang Z, Kruger M, Luna EJ, Linder S (2012). Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J Cell Sci 125, 2300-2314.
6. Carleton M, Mao M, Biery M, Warrener P, Kim S, Buser C, Marshall CG, Fernandes C, Annis J, Linsley PS (2006). RNA interference-mediated silencing of mitotic kinesin KIF14 disrupts cell cycle progression and induces cytokinesis failure. Mol Cell Biol 26, 3853-3863.
7. Chalamalasetty RB, Hummer S, Nigg EA, Sillje HH (2006). Influence of human Ect2 depletion and overexpression on cleavage furrow formation and abscission. J Cell Sci 119, 3008-3019.
8. Chen Y, Takizawa N, Crowley JL, Oh SW, Gatto CL, Kambara T, Sato O, Li X, Ikebe M, Luna EJ (2003). F-actin and myosin II binding domains in supervillin. J Biol Chem 278, 46094-46106.
9. Chircop M, Oakes V, Graham ME, Ma MP, Smith CM, Robinson PJ, Khanna KK (2009). The actin-binding and bundling protein, EPLIN, is required for cytokinesis. Cell Cycle 8, 757-764.
10. Crowley JL, Smith TC, Fang Z, Takizawa N, Luna EJ (2009). Supervillin reorganizes the actin cytoskeleton and increases invadopodial efficiency. Mol Biol Cell 20, 948-962.
11. D'Avino PP (2009). How to scaffold the contractile ring for a safe cytokinesis - lessons from anillin-related proteins. J Cell Sci 122, 1071-1079.
12. Dean SO, Rogers SL, Stuurman N, Vale RD, Spudich JA (2005). Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc Natl Acad Sci USA 102, 13473-13478.
13. Domanski M, Molloy K, Jiang H, Chait BT, Rout MP, Jensen TH, LaCava J (2012). Improved methodology for the affinity isolation of human protein complexes expressed at near endogenous levels. Biotechniques, doi: 10.2144/000113864.
14. Dulyaninova NG, Patskovsky YV, Bresnick AR (2004). The N-terminus of the long MLCK induces a disruption in normal spindle morphology and metaphase arrest. J Cell Sci 117, 1481-1493.
15. Echard A, Hickson GR, Foley E, O'Farrell PH (2004). Terminal cytokinesis events uncovered after an RNAi screen. Curr Biol 14, 1685-1693.
16. Fang ZY, Luna EJ (2013). Supervillin-mediated suppression of p53 protein enhances cell survival. J Biol Chem 288, 7918-7929.
17. Fang Z, Takizawa N, Wilson KA, Smith TC, Delprato A, Davidson MW, Lambright DG, Luna EJ (2010). The membrane-associated protein, supervillin, accelerates F-actin-dependent rapid integrin recycling and cell motility. Traffic 11, 782-799.
18. Fedechkin SO, Brockerman J, Luna EJ, Yu Lobanov M, Galzitskaya OV, Smirnov SL (2013). An N-terminal, 830-residue intrinsically disordered region of the cytoskeleton-regulatory protein supervillin contains myosin II-and F-actin-binding sites. J Biomol Struct Dyn 31, 1150-1159.
19. Field CM, Alberts BM (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131, 165-178.
20. Freeman AK, Morrison DK (2011). 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol 22, 681-687.
21. Frenette P, Haines E, Loloyan M, Kinal M, Pakarian P, Piekny A (2012). An anillin-Ect2 complex stabilizes central spindle microtubules at the cortex during cytokinesis. PLoS One 7, e34888.
22. Gai M, Camera P, Dema A, Bianchi F, Berto G, Scarpa E, Germena G, Di Cunto F (2011). Citron kinase controls abscission through RhoA and anillin. Mol Biol Cell 22, 3768-3778.
23. Goyal A, Simanis V (2012). Characterization of ypa1 and ypa2, the Schizosaccharomyces pombe orthologs of the peptidyl proyl isomerases that activate PP2A, reveals a role for Ypa2p in the regulation of cytokinesis. Genetics 190, 1235-1250.
24. Green RA, Paluch E, Oegema K (2012). Cytokinesis in animal cells. Annu Rev Cell Dev Biol 28, 29-58.
25. Gruneberg U, Neef R, Li X, Chan EH, Chalamalasetty RB, Nigg EA, Barr FA (2006). KIF14 and citron kinase act together to promote efficient cytokinesis. J Cell Biol 172, 363-372.
26. Haglund K, Nezis IP, Lemus D, Grabbe C, Wesche J, Liestol K, Dikic I, Palmer R, Stenmark H (2010). Cindr interacts with anillin to control cytokinesis in Drosophila melanogaster. Curr Biol 20, 944-950.
27. Han MY, Kosako H, Watanabe T, Hattori S (2007). Extracellular signal-regulated kinase/mitogen-activated protein kinase regulates actin organization and cell motility by phosphorylating the actin cross-linking protein EPLIN. Mol Cell Biol 27, 8190-8204.
28. Hasegawa H, Hyodo T, Asano E, Ito S, Maeda M, Kuribayashi H, Natsume A, Wakabayashi T, Hamaguchi M, Senga T (2013). Role of SVIL phosphorylation by PLK1 in myosin II activation and cytokinetic furrowing. J Cell Sci 126, 3627-3637.
29. Havrylov S, Ichioka F, Powell K, Borthwick EB, Baranska J, Maki M, Buchman VL (2008). Adaptor protein Ruk/CIN85 is associated with a subset of COPI-coated membranes of the Golgi complex. Traffic 9, 798-812.
30. Hickson GR, O'Farrell PH (2008). Rho-dependent control of anillin behavior during cytokinesis. J Cell Biol 180, 285-294.
31. Higashi T, Ikeda T, Murakami T, Shirakawa R, Kawato M, Okawa K, Furuse M, Kimura T, Kita T, Horiuchi H (2010). Flightless-I (Fli-I) regulates the actin assembly activity of diaphanous-related formins (DRFs) Daam1 and mDia1 in cooperation with active Rho GTPase. J Biol Chem 285, 16231-16238.
32. Hill R, Lee PW (2010). The DNA-dependent protein kinase (DNA-PK): more than just a case of making ends meet? Cell Cycle 9, 3460-3469.
33. Hu CK, Ozlu N, Coughlin M, Steen JJ, Mitchison TJ (2012). Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol Biol Cell 23, 2702-2711.
34. Jin J et al. (2004). Proteomic, functional, domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol 14, 1436-1450.
35. Johnson RI, Seppa MJ, Cagan RL (2008). The Drosophila CD2AP/CIN85 orthologue Cindr regulates junctions and cytoskeleton dynamics during tissue patterning. J Cell Biol 180, 1191-1204.
36. Knecht DA, Loomis WF (1987). Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236, 1081-1086.
37. Koga Y, Ikebe M (2005). p116Rip decreases myosin II phosphorylation by activating myosin light chain phosphatase and by inactivating RhoA. J Biol Chem 280, 4983-4991.
38. Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. Li M, Brooks CL, Kon N, Gu W (2004). A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol Cell 13, 879-886.
40. Lucero A, Stack C, Bresnick AR, Shuster CB (2006). A global, myosin light chain kinase-dependent increase in myosin II contractility accompanies the metaphase-anaphase transition in sea urchin eggs. Mol Biol Cell 17, 4093-4104.
41. Maddox AS, Habermann B, Desai A, Oegema K (2005). Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132, 2837-2848.
42. Matsumura F, Ono S, Yamakita Y, Totsukawa G, Yamashiro S (1998). Specific localization of serine 19 phosphorylated myosin II during cell locomotion and mitosis of cultured cells. J Cell Biol 140, 119-129.
43. Maupin P, Phillips CL, Adelstein RS, Pollard TD (1994). Differential localization of myosin-II isozymes in human cultured cells and blood cells. J Cell Sci 107(Pt 11), 3077-3090.
44. Meszaros B, Simon I, Dosztanyi Z (2009). Prediction of protein binding regions in disordered proteins. PLoS Comput Biol 5, e1000376.
45. Monzo P, Gauthier NC, Keslair F, Loubat A, Field CM, Le Marchand-Brustel Y, Cormont M (2005). Clues to CD2-associated protein involvement in cytokinesis. Mol Biol Cell 16, 2891-2902.
46. Nebl T, Pestonjamasp KN, Leszyk JD, Crowley JL, Oh SW, Luna EJ (2002). Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 277, 43399-43409.
47. Neef R, Gruneberg U, Kopajtich R, Li X, Nigg EA, Sillje H, Barr FA (2007). Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat Cell Biol 9, 436-444.
48. Oegema K, Savoian MS, Mitchison TJ, Field CM (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.
49. Oh SW, Pope RK, Smith KP, Crowley JL, Nebl T, Lawrence JB, Luna EJ (2003). Archvillin, a muscle-specific isoform of supervillin, is an early expressed component of the costameric membrane skeleton. J Cell Sci 116, 2261-2275.
50. Pellinen T et al. (2008). Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev Cell 15, 371-385.
51. Pestonjamasp KN, Pope RK, Wulfkuhle JD, Luna EJ (1997). Supervillin (p205): A novel membrane-associated, F-actin-binding protein in the villin/gelsolin superfamily. J Cell Biol 139, 1255-1269.
52. Piekny AJ, Glotzer M (2008). Anillin is a scaffold protein that links RhoA, actin, myosin during cytokinesis. Curr Biol 18, 30-36.
53. Poirier CC, Ng WP, Robinson DN, Iglesias PA (2012). Deconvolution of the cellular force-generating subsystems that govern cytokinesis furrow ingression. PLoS Comput Biol 8, e1002467.
54. Pope RK, Pestonjamasp KN, Smith KP, Wulfkuhle JD, Strassel CP, Lawrence JB, Luna EJ (1998). Cloning, characterization, and chromosomal localization of human supervillin (SVIL). Genomics 52, 342-351.
55. Poperechnaya A, Varlamova O, Lin PJ, Stull JT, Bresnick AR (2000). Localization and activity of myosin light chain kinase isoforms during the cell cycle. J Cell Biol 151, 697-708.
56. Rai V, Egelhoff TT (2011). Role of B regulatory subunits of protein phosphatase type 2A in myosin II assembly control in Dictyostelium discoideum. Eukaryotic Cell 10, 604-610.
57. Robinson DN, Cavet G, Warrick HM, Spudich JA (2002). Quantitation of the distribution and flux of myosin-II during cytokinesis. BMC Cell Biol 3, 4.
58. Salbreux G, Charras G, Paluch E (2012). Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol 22, 536-545.
59. Samoylenko A et al. (2012). Increased levels of the HER1 adaptor protein Rukl/CIN85 contribute to breast cancer malignancy. Carcinogenesis 33, 1976-1984.
60. Schiel JA, Prekeris R (2013). Membrane dynamics during cytokinesis. Curr Opin Cell Biol 25, 92-98.
61. Shannon KB (2012). IQGAP family members in yeast, Dictyostelium, and mammalian cells. Int J Cell Biol 2012, 894817.
62. Shrestha S, Wilmeth LJ, Eyer J, Shuster CB (2012). PRC1 controls spindle polarization and recruitment of cytokinetic factors during monopolar cytokinesis. Mol Biol Cell 23, 1196-1207.
63. Smith TC, Fang Z, Luna EJ (2010). Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton (Hoboken) 67, 346-364.
64. Somlyo AV, Wang H, Choudhury N, Khromov AS, Majesky M, Owens GK, Somlyo AP (2004). Myosin light chain kinase knockout. J Muscle Res Cell Motil 25, 241-242.
65. Stephan H, Concannon C, Kremmer E, Carty MP, Nasheuer HP (2009). Ionizing radiation-dependent and independent phosphorylation of the 32-kDa subunit of replication protein A during mitosis. Nucleic Acids Res 37, 6028-6041.
66. Straight AF, Field CM, Mitchison TJ (2005). Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol Biol Cell 16, 193-201.
67. Surks HK, Riddick N, Ohtani K (2005). M-RIP targets myosin phosphatase to stress fibers to regulate myosin light chain phosphorylation in vascular smooth muscle cells. J Biol Chem 280, 42543-42551.
68. Swaffield JC, Johnston SA (2001). Affinity purification of proteins binding to GST fusion proteins. Curr Protoc Mol Biol Chapter 20, Unit 20.22.
69. Takizawa N, Ikebe R, Ikebe M, Luna EJ (2007). Supervillin slows cell spreading by facilitating myosin II activation at the cell periphery. J Cell Sci 120, 3792-3803.
70. Uehara R, Hosoya H, Mabuchi I (2008). In vivo phosphorylation of regulatory light chain of myosin II in sea urchin eggs and its role in controlling myosin localization and function during cytokinesis. Cell Motil Cytoskeleton 65, 100-115.
71. Vardar D, Chishti AH, Frank BS, Luna EJ, Noegel AA, Oh SW, Schleicher M, McKnight CJ (2002). Villin-type headpiece domains show a wide range of F-actin-binding affinities. Cell Motil Cytoskeleton 52, 9-21.
72. Vassilev LT (2006). Cell cycle synchronization at the G2/M phase border by reversible inhibition of CDK1. Cell Cycle 5, 2555-2556.
73. Wang YL (2005). The mechanism of cortical ingression during early cytokinesis: thinking beyond the contractile ring hypothesis. Trends Cell Biol 15, 581-588.
74. Watanabe S, De Zan T, Ishizaki T, Narumiya S (2013). Citron kinase mediates transition from constriction to abscission through its coiled-coil domain. J Cell Sci 126, 1773-1784.
75. Werner M, Munro E, Glotzer M (2007). Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr Biol 17, 1286-1297.
76. Wulfkuhle JD, Donina IE, Stark NH, Pope RK, Pestonjamasp KN, Niswonger ML, Luna EJ (1999). Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J Cell Sci 112, 2125-2136.
77. Zhao WM, Fang G (2005). Anillin is a substrate of anaphase-promoting complex/cyclosome (APC/C) that controls spatial contractility of myosin during late cytokinesis. J Biol Chem 280, 33516-33524.
78. Zhou Q et al. (2010). 14-3-3 coordinates microtubules, Rac, myosin II to control cell mechanics and cytokinesis. Curr Biol 20, 1881-1889.
79. Zhu C, Zhao J, Bibikova M, Leverson JD, Bossy-Wetzel E, Fan JB, Abraham RT, Jiang W (2005). Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol Biol Cell 16, 3187-3199.