Exocyst-mediated membrane trafficking is required for branch outgrowth in Drosophila tracheal terminal cells

Developmental Biology

Volumn 390, Issue 1, 2014, Pages 41-50

  Jones, Tiffani A ^a   Nikolova, Linda S ^a   Schjelderup, Ani ^a   Metzstein, Mark M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Branching morphogenesis; Drosophila; Exocyst complex; Lumenogenesis; PAR complex; Terminal cells; Trachea

Indexed keywords

EXOCYST; RAB 10 PROTEIN; RAB 11 PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG; PAR COMPLEX; PEPTIDES AND PROTEINS; PROTEIN CDC42; PROTEIN RAB10; RAB11 PROTEIN;

ANIMAL CELL; ARTICLE; BRANCHING MORPHOGENESIS; CELL GROWTH; CELL MEMBRANE; CELL POLARITY; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; ENDOCYTOSIS; INSECT CELL; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TRACHEAL TERMINAL CELL; CELL MIGRATION; CELL TYPE; CELLULAR DISTRIBUTION; CYTOPLASM VESICLE; ENZYME ACTIVITY;

HEXAPODA;

BRANCHING MORPHOGENESIS; DROSOPHILA; EXOCYST COMPLEX; LUMENOGENESIS; PAR COMPLEX; TERMINAL CELLS; TRACHEA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL TRANSPORT; CELL PROLIFERATION; CYTOPLASMIC VESICLES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MORPHOGENESIS; MULTIPROTEIN COMPLEXES; PROTEIN KINASE C; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; TRACHEA; VESICULAR TRANSPORT PROTEINS;

EID: 84897576506     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.02.021     Document Type: Article

References (89)

1. Babbey C.M., Bacallao R.L., Dunn K.W. Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am. J. Physiol. Ren. Physiol. 2010, 299:F495-F506.
2. Baer M.M., Bilstein A., Leptin M. A clonal genetic screen for mutants causing defects in larval tracheal morphogenesis in Drosophila. Genetics 2007, 176:2279-2291.
3. Beronja S., Laprise P., Papoulas O., Pellikka M., Sisson J., Tepass U. Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J. Cell Biol. 2005, 169:635-646.
4. Bilimoria P.M., Bonni A. Molecular control of axon branching. Neuroscientist 2013, 19:16-24.
5. Bryant D.M., Datta A., Rodríguez-Fraticelli A.E., Peränen J., Martín-Belmonte F., Mostov K.E. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 2010, 12:1035-1045.
6. Carmeliet P., Jain R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473:298-307.
7. Chen W., Feng Y., Chen D., Wandinger-Ness A. Rab11 is required for trans-Golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol. Biol. Cell 1998, 9:3241-3257.
8. Chernyshova Y., Leshchyns'ka I., Hsu S.-C., Schachner M., Sytnyk V. The neural cell adhesion molecule promotes FGFR-dependent phosphorylation and membrane targeting of the exocyst complex to induce exocytosis in growth cones. J. Neurosci. 2011, 31:3522-3535.
9. Chou T. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 1996, 144:1673-1679.
10. Cole R.A., Fowler J.E. Polarized growth: maintaining focus on the tip. Curr. Opin. Plant Biol. 2006, 9:579-588.
11. Conibear E. Converging views of endocytosis in yeast and mammals. Curr. Opin. Cell Biol. 2010, 22:513-518.
12. Conway E.M., Collen D., Carmeliet P. Molecular mechanisms of blood vessel growth. Cardiovasc. Res. 2001, 49:507-521.
13. Das A., Gajendra S., Falenta K., Oudin M.J., Peschard P., Feng S., Wu B., Marshall C.J., Doherty P., Guo W., Lalli G. RalA promotes a direct exocyst-Par6 interaction to regulate polarity in neuronal development. J. Cell Sci 2014, 127:686-699.
14. Das A., Guo W. Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 2011, 21:383-386.
15. Dupraz S., Grassi D., Bernis M.E., Sosa L., Bisbal M., Gastaldi L., Jausoro I., Cáceres A., Pfenninger K.H., Quiroga S. The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J. Neurosci. 2009, 29:13292-13301.
16. Englund C., Steneberg P., Falileeva L., Xylourgidis N., Samakovlis C. Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. Development 2002, 129:4941-4951.
17. Estravís M., Rincón S.A., Santos B., Pérez P. Cdc42 regulates multiple membrane traffic events in fission yeast. Traffic 2011, 12:1744-1758.
18. Feng S., Knödler A., Ren J., Zhang J., Zhang X., Hong Y., Huang S., Peränen J., Guo W. A Rab8 guanine nucleotide exchange factor-effector interaction network regulates primary ciliogenesis. J. Biol. Chem. 2012, 287:15602-15609.
19. Fujita A., Koinuma S., Yasuda S., Nagai H., Kamiguchi H., Wada N., Nakamura T. GTP hydrolysis of TC10 promotes neurite outgrowth through exocytic fusion of Rab11- and L1-containing vesicles by releasing exocyst component Exo70. PLoS One 2013, 8:e79689.
20. Funamoto S., Meili R., Lee S., Parry L., Firtel R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 2002, 109:611-623.
21. Gehr P., Mwangi D.K., Ammann A., Maloiy G.M., Taylor C.R., Weibel E.R. Design of the mammalian respiratory system. V. Scaling morphometric pulmonary diffusing capacity to body mass: wild and domestic mammals. Respir. Physiol. 1981, 44:61-86.
22. Gervais L., Casanova J. In vivo coupling of cell elongation and lumen formation in a single cell. Curr. Biol. 2010, 20:359-366.
23. Gervais L., Casanova J. The Drosophila homologue of SRF acts as a boosting mechanism to sustain FGF-induced terminal branching in the tracheal system. Development 2011, 138:1269-1274.
24. Ghabrial A.S., Levi B.P., Krasnow M.A. A systematic screen for tube morphogenesis and branching genes in the Drosophila tracheal system. PLoS Genet. 2011, 7:e1002087.
25. Ghabrial A.S., Luschnig S., Metzstein M.M., Krasnow M.A. Branching morphogenesis of the Drosophila tracheal system. Annu. Rev. Cell Dev. Biol. 2003, 19:623-647.
26. Guillemin K., Groppe J., Ducker K., Treisman R., Hafen E., Affolter M., Krasnow M.A. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 1996, 122:1353-1362.
27. Guo W., Grant A., Novick P. Exo84p is an exocyst protein essential for secretion. J. Biol. Chem. 1999, 274:23558-23564.
28. Hazuka C.D., Foletti D.L., Hsu S.-C., Kee Y., Hopf F.W., Scheller R.H. The sec6/8 complex is located at neurite outgrowth and axonal synapse-assembly domains. J. Neurosci. 1999, 19:1324-1334.
29. He B., Guo W. The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 2009, 21:537-542.
30. Heider M.R., Munson M. Exorcising the exocyst complex. Traffic 2012, 13:898-907.
31. Jarecki J., Johnson E., Krasnow M.A. Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 1999, 99:211-220.
32. Jayanandanan N., Mathew R., Leptin M. Guidance of subcellular tubulogenesis by actin under the control of a synaptotagmin-like protein and moesin. Nat. Commun. 2014, 5:3036.
33. Jiu Y., Hasygar K., Tang L., Liu Y., Holmberg C.I., Bürglin T.R., Hietakangas V., Jäntti J. par-1, Atypical pkc, and PP2A/B55 sur-6 are implicated in the regulation of exocyst-mediated membrane trafficking in Caenorhabditis elegans. G3 (Bethesda) 2014, 4:173-183.
34. Jones T.A., Metzstein M.M. A novel function for the PAR complex in subcellular morphogenesis of tracheal terminal cells in Drosophila melanogaster. Genetics 2011, 189:153-164.
35. Jones T.A., Metzstein M.M. Examination of Drosophila larval tracheal terminal cells by light microscopy. J. Vis. Exp. 2013, (77):e50496.
36. Kanzaki M., Pessin J.E. Insulin signaling: GLUT4 vesicles exit via the exocyst. Curr. Biol. 2003, 13:R574-R576.
37. Kawase K., Nakamura T., Takaya A., Aoki K., Namikawa K., Kiyama H., Inagaki S., Takemoto H., Saltiel A.R., Matsuda M. GTP hydrolysis by the Rho family GTPase TC10 promotes exocytic vesicle fusion. Dev. Cell 2006, 11:411-421.
38. Lalli G. RalA and the exocyst complex influence neuronal polarity through PAR-3 and aPKC. J. Cell Sci. 2009, 122:1499-1506.
39. Lalli G., Hall A. Ral GTPases regulate neurite branching through GAP-43 and the exocyst complex. J. Cell Biol. 2005, 171:857-869.
40. Lee T., Hacohen N., Krasnow M., Montell D.J. Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev. 1996, 10:2912-2921.
41. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
42. Lerner D.W., McCoy D., Isabella A.J., Mahowald A.P., Gerlach G.F., Chaudhry T.A., Horne-Badovinac S. A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev. Cell 2013, 24:159-168.
43. Levi B.P., Ghabrial A.S., Krasnow M.A. Drosophila talin and integrin genes are required for maintenance of tracheal terminal branches and luminal organization. Development 2006, 133:2383-2393.
44. Lipschutz J.H., Mostov K.E. Exocytosis: the many masters of the exocyst. Curr. Biol. 2002, 12:R212-R214.
45. Locke M. The structure of insect tracheae. J. Microsc. Sci. 1957, 98:487-492.
46. Masur S.K., Kim Y.-T., Wu C.-F. Reversible inhibition of endocytosis in cultured neurons from the Drosophila temperature-sensitive mutant Shibire. J. Neurogenet. 1990, 6:191-206.
47. McDonald K., Müller-Reichert T. Cryomethods for thin section electron microscopy. Methods Enzymol. 2002, 351:96-123.
48. Mehta S.Q., Hiesinger P.R., Beronja S., Zhai R.G., Schulze K.L., Verstreken P., Cao Y., Zhou Y., Tepass U., Crair M.C., Bellen H.J. Mutations in Drosophila sec15 reveal a function in neuronal targeting for a subset of exocyst components. Neuron 2005, 46:219-232.
49. Murthy M., Garza D., Scheller R.H., Schwarz T.L. Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 2003, 37:433-447.
50. Novick P., Medkova M., Dong G., Hutagalung A., Reinisch K., Grosshans B. Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem. Soc. Trans. 2006, 34:683-686.
51. Ory S., Gasman S. Rho GTPases and exocytosis: what are the molecular links?. Semin. Cell Dev. Biol. 2011, 22:27-32.
52. Pfeffer S.R. Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol. 2001, 11:487-491.
53. Pfeffer S.R. Rab GTPase localization and Rab cascades in Golgi transport. Biochem. Soc. Trans. 2012, 40:1373-1377.
54. Ponnambalam S., Baldwin S.A. Constitutive protein secretion from the trans-Golgi network to the plasma membrane. Mol. Membr. Biol. 2003, 20:129-139.
55. Prigent M., Dubois T., Raposo G., Derrien V., Tenza D., Rosse C., Camonis J., Chavrier P. ARF6 controls post-endocytic recycling through its downstream exocyst complex effector. J. Cell Biol. 2003, 163:1111-1121.
56. Ramachandran R. Vesicle scission: dynamin. Semin. Cell Dev. Biol. 2011, 22:10-17.
57. Rivera-Molina F., Toomre D. Live-cell imaging of exocyst links its spatiotemporal dynamics to various stages of vesicle fusion. J. Cell Biol. 2013, 201:673-680.
58. Rogers K.K., Wilson P.D., Snyder R.W., Zhang X., Guo W., Burrow C.R., Lipschutz J.H. The exocyst localizes to the primary cilium in MDCK cells. Biochem. Biophys. Res. Commun. 2004, 319:138-143.
59. Ruiz O.E., Nikolova L.S., Metzstein M.M. Drosophila Zpr1 (Zinc Finger Protein 1) is required downstream of both EGFR And FGFR signaling in tracheal subcellular lumen formation. PLoS One 2012, 7:e45649.
60. Samakovlis C., Hacohen N., Manning G. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 1996, 122:1395-1407.
61. Sann S., Wang Z., Brown H., Jin Y. Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol. 2009, 19:317-324.
62. Sano H., Eguez L., Teruel M.N., Fukuda M., Chuang T.D., Chavez J.A., Lienhard G.E., McGraw T.E. Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab. 2007, 5:293-303.
63. Satoh A.K., O'Tousa J.E., Ozaki K., Ready D.F. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 2005, 132:1487-1497.
64. Schottenfeld-Roames J., Ghabrial A.S. Whacked and Rab35 polarize dynein-motor-complex-dependent seamless tube growth. Nature 2012, 14:386-393.
65. Steneberg P., Samakovlis C. A novel stop codon readthrough mechanism produces functional Headcase protein in Drosophila trachea. EMBO Rep. 2001, 2:593-597.
66. Sutherland D., Samakovlis C., Krasnow M.A. branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 1996, 87:1091-1101.
67. Swan L.E. Initiation of clathrin-mediated endocytosis: all you need is two?. Bioessays 2013, 35:425-429.
68. Takahashi S., Kubo K., Waguri S., Yabashi A., Shin H.W., Katoh Y., Nakayama K. Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J. Cell Sci. 2012, 125:4049-4057.
69. Tekirian T.L. The central role of the trans-Golgi network as a gateway of the early secretory pathway: physiologic vs. nonphysiologic protein transit. Exp. Cell Res. 2002, 281:9-18.
70. TerBush D.R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 1996, 15:6483-6494.
71. Vega I.E., Hsu S.C. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J. Neurosci. 2001, 21:3839-3848.
72. Vetter P., Roth A., Häusser M. Propagation of action potentials in dendrites depends on dendritic morphology. J. Neurophysiol. 2001, 85:926-937.
73. Walther P., Ziegler A. Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J. Microsc. 2002, 208:3-10.
74. Wang T., Liu Y., Xu X.-H., Deng C.-Y., Wu K.-Y., Zhu J., Fu X.-Q., He M., Luo Z.-G. Lgl1 activation of Rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev. Cell 2011, 21(3):431-444.
75. Warburton D., Bellusci S., De Langhe S., Del Moral P.M., Fleury V., Mailleux A., Tefft D., Unbekandt M., Wang K., Shi W. Molecular mechanisms of early lung specification and branching morphogenesis. Pediatr. Res. 2005, 57:26R-37R.
76. Warburton D., El-Hashash A., Carraro G., Tiozzo C., Sala F., Rogers O., De Langhe S., Kemp P.J., Riccardi D., Torday J., Bellusci S., Shi W., Lubkin S.R., Jesudason E. Lung organogenesis. Curr. Top. Dev. Biol. 2010, 90:73-158.
77. Warburton D., Schwarz M., Tefft D., Flores-Delgado G., Anderson K.D., Cardoso W.V. The molecular basis of lung morphogenesis. Mech. Dev. 2000, 92:55-81.
78. Whyte J.R.C., Munro S. Vesicle tethering complexes in membrane traffic. J. Cell Sci. 2002, 115:2627-2637.
79. Wodarz A., Ramrath A., Grimm A., Knust E. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 2000, 150:1361-1374.
80. Wu H., Turner C., Gardner J., Temple B., Brennwald P. The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell 2010, 21:430-442.
81. Wu S., Mehta S.Q., Pichaud F., Bellen H.J., Quiocho F.A. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 2005, 12:879-885.
82. Wucherpfennig T., Wilsch-Bräuninger M., González-Gaitán M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 2003, 161:609-624.
83. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
84. Yang H.W., Shin M.G., Lee S., Kim J.R., Park W.S., Cho K.H., Meyer T., Do Heo W. Cooperative activation of PI3K by Ras and Rho family small GTPases. Mol. Cell 2012, 47:281-290.
85. Zhang J., Schulze K.L., Hiesinger P.R., Suyama K., Wang S., Fish M., Acar M., Hoskins R.A., Bellen H.J., Scott M.P. Thirty-one flavors of Drosophila rab proteins. Genetics 2007, 176:1307-1322.
86. Zhang X. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 2001, 276:46745-46750.
87. Zhang X.M., Ellis S., Sriratana A., Mitchell C.A., Rowe T. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J. Biol. Chem. 2004, 279:43027-43034.
88. Zhou D., Xue J., Chen J., Morcillo P., Lambert J.D., White K.P., Haddad G.G. Experimental selection for Drosophila survival in extremely low O(2) environment. PLoS One 2007, 2:e490.
89. Zuo X., Guo W., Lipschutz J.H. The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 2009, 20:2522-2529.