An Arabidopsis Class II Formin,AtFH19,Nucleates Actin Assembly,Binds to the Barbed End of Actin Filaments,and Antagonizes the Effect of AtFH1 on Actin Dynamics

详细信息    查看全文 | 推荐本文 |

英文篇名：An Arabidopsis Class II Formin,AtFH19,Nucleates Actin Assembly,Binds to the Barbed End of Actin Filaments,and Antagonizes the Effect of AtFH1 on Actin Dynamics 英文作者：Yiyan Zheng 1,2,Haibo Xin 3,Jinxing Lin 1,Chun-Ming Liu 1 and Shanjin Huang 1 1 Key Laboratory of Plant Molecular Physiology,Institute of Botany,the Chinese Academy of Sciences,Beijing 100093,China 2 University of Chinese Academy of Sciences,Beijing 10049,China 3 Ornamental Horticulture and Landscape Architecture,China Agricultural University,Beijing 100094,China 英文关键词：Actin;actin-binding proteins;actin nucleation;Arabidopsis;cytoskeleton;formin. 中文刊名：ZWXB 英文刊名：植物学报(英文版) 出版日期：2012-10-15 出版单位：Journal of Integrative Plant Biology 年：2012 期：v.54 基金：supported by the China National Fund for Distinguished Young Scholars(31125004);; partially supported by the CAS/SAFEA International Partnership Program for Creative Research Teams and SRF for ROCS,SEM 语种：英文; 页：ZWXB201210011 页数：14 CN：10 ISSN：11-5067/Q 分类号：126-139

摘要

Formin is a major protein responsible for regulating the nucleation of actin filaments,and as such,it permits the cell to control where and when to assemble actin arrays.It is encoded by a multigene family comprising 21 members in Arabidopsis thaliana.The Arabidopsis formins can be separated into two phylogenetically-distinct classes:there are 11 class I formins and 10 class II formins.Significant questions remain unanswered regarding the molecular mechanism of actin nucleation and elongation stimulated by each formin isovariant,and how the different isovariants coordinate to regulate actin dynamics in cells.Here,we characterize a class II formin,AtFH19,biochemically.We found that AtFH19 retains all general properties of the formin family,including nucleation and barbed end capping activity.It can also generate actin filaments from a pool of actin monomers bound to profilin.However,both the nucleation and barbed end capping activities of AtFH19 are less efficient compared to those of another well-characterized formin,AtFH1.Interestingly,AtFH19 FH1FH2 competes with AtFH1 FH1FH2 in binding actin filament barbed ends,and inhibits the effect of AtFH1 FH1FH2 on actin.We thus propose a mechanism in which two quantitatively different formins coordinate to regulate actin dynamics by competing for actin filament barbed ends.
        Formin is a major protein responsible for regulating the nucleation of actin filaments,and as such,it permits the cell to control where and when to assemble actin arrays.It is encoded by a multigene family comprising 21 members in Arabidopsis thaliana.The Arabidopsis formins can be separated into two phylogenetically-distinct classes:there are 11 class I formins and 10 class II formins.Significant questions remain unanswered regarding the molecular mechanism of actin nucleation and elongation stimulated by each formin isovariant,and how the different isovariants coordinate to regulate actin dynamics in cells.Here,we characterize a class II formin,AtFH19,biochemically.We found that AtFH19 retains all general properties of the formin family,including nucleation and barbed end capping activity.It can also generate actin filaments from a pool of actin monomers bound to profilin.However,both the nucleation and barbed end capping activities of AtFH19 are less efficient compared to those of another well-characterized formin,AtFH1.Interestingly,AtFH19 FH1FH2 competes with AtFH1 FH1FH2 in binding actin filament barbed ends,and inhibits the effect of AtFH1 FH1FH2 on actin.We thus propose a mechanism in which two quantitatively different formins coordinate to regulate actin dynamics by competing for actin filament barbed ends.

引文

Basu D,Le J,El-Essal Sel D,Huang S,Zhang C,Mallery EL,Ko-liantz G,Staiger CJ,Szymanski DB(2005)DISTORTED3/SCAR2is a putative Arabidopsis WAVE complex subunit that activates theArp2/3complex and is required for epidermal morphogenesis.PlantCell17,502-524.
    Blanchoin L,Staiger CJ(2010)Plant formins:Diverse isoforms andunique molecular mechanism.Biochim.Biophys.Acta1803,201-206.
    Blanchoin L,Amann KJ,Higgs HN,Marchand JB,Kaiser DA,Pollard TD(2000)Direct observation of dendritic actin filamentnetworks nucleated by Arp2/3complex and WASP/Scar proteins.Nature404,1007-1011.
    Carlier MF(2011)A new twist in actin filament nucleation.Nat.Struct.Mol.Biol.18,967-969.
    Chesarone MA,DuPage AG,Goode BL(2010)Unleashing forminsto remodel the actin and microtubule cytoskeletons.Nat.Rev.Mol.Cell Biol.11,62-74.
    Cheung AY,Wu HM(2004)Overexpression of an Arabidopsis forminstimulates supernumerary actin cable formation from pollen tubecell membrane.Plant Cell16,257-269.
    Cvrckova F(2000)Are plant formins integral membrane proteins?Genome Biol.1,RESEARCH001.
    Cvrckova F,Novotny M,Pickova D,Zarsky V(2004)Formin ho-mology2domains occur in multiple contexts in angiosperms.BMCGenomics5,44.
    Deeks MJ,Hussey PJ,Davies B(2002)Formins:Intermediates insignal-transduction cascades that affect cytoskeletal reorganization.Trends Plant Sci.7,492-498.
    Deeks MJ,Cvrckova F,Machesky LM,Mikitova V,Ketelaar T,Zarsky V,Davies B,Hussey PJ(2005)Arabidopsis group Ieformins localize to specific cell membrane domains,interact withactin-binding proteins and cause defects in cell expansion uponaberrant expression.New Phytol.168,529-540.
    Favery B,Chelysheva LA,Lebris M,Jammes F,Marmagne A,DeAlmeida-Engler J,Lecomte P,Vaury C,Arkowitz RA,Abad P(2004)Arabidopsis formin AtFH6is a plasma membrane-associatedprotein upregulated in giant cells induced by parasitic nematodes.Plant Cell16,2529-2540.
    Fedorov AA,Pollard TD,Almo SC(1994)Purification,characteri-zation and crystallization of human platelet profilin expressed inEscherichia coli.J.Mol.Biol.241,480-482.
    Firat-Karalar EN,Welch MD(2011)New mechanisms and functionsof actin nucleation.Curr.Opin.Cell Biol.23,4-13.
    Grunt M,Zarsky V,Cvrckova F(2008)Roots of angiosperm formins:The evolutionary history of plant FH2domain-containing proteins.BMC Evol.Biol.8,115.
    Harris ES,Li F,Higgs HN(2004)The mouse formin,FRLalpha,slows actin filament barbed end elongation,competes with cappingprotein,accelerates polymerization from monomers,and seversfilaments.J.Biol.Chem.279,20076-20087.
    Harris ES,Rouiller I,Hanein D,Higgs HN(2006)Mechanistic differ-ences in actin bundling activity of two mammalian formins,FRL1and mDia2.J.Biol.Chem.281,14383-14392.
    Higashida C,Miyoshi T,Fujita A,Oceguera-Yanez F,Monypenny J,Andou Y,Narumiya S,Watanabe N(2004)Actin polymerization-driven molecular movement of mDia1in living cells.Science303,2007-2010.
    Higgs HN(2005)Formin proteins:A domain-based approach.TrendsBiochem.Sci.30,342-353.
    Higgs HN,Peterson KJ(2005)Phylogenetic analysis of the forminhomology2domain.Mol.Biol.Cell16,1-13.
    Higgs HN,Blanchoin L,Pollard TD(1999)In?uence of the C termi-nus of Wiskott-Aldrich syndrome protein(WASp)and the Arp2/3complex on actin polymerization.Biochemistry38,15212-15222.
    Huang S,Blanchoin L,Kovar DR,Staiger CJ(2003)Arabidopsiscapping protein(AtCP)is a heterodimer that regulates assemblyat the barbed ends of actin filaments.J.Biol.Chem.278,44832-44842.
    Huang S,Robinson RC,Gao LY,Matsumoto T,Brunet A,BlanchoinL,Staiger CJ(2005)Arabidopsis VILLIN1generates actin filamentcables that are resistant to depolymerization.Plant Cell17,486-501.
    Ingouff M,Fitz Gerald JN,Guerin C,Robert H,Sorensen MB,VanDamme D,Geelen D,Blanchoin L,Berger F(2005)Plant forminAtFH5is an evolutionarily conserved actin nucleator involved incytokinesis.Nat.Cell Biol.7,374-380.
    Kleinebrecht J,Selow J,Winkler W(1982)The mouse mutant limb-deformity(ld).Anat.Anz.152,313-324.
    Kovar DR,Pollard TD(2004)Insertional assembly of actin filamentbarbed ends in association with formins produces piconewtonforces.Proc.Natl.Acad.Sci.USA101,14725-14730.
    Kovar D.R,Kuhn JR,Tichy AL,Pollard TD(2003)The fission yeastcytokinesis formin Cdc12p is a barbed end actin filament cappingprotein gated by profilin.J.Cell Biol.161,875-887.
    Kovar DR,Harris ES,Mahaffy R,Higgs HN,Pollard TD(2006)Control of the assembly of ATP-and ADP-actin by formins andprofilin.Cell124,423-435.
    Le J,El-Assal Sel D,Basu D,Saad ME,Szymanski DB(2003)Re-quirements for Arabidopsis ATARP2and ATARP3during epidermaldevelopment.Curr.Biol.13,1341-1347.
    Li F,Higgs HN(2003)The mouse Formin mDia1is a potent actinnucleation factor regulated by autoinhibition.Curr.Biol.13,1335-1340.
    Li S,Blanchoin L,Yang Z,Lord EM(2003)The putative Arabidopsisarp2/3complex controls leaf cell morphogenesis.Plant Physiol.132,2034-2044.
    Michelot A,Guerin C,Huang S,Ingouff M,Richard S,Rodiuc N,Staiger CJ,Blanchoin L(2005)The formin homology1domainmodulates the actin nucleation and bundling activity of ArabidopsisFORMIN1.Plant Cell17,2296-2313.
    Michelot A,Derivery E,Paterski-Boujemaa R,Guerin C,Huang S,Parcy F,Staiger CJ,Blanchoin L(2006)A novel mechanism forthe formation of actin-filament bundles by a nonprocessive formin.Curr.Biol.16,1924-1930.
    Moseley JB,Goode BL(2005)Differential activities and regulation ofSaccharomyces cerevisiae formin proteins Bni1and Bnr1by Bud6.J.Biol.Chem.280,28023-28033.
    Mullins RD,Heuser JA,Pollard TD(1998)The interaction of Arp2/3complex with actin:Nucleation,high affinity pointed end capping,and formation of branching networks of filaments.Proc.Natl.Acad.Sci.USA95,6181-6186.
    Paul AS,Pollard TD(2008)The role of the FH1domain and profilinin formin-mediated actin-filament elongation and nucleation.Curr.Biol.18,9-19.
    Pollard TD(1984)Polymerization of ADP-actin.J.Cell Biol.99,769-777.
    Pollard TD,Borisy GG(2003)Cellular motility driven by assembly anddisassembly of actin filaments.Cell112,453-465.
    Pollard TD,Cooper JA(2009)Actin,a central player in cell shape andmovement.Science326,1208-1212.
    Pruyne D,Evangelista M,Yang C,Bi E,Zigmond S,Bretscher A,Boone C(2002)Role of formins in actin assembly:Nucleation andbarbed-end association.Science297,612-615.
    Ren H,Gibbon BC,Ashworth SL,Sherman DM,Yuan M,StaigerCJ(1997)Actin purified from maize pollen functions in living plantcells.Plant Cell9,1445-1457.
    Romero S,Le Clainche C,Didry D,Egile C,Pantaloni D,CarlierMF(2004)Formin is a processive motor that requires profilin toaccelerate actin assembly and associated ATP hydrolysis.Cell119,419-429.
    Sagot I,Klee SK,Pellman D(2002a)Yeast formins regulate cellpolarity by controlling the assembly of actin cables.Nat.Cell Biol.4,42-50.
    Sagot I,Rodal AA,Moseley J,Goode BL,Pellman D(2002b)Anactin nucleation mechanism mediated by Bni1and profilin.Nat.CellBiol.4,626-631.
    Schmid M,Davison TS,Henz SR,Pape UJ,Demar M,Vingron M,Scholkopf B,Weigel D,Lohmann JU(2005)A gene expressionmap of Arabidopsis thaliana development.Nat.Genet.37,501-506.
    Spudich JA,Watt S(1971)The regulation of rabbit skeletal mus-cle contraction.I.Biochemical studies of the interaction of thetropomyosin-troponin complex with actin and the proteolytic frag-ments of myosin.J.Biol.Chem.246,4866-4871.
    Vavylonis D,Kovar DR,O’Shaughnessy B,Pollard TD(2006)Modelof formin-associated actin filament elongation.Mol.Cell21,455-466.
    Vidali L,van Gisbergen PA,Guerin C,Franco P,Li M,Burkart GM,Augustine RC,Blanchoin L,Bezanilla M(2009)Rapid formin-mediated actin-filament elongation is essential for polarized plantcell growth.Proc.Natl.Acad.Sci.USA106,13341-13346.
    Wasteneys GO,Yang Z(2004)New views on the plant cytoskeleton.Plant Physiol.136,3884-3891.
    Xu Y,Moseley JB,Sagot I,Poy F,Pellman D,Goode BL,Eck MJ(2004)Crystal structures of a formin homology-2domain reveal atethered dimer architecture.Cell116,711-723.
    Yang W,Ren S,Zhang X,Gao M,Ye S,Qi Y,Zheng Y,Wang J,ZengL,Li Q,Huang S,He Z(2011)BENT UPPERMOST INTERNODE1encodes the class II formin FH5crucial for actin organization andrice development.Plant Cell23,661-680.
    Ye J,Zheng Y,Yan A,Chen N,Wang Z,Huang S,Yang Z(2009)Ara-bidopsis formin3directs the formation of actin cables and polarizedgrowth in pollen tubes.Plant Cell21,3868-3884.
    Yi K,Guo C,Chen D,Zhao B,Yang B,Ren H(2005)Cloning andfunctional characterization of a formin-like protein(AtFH8)fromArabidopsis.Plant Physiol.138,1071-1082.
    Zhang Z,Zhang Y,Tan H,Wang Y,Li G,Liang W,Yuan Z,Hu J,Ren H,Zhang D(2011)RICE MORPHOLOGY DETERMINANT encodes the type II formin FH5and regulates rice morphogenesis.Plant Cell23,681-700.
    Zigmond SH,Evangelista M,Boone C,Yang C,Dar AC,SicherF,Forkey J,Pring M(2003)Formin leaky cap allows elongationin the presence of tight capping proteins.Curr.Biol.13,1820-1823.