Cytoneme-mediated cell-to-cell signaling during development

Cell and Tissue Research

Volumn 352, Issue 1, 2013, Pages 59-66

  Gradilla, Ana Citlali ^a   Guerrero, Isabel ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Cytonemes; Decapentaplegic (Dpp); Epithermal growth factor (EGF); Exovesicles; Fibroblast growth factor (FGF); Hedgehog; Notch Delta; Wnt

Indexed keywords

EPIDERMAL GROWTH FACTOR; EZRIN; FIBROBLAST GROWTH FACTOR; RADIXIN; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

CELL COMMUNICATION; CELL CONTACT; CELL DIFFERENTIATION; CELL GROWTH; CELL POLARITY; CYTONEME; DROSOPHILA; FILOPODIUM; INTERMEDIATE FILAMENT; MECHANOTRANSDUCTION; MORPHOGENESIS; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ANIMALS; CELL COMMUNICATION; GROWTH AND DEVELOPMENT; HUMANS; PSEUDOPODIA; SIGNAL TRANSDUCTION;

ANIMALIA; ERINACEIDAE;

EID: 84875241168     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1578-x     Document Type: Review

References (58)

1. Affolter M, Basler K (2011) Cell biology. Cytonemes show their colors. Science 332:312-313
2. Baeg GH, Lin X, Khare N, Baumgartner S, Perrimon N (2001) Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128:87-94
3. Beckett K, Monier S, Palmer L, Alexandre C, Green H, Bonneil E, Raposo G, Thibault P, Borgne RL, Vincent JP (2012) Drosophila S2 cells secrete Wingless on exosome-like vesicles but the Wingless gradient forms independently of exosomes. Traffic 14:82-96
4. Bilioni A, Sánchez-Hernández D, Callejo A, Gradilla AC, Ibáñez C, Mollica E, Carmen Rodríguez-Navas M, Simon E, Guerrero I (2012) Balancing hedgehog, a retention and release equilibrium given by Dally, Ihog, Boi and shifted/dWif. Dev Biol. doi: 10.1016/j.ydbio.2012.12.013
5. Block J, Stradal TE, Hänisch J, Geffers R, Köstler SA, Urban E, Small JV, Rottner K, Faix J (2008) Filopodia formation induced by active mDia2/Drf3. J Microsc 231:506-517
6. Callejo A, Bilioni A, Mollica E, Gorfinkiel N, Andrés G, Ibáñez C, Torroja C, Doglio L, Sierra J, 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 USA 108:12591-12598
7. Castrillon DH, Wasserman SA (1994) Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120:3367-3377
8. Chu T, Chiu M, Zhang E, Kunes S (2006) A C-terminal motif targets Hedgehog to axons, coordinating assembly of the Drosophila eye and brain. Dev Cell 10:635-646
9. Cohen M, Georgiou M, Stevenson NL, Miodownik M, Baum B (2010) Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. Dev Cell 19:78-89
10. Crick F (1970) Diffusion in embryogenesis. Nature 225:420-422
11. Davis DM, Sowinski S (2008) Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 9:431-436
12. De Joussineau C, Soulé J, Martin M, Anguille C, Montcourrier P, Alexandre D (2003) Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila. Nature 426:555-559
13. Entchev EV, Schwabedissen A, González-Gaitán M (2000) Gradient formation of the TGF-beta homolog Dpp. Cell 103:981-991
14. Georgiou M, Baum B (2010) Polarity proteins and Rho GTPases cooperate to spatially organise epithelial actin-based protrusions. J Cell Sci 123:1089-1098
15. Gerdes HH, Carvalho RN (2008) Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol 20:470-475
16. Gerdes HH, Rustom A, Wang X (2012) Tunneling nanotubes, an emerging intercellular communication route in development. Mech Dev (in press9
17. Gibson MC, Schubiger G (2000) Peripodial cells regulate proliferation and patterning of Drosophila imaginal discs. Cell 103:343-350
18. Greco V, Hannus M, Eaton S (2001) Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106:633-645
19. Gross JC, Chaudhary V, Bartscherer K, Boutros M (2012) Active Wnt proteins are secreted on exosomes. Nat Cell Biol 14:1036-1045
20. Guerrero I, Chiang C (2007) A conserved mechanism of Hedgehog gradient formation by lipid modifications. Trends Cell Biol 17:1-5
21. Hanna-Alava A (1958) Morphology and chaetotaxy of the legs of Drosophila melanogaster. J Morphol 103:281-310
22. Hsiung F, Ramirez-Weber FA, Iwaki DD, Kornberg TB (2005) Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature 437:560-563
23. Huang Z, Kunes S (1996) Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86:411-422
24. Kalinina J, Byron SA, Makarenkova HP, Olsen SK, Eliseenkova AV, Larochelle WJ, Dhanabal M, Blais S, Ornitz DM, Day LA, Neubert TA, Pollock PM, Mohammadi M (2009) Homodimerization controls the fibroblast growth factor 9 subfamily's receptor binding and heparan sulfate-dependent diffusion in the extracellular matrix. Mol Cell Biol 29:4663-4678
25. Kicheva A, Pantazis P, Bollenbach T, Kalaidzidis Y, Bittig T, Jülicher F, González-Gaitán M (2007) Kinetics of morphogen gradient formation. Science 315:521-525
26. Kimura S, Hase K, Ohno H (2012) The molecular basis of induction and formation of tunneling nanotubes. Cell Tissue Res (in press)
27. Koizumi K, Takano K, Kaneyasu A, Watanabe-Takano H, Tokuda E, Abe T, Watanabe N, Takenawa T, Endo T (2012) RhoD activated by fibroblast growth factor induces cytoneme-like cellular protrusions through mDia3C. Mol Biol Cell 23:4647-4661
28. Koles K, Nunnari J, Korkut C, Barria R, Brewer C, Li Y, Leszyk J, Zhang B, Budnik V (2012) Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 287:16820-16834
29. Korkut C, Ataman B, Ramachandran P, Ashley J, Barria R, Gherbesi N, Budnik V (2009) Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 139:393-404
30. Kornberg TB (2012) The imperative of context and contour for morphogen dispersion. Biophys J 103:2252-2256
31. Lawrence PA (2001) Morphogens: how big is the big picture? Nat Cell Biol 3:E151-E154
32. Miura GI, Treisman JE (2006) Lipid modification of secreted signaling proteins. Cell Cycle 5:1184-1188
33. Miura GI, Buglino J, Alvarado D, Lemmon MA, Resh MD, Treisman JE (2006) Palmitoylation of the EGFR ligand Spitz by rasp increases Spitz activity by restricting its diffusion. Dev Cell 10:167-176
34. Müller P, Rogers KW, Jordan BM, Lee JS, Robson D, Ramanathan SW, Schier AF (2012) Differential diffusivity of Nodal and Lefty underlies a reaction-diffusion patterning system. Science 336:721-724
35. Musse AA, Meloty-Kapella L, Weinmaster G (2012) Notch ligand endocytosis: mechanistic basis of signaling activity. Semin Cell Dev Biol 23:429-436
36. Panakova D, Sprong H, Marois E, Thiele C, Eaton S (2005) Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435:58-65
37. Peng Y, Han C, Axelrod JD (2012) Planar polarized protrusions break the symmetry of EGFR signaling during Drosophila bract cell fate induction. Dev Cell 23:507-518
38. Pepinsky RB, Zeng C, Wen D, Rayhorn P, Baker DP, Williams KP et al (1998) Identification of a palmitic acid-modified form of human Sonic hedgehog. J Biol Chem 273:14037-14045
39. Pyrgaki C, Trainor P, Hadjantonakis AK, Niswander L (2010) Dynamic imaging of mammalian neural tube closure. Dev Biol 344:941-947
40. Ramirez-Weber FA, Kornberg TB (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97:599-607
41. Reed CT, Murphy C, Fristrom D (1975) The ultrastructure of the differentiating pupal leg of Drosophila melanogaster. Roux's Arch Dev Biol 178:285-302
42. 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 Biol 10:e1001298
43. Roy S, Kornberg TB (2011) Direct delivery mechanisms of morphogen dispersion. Sci Signal 4:pt8
44. Roy S, Hsiung F, Kornberg TB (2011) Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332:354-358
45. Salas-Vidal E, Lomeli H (2004) Imaging filopodia dynamics in the mouse blastocyst. Dev Biol 265:75-89
46. Sato M, Kornberg TB (2002) FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev Cell 3:195-207
47. Schirenbeck A, Bretschneider T, Arasada R, Schleicher M, Faix J (2005) The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat Cell Biol 7:619-625
48. Steinhauer J, Treisman JE (2009) Lipid-modified morphogens: functions of fats. Curr Opin Genet Dev 19:308-314
49. Steinhauer J, Gijón MA, Riekhof WR, Voelker DR, Murphy RC, Treisman JE (2009) Drosophila lysophospholipid acyltransferases are specifically required for germ cell development. Mol Biol Cell 20:5224-5235
50. Tien AC, Rajan A, Bellen HJ (2009) A Notch updated. J Cell Biol 184:621-629
51. Walt H, Tobler H (1978) Ultrastructural analysis of differentiating bristles organs in wild type, shaven-depilated and Mytomycin C-treated larvae of Drosophila melanogaster. Biol Cell 32:291-298
52. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T et al (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448-452
53. Yan D, Wu Y, Yang Y, Belenkaya TY, Tang X, Lin X (2010) The cell-surface proteins Dally-like and Ihog differentially regulate Hedgehog signaling strength and range during development. Development 137:2033-2044
54. Yang C, Czech L, Gerboth S, Kojima S, Scita G, Svitkina T (2007) Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5:e317
55. Yu SR, Burkhardt M, Nowak M, Ries J, Petrásek Z, Scholpp S, Schwille P, Brand M (2009) Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461:533-536
56. Zeng X, Goetz JA, Suber LM, Scott WJ Jr, Schreiner CM, Robbins DJ (2001) A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature 411:716-720
57. Zheng X, Mann RK, Sever N, Beachy PA (2010) Genetic and biochemical definition of the Hedgehog receptor. Genes Dev 24:57-71
58. Zhou S, Lo WC, Suhalim JL, Digman MA, Gratton E, Nie Q, Lander AD (2012) Free extracellular diffusion creates the Dpp morphogen gradient of the Drosophila wing disc. Curr Biol 22:668-675