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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.[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] 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,[5] and subsequent characterizations support the idea that they convey patterning signals between cells.[6][7] 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,[8][9] 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][10] trachea,[11][12] lymph glands[13] and ovaries.[14] They have also been described in spider embryos,[15] earwig ovaries,[16] Rhodnius,[17] Calpodes,[17] earthworms,[18] retroviral-infected cells,[19] mast cells,[20] B-lymphocytes[21] and neutrophils.[22] 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[23] where they transport Wnt8a and of the chick limb where they transport Sonic hedgehog.[24]

References

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  1. ^ a b c d Ramírez-Weber FA, Kornberg TB (May 1999). "Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs". Cell. 97 (5): 599–607. doi:10.1016/S0092-8674(00)80771-0. PMID 10367889.
  2. ^ Callejo A, Bilioni A, Mollica E, Gorfinkiel N, Andrés G, Ibáñez C, Torroja C, Doglio L, Sierra J, Guerrero I (August 2011). "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. Bibcode:2011PNAS..10812591C. doi:10.1073/pnas.1106881108. PMC 3150953. PMID 21690386.
  3. ^ a b c Hsiung F, Ramirez-Weber FA, Iwaki DD, Kornberg TB (September 2005). "Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic". Nature. 437 (7058): 560–3. Bibcode:2005Natur.437..560H. doi:10.1038/nature03951. PMID 16177792. S2CID 4428028.
  4. ^ a b Roy S, Hsiung F, Kornberg TB (April 2011). "Specificity of Drosophila cytonemes for distinct signaling pathways". Science. 332 (6027): 354–8. Bibcode:2011Sci...332..354R. doi:10.1126/science.1198949. PMC 3109072. PMID 21493861.
  5. ^ Gustafson T, Wolpert L (January 1961). "Studies on the cellular basis of morphogenesis in the sea urchin embryo. Gastrulation in vegetalized larvae". Experimental Cell Research. 22: 437–49. doi:10.1016/0014-4827(61)90120-3. PMID 13709961.
  6. ^ Miller J, Fraser SE, McClay D (August 1995). "Dynamics of thin filopodia during sea urchin gastrulation". Development. 121 (8): 2501–11. doi:10.1242/dev.121.8.2501. PMID 7671814.
  7. ^ McClay DR (December 1999). "The role of thin filopodia in motility and morphogenesis". Experimental Cell Research. 253 (2): 296–301. doi:10.1006/excr.1999.4723. PMID 10585250.
  8. ^ Posakony LG, Raftery LA, Gelbart WM (December 1990). "Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary". Mechanisms of Development. 33 (1): 69–82. doi:10.1016/0925-4773(90)90136-a. PMID 2129012. S2CID 24420940.
  9. ^ Tabata T, Schwartz C, Gustavson E, Ali Z, Kornberg TB (October 1995). "Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis". Development. 121 (10): 3359–69. doi:10.1242/dev.121.10.3359. PMID 7588069.
  10. ^ Cohen M, Georgiou M, Stevenson NL, Miodownik M, Baum B (July 2010). "Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition". Developmental Cell. 19 (1): 78–89. doi:10.1016/j.devcel.2010.06.006. PMID 20643352.
  11. ^ Ribeiro C, Ebner A, Affolter M (May 2002). "In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis". Developmental Cell. 2 (5): 677–83. doi:10.1016/S1534-5807(02)00171-5. PMID 12015974.
  12. ^ Sato M, Kornberg TB (August 2002). "FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system". Developmental Cell. 3 (2): 195–207. doi:10.1016/S1534-5807(02)00202-2. PMID 12194851.
  13. ^ Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U (March 2007). "A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors". Nature. 446 (7133): 320–4. Bibcode:2007Natur.446..320M. doi:10.1038/nature05585. PMC 2807630. PMID 17361183.
  14. ^ Rojas-Ríos P, Guerrero I, González-Reyes A (2012). "Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila". PLOS Biology. 10 (4): e1001298. doi:10.1371/journal.pbio.1001298. PMC 3317903. PMID 22509132.
  15. ^ Akiyama-Oda Y, Oda H (May 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. doi:10.1242/dev.00390. PMID 12642480.
  16. ^ Tworzydlo W, Kloc M, Bilinski SM (May 2010). "Female germline stem cell niches of earwigs are structurally simple and different from those of Drosophila melanogaster". Journal of Morphology. 271 (5): 634–40. doi:10.1002/jmor.10824. PMID 20029934. S2CID 28360965.
  17. ^ a b Locke M (1987). "The very rapid induction of filopodia in insect cells". Tissue & Cell. 19 (2): 301–18. doi:10.1016/0040-8166(87)90014-0. PMID 18620200.
  18. ^ Kasschau MR, Ngo TD, Sperber LM, Tran KL (2007). "Formation of filopodia in earthworm (Lumbricus terrestris) coelomocytes in response to osmotic stress". Zoology. 110 (1): 66–76. doi:10.1016/j.zool.2006.07.002. PMID 17174079.
  19. ^ Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W (March 2007). "Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission". Nature Cell Biology. 9 (3): 310–5. doi:10.1038/ncb1544. PMC 2628976. PMID 17293854.
  20. ^ Fifadara NH, Beer F, Ono S, Ono SJ (February 2010). "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. doi:10.1093/intimm/dxp118. PMC 2825160. PMID 20173038.
  21. ^ Gupta N, DeFranco AL (February 2003). "Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation". Molecular Biology of the Cell. 14 (2): 432–44. doi:10.1091/mbc.02-05-0078. PMC 149983. PMID 12589045.
  22. ^ Galkina SI, Molotkovsky JG, Ullrich V, Sud'ina GF (April 2005). "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. doi:10.1016/j.yexcr.2004.12.005. PMID 15748905.
  23. ^ Stanganello E, Hagemann AI, Mattes B, Sinner C, Meyen D, Weber S, Schug A, Raz E, Scholpp S (January 2015). "Filopodia-based Wnt transport during vertebrate tissue patterning". Nature Communications. 6: 5846. Bibcode:2015NatCo...6.5846S. doi:10.1038/ncomms6846. PMID 25556612.
  24. ^ Sanders TA, Llagostera E, Barna M (May 2013). "Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning". Nature. 497 (7451): 628–32. Bibcode:2013Natur.497..628S. doi:10.1038/nature12157. PMC 4197975. PMID 23624372.
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