DOI: 10.1091/mbc.e04-03-0225. TetraThymosinβ Is Required for Actin Dynamics in<i>Caenorhabditis elegans</i>and Acts via Functionally Different Actin-binding Repeats

TetraThymosinβ Is Required for Actin Dynamics inCaenorhabditis elegansand Acts via Functionally Different Actin-binding Repeats

10.1091/mbc.e04-03-0225

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Generating specific actin structures via controlled actin polymerization is a prerequisite for eukaryote development and reproduction. We here report on an essential Caenorhabditis elegans protein tetraThymosinβ expressed in developing neurons and crucial during oocyte maturation in adults. TetraThymosinβ has four repeats, each related to the actin monomer-sequestering protein thymosinβ 4 and assists in actin filament elongation. For homologues with similar multirepeat structures, a profilin-like mechanism of ushering actin onto filament barbed ends, based on the formation of a 1:1 complex, is proposed to underlie this activity. We, however, demonstrate that tetraThymosinβ binds multiple actin monomers via different repeats and in addition also interacts with filamentous actin. All repeats need to be functional for attaining full activity in various in vitro assays. The activities on actin are thus a direct consequence of the repeated structure. In containing both G- and F-actin interaction sites, tetraThymosinβ may be reminiscent of nonhomologous multimodular actin regulatory proteins implicated in actin filament dynamics. A mutation that suppresses expression of tetraThymosinβ is homozygous lethal. Mutant organisms develop into adults but display a dumpy phenotype and fail to reproduce as their oocytes lack essential actin structures. This strongly suggests that the activity of tetraThymosinβ is of crucial importance at specific developmental stages requiring actin polymerization.

Bibliography

Van Troys, M., Ono, K., Dewitte, D., Jonckheere, V., De Ruyck, N., Vandekerckhove, J., Ono, S., & Ampe, C. (2004). TetraThymosinÎ² Is Required for Actin Dynamics inCaenorhabditis elegansand Acts via Functionally Different Actin-binding Repeats. Molecular Biology of the Cell, 15(10), 4735â4748.

Authors 8

Marleen Van Troys (first)
Kanako Ono (additional)
Daisy Dewitte (additional)
Veronique Jonckheere (additional)
Natalie De Ruyck (additional)
Joël Vandekerckhove (additional)
Shoichiro Ono (additional)
Christophe Ampe (additional)

References 53 Referenced 32

Dates

Type	When
Created	21 years, 1 month ago (July 21, 2004, 10:46 p.m.)
Deposited	2 years, 4 months ago (April 28, 2023, 9:50 p.m.)
Indexed	1 month ago (July 30, 2025, 11:31 a.m.)
Issued	20 years, 11 months ago (Oct. 1, 2004)
Published	20 years, 11 months ago (Oct. 1, 2004)
Published Print	20 years, 11 months ago (Oct. 1, 2004)

Funders 0

None

BibTeX

@article{Van_Troys_2004, title={TetraThymosinβ Is Required for Actin Dynamics inCaenorhabditis elegansand Acts via Functionally Different Actin-binding Repeats}, volume={15}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e04-03-0225}, DOI={10.1091/mbc.e04-03-0225}, number={10}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Van Troys, Marleen and Ono, Kanako and Dewitte, Daisy and Jonckheere, Veronique and De Ruyck, Natalie and Vandekerckhove, Joël and Ono, Shoichiro and Ampe, Christophe}, year={2004}, month=oct, pages={4735–4748} }

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  "abstract": "<jats:p>Generating specific actin structures via controlled actin polymerization is a prerequisite for eukaryote development and reproduction. We here report on an essential Caenorhabditis elegans protein tetraThymosin\u03b2 expressed in developing neurons and crucial during oocyte maturation in adults. TetraThymosin\u03b2 has four repeats, each related to the actin monomer-sequestering protein thymosin\u03b2 4 and assists in actin filament elongation. For homologues with similar multirepeat structures, a profilin-like mechanism of ushering actin onto filament barbed ends, based on the formation of a 1:1 complex, is proposed to underlie this activity. We, however, demonstrate that tetraThymosin\u03b2 binds multiple actin monomers via different repeats and in addition also interacts with filamentous actin. All repeats need to be functional for attaining full activity in various in vitro assays. The activities on actin are thus a direct consequence of the repeated structure. In containing both G- and F-actin interaction sites, tetraThymosin\u03b2 may be reminiscent of nonhomologous multimodular actin regulatory proteins implicated in actin filament dynamics. A mutation that suppresses expression of tetraThymosin\u03b2 is homozygous lethal. Mutant organisms develop into adults but display a dumpy phenotype and fail to reproduce as their oocytes lack essential actin structures. This strongly suggests that the activity of tetraThymosin\u03b2 is of crucial importance at specific developmental stages requiring actin polymerization.</jats:p>",
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      "unstructured": "Bachmann, C., Fischer, L., Walterand, U., and Reinhard, M. (1999). The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation.J. Biol. Chem.274, 23549-23557.",
      "DOI": "10.1074/jbc.274.33.23549"
    },
    {
      "key": "REF2",
      "doi-asserted-by": "crossref",
      "unstructured": "Ballweber, E., Hannappel, E., Huff, T., Stephan, H., Haener, M., Taschner, N., Stoffler, D., Aebi, U., and Mannherz, H.G. (2002). Polymerisation of chemically cross-linked actin:thymosin beta(4) complex to filamentous actin: alteration in helical parameters and visualisation of thymosin beta(4) binding on F-actin.J. Mol. Biol.315, 613-625.",
      "DOI": "10.1006/jmbi.2001.5281"
    },
    {
      "key": "REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Barstead, R.J., and Waterston, R.H. (1991). Vinculin is essential for muscle function in the nematode.J. Biol. Chem.114, 715-724.",
      "DOI": "10.1083/jcb.114.4.715"
    },
    {
      "key": "REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Boquet, I., Boujemaa, R., Carlier, M.F., and Preat, T. (2000). Ciboulot regulates actin assembly during Drosophila brain metamorphosis.Cell102, 797-808.",
      "DOI": "10.1016/S0092-8674(00)00068-4"
    },
    {
      "key": "REF5",
      "doi-asserted-by": "crossref",
      "unstructured": "Bubb, M.R., Lewis, M.S., and Korn, E.D. (1994). Actobindin binds with high affinity to a covalently cross-linked actin dimer.J. Biol. Chem.269, 25587-25591.",
      "DOI": "10.1016/S0021-9258(18)47290-0"
    },
    {
      "key": "REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Carlier, M.F.et al.(1996). Tbeta 4 is not a simple G-actin sequestering protein and interacts with F-actin at high concentration.J. Biol. Chem.271, 9231-9239.",
      "DOI": "10.1074/jbc.271.16.9231"
    },
    {
      "key": "REF7",
      "unstructured": "Condeelis, J. (2001). How is actin polymerization nucleated in vivo?Trends Cell Biol.11, 288-293."
    },
    {
      "key": "REF8",
      "doi-asserted-by": "crossref",
      "unstructured": "Detmers, P., Weber, A., Elzinga, M., and Stephens, R.E. (1981). 7-Chloro-4-nitrobenzeno-2-oxa-1,3-diazole actin as a probe for actin polymerization.J. Biol. Chem.256, 99-105.",
      "DOI": "10.1016/S0021-9258(19)70103-3"
    },
    {
      "key": "REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Dickinson, R.B., and Purich, D.L. (2002). Clamped-filament elongation model for actin-based motors.Biophys. J.82, 605-617.",
      "DOI": "10.1016/S0006-3495(02)75425-8"
    },
    {
      "key": "REF10",
      "doi-asserted-by": "crossref",
      "unstructured": "Dickinson, R.B., Southwick, F.S., and Purich, D.L. (2002). A direct-transfer polymerization model explains how the multiple profilin-binding sites in the actoclampin motor promote rapid actin-based motility.Arch. Biochem. Biophys.406, 296-301.",
      "DOI": "10.1016/S0003-9861(02)00212-6"
    },
    {
      "key": "REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Domanski, M., Hertzog, M., Coutant, J., Gutsche-Perelroizen, I., Bontems, F., Carlier, M.F., Guittet, E., and van Heijenoort, C. (2004). Coupling of folding and binding of thymosin beta4 upon interaction with monomeric actin monitored by nuclear magnetic resonance.J. Biol. Chem.279, 23637-23645.",
      "DOI": "10.1074/jbc.M311413200"
    },
    {
      "key": "REF12",
      "doi-asserted-by": "crossref",
      "unstructured": "Epstein, H.F., Casey, D.L., and Ortiz, I. (1993). Myosin and paramyosin ofCaenorhabditis elegansembryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages.J. Cell Biol.122, 845-858.",
      "DOI": "10.1083/jcb.122.4.845"
    },
    {
      "key": "REF13",
      "unstructured": "Eyckerman, S., Waelput, W., Verhee, A., Broekaert, D., Vandekerckhove, J., and Tavernier, J. (1999). Analysis of Tyr to Phe and fa/fa leptin receptor mutations in the PC12 cell line.Eur. Cytokine Netw.10, 549-556."
    },
    {
      "key": "REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Finney, M., and Ruvkun, G. (1990). The unc-86 gene product couples cell lineage and cell identity in C. elegans.Cell63, 895-905.",
      "DOI": "10.1016/0092-8674(90)90493-X"
    },
    {
      "key": "REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Gimona, M., Djinovic-Carugo, K., Kranewitter, W.J., and Winder, S.J. (2002). Functional plasticity of CH domains.FEBS Lett.513, 98-106.",
      "DOI": "10.1016/S0014-5793(01)03240-9"
    },
    {
      "key": "REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Hertzog, M., Yarmola, E.G., Didry, D., Bubb, M.R., and Carlier, M.F. (2002). Control of actin dynamics by proteins made of beta-thymosin repeats: the actobindin family.J. Biol. Chem.277, 14786-14792.",
      "DOI": "10.1074/jbc.M112064200"
    },
    {
      "key": "REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Hertzog, M.et al.(2004). The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly.Cell117, 611-623.",
      "DOI": "10.1016/S0092-8674(04)00403-9"
    },
    {
      "key": "REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Hubbard, E.J., and Greenstein, D. (2000). TheCaenorhabditis elegansgonad: a test tube for cell and developmental biology.Dev. Dyn.218, 2-22.",
      "DOI": "10.1002/(SICI)1097-0177(200005)218:1<2::AID-DVDY2>3.0.CO;2-W"
    },
    {
      "key": "atypb1",
      "doi-asserted-by": "crossref",
      "unstructured": "Huff, T., Muller, C.S., Otto, A.M., Netzker, R., and Hannappel, E. (2001). beta-Thymosins, small acidic peptides with multiple functions.Int. J. Biochem. Cell Biol.33, 205-220.",
      "DOI": "10.1016/S1357-2725(00)00087-X"
    },
    {
      "key": "REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Kamath, R.S.et al.(2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi.Nature421, 231-237.",
      "DOI": "10.1038/nature01278"
    },
    {
      "key": "REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "Kang, F., Purich, D.L., and Southwick, F.S. (1999). Profilin promotes barbedend actin filament assembly without lowering the critical concentration.J. Biol. Chem.274, 36963-36972.",
      "DOI": "10.1074/jbc.274.52.36963"
    },
    {
      "key": "atypb2",
      "doi-asserted-by": "crossref",
      "unstructured": "Kouyama, T., and Mihashi, K. (1981). Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin.Eur. J. Biochem.114, 33-38.",
      "DOI": "10.1111/j.1432-1033.1981.tb06167.x"
    },
    {
      "key": "REF23",
      "doi-asserted-by": "crossref",
      "unstructured": "Lambooy, P.K., and Korn, E.D. (1986). Purification and characterization of actobindin, a new actin monomer-binding protein from Acanthamoeba castellanii.J. Biol. Chem.261, 17150-17155.",
      "DOI": "10.1016/S0021-9258(19)76011-6"
    },
    {
      "key": "REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "Mattila, P.K., Salminen, M., Yamashiro, T., and Lappalainen, P. (2003). Mouse MIM, a tissue-specific regulator of cytoskeletal dynamics, interacts with ATP-actin monomers through its C-terminal WH2 domain.J. Biol. Chem.278, 8452-8459.",
      "DOI": "10.1074/jbc.M212113200"
    },
    {
      "key": "REF25",
      "doi-asserted-by": "crossref",
      "unstructured": "Mertens, N., Remaut, E., and Fiers, W. (1995). Tight transcriptional control mechanism ensures stable high-level expression from T7 promoter-based expression plasmids.Biotechnology13, 175-179.",
      "DOI": "10.1038/nbt0295-175"
    },
    {
      "key": "REF26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.e02-03-0157"
    },
    {
      "key": "REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "Ono, S., Baillie, D.L., and Benian, G.M. (1999). UNC-60B, an ADF/cofilin family protein, is required for proper assembly of actin into myofibrils inCaenorhabditis elegansbody wall muscle.J. Cell Biol.145, 491-502.",
      "DOI": "10.1083/jcb.145.3.491"
    },
    {
      "key": "REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Ono, S. (2001). The Caenorhabditis elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organized assembly of muscle actin filamentsJ. Cell Biol.152, 1313-1319.",
      "DOI": "10.1083/jcb.152.6.1313"
    },
    {
      "key": "REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Ono, S., and Ono, K. (2002). Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics.J. Cell Biol.156, 1065-1076.",
      "DOI": "10.1083/jcb.200110013"
    },
    {
      "key": "REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Pantaloni, D. and Carlier, M.F. (1993). How profilin promotes actin filament assembly in the presence of thymosin beta 4.Cell75, 1007-1014.",
      "DOI": "10.1016/0092-8674(93)90544-Z"
    },
    {
      "key": "REF31",
      "doi-asserted-by": "crossref",
      "unstructured": "Paunola, E., Mattila, P.K., and Lappalainen, P. (2002). WH2 domain: a small, versatile adapter for actin monomers.FEBS Lett.513, 92-97.",
      "DOI": "10.1016/S0014-5793(01)03242-2"
    },
    {
      "key": "REF32",
      "doi-asserted-by": "crossref",
      "unstructured": "Pollard, T.D., and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments.Cell112, 453-465.",
      "DOI": "10.1016/S0092-8674(03)00120-X"
    },
    {
      "key": "REF33",
      "doi-asserted-by": "crossref",
      "unstructured": "Pope, B., Way, M., and Weeds, A.G. (1991). Two of the three actin-binding domains of gelsolin bind to the same subdomain of actin. Implications of capping and severing mechanisms.FEBS Lett.280, 70-74.",
      "DOI": "10.1016/0014-5793(91)80206-I"
    },
    {
      "key": "REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Reboul, J.et al.(2003).C. elegansORFeome version 1. 1, experimental verification of the genome annotation and resource for proteome-scale protein expression.Nat. Genet.34, 35-41.",
      "DOI": "10.1038/ng1140"
    },
    {
      "key": "REF35",
      "doi-asserted-by": "crossref",
      "unstructured": "Rose, K.L., Winfrey, V.P., Hoffman, L.H., Hall, D.H., Furuta, T., and Greenstein, D. (1997). The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation inCaenorhabditis elegans.Dev. Biol.192, 59-77.",
      "DOI": "10.1006/dbio.1997.8728"
    },
    {
      "key": "REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Rossenu, S., Dewitte, D., Vandekerckhove, J., and Ampe, C. (1997). A phage display technique for a fast, sensitive, and systematic investigation of protein-protein interactions.J. Protein Chem.16, 499-503.",
      "DOI": "10.1023/A:1026317612554"
    },
    {
      "key": "REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Rossenu, S., Leyman, S., Dewitte, D., Peelaers, D., Jonckheere, V., Van Troys, M., Vandekerckhove, J., and Ampe, C. (2003). A phage display based method for determination of relative affinities of mutants; application to the actin binding motifs in thymosin beta 4 and Villin headpiece.J. Biol. Chem.278, 16642-16650.",
      "DOI": "10.1074/jbc.M208311200"
    },
    {
      "key": "REF38",
      "doi-asserted-by": "crossref",
      "unstructured": "Safer, D. (1989). An electrophoretic procedure for detecting proteins that bind actin monomers.Anal. Biochem.178, 32-37.",
      "DOI": "10.1016/0003-2697(89)90351-5"
    },
    {
      "key": "REF39",
      "doi-asserted-by": "crossref",
      "unstructured": "Safer, D., Sosnick, T.R., and Elzinga, M. (1997). Thymosin \u03b24 binds actin in an extended conformation and contacts both the barbed and pointed end.Biochemistry36, 5806-5816.",
      "DOI": "10.1021/bi970185v"
    },
    {
      "key": "REF40",
      "doi-asserted-by": "crossref",
      "unstructured": "Severson, A.F., Baillie, D.L., and Bowerman, B. (2002). A formin homology protein and a profilin are required for cytokinesis and Arp2/3-independent assembly of cortical microfilaments inC. elegans.Curr. Biol.12, 2066-2075.",
      "DOI": "10.1016/S0960-9822(02)01355-6"
    },
    {
      "key": "REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Simenel, C., Van Troys, M., Vandekerckhove, J., Ampe, C., and Delepierre, M. (2000). Structural requirements for thymosin beta4 in its contact with actin.Eur. J. Biochem.267, 3530-3538.",
      "DOI": "10.1046/j.1432-1327.2000.01380.x"
    },
    {
      "key": "REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Small, J.V., Stradal, T., Vignal, E., and Rottner, K. (2002). The lamellipodium: where motility begins.Trends Cell Biol.12, 112-120.",
      "DOI": "10.1016/S0962-8924(01)02237-1"
    },
    {
      "key": "REF43",
      "doi-asserted-by": "crossref",
      "unstructured": "Spudich, J.A., and Watt, S. (1971). The regulation of rabbit skeletal muscle contraction.J. Biol. Chem.246, 4866-4871.",
      "DOI": "10.1016/S0021-9258(18)62016-2"
    },
    {
      "key": "REF44",
      "doi-asserted-by": "crossref",
      "unstructured": "Strome, S. (1986). Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans.J. Cell Biol.103, 2241-2252.",
      "DOI": "10.1083/jcb.103.6.2241"
    },
    {
      "key": "REF45",
      "unstructured": "Sulston, J., and Hodgkin, J. (1988). Methods. In: The NematodeCaenorhabditis elegans, ed. W.B. Woods, Cold Spring Harbor, NY: Cold Spring Harbor Press, 81-121"
    },
    {
      "key": "REF46",
      "doi-asserted-by": "crossref",
      "unstructured": "Vancompernolle, K., Vandekerckhove, J., Bubb, M.R., and Korn, E.D. (1991). The interfaces of actin andAcanthamoebaactobindin. Identification of a new actin-binding motif.J. Biol. Chem.266, 15427-15431.",
      "DOI": "10.1016/S0021-9258(18)98633-3"
    },
    {
      "key": "REF47",
      "doi-asserted-by": "crossref",
      "unstructured": "Vancompernolle, K., Goethals, M., Huet, C., Louvard, D., and Vandekerckhove, J. (1992). G- to F-actin modulation by a single amino acid substitution in the actin binding site of actobindin and thymosin\u03b24.EMBO J.11, 4739-4746.",
      "DOI": "10.1002/j.1460-2075.1992.tb05579.x"
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      "DOI": "10.1002/j.1460-2075.1996.tb00350.x"
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