Biology: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.[citation needed]

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][14] vasculogenesis,[15] cell adhesion,[16] cell migration, and cancer metastasis. Filopodia have been given various names: microspikes, pseudopods, thin filopodia,[17] thick filopodia,[18] gliopodia,[19] myopodia,[20] invadopodia,[21] podosomes,[22] telopodes,[23] tunneling nanotubes[24] 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.[citation needed]

Filopodia with behaviors suggestive of roles in sensing patterning information were first observed in sea urchin embryos,[25] and subsequent characterizations support the idea that they convey patterning signals between cells.[17][18] 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,[26][27] 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] trachea,[28][29] lymph glands[30] and ovaries.[31] They have also been described in spider embryos,[32] earwig ovaries,[33] Rhodnius,[34] Calpodes,[34] earthworms,[35] retroviral-infected cells,[36] mast cells,[37] B-lymphocytes[38] and neutrophils.[39] Recent observations 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[40] where they transport Wnt8a and of the chick limb where they transport Sonic hedgehog.[41]

References

  1. ↑ 1.0 1.1 1.2 1.3 "Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs". Cell 97 (5): 599–607. May 1999. doi:10.1016/S0092-8674(00)80771-0. PMID 10367889. 
  2. ↑ "Dispatched mediates Hedgehog basolateral release to form the long-range morphogenetic gradient in the Drosophila wing disk epithelium". Proceedings of the National Academy of Sciences of the United States of America 108 (31): 12591–8. August 2011. doi:10.1073/pnas.1106881108. PMID 21690386. Bibcode: 2011PNAS..10812591C. 
  3. ↑ 3.0 3.1 3.2 "Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic". Nature 437 (7058): 560–3. September 2005. doi:10.1038/nature03951. PMID 16177792. Bibcode: 2005Natur.437..560H. 
  4. ↑ 4.0 4.1 "Specificity of Drosophila cytonemes for distinct signaling pathways". Science 332 (6027): 354–8. April 2011. doi:10.1126/science.1198949. PMID 21493861. Bibcode: 2011Sci...332..354R. 
  5. ↑ "Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment". Nature 323 (6090): 712–5. 1986. doi:10.1038/323712a0. PMID 3773996. Bibcode: 1986Natur.323..712B. 
  6. ↑ "Genesis of dendritic spines: insights from ultrastructural and imaging studies". Nature Reviews. Neuroscience 5 (1): 24–34. January 2004. doi:10.1038/nrn1300. PMID 14708001. 
  7. ↑ "Functional analysis of B144/LST1: a gene in the tumor necrosis factor cluster that induces formation of long filopodia in eukaryotic cells". Experimental Cell Research 268 (2): 230–44. August 2001. doi:10.1006/excr.2001.5290. PMID 11478849. 
  8. ↑ "Filopodia act as phagocytic tentacles and pull with discrete steps and a load-dependent velocity". Proceedings of the National Academy of Sciences of the United States of America 104 (28): 11633–8. July 2007. doi:10.1073/pnas.0702449104. PMID 17620618. Bibcode: 2007PNAS..10411633K. 
  9. ↑ "Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells". The Journal of Cell Biology 170 (2): 317–25. July 2005. doi:10.1083/jcb.200503059. PMID 16027225. 
  10. ↑ "Epithelial wound closure in the rabbit cornea. A biphasic process". Investigative Ophthalmology & Visual Science 27 (4): 464–73. April 1986. PMID 3957565. http://iovs.arvojournals.org/article.aspx?volume=27&page=464. 
  11. ↑ "Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure". Current Biology 10 (22): 1420–6. November 2000. doi:10.1016/S0960-9822(00)00796-X. PMID 11102803. 
  12. ↑ "Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in dictyostelium". The Journal of Biological Chemistry 277 (51): 49877–87. December 2002. doi:10.1074/jbc.M209107200. PMID 12388544. 
  13. ↑ 13.0 13.1 "Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition". Developmental Cell 19 (1): 78–89. July 2010. doi:10.1016/j.devcel.2010.06.006. PMID 20643352. 
  14. ↑ "Coupling dynamics of 2D Notch-Delta signalling". Mathematical Biosciences 360 (1). June 2023. doi:10.1016/j.mbs.2023.109012. PMID 37142213. 
  15. ↑ "In vivo imaging of embryonic vascular development using transgenic zebrafish". Developmental Biology 248 (2): 307–18. August 2002. doi:10.1006/dbio.2002.0711. PMID 12167406. 
  16. ↑ "Directed actin polymerization is the driving force for epithelial cell-cell adhesion". Cell 100 (2): 209–19. January 2000. doi:10.1016/S0092-8674(00)81559-7. PMID 10660044. 
  17. ↑ 17.0 17.1 "Dynamics of thin filopodia during sea urchin gastrulation". Development 121 (8): 2501–11. August 1995. doi:10.1242/dev.121.8.2501. PMID 7671814. http://dev.biologists.org/cgi/pmidlookup?view=long&pmid=7671814. 
  18. ↑ 18.0 18.1 "The role of thin filopodia in motility and morphogenesis". Experimental Cell Research 253 (2): 296–301. December 1999. doi:10.1006/excr.1999.4723. PMID 10585250. 
  19. ↑ "Gliopodia extend the range of direct glia-neuron communication during the CNS development in Drosophila". Molecular and Cellular Neurosciences 31 (1): 123–30. January 2006. doi:10.1016/j.mcn.2005.10.001. PMID 16298140. 
  20. ↑ "Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons". Nature Neuroscience 3 (10): 1012–7. October 2000. doi:10.1038/79833. PMID 11017174. 
  21. ↑ "Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells". The Journal of Experimental Zoology 251 (2): 167–85. August 1989. doi:10.1002/jez.1402510206. PMID 2549171. 
  22. ↑ "Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes". Experimental Cell Research 159 (1): 141–57. July 1985. doi:10.1016/S0014-4827(85)80044-6. PMID 2411576. 
  23. ↑ "TELOCYTES - a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES". Journal of Cellular and Molecular Medicine 14 (4): 729–40. April 2010. doi:10.1111/j.1582-4934.2010.01059.x. PMID 20367664. 
  24. ↑ "Nanotubular highways for intercellular organelle transport". Science 303 (5660): 1007–10. February 2004. doi:10.1126/science.1093133. PMID 14963329. Bibcode: 2004Sci...303.1007R. 
  25. ↑ "Studies on the cellular basis of morphogenesis in the sea urchin embryo. Gastrulation in vegetalized larvae". Experimental Cell Research 22: 437–49. January 1961. doi:10.1016/0014-4827(61)90120-3. PMID 13709961. 
  26. ↑ "Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary". Mechanisms of Development 33 (1): 69–82. December 1990. doi:10.1016/0925-4773(90)90136-a. PMID 2129012. 
  27. ↑ "Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis". Development 121 (10): 3359–69. October 1995. doi:10.1242/dev.121.10.3359. PMID 7588069. http://dev.biologists.org/cgi/pmidlookup?view=long&pmid=7588069. 
  28. ↑ "In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis". Developmental Cell 2 (5): 677–83. May 2002. doi:10.1016/S1534-5807(02)00171-5. PMID 12015974. 
  29. ↑ "FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system". Developmental Cell 3 (2): 195–207. August 2002. doi:10.1016/S1534-5807(02)00202-2. PMID 12194851. 
  30. ↑ "A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors". Nature 446 (7133): 320–4. March 2007. doi:10.1038/nature05585. PMID 17361183. Bibcode: 2007Natur.446..320M. 
  31. ↑ "Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila". PLOS Biology 10 (4): e1001298. 2012. doi:10.1371/journal.pbio.1001298. PMID 22509132. 
  32. ↑ "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. May 2003. doi:10.1242/dev.00390. PMID 12642480. http://dev.biologists.org/cgi/pmidlookup?view=long&pmid=12642480. 
  33. ↑ "Female germline stem cell niches of earwigs are structurally simple and different from those of Drosophila melanogaster". Journal of Morphology 271 (5): 634–40. May 2010. doi:10.1002/jmor.10824. PMID 20029934. 
  34. ↑ 34.0 34.1 "The very rapid induction of filopodia in insect cells". Tissue & Cell 19 (2): 301–18. 1987. doi:10.1016/0040-8166(87)90014-0. PMID 18620200. 
  35. ↑ "Formation of filopodia in earthworm (Lumbricus terrestris) coelomocytes in response to osmotic stress". Zoology 110 (1): 66–76. 2007. doi:10.1016/j.zool.2006.07.002. PMID 17174079. 
  36. ↑ "Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission". Nature Cell Biology 9 (3): 310–5. March 2007. doi:10.1038/ncb1544. PMID 17293854. 
  37. ↑ "Interaction between activated chemokine receptor 1 and FcepsilonRI at membrane rafts promotes communication and F-actin-rich cytoneme extensions between mast cells". International Immunology 22 (2): 113–28. February 2010. doi:10.1093/intimm/dxp118. PMID 20173038. 
  38. ↑ "Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation". Molecular Biology of the Cell 14 (2): 432–44. February 2003. doi:10.1091/mbc.02-05-0078. PMID 12589045. 
  39. ↑ "Scanning electron microscopy study of neutrophil membrane tubulovesicular extensions (cytonemes) and their role in anchoring, aggregation and phagocytosis. The effect of nitric oxide". Experimental Cell Research 304 (2): 620–9. April 2005. doi:10.1016/j.yexcr.2004.12.005. PMID 15748905. 
  40. ↑ "Filopodia-based Wnt transport during vertebrate tissue patterning". Nature Communications 6: 5846. January 2015. doi:10.1038/ncomms6846. PMID 25556612. Bibcode: 2015NatCo...6.5846S. 
  41. ↑ "Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning". Nature 497 (7451): 628–32. May 2013. doi:10.1038/nature12157. PMID 23624372. Bibcode: 2013Natur.497..628S. 



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