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Cytoneme

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Cytonemes take up and transport morphogens. This Micrograph shows tissues from a Drosophila larva whose tracheal cells are marked with membrane-tethered mCherry fluorescent protein. Some of the cytonemes that extend from the tracheal branch contact the underlying wing imaginal disc and transport the Dpp morphogen protein (marked with Green Fluorescent Protein) to the tracheal cells.

Cytonemes are thin, cellular projections that are specialized for exchange of signaling proteins between cells.[1] Cytonemes emanate from cells that make signaling proteins, extending directly to cells that receive signaling proteins.[2] Cytonemes also extend directly from cells that receive signaling proteins to cells that make them.[1][3][4]
A cytoneme is a type of filopodium - a thin, tubular extension of a cell’s plasma membrane that has a core composed of tightly bundled, parallel actin filaments. Filopodia can extend more than 100 μm and have been measured as thin as 0.1 μm and as thick as 0.5 μm. Cytonemes with a diameter of approximately 0.2 μm and as long as 80 μm have been observed in the Drosophila wing imaginal disc[1]

Many cell types have filopodia. The functions of filopodia have been attributed to pathfinding of neurons,[5] early stages of synapse formation,[6] antigen presentation by dendritic cells of the immune system,[7] force generation by macrophages[8] and virus transmission.[9] They have been associated with wound closure,[10] dorsal closure of Drosophila embryos,[11] chemotaxis in Dictyostelium,[12] Delta-Notch signaling,[13] vasculogenesis,[14] cell adhesion,[15] cell migration, and cancer metastasis. Filopodia have been given various names: microspikes, pseudopods, thin filopodia,[16] thick filopodia,[17] gliopodia,[18] myopodia,[19] invadopodia,[20] podosomes,[21] telopodes,[22] tunneling nanotubes[23] and dendrites. The term cytoneme was coined to denote the presence of cytoplasm in their interior (cyto-) and their finger-like appearance (-neme), and to distinguish their role as signaling, rather than structural or force-generating, organelles.

Filopodia with behaviors suggestive of roles in sensing patterning information were first observed in sea urchin embryos,[24] and subsequent characterizations support the idea that they convey patterning signals between cells.[16][17] The discovery of cytonemes in Drosophila imaginal discs[1] correlated for the first time the presence and behavior of filopodia with a known morphogen signaling protein - Decapentaplegic. Decapentaplegic is expressed in the wing disc by cells that function as a developmental organizer,[25][26] and cytonemes that are responsive to Decapentaplegic orient toward this developmental organizer. Receptors for signaling proteins are present in motile vesicles in cytonemes,[3] and receptors for different signaling proteins segregate specifically to different types of cytonemes.[4] In Drosophila, cytonemes have been found in wing and eye imaginal discs,[3][13][27] lymph glands[28] and ovaries.[29] They have also been described in spider embryos,[30] earwig ovaries,[31] Rhodnius,[32] Calpodes,[32] earthworms,[33] retroviral-infected cells,[34] mast cells,[35] B-lymphocytes[36] and neutrophils.[37] Recent obserrvations suggest that cytonemes have also an important role during vertebrate development. Recent observations suggest that cytonemes also have an important role during development of the zebrafish neural plate [38] where they transport Wnt8a and of the chick limb where they transport Sonic hedgehog. [39]

References

  1. ^ a b c d Ramirez-Weber FA and Kornberg TB (1999) "Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs" Cell 97 (5): 599-607 PMID 10367889.
  2. ^ Callejo A, Bilioni A, Mollica E, Gorfinkiel N, Andres G, Ibanez C, Torroja C, Doglio L, Sierra J, and Guerrero I (2011) "Dispatched mediates Hedgehog basolateral release to form the long-range morphogenetic gradient in the Drosophila wing disk epithelium" Proc Natl Acad Sci U S A 108 (31): 12591-8 DOI: 10.1073/pnas.1106881108 PMID 21690386.
  3. ^ a b c Hsiung F, Ramirez-Weber FA, Iwaki DD, and Kornberg TB (2005) "Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic" Nature 437 (7058): 560-3 DOI: 10.1038/nature03951 PMID 16177792.
  4. ^ a b Roy S, Hsiung F, and Kornberg TB (2011) "Specificity of Drosophila cytonemes for distinct signaling pathways" Science 332 (6027): 354-8 DOI: 10.1126/science.1198949 PMID 21493861.
  5. ^ Bentley D and Toroian-Raymond A (1986) "Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment" Nature 323 (6090): 712-5 DOI: 10.1038/323712a0 PMID 3773996.
  6. ^ Yuste R and Bonhoeffer T (2004) "Genesis of dendritic spines: insights from ultrastructural and imaging studies" Nat Rev Neurosci 5 (1): 24-34 DOI: 10.1038/nrn1300 PMID 14708001.
  7. ^ Raghunathan A, Sivakamasundari R, Wolenski J, Poddar R, and Weissman SM (2001) "Functional analysis of B144/LST1: a gene in the tumor necrosis factor cluster that induces formation of long filopodia in eukaryotic cells" Exp Cell Res 268 (2): 230-44 DOI: S0014-4827(01)95290-5 [pii] PMID 11478849.
  8. ^ Kress H, Stelzer EH, Holzer D, Buss F, Griffiths G, and Rohrbach A (2007) "Filopodia act as phagocytic tentacles and pull with discrete steps and a load-dependent velocity" Proc Natl Acad Sci U S A 104 (28): 11633-8 DOI: 10.1073/pnas.0702449104 PMID 17620618.
  9. ^ Lehmann MJ, Sherer NM, Marks CB, Pypaert M, and Mothes W (2005) "Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells" J Cell Biol 170 (2): 317-25 DOI: 10.1083/jcb.200503059 PMID 16027225.
  10. ^ Crosson CE, Klyce SD, and Beuerman RW (1986) "Epithelial wound closure in the rabbit cornea. A biphasic process" Invest Ophthalmol Vis Sci 27 (4): 464-73 PMID 3957565.
  11. ^ Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, and Martin P (2000) "Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure" Curr Biol 10 (22): 1420-6 DOI: S0960-9822(00)00796-X [pii] PMID 11102803.
  12. ^ Han YH, Chung CY, Wessels D, Stephens S, Titus MA, Soll DR, and Firtel RA (2002) "Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in dictyostelium" J Biol Chem 277 (51): 49877-87 DOI: 10.1074/jbc.M209107200 PMID 12388544.
  13. ^ a b Cohen M, Georgiou M, Stevenson NL, Miodownik M, and Baum B (2010) "Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition" Dev Cell 19 (1): 78-89 DOI: 10.1016/j.devcel.2010.06.006 PMID 20643352. Cite error: The named reference "cytoneme6" was defined multiple times with different content (see the help page).
  14. ^ Lawson ND and Weinstein BM (2002) "In vivo imaging of embryonic vascular development using transgenic zebrafish" Dev Biol 248 (2): 307-18 PMID 12167406.
  15. ^ Vasioukhin V, Bauer C, Yin M, and Fuchs E (2000) "Directed actin polymerization is the driving force for epithelial cell-cell adhesion" Cell 100 (2): 209-19 DOI: S0092-8674(00)81559-7 [pii] PMID 10660044.
  16. ^ a b Miller J, Fraser SE, and McClay D (1995) "Dynamics of thin filopodia during sea urchin gastrulation" Development 121 (8): 2501-2511.
  17. ^ a b McClay DR (1999) "The role of thin filopodia in motility and morphogenesis" Exp Cell Res 253 (2): 296-301 DOI: S0014-4827(99)94723-7 [pii] PMID 10585250.
  18. ^ Vasenkova I, Luginbuhl D, and Chiba A (2006) "Gliopodia extend the range of direct glia-neuron communication during the CNS development in Drosophila" Mol Cell Neurosci 31 (1): 123-30 DOI: 10.1016/j.mcn.2005.10.001 PMID 16298140.
  19. ^ Ritzenthaler S, Suzuki E, and Chiba A (2000) "Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons" Nat Neurosci 3 (10): 1012-7 PMID 11017174.
  20. ^ Chen WT (1989) "Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells" J Exp Zool 251 (2): 167-85 DOI: 10.1002/jez.1402510206 PMID 2549171.
  21. ^ Tarone G, Cirillo D, Giancotti FG, Comoglio PM, and Marchisio PC (1985) "Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes" Exp Cell Res 159 (1): 141-57 DOI: S0014-4827(85)80044-6 [pii] PMID 2411576.
  22. ^ Popescu LM and Faussone-Pellegrini MS (2010) "TELOCYTES - a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES" J Cell Mol Med 14 (4): 729-40 DOI: 10.1111/j.1582-4934.2010.01059.x PMID 20367664.
  23. ^ Rustom A, Saffrich R, Markovic I, Walther P, and Gerdes HH (2004) "Nanotubular highways for intercellular organelle transport" Science 303 (5660): 1007-10 PMID 14963329.
  24. ^ Gustafson T and Wolpert L (1961) "Studies on the cellular basis of morphogenesis in the sea urchin embryo. Gastrulation in vegetalized larvae" Experimental Cell Research 22: 437-449.
  25. ^ Posakony LG, Raftery LA, and Gelbart WM (1990) "Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary" Mech Dev 33 (1): 69-82 PMID 2129012.
  26. ^ Tabata T, Schwartz C, Gustavson E, Ali Z, and Kornberg TB (1995) "Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis" Development 121 (10): 3359-69.
  27. ^ Sato M and Kornberg TB (2002) "FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system" Dev Cell 3 (2): 195-207 PMID 12194851.
  28. ^ Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, and Banerjee U (2007) "A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors" Nature 446 (7133): 320-4 DOI: 10.1038/nature05585 PMID 17361183.
  29. ^ Rojas-Rios P, Guerrero I, and Gonzalez-Reyes A (2012) "Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila" PLoS Biol 10 (4): e1001298 DOI: 10.1371/journal.pbio.1001298 PMID 22509132.
  30. ^ Akiyama-Oda Y and Oda H (2003) "Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells" Development 130 (9): 1735-47 PMID 12642480.
  31. ^ Tworzydlo W, Kloc M, and Bilinski SM (2009) "Female germline stem cell niches of earwigs are structurally simple and different from those of Drosophila melanogaster" J Morphol 271 (5): 634-40 DOI: 10.1002/jmor.10824 PMID 20029934.
  32. ^ a b Locke M (1987) "The very rapid induction of filopodia in insect cells" Tissue Cell 19 (2): 301-18 DOI: 0040-8166(87)90014-0 [pii] PMID 18620200.
  33. ^ Kasschau MR, Ngo TD, Sperber LM, and Tran KL (2007) "Formation of filopodia in earthworm (Lumbricus terrestris) coelomocytes in response to osmotic stress" Zoology (Jena) 110 (1): 66-76 DOI: 10.1016/j.zool.2006.07.002 PMID 17174079.
  34. ^ Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, and Mothes W (2007) "Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission" Nat Cell Biol 9 (3): 310-5 DOI: 10.1038/ncb1544 PMID 17293854.
  35. ^ Fifadara NH, Beer F, Ono S, and Ono SJ (2010) "Interaction between activated chemokine receptor 1 and FcepsilonRI at membrane rafts promotes communication and F-actin-rich cytoneme extensions between mast cells" Int Immunol 22 (2): 113-28 DOI: 10.1093/intimm/dxp118 PMID 20173038.
  36. ^ Gupta N and DeFranco AL (2003) "Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation" Mol Biol Cell 14 (2): 432-44 DOI: 10.1091/mbc.02-05-0078 PMID 12589045.
  37. ^ Galkina SI, Molotkovsky JG, Ullrich V, and Sud'ina GF (2005) "Scanning electron microscopy study of neutrophil membrane tubulovesicular extensions (cytonemes) and their role in anchoring, aggregation and phagocytosis. The effect of nitric oxide" Exp Cell Res 304 (2): 620-9 DOI: 10.1016/j.yexcr.2004.12.005 PMID 15748905.
  38. ^ Stanganello, E., A.I. Hagemann, B. Mattes, C. Sinner, D. Meyen, S. Weber, A. Schug, E. Raz, and S. Scholpp (2015) "Filopodia-based Wnt transport during vertebrate tissue patterning" Nat Commun 6: p. 5846 10.1038/ncomms6846
  39. ^ Sanders, T.A., E. Llagostera, and M. Barna (2013) "Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning" Nature 497(7451): p. 628-32 10.1038/nature12157
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