Endocytic trafficking during Drosophila development

Mechanisms of Development

Volumn 120, Issue 11, 2003, Pages 1265-1282

  González Gaitán, Marcos ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Decapentaplegic; Delta; Endocytic trafficking; Hedgehog; Morphogenetic signaling; Morphogens; Notch; Wingless

Indexed keywords

CANCER GROWTH FACTOR; CHOLESTEROL;

BUDDING; CELL COMMUNICATION; CELL CULTURE; CELL DIVISION; CELL FUSION; CELL INTERACTION; CELL MATURATION; CELL MEMBRANE; CELL MOTILITY; CELL VACUOLE; CYTOLOGY; DIFFUSION; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; INSECT DEVELOPMENT; LYSOSOME; MAMMAL CELL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ERINACEIDAE; MAMMALIA;

EID: 0242413168     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2003.06.002     Document Type: Article

References (92)

1. Alexandre C., Lecourtois M., Vincent J. Wingless and Hedgehog pattern Drosophila denticle belts by regulating the production of short-range signals. Development. 126:1999;5689-5698.
2. Banerjee U., Renfranz P.J., Hinton D.R., Rabin B.A., Benzer S. The sevenless+ protein is expressed apically in cell membranes of developing Drosophila retina; it is not restricted to cell R7. Cell. 51:1987;151-158.
3. Beachy P.A., Cooper M.K., Young K.E., von Kessler D.P., Park W.J., Hall T.M., et al. Multiple roles of cholesterol in hedgehog protein biogenesis and signaling. Cold Spring Harb Symp Quant Biol. 62:1997;191-204.
4. Bejsovec A., Wieschaus E. Signaling activities of the Drosophila wingless gene are separately mutable and appear to be transduced at the cell surface. Genetics. 139:1995;309-320.
5. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 394:1998;85-88.
6. Bennett D., Alphey L. PP1 binds Sara and negatively regulates Dpp signaling in Drosophila melanogaster. Nat. Genet. 31:2002;419-423.
7. Berdnik D., Torok T., Gonzalez-Gaitan M., Knoblich J.A. The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell. 3:2002;221-231.
8. Burke R., Basler K. Dpp receptors are autonomously required for cell proliferation in the entire developing wing. Development. 122:1996;2261-2269.
9. Burke R., Nellen D., Bellotto M., Hafen E., Senti K.A., Dickson B.J., Basler K. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell. 99:1999;803-815.
10. Capdevila J., Pariente F., Sampedro J., Alonso J.L., Guerrero I. Subcellular localization of the segment polarity protein patched suggests an interaction with the wingless receptor complex in Drosophila embryos. Development. 120:1994;987-998.
11. Chamoun Z., Mann R.K., Nellen D., von Kessler D.P., Bellotto M., Beachy P.A., Basler K. Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science. 293:2001;2080-2084.
12. Chen Y., Struhl G. Dual roles for Patched in sequestering and transducing Hedgehog. Cell. 87:1996;553-563.
13. Denef N., Neubueser D., Perez L., Cohen S.M. Hedgehog induces opposite changes in turnover and subcellular localization of patched and smoothened. Cell. 102:2000;521-531.
14. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., Wrana J.L. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 5:2003;410-421.
15. DiNardo S., Sher E., Heemskerk-Jongens J., Kassis J.A., O'Farrell P.H. Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature. 332:1988;604-609.
16. Dubois L., Lecourtois M., Alexandre C., Hirst E., Vincent J.P. Regulated endocytic routing modulates wingless signaling in Drosophila embryos. Cell. 105:2001;613-624.
17. Ebisawa T., Fukuchi M., Murakami G., Chiba T., Tanaka K., Imamura T., Miyazono K. Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276:2001;12477-12480.
18. Entchev E.V., Schwabedissen A., Gonzalez-Gaitan M. Gradient formation of the TGF-beta homolog Dpp. Cell. 103:2000;981-991.
19. Fehon R.G., Johansen K., Rebay I., Artavanis-Tsakonas S. Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function. J. Cell Biol. 113:1991;657-669.
20. Frise E., Knoblich J.A., Younger-Shepherd S., Jan L.Y., Jan Y.N. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl Acad. Sci. USA. 93:1996;11925-11932.
21. Gallet A., Rodriguez R., Ruel L., Therond P.P. Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetric cellular response to hedgehog. Dev. Cell. 4:2003;191-204.
22. Gho M., Bellaiche Y., Schweisguth F. Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development. 126:1999;3573-3584.
23. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. Eur. Mol. Biol. Org. J. 19:2000;4577-4588.
24. Gillooly D.J., Simonsen A., Stenmark H. Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins. Biochem. J. 355:2001;249-258.
25. Golembo M., Raz E., Shilo B.Z. The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development. 122:1996;3363-3370.
26. Gonzalez F., Swales L.S., Bejsovec A., Skaer H., Martinez Arias A. Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech. Dev. 35:1991;43-54.
27. González-Gaitán M.A., Jäckle H. Role of Drosophila α-adaptin during synaptic vesicle recycling. Cell. 88:1997;767-776.
28. González-Gaitán M.A., Jäckle H. The range of spalt-activating Dpp signalling is reduced in endocytosis-defective Drosophila wing discs. Mech. Dev. 87:1999;143-151.
29. Greco V., Hannus M., Eaton S. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell. 106:2001;633-645.
30. Grindstaff K.K., Yeaman C., Anandasabapathy N., Hsu S.C., Rodriguez-Boulan E., Scheller R.H., Nelson W.J. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell. 93:1998;731-740.
31. Gritzan U., Hatini V., DiNardo S. Mutual antagonism between signals secreted by adjacent wingless and engrailed cells leads to specification of complementary regions of the Drosophila parasegment. Development. 126:1999;4107-4115.
32. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron. 17:1996;27-41.
33. Hartenstein V., Posakony J.W. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development. 107:1989;389-405.
34. Hayes S., Chawla A., Corvera S. TGF beta receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol. 158:2002;1239-1249.
35. van den Heuvel M., Nusse R., Johnston P., Lawrence P.A. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell. 59:1989;739-749.
36. Incardona J.P., Gruenberg J., Roelink H. Sonic hedgehog induces the segregation of patched and smoothened in endosomes. Curr. Biol. 12:2002;983-995.
37. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15:2001;3059-3087.
38. Ingham P.W., Baker N.E., Martinez-Arias A. Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature. 331:1988;73-75.
39. Itoh F., Divecha N., Brocks L., Oomen L., Janssen H., Calafat J., et al. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling. Genes Cells. 7:2002;321-331.
40. Iwasaki S., Tsuruoka N., Hattori A., Sato M., Tsujimoto M., Kohno M. Distribution and characterization of specific cellular binding proteins for bone morphogenetic protein-2. J. Biol. Chem. 270:1995;5476-5482.
41. Kavsak P., Rasmussen R.K., Causing C.G., Bonni S., Zhu H., Thomsen G.H., Wrana J.L. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell. 6:2000;1365-1375.
42. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature. 377:1995;624-627.
43. Kuwabara P.E., Labouesse M. The sterol-sensing domain: multiple families, a unique role? Trends Genet. 18:2002;193-201.
44. Lander A.D., Nie Q., Wan F.Y. Do morphogen gradients arise by diffusion? Dev. Cell. 2:2002;785-796.
45. Lanzetti L., Rybin V., Malabarba M.G., Christoforidis S., Scita G., Zerial M., Di Fiore P.P. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature. 408:2000;374-377.
46. Lauffenburger D.A., Linderman J.J. Receptors. Models for Binding, Trafficking and Signaling. 1993;Oxford University Press, New York.
47. Lecuit T., Cohen S.M. Dpp receptor levels contribute to shaping the Dpp morphogen gradient in the Drosophila wing imaginal disc. Development. 125:1998;4901-4907.
48. Lecuit T., Brook W.J., Ng M., Calleja M., Sun H., Cohen S.M. Two distinct mechanisms for long-range patterning by decapentaplegic in the Drosophila wing. Nature. 381:1996;387-393.
49. Lewis P.M., Dunn M.P., McMahon J.A., Logan M., Martin J.F., St-Jacques B., McMahon A.P. Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell. 105:2001;599-612.
50. Lin X., Liang M., Feng X.H. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 275:2000;36818-36822.
51. Ma Y., Erkner A., Gong R., Yao S., Taipale J., Basler K., Beachy P.A. Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell. 111:2002;63-75.
52. Martin V., Carrillo G., Torroja C., Guerrero I. The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr. Biol. 11:2001;601-607.
53. Martinez Arias A. Wnts as morphogens? The view from the wing of Drosophila. Nat. Rev. Mol. Cell Biol. 4:2003;321-325.
54. Massagué J. TGF-β signal transduction. Annu. Rev. Biochem. 67:1998;753-791.
55. Massague J., Kelly B. Internalization of transforming growth factor-beta and its receptor in BALB/c 3T3 fibroblasts. J. Cell Physiol. 128:1986;216-222.
56. Miyazono K. TGF-beta signaling by Smad proteins. Cytokine Growth Factor Rev. 11:2000;15-22.
57. Moline M.M., Southern C., Bejsovec A. Directionality of Wingless protein transport influences epidermal patterning in the Drosophila embryo. Development. 126:1999;4375-4384.
58. Mukherjee S., Ghosh R.N., Maxfield F.R. Endocytosis. Physiol. Rev. 77:1997;759-803.
59. Natsume T., Tomita S., Iemura S., Kinto N., Yamaguchi A., Ueno N. Interaction between soluble type I receptor for bone morphogenetic protein and bone morphogenetic protein-4. J. Biol. Chem. 272:1997;11535-11540.
60. Nellen N., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell. 85:1996;357-368.
61. Novick P., Zerial M. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:1997;496-504.
62. Panopoulou E., Gillooly D.J., Wrana J.L., Zerial M., Stenmark H., Murphy C., Fotsis T. Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem. 277:2002;18046-18052.
63. Payre F., Vincent A., Carreno S. ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature. 400:1999;271-275.
64. Penheiter S.G., Mitchell H., Garamszegi N., Edens M., Dore J.J. Jr., Leof E.B. Internalization-dependent and -independent requirements for transforming growth factor beta receptor signaling via the Smad pathway. Mol. Cell Biol. 22:2002;4750-4759.
65. Pepinsky R.B., Zeng C., Wen D., Rayhorn P., Baker D.P., Williams K.P., et al. Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273:1998;14037-14045.
66. Pfeiffer S., Ricardo S., Manneville J.B., Alexandre C., Vincent J.P. Producing cells retain and recycle Wingless in Drosophila embryos. Curr. Biol. 12:2002;957-962.
67. Podos S.D., Hanson K.K., Wang Y.C., Ferguson E.L. The DSmurf ubiquitin-protein ligase restricts BMP signaling spatially and temporally during Drosophila embryogenesis. Dev. Cell. 1:2001;567-578.
68. Porter J.A., Young K.E., Beachy P.A. Cholesterol modification of Hedgehog signaling proteins in animal development. Science. 274:1996;255-259.
69. Rhyu M.S., Jan L.Y., Jan Y.N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 76:1994;477-491.
70. Rietveld A., Neutz S., Simons K., Eaton S. Association of sterol- and glycosylphosphatidylinositol-linked proteins with Drosophila raft Lipid microdomains. J. Biol. Chem. 274:1999;12049-12054.
71. Sanson B., Alexandre C., Fascetti N., Vincent J.P. Engrailed and hedgehog make the range of Wingless asymmetric in Drosophila embryos. Cell. 98:1999;207-216.
72. Santolini E., Puri C., Salcini A.E., Gagliani M.C., Pelicci P.G., Tacchetti C., Di Fiore P.P. Numb is an endocytic protein. J. Cell Biol. 151:2000;1345-1352.
73. Sathre K.A., Tsang M.L., Weatherbee J.A., Steer C.J. Binding and internalization of transforming growth factor-beta 1 by human hepatoma cells: evidence for receptor recycling. Hepatology. 14:1991;287-295.
74. Seugnet L., Simpson P., Haenlin M. Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192:1997;585-598.
75. Sheff D.R., Daro E.A., Hull M., Mellman I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145:1999;123-139.
76. Shitara Y., Kato Y., Sugiyama Y. Effect of brefeldin A and lysosomotropic reagents on intracellular trafficking of epidermal growth factor and transferrin in Madin-Darby canine kidney epithelial cells. J. Control Release. 55:1998;35-43.
77. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
78. Strigini M., Cohen S.M. Formation of morphogen gradients in the Drosophila wing. Semin. Cell Dev. Biol. 10:1999;335-344.
79. Strutt H., Thomas C., Nakano Y., Stark D., Neave B., Taylor A.M., Ingham P.W. Mutations in the sterol-sensing domain of Patched suggest a role for vesicular trafficking in Smoothened regulation. Curr. Biol. 11:2001;608-613.
80. Tall G.G., Barbieri M.A., Stahl P.D., Horazdovsky B.F. Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell. 1:2001;73-82.
81. The I., Bellaiche Y., Perrimon N. Hedgehog movement is regulated through Tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell. 4:1999;633-639.
82. Tomlinson A., Bowtell D.D., Hafen E., Rubin G.M. Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginal disc of Drosophila. Cell. 51:1987;143-150.
83. Tsukazaki T., Chiang T.A., Davidson A.F., Attisano L., Wrana J.L. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell. 95:1998;779-791.
84. Turing A.M. The chemical basis of morphogenesis. Philos. Trans. R. Soc. (London). 237:1952;37-72.
85. Uemura T., Shepherd S., Ackerman L., Jan L.Y., Jan Y.N. Numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell. 58:1989;349-360.
86. Wiellette E.L., McGinnis W. Hox genes differentially regulate Serrate to generate segment-specific structures. Development. 126:1999;1985-1995.
87. Willert K., Brown J.D., Danenberg E., Duncan A.W., Weissman I.L., Reya T., et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature. 423:2003;448-452.
88. Wolpert L. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1969;1-47.
89. Wrana J.L., Attisano L., Wieser R., Ventura F., Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 370:1994;341-347.
90. Wurmser A.E., Gary J.D., Emr S.D. Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J. Biol. Chem. 274:1999;9129-9132.
91. Zeng C., Younger-Shepherd S., Jan L.Y., Jan Y.N. Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 12:1998;1086-1091.
92. Zhu H., Kavsak P., Abdollah S., Wrana J.L., Thomsen G.H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature. 400:1999;687-693.