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Signaling filopodia in avian embryogenesis: formation and function

  • Received: 30 August 2016 Accepted: 18 November 2016 Published: 22 November 2016
  • In vertebrates and invertebrates specialized cellular protrusions, called signaling filopodia or cytonemes, play an important role in cell-cell communication by carrying receptors and ligands to distant cells to activate various signaling pathways. In the chicken embryo, signaling filopodia were described in limb bud mesenchyme and in somite epithelia. The formation of signaling filopodia depends on the activity of Rho GTPases and reorganization of the cytoskeleton. Here, we give a short overview on the present knowledge on avian signaling filopodia and discuss the molecular basis of cytoskeletal rearrangements leading to filopodia formation.

    Citation: Margarethe Draga, Martin Scaal, Felicitas Pröls. Signaling filopodia in avian embryogenesis: formation and function[J]. AIMS Molecular Science, 2016, 3(4): 683-691. doi: 10.3934/molsci.2016.4.683

    Related Papers:

  • In vertebrates and invertebrates specialized cellular protrusions, called signaling filopodia or cytonemes, play an important role in cell-cell communication by carrying receptors and ligands to distant cells to activate various signaling pathways. In the chicken embryo, signaling filopodia were described in limb bud mesenchyme and in somite epithelia. The formation of signaling filopodia depends on the activity of Rho GTPases and reorganization of the cytoskeleton. Here, we give a short overview on the present knowledge on avian signaling filopodia and discuss the molecular basis of cytoskeletal rearrangements leading to filopodia formation.


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    [1] Gustafson T, Wolpert L (1967) Cellular movement and contact in sea urchin morphogenesis. Biol Rev Camb Philos Soc 42: 442-498. doi: 10.1111/j.1469-185X.1967.tb01482.x
    [2] Miller J, Fraser SE, McClay D (1995) Dynamics of thin filopodia during sea urchin gastrulation. Development 121: 2501-2511.
    [3] Ramirez-Weber FA, Kornberg TB (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97: 599-607. doi: 10.1016/S0092-8674(00)80771-0
    [4] Roy S, Huang H, Liu S, et al. (2014) Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein. Science 343: 1244624. doi: 10.1126/science.1244624
    [5] Kornberg TB (2014) Cytonemes and the dispersion of morphogens. Wiley Interdiscip Rev Dev Biol 3: 445-463. doi: 10.1002/wdev.151
    [6] Prols F, Sagar, Scaal M (2016) Signaling filopodia in vertebrate embryonic development. Cell Mol Life Sci 73: 961-974. doi: 10.1007/s00018-015-2097-6
    [7] Sanders TA, Llagostera E, Barna M (2013) Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning. Nature 497: 628-632. doi: 10.1038/nature12157
    [8] Yang Y, Drossopoulou G, Chuang PT, et al. (1997) Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124: 4393-4404.
    [9] Sagar, Prols F, Wiegreffe C, et al. (2015) Communication between distant epithelial cells by filopodia-like protrusions during embryonic development. Development 142: 665-671. doi: 10.1242/dev.115964
    [10] Holzer T, Liffers K, Rahm K, et al. (2012) Live imaging of active fluorophore labelled Wnt proteins. FEBS Lett 586: 1638-1644. doi: 10.1016/j.febslet.2012.04.035
    [11] Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1121. doi: 10.1038/ncb1007-1110
    [12] Rengan R, Ochs HD (2000) Molecular biology of the Wiskott-Aldrich syndrome. Rev Immunogenet 2: 243-255.
    [13] Pruyne D, Evangelista M, Yang C, et al. (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615. doi: 10.1126/science.1072309
    [14] Sagot I, Rodal AA, Moseley J, et al. (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4: 626-631.
    [15] Goode BL, Eck MJ (2007) Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76: 593-627. doi: 10.1146/annurev.biochem.75.103004.142647
    [16] Yang C, Czech L, Gerboth S, et al. (2007) Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5: e317. doi: 10.1371/journal.pbio.0050317
    [17] Bravo-Cordero JJ, Magalhaes MA, Eddy RJ, et al. (2013) Functions of cofilin in cell locomotion and invasion. Nat Rev Mol Cell Biol 14: 405-415. doi: 10.1038/nrm3609
    [18] Yamashiro-Matsumura S, Matsumura F (1985) Purification and characterization of an F-actin-bundling 55-kilodalton protein from HeLa cells. J Biol Chem 260: 5087-5097.
    [19] Yang S, Huang FK, Huang J, et al. (2013) Molecular mechanism of fascin function in filopodial formation. J Biol Chem 288: 274-284. doi: 10.1074/jbc.M112.427971
    [20] Mattila PK, Lappalainen P (2008) Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9: 446-454. doi: 10.1038/nrm2406
    [21] Vignjevic D, Kojima S, Aratyn Y, et al. (2006) Role of fascin in filopodial protrusion. J Cell Biol 174: 863-875. doi: 10.1083/jcb.200603013
    [22] Huang FK, Han S, Xing B, et al. (2015) Targeted inhibition of fascin function blocks tumour invasion and metastatic colonization. Nat Commun 6: 7465. doi: 10.1038/ncomms8465
    [23] George SP, Chen H, Conrad JC, et al. (2013) Regulation of directional cell migration by membrane-induced actin bundling. J Cell Sci 126: 312-326. doi: 10.1242/jcs.116244
    [24] Khurana S, George SP (2011) The role of actin bundling proteins in the assembly of filopodia in epithelial cells. Cell Adh Migr 5: 409-420. doi: 10.4161/cam.5.5.17644
    [25] Kerber ML, Cheney RE (2011) Myosin-X: a MyTH-FERM myosin at the tips of filopodia. J Cell Sci 124: 3733-3741. doi: 10.1242/jcs.023549
    [26] Ohi R, Zanic M (2016) Ahead of the Curve: New Insights into Microtubule Dynamics. F1000Res 5: 314. doi: 10.12688/f1000research.7439.1
    [27] Bhabha G, Johnson GT, Schroeder CM, et al. (2016) How Dynein Moves Along Microtubules. Trends Biochem Sci 41: 94-105. doi: 10.1016/j.tibs.2015.11.004
    [28] Francou A, Saint-Michel E, Mesbah K, et al. (2014) TBX1 regulates epithelial polarity and dynamic basal filopodia in the second heart field. Development 141: 4320-4331. doi: 10.1242/dev.115022
    [29] Salas-Vidal E, Lomeli H (2004) Imaging filopodia dynamics in the mouse blastocyst. Dev Biol 265: 75-89. doi: 10.1016/j.ydbio.2003.09.012
    [30] Koizumi K, Takano K, Kaneyasu A, et al. (2012) RhoD activated by fibroblast growth factor induces cytoneme-like cellular protrusions through mDia3C. Mol Biol Cell 23: 4647-4661. doi: 10.1091/mbc.E12-04-0315
    [31] Ketschek A, Jones S, Spillane M, et al. (2015) Nerve growth factor promotes reorganization of the axonal microtubule array at sites of axon collateral branching. Dev Neurobiol 75: 1441-1461. doi: 10.1002/dneu.22294
    [32] Eira J, Silva CS, Sousa MM, et al. (2016) The cytoskeleton as a novel therapeutic target for old neurodegenerative disorders. Prog Neurobiol 141: 61-82. doi: 10.1016/j.pneurobio.2016.04.007
    [33] Lin C, Schuster M, Guimaraes SC, et al. (2016) Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells. Nat Commun 7: 11814. doi: 10.1038/ncomms11814
    [34] Roy S, Hsiung F, Kornberg TB (2011) Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332: 354-358. doi: 10.1126/science.1198949
    [35] Ridley AJ, Hall A (1994) Signal transduction pathways regulating Rho-mediated stress fibre formation: requirement for a tyrosine kinase. EMBO J 13: 2600-2610.
    [36] Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399. doi: 10.1016/0092-8674(92)90163-7
    [37] Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514. doi: 10.1126/science.279.5350.509
    [38] Ridley AJ (1995) Rho-related proteins: actin cytoskeleton and cell cycle. Curr Opin Genet Dev 5: 24-30. doi: 10.1016/S0959-437X(95)90049-7
    [39] Machesky LM, Hall A (1996) Rho: a connection between membrane receptor signalling and the cytoskeleton. Trends Cell Biol 6: 304-310. doi: 10.1016/0962-8924(96)10026-X
    [40] Boureux A, Vignal E, Faure S, et al. (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol 24: 203-216.
    [41] Van Aelst L, D'Souza-Schorey C (1997) Rho GTPases and signaling networks. Genes Dev 11: 2295-2322. doi: 10.1101/gad.11.18.2295
    [42] Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90: 259-289. doi: 10.1152/physrev.00036.2009
    [43] Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17: 295-309. doi: 10.1101/gad.1022203
    [44] Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107: 843-854. doi: 10.1016/S0092-8674(01)00614-6
    [45] Schiller MR (2006) Coupling receptor tyrosine kinases to Rho GTPases--GEFs what's the link. Cell Signal 18: 1834-1843. doi: 10.1016/j.cellsig.2006.01.022
    [46] Stanganello E, Hagemann AI, Mattes B, et al. (2015) Filopodia-based Wnt transport during vertebrate tissue patterning. Nat Commun 6: 5846. doi: 10.1038/ncomms6846
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