Subcellular trafficking of FGF controls tracheal invasion of Drosophila flight muscle

Cell

Volumn 160, Issue 1-2, 2015, Pages 313-323

  Peterson, Soren J ^a   Krasnow, Mark A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMPHIPHYSIN; BETA INTEGRIN; CHEMOATTRACTANT; CLATHRIN; CLATHRIN ASSEMBLY PROTEIN; DYSTROGLYCAN; DYSTROPHIN; FIBROBLAST GROWTH FACTOR; MEMBRANE PROTEIN; DROSOPHILA PROTEIN;

ADULT; AIR SAC; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EPITHELIUM CELL; EXCITATION CONTRACTION COUPLING; FLIGHT MUSCLE; GENE EXPRESSION; GENE SILENCING; HETEROZYGOTE; MUSCLE CELL; MUSCLE FIBER MEMBRANE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SCANNING ELECTRON MICROSCOPY; TARGET CELL; TRACHEA; TRANSGENIC DROSOPHILA; TRANSVERSE TUBULAR SYSTEM; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CELL MEMBRANE; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; FORELIMB; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; SKELETAL MUSCLE;

HEXAPODA;

ANIMALS; CELL MEMBRANE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FIBROBLAST GROWTH FACTORS; LARVA; MEMBRANE PROTEINS; MUSCLE CELLS; MUSCLE, SKELETAL; TRACHEA; WING;

EID: 84920996688     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.11.043     Document Type: Article

References (71)

1. L. Al-Qusairi, and J. Laporte T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases Skelet Muscle 1 2011 26
2. M.G. Anderson, S.J. Certel, K. Certel, T. Lee, D.J. Montell, and W.A. Johnson Function of the Drosophila POU domain transcription factor drifter as an upstream regulator of breathless receptor tyrosine kinase expression in developing trachea Development 122 1996 4169 4178
3. F. Ango, G. di Cristo, H. Higashiyama, V. Bennett, P. Wu, and Z.J. Huang Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment Cell 119 2004 257 272
4. G. Ayalon, J.D. Hostettler, J. Hoffman, K. Kizhatil, J.Q. Davis, and V. Bennett Ankyrin-B interactions with spectrin and dynactin-4 are required for dystrophin-based protection of skeletal muscle from exercise injury J. Biol. Chem. 286 2011 7370 7378
5. T.Y. Belenkaya, C. Han, D. Yan, R.J. Opoka, M. Khodoun, H. Liu, and X. Lin Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans Cell 119 2004 231 244
6. N. Benhra, S. Lallet, M. Cotton, S. Le Bras, A. Dussert, and R. Le Borgne AP-1 controls the trafficking of Notch and Sanpodo toward E-cadherin junctions in sensory organ precursors Curr. Biol. 21 2011 87 95
7. D. Bilder, and N. Perrimon Localization of apical epithelial determinants by the basolateral PDZ protein Scribble Nature 403 2000 676 680
8. C.J. Blaisdell, R.D. Edmonds, X.T. Wang, S. Guggino, and P.L. Zeitlin pH-regulated chloride secretion in fetal lung epithelia Am. J. Physiol. Lung Cell. Mol. Physiol. 278 2000 L1248 L1255
9. R.J. Bloch, P. Reed, A. O'Neill, J. Strong, M. Williams, N. Porter, and H. González-Serratos Costameres mediate force transduction in healthy skeletal muscle and are altered in muscular dystrophies J. Muscle Res. Cell Motil. 25 2004 590 592
10. L. Bogdanik, B. Framery, A. Frölich, B. Franco, D. Mornet, J. Bockaert, S.J. Sigrist, Y. Grau, and M.L. Parmentier Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction PLoS ONE 3 2008 e2084
11. A.H. Brand, A.S. Manoukian, and N. Perrimon Ectopic expression in Drosophila Methods Cell Biol. 44 1994 635 654
12. N.A. Bulgakova, and E. Knust The Crumbs complex: from epithelial-cell polarity to retinal degeneration J. Cell Sci. 122 2009 2587 2596
13. S.R.y. Cajal Coloration par la méthode de Golgi des terminaisons des trachées et des nerfs dans les muscles des ailes des insectes Z. Wissensch. Mikr. 7 1890 332 342
14. F. Chen, and M.A. Krasnow Progenitor outgrowth from the niche in Drosophila trachea is guided by FGF from decaying branches Science 343 2014 186 189
15. B.M. Curtis, and W.A. Catterall Solubilization of the calcium antagonist receptor from rat brain J. Biol. Chem. 258 1983 7280 7283
16. W.M. Deng, M. Schneider, R. Frock, C. Castillejo-Lopez, E.A. Gaman, S. Baumgartner, and H. Ruohola-Baker Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila Development 130 2003 173 184
17. G. Dietzl, D. Chen, F. Schnorrer, K.C. Su, Y. Barinova, M. Fellner, B. Gasser, K. Kinsey, S. Oppel, and S. Scheiblauer A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila Nature 448 2007 151 156
18. M.R. Dreher, W. Liu, C.R. Michelich, M.W. Dewhirst, F. Yuan, and A. Chilkoti Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers J. Natl. Cancer Inst. 98 2006 335 344
19. D. Dutta, S. Anant, M. Ruiz-Gomez, M. Bate, and K. VijayRaghavan Founder myoblasts and fibre number during adult myogenesis in Drosophila Development 131 2004 3761 3772
20. A. Fernández-Miñán, M.D. Martín-Bermudo, and A. González-Reyes Integrin signaling regulates spindle orientation in Drosophila to preserve the follicular-epithelium monolayer Curr. Biol. 17 2007 683 688
21. M. Fosset, E. Jaimovich, E. Delpont, and M. Lazdunski [3H]nitrendipine receptors in skeletal muscle J. Biol. Chem. 258 1983 6086 6092
22. Y. Gan, T.E. McGraw, and E. Rodriguez-Boulan The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane Nat. Cell Biol. 4 2002 605 609
23. J.L. Genova, and R.G. Fehon Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila J. Cell Biol. 161 2003 979 989
24. E. Giniger, L.Y. Jan, and Y.N. Jan Specifying the path of the intersegmental nerve of the Drosophila embryo: a role for Delta and Notch Development 117 1993 431 440
25. L. Glazer, and B.Z. Shilo The Drosophila FGF-R homolog is expressed in the embryonic tracheal system and appears to be required for directed tracheal cell extension Genes Dev. 5 1991 697 705
26. X. Guo, R. Mattera, X. Ren, Y. Chen, C. Retamal, A. González, and J.S. Bonifacino The adaptor protein-1 μ1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells Dev. Cell 27 2013 353 366
27. N. Hacohen, S. Kramer, D. Sutherland, Y. Hiromi, and M.A. Krasnow sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways Cell 92 1998 253 263
28. V. Hartenstein The Atlas of Drosophila Development 1993 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
29. A. Icking, M. Amaddii, M. Ruonala, S. Höning, and R. Tikkanen Polarized transport of Alzheimer amyloid precursor protein is mediated by adaptor protein complex AP1-1B Traffic 8 2007 285 296
30. M. Jareb, and G. Banker The polarized sorting of membrane proteins expressed in cultured hippocampal neurons using viral vectors Neuron 20 1998 855 867
31. J. Jarecki, E. Johnson, and M.A. Krasnow Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF Cell 99 1999 211 220
32. C. Klämbt, L. Glazer, and B.Z. Shilo Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells Genes Dev. 6 1992 1668 1678
33. P. Laprise, and U. Tepass Novel insights into epithelial polarity proteins in Drosophila Trends Cell Biol. 21 2011 401 408
34. P. Laprise, K.M. Lau, K.P. Harris, N.F. Silva-Gagliardi, S.M. Paul, S. Beronja, G.J. Beitel, C.J. McGlade, and U. Tepass Yurt, Coracle, Neurexin IV and the Na(+),K(+)-ATPase form a novel group of epithelial polarity proteins Nature 459 2009 1141 1145
35. T. Lee, and L. Luo Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 1999 451 461
36. F. Leydig Zur Anatomic der Insecten (part 2), section 9. Zum Bau der Tracheen Arch. Anat. Physiol. u Wissensch. Med. 1859 160 162
37. M.A. Margeta, G.J. Wang, and K. Shen Clathrin adaptor AP-1 complex excludes multiple postsynaptic receptors from axons in C. elegans Proc. Natl. Acad. Sci. USA 106 2009 1632 1637
38. M.A. McGill, R.F. McKinley, and T.J. Harris Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions J. Cell Biol. 185 2009 787 796
39. S.E. McGuire, Z. Mao, and R.L. Davis Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila Sci. STKE 2004 2004 pl6
40. E.P. Meyer Corrosion casts as a method for investigation of the insect tracheal system Cell Tissue Res. 256 1989 1 6
41. 3 receptor in a cardiac T-tubule/SR microdomain PLoS Biol. 3 2005 e423
42. T. Ohshiro, and K. Saigo Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea Development 124 1997 3975 3986
43. J.V. Pardo, J.D. Siliciano, and S.W. Craig A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma Proc. Natl. Acad. Sci. USA 80 1983 1008 1012
44. G. Peña-Münzenmayer, M. Catalán, I. Cornejo, C.D. Figueroa, J.E. Melvin, M.I. Niemeyer, L.P. Cid, and F.V. Sepúlveda Basolateral localization of native ClC-2 chloride channels in absorptive intestinal epithelial cells and basolateral sorting encoded by a CBS-2 domain di-leucine motif J. Cell Sci. 118 2005 4243 4252
45. Y.H. Peng, W.K. Yang, W.H. Lin, T.T. Lai, and C.T. Chien Nak regulates Dlg basal localization in Drosophila salivary gland cells Biochem. Biophys. Res. Commun. 382 2009 108 113
46. M. Petronczki, and J.A. Knoblich DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila Nat. Cell Biol. 3 2001 43 49
47. P. Rahkila, T.E. Takala, R.G. Parton, and K. Metsikkö Protein targeting to the plasma membrane of adult skeletal muscle fiber: an organized mosaic of functional domains Exp. Cell Res. 267 2001 61 72
48. G. Ranganayakulu, B. Zhao, A. Dokidis, J.D. Molkentin, E.N. Olson, and R.A. Schulz A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila Dev. Biol. 171 1995 169 181
49. A. Razzaq, I.M. Robinson, H.T. McMahon, J.N. Skepper, Y. Su, A.C. Zelhof, A.P. Jackson, N.J. Gay, and C.J. O'Kane Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila Genes Dev. 15 2001 2967 2979
50. M. Reichman-Fried, B. Dickson, E. Hafen, and B.Z. Shilo Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration Genes Dev. 8 1994 428 439
51. I. Ribeiro, L. Yuan, G. Tanentzapf, J.J. Dowling, and A. Kiger Phosphoinositide regulation of integrin trafficking required for muscle attachment and maintenance PLoS Genet. 7 2011 e1001295
52. E. Rodriguez-Boulan, A. Perez-Bay, R. Schreiner, and D. Gravotta Response: the "tail" of the twin adaptors Dev. Cell 27 2013 247 248
53. M.M. Rolls, R. Albertson, H.P. Shih, C.Y. Lee, and C.Q. Doe Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia J. Cell Biol. 163 2003 1089 1098
54. D. Rosin, E. Schejter, T. Volk, and B.Z. Shilo Apical accumulation of the Drosophila PDGF/VEGF receptor ligands provides a mechanism for triggering localized actin polymerization Development 131 2004 1939 1948
55. I.N. Rybakova, J.R. Patel, and J.M. Ervasti The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin J. Cell Biol. 150 2000 1209 1214
56. M. Sato, and T.B. Kornberg FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system Dev. Cell 3 2002 195 207
57. M. Schober, M. Schaefer, and J.A. Knoblich Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts Nature 402 1999 548 551
58. D.S. Smith Reticular organizations within the striated muscle cell: an historical survey of light microscopic studies J. Biophys. Biochem. Cytol. 10 1961 61 87
59. D.S. Smith The structure of insect fibrillar flight muscle: a study made with special reference to the membrane systems of the fiber J. Biophys. Biochem. Cytol. 10 1961 123 158
60. M. Strigini, and S.M. Cohen Wingless gradient formation in the Drosophila wing Curr. Biol. 10 2000 293 300
61. D. Sutherland, C. Samakovlis, and M.A. Krasnow branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching Cell 87 1996 1091 1101
62. G. Tanentzapf, and U. Tepass Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization Nat. Cell Biol. 5 2003 46 52
63. U. Thomas, S. Ebitsch, M. Gorczyca, Y.H. Koh, C.D. Hough, D. Woods, E.D. Gundelfinger, and V. Budnik Synaptic targeting and localization of discs-large is a stepwise process controlled by different domains of the protein Curr. Biol. 10 2000 1108 1117
64. L.M. Traub, and G. Apodaca AP-1B: polarized sorting at the endosome Nat. Cell Biol. 5 2003 1045 1047
65. M.C. van der Plas, G.S. Pilgram, J.J. Plomp, A. de Jong, L.G. Fradkin, and J.N. Noordermeer Dystrophin is required for appropriate retrograde control of neurotransmitter release at the Drosophila neuromuscular junction J. Neurosci. 26 2006 333 344
66. M. Weaver, and M.A. Krasnow Dual origin of tissue-specific progenitor cells in Drosophila tracheal remodeling Science 321 2008 1496 1499
67. T. Weis-Fogh Power in flapping flight J.A. Ramsay, V.B. Wigglesworth, The Cell and the Organism 1961 Cambridge University Press London 283 300
68. T. Weis-Fogh Diffusion in insect wing muscle, the most active tissue known J. Exp. Biol. 41 1964 229 256
69. V.B. Wigglesworth, and W.M. Lee The supply of oxygen to the flight muscles of insects: a theory of tracheole physiology Tissue Cell 14 1982 501 518
70. D.F. Woods, J.W. Wu, and P.J. Bryant Localization of proteins to the apico-lateral junctions of Drosophila epithelia Dev. Genet. 20 1997 111 118
71. P.I. Zhuravlev, and G.A. Papoian Molecular noise of capping protein binding induces macroscopic instability in filopodial dynamics Proc. Natl. Acad. Sci. USA 106 2009 11570 11575