The myriad roles of Anillin during cytokinesis


The myriad roles of Anillin during cytokinesis

Piekny, Alisa J and Maddox, Amy Shaub (2010) The myriad roles of Anillin during cytokinesis. Seminars in Cell and Developmental Biology, 21 (9). pp. 881-891. ISSN 1084-9521

PDF (Review article) - Accepted Version

Official URL:


Anillin is a highly conserved multidomain protein that interacts with cytoskeletal components as well as their regulators. Throughout phylogeny, Anillins contribute to cytokinesis, the cell shape change that occurs at the end of meiosis and mitosis to separate a cell into daughter cells. Failed cytokinesis results in binucleation, which can lead to genomic instability. Study of Anillin in several model organisms has provided us with insight into how the cytoskeleton is coordinated to ensure that cytokinesis occurs with high fidelity. Here we review Anillin’s interacting partners and the relevance of these interactions in vivo. We also discuss questions of how these interactions are coordinated, and finally provide some perspective regarding Anillin’s role in cancer.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Piekny, Alisa J and Maddox, Amy Shaub
Journal or Publication:Seminars in Cell and Developmental Biology
Date:December 2010
Keywords:cytoskeleton; cytokinesis; Rho; F-actin; cellularization
ID Code:7014
Deposited On:18 Jan 2011 14:31
Last Modified:18 Jan 2011 14:31
[1] Oliferenko S, Chew TG, Balasubramanian MK. Positioning cytokinesis. Genes Dev 2009;23(6):660–74.
[2] von Dassow G. Concurrent cues for cytokinetic furrow induction in animal cells. Trends Cell Biol 2009;19(4):165–73.
[3] Piekny A, Werner M, Glotzer M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol 2005;15(12):651–8.
[4] D’Avino PP. How to scaffold the contractile ring for a safe cytokinesis—lessons from Anillin-related proteins. J Cell Sci 2009;122(Pt 8):1071–9.
[5] Hickson GR, O’Farrell PH. Anillin: a pivotal organizer of the cytokinetic machinery. Biochem Soc Trans 2008;36(Pt 3):439–41.
[6] Zhang L, Maddox AS. Anillin. Curr Biol 2010;20(4):R135–6.
[7] Miller KG, Field CM, Alberts BM. Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatography. J Cell Biol 1989;109(6 Pt 1):2963–75.
[8] Field CM, Coughlin M, Doberstein S, Marty T, Sullivan W. Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 2005;132(12):2849–60.
[9] Field CM, Alberts BM. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 1995;131(1):165–78.
[10] Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ. Self- and actintemplated assembly of Mammalian septins. Dev Cell 2002;3(6):791–802.
[11] Giansanti MG, Bonaccorsi S, Gatti M. The role of anillin in meiotic cytokinesis of Drosophila males. J Cell Sci 1999;112(Pt 14):2323–34.
[12] Goldbach P, Wong R, Beise N, Sarpal R, Trimble WS, Brill JA. Stabilization of the actomyosin ring enables spermatocyte cytokinesis in Drosophila. Mol Biol Cell 2010;21(9):1482–93.
[13] Hickson GR, O’Farrell PH. Rho-dependent control of anillin behavior during cytokinesis. J Cell Biol 2008;180(2):285–94.
[14] Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, et al. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003;299(5613):1743–7.
[15] Oegema K, Savoian MS, Mitchison TJ, Field CM. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J Cell Biol 2000;150(3):539–52.
[16] Watanabe S, Okawa K,Miki T, Sakamoto S, Morinaga T, Segawa K, et al. Rho and Anillin-dependent control of mDia2 localization and function in cytokinesis. Mol Biol Cell 2010 (Epub ahead of print).
[17] Watanabe S, Ando Y, Yasuda S, Hosoya H, Watanabe N, Ishizaki T, et al. mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol Biol Cell 2008;19(5):2328–38.
[18] Straight AF, Field CM, Mitchison TJ. Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol Biol Cell 2005;16(1):193–201.
[19] Maddox AS, Habermann B, Desai A, Oegema K. Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 2005;132(12):2837–48.
[20] D’Avino PP, Takeda T, Capalbo L, Zhang W, Lilley KS, Laue ED, et al. Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J Cell Sci 2008;121(Pt 8):1151–8.
[21] Piekny AJ, Glotzer M. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr Biol 2008;18(1):30–6.
[22] Zhao WM, 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(39):33516–24.
[23] Werner M, Glotzer M. Control of cortical contractility during cytokinesis. Biochem Soc Trans 2008;36(Pt 3):371–7.
[24] Maddox AS, Lewellyn L, Desai A, Oegema K. Anillin and the septins promote asymmetric ingression of the cytokinetic furrow. Dev Cell 2007;12(5):827–35.
[25] Higuchi H, Endow SA. Directionality and processivity of molecular motors. Curr Opin Cell Biol 2002;14(1):5–7.
[26] Weirich CS, Erzberger JP, Barral Y. The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 2008;9(6):478–89.
[27] Versele M, Thorner J. Some assembly required: yeast septins provide the instruction manual. Trends Cell Biol 2005;15(8):414–24.
[28] Adam JC, Pringle JR, Peifer M. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell 2000;11(9):3123–35.
[29] Tasto JJ, Morrell JL, Gould KL. An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J Cell Biol 2003;160(7):1093–103.
[30] Berlin A, Paoletti A, Chang F. Mid2p stabilizes septin rings during cytokinesis in fission yeast. J Cell Biol 2003;160(7):1083–92.
[31] Casamayor A, SnyderM.Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol Cell Biol 2003;23(8):2762–77.
[32] Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol 1999;9(24):1458–67.
[33] Rodal AA, Kozubowski L, Goode BL, Drubin DG, Hartwig JH. Actin and septin ultrastructures at the budding yeast cell cortex. Mol Biol Cell 2005;16(1):372–84.
[34] Monzo P, Gauthier NC, Keslair F, Loubat A, Field CM, Le Marchand-Brustel Y, et al. Clues to CD2-associated protein involvement in cytokinesis. Mol Biol Cell 2005;16(6):2891–902.
[35] Haglund K, Nezis IP, Lemus D, Grabbe C, Wesche J, Liestøl K, et al. Cindr interacts with anillin to control cytokinesis in Drosophila melanogaster. Curr Biol 2010;20(10):944–50.
[36] Drechsel DN, Hyman AA, Hall A, Glotzer M. A equirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr Biol 1997;7(1):12–23.
[37] Jantsch-Plunger V, Gönczy P, Romano A, Schnabel H, Hamill D, Schnabel R, et al. CYK-4: a Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol 2000;149(7):1391–404.
[38] Prokopenko SN, Brumby A, O’Keefe L, Prior L, He Y, Saint R, et al. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev 1999;13(17):2301–14.
[39] Yuce O, Piekny A, Glotzer M. An ECT2–centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 2005;170(4):571–82.
[40] Suzuki C, Daigo Y, Ishikawa N, Kato T, Hayama S, Ito T, et al. 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(24):11314–25.
[41] Solski PA, Wilder RS, Rossman KL, Sondek J, Cox AD, Campbell SL, et al. Requirement for C-terminal sequences in regulation of Ect2 guanine nucleotide exchange specificity and transformation. J Biol Chem 2004;279(24):25226–33.
[42] Glotzer M. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 2009;10(1):9–20.
[43] Gregory SL, Ebrahimi S,Milverton J, Jones WM, Bejsovec A, Saint R. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol 2008;18(1):25–9.
[44] Sisson JC, Field C, Ventura R, Royou A, Sullivan W. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 2000;151(4):905–18.
[45] Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 2008;9(2):99–111.
[46] Celton-Morizur S, Bordes N, Fraisier V, Tran PT, Paoletti A. C-terminal anchoring of mid1p to membranes stabilizes cytokinetic ring position in early mitosis in fission yeast. Mol Cell Biol 2004;24(24):10621–35.
[47] Clifford DM, Wolfe BA, Roberts-Galbraith RH, McDonald WH, Yates 3rd JR, Gould KL. The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J Cell Biol 2008;181(1): 79–88.
[48] Chitu V, Stanley ER. Pombe Cdc15 homology (PCH) proteins: coordinators of membrane–cytoskeletal interactions. Trends Cell Biol 2007;17(3):145–56.
[49] Trautmann S, McCollum D. Cell cycle: new functions for Cdc14 family phosphatases. Curr Biol 2002;12(21):R733–5.
[50] Wagstaff KM, Jans DA. Importins and beyond: non-conventional nuclear transport mechanisms. Traffic 2009;10(9):1188–98.
[51] Silverman-Gavrila RV, Hales KG, Wilde A. Anillin-mediated targeting of peanut to pseudocleavage furrows is regulated by the GTPase Ran. Mol Biol Cell 2008;19(9):3735–44.
[52] Hall PA, Todd CB, Hyland PL, McDade SS, Grabsch H, Dattani M, et al. The septinbinding protein anillin is overexpressed in diverse human tumors. Clin Cancer Res 2005;11(19 Pt 1):6780–6.
[53] Russell SE, Hall PA. Do septins have a role in cancer? Br J Cancer 2005;93(5):499–503.
[54] 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(21):2707–19.
[55] Engel FB, Schebesta M, Keating MT. Anillin localization defect in cardiomyocyte binucleation. J Mol Cell Cardiol 2006;41(4):601–12.
[56] Bahler J, Steever AB, Wheatley S, Wang Y, Pringle JR, Gould KL, et al. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J Cell Biol 1998;143(6):1603–16.
[57] Pollard TD, Wu JQ. Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 2010;11(2):149–55.
[58] Hu CK, Coughlin M, Field CM, Mitchison TJ. Cell polarization during monopolar cytokinesis. J Cell Biol 2008;181(2):195–202.
[59] Somma MP, Fasulo B, Cenci G, Cundari E, Gatti M. Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells. Mol Biol Cell 2002;13(7):2448–60.
[60] WuJQ, Kuhn JR, Kovar DR, Pollard TD. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 2003;5(5):723–34.
[61] Hachet O, Simanis V. Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev 2008;22(22):3205–16.
[62] Huang Y, Yan H, Balasubramanian MK. Assembly of normal actomyosin rings in the absence of Mid1p and cortical nodes in fission yeast. J Cell Biol 2008;183(6):979–88.
[63] Thomas JH, Wieschaus E. src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development 2004;131(4): 863–71.
[64] Skop AR, Liu H, Yates 3rd J, Meyer BJ, Heald R. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 2004;305(5680):61–6.
[65] Echard A, Hickson GR, Foley E, O’Farrell PH. Terminal cytokinesis events uncovered after an RNAi screen. Curr Biol 2004;14(18):1685–93.
[66] Hallett MA, Lo HS, Bender A. Probing the importance and potential roles of the binding of the PH-domain protein Boi1 to acidic phospholipids. BMC Cell Biol 2002;3:16.
[67] Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y. The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 2006;125(1):85–98.
[68] Matsui Y, Matsui R, Akada R, Toh-e A. Yeast src homology region 3 domain-binding proteins involved in bud formation. J Cell Biol 1996;133(4): 865–78.
[69] Olakowski M, Tyszkiewicz T, Jarzab M, Król R, Oczko-Wojciechowska M, Kowalska M, et al. NBL1 and anillin (ANLN) genes over-expression in pancreatic carcinoma. Folia Histochem Cytobiol 2009;47(2):249–55
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page

Document Downloads

More statistics for this item...

Concordia University - Footer