Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in the regulation of E-cadherin in epithelial morphogenesis

Journal of Cell Science

Volumn 128, Issue 3, 2015, Pages 499-515

  Zobel, Thomas ^a   Brinkmann, Klaus ^a   Koch, Nicole ^b   Schneider, Katharina ^b   Seemann, Eric ^b   Fleige, Astrid ^a   Qualmann, Britta ^b   Kessels, Michael M ^b   Bogdan, Sven ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Cell polarity; Cip4; Drosophila; E cadherin; F BAR proteins; Kinesins; Membrane trafficking; Microtubules; Nostrin; Oogenesis; Toca 1; Wing epithelium

Indexed keywords

CIP4 PROTEIN; F BAR PROTEIN; INSECT PROTEIN; NOSTRIN PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; CARRIER PROTEIN; CIP4 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; KINESIN; KINESIN-73 PROTEIN, DROSOPHILA; MICROTUBULE ASSOCIATED PROTEIN; NOSTRIN PROTEIN, DROSOPHILA; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EPITHELIUM; FEMALE; GENETIC ANALYSIS; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; EMBRYOLOGY; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; FORELIMB; GENETICS; METABOLISM; MICROTUBULE; OOCYTE; PHYSIOLOGY; PROTEIN TRANSPORT; RNA INTERFERENCE;

DROSOPHILA MELANOGASTER;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; ENDOSOMES; EPITHELIAL CELLS; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MORPHOGENESIS; OVUM; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, SMALL INTERFERING; WINGS, ANIMAL;

EID: 84961287909     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.155929     Document Type: Article

References (73)

1. Adler, P. N. (2012). Chapter one - the frizzled/stan pathway and planar cell polarity in the Drosophila wing. In Current Topics in Developmental Biology (ed. Y. Yang), pp. 1-31. San Diego, CA: Academic Press.
2. Adler, P. N., Sobala, L. F., Thom, D. and Nagaraj, R. (2013). dusky-like is required to maintain the integrity and planar cell polarity of hairs during the development of the Drosophila wing. Dev. Biol. 379, 76-91.
3. Ahmed, S., Bu, W., Lee, R. T. C., Maurer-Stroh, S. and Goh, W. I. (2010). F-BAR domain proteins: families and function. Commun. Integr. Biol. 3, 116-121.
4. Aspenström, P. (2008). Roles of F-BAR/PCH proteins in the regulation of membrane dynamics and actin reorganization. Int. Rev. Cell Mol. Biol. 272, 1-31.
5. Beetz, C., Koch, N., Khundadze, M., Zimmer, G., Nietzsche, S., Hertel, N., Huebner, A. K., Mumtaz, R., Schweizer, M., Dirren, E. et al. (2013). A spastic paraplegia mouse model reveals REEP1-dependent ER shaping. J. Clin. Invest. 123, 4273-4282.
6. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
7. Bogard, N., Lan, L., Xu, J. and Cohen, R. S. (2007). Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development 134, 3413-3418.
8. Bogdan, S., Stephan, R., Löbke, C., Mertens, A. and Klämbt, C. (2005). Abi activatesWASP to promote sensory organ development. Nat. Cell Biol. 7, 977-984.
9. Bu, W., Lim, K. B., Yu, Y. H., Chou, A. M., Sudhaharan, T. and Ahmed, S. (2010). Cdc42 interaction with N-WASP and Toca-1 regulates membrane tubulation, vesicle formation and vesicle motility: implications for endocytosis. PLoS ONE 5, e12153.
10. Chen, Y., Aardema, J., Kale, S., Whichard, Z. L., Awomolo, A., Blanchard, E., Chang, B., Myers, D. R., Ju, L., Tran, R. et al. (2013). Loss of the F-BAR protein CIP4 reduces platelet production by impairing membrane-cytoskeleton remodeling. Blood 122, 1695-1706.
11. Classen, A.-K., Anderson, K. I., Marois, E. and Eaton, S. (2005). Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817.
12. Delevoye, C., Miserey-Lenkei, S., Montagnac, G., Gilles-Marsens, F., Paul-Gilloteaux, P., Giordano, F., Waharte, F., Marks, M. S., Goud, B. and Raposo, G. (2014). Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Reports 6, 445-454.
13. Demeter, J. and Sazer, S. (1998). imp2, a new component of the actin ring in the fission yeast Schizosaccharomyces pombe. J. Cell Biol. 143, 415-427.
14. Dharmalingam, E., Haeckel, A., Pinyol, R., Schwintzer, L., Koch, D., Kessels, M. M. and Qualmann, B. (2009). F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis. J. Neurosci. 29, 13315-13327.
15. Dodding, M. P., Mitter, R., Humphries, A. C. and Way, M. (2011). A kinesin-1 binding motif in vaccinia virus that is widespread throughout the human genome. Embo J. 30, 4523-4538.
16. Doyle, K., Hogan, J., Lester, M. and Collier, S. (2008). The Frizzled Planar Cell Polarity signaling pathway controls Drosophila wing topography. Dev. Biol. 317, 354-367.
17. Fankhauser, C., Reymond, A., Cerutti, L., Utzig, S., Hofmann, K. and Simanis, V. (1995). The S. pombe cdc15 gene is a key element in the reorganization of Factin at mitosis. Cell 82, 435-444.
18. Feng, Y., Hartig, S. M., Bechill, J. E., Blanchard, E. G., Caudell, E. and Corey, S. J. (2010). The Cdc42-interacting protein-4 (CIP4) gene knock-out mouse reveals delayed and decreased endocytosis. J. Biol. Chem. 285, 4348-4354.
19. Fricke, R., Gohl, C., Dharmalingam, E., Grevelhörster, A., Zahedi, B., Harden, N., Kessels, M., Qualmann, B. and Bogdan, S. (2009). Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr. Biol. 19, 1429-1437.
20. Fricke, R., Gohl, C. and Bogdan, S. (2010). The F-BAR protein family Actin' on the membrane. Commun. Integr. Biol. 3, 89-94.
21. Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E. H., De Camilli, P. and Unger, V. M. (2008). Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817.
22. Frost, A., Unger, V. M. and De Camilli, P. (2009). The BAR domain superfamily: membrane-molding macromolecules. Cell 137, 191-196.
23. Fütterer, K. and Machesky, L. M. (2007). "Wunder" F-BAR domains: going from pits to vesicles. Cell 129, 655-657.
24. Gault, W. J., Olguin, P., Weber, U. and Mlodzik, M. (2012). Drosophila CK1-c, gilgamesh, controls PCP-mediated morphogenesis through regulation of vesicle trafficking. J. Cell Biol. 196, 605-621.
25. Gelbart, W. M. and Emmert, D. B. (2013). FlyBase High Throughput Expression Pattern Data. FBrf0221009.
26. Godt, D. and Tepass, U. (1998). Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387-391.
27. Gohl, C., Banovic, D., Grevelhörster, A. and Bogdan, S. (2010). WAVE forms hetero- and homo-oligomeric complexes at integrin junctions in Drosophila visualized by bimolecular fluorescence complementation. J. Biol. Chem. 285, 40171-40179.
28. Golic, K. G. and Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509.
29. González-Reyes, A. and St Johnston, D. (1998). Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis. Development 125, 2837-2846.
30. Grammont, M. and Irvine, K. D. (2001). fringe and Notch specify polar cell fate during Drosophila oogenesis. Development 128, 2243-2253.
31. Harumoto, T., Ito, M., Shimada, Y., Kobayashi, T. J., Ueda, H. R., Lu, B. and Uemura, T. (2010). Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev. Cell 19, 389-401.
32. Heath, R. J. W. and Insall, R. H. (2008). F-BAR domains: multifunctional regulators of membrane curvature. J. Cell Sci. 121, 1951-1954.
33. Henne, W. M., Boucrot, E., Meinecke, M., Evergren, E., Vallis, Y., Mittal, R. and McMahon, H. T. (2010). FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284.
34. Ho, H.-Y. H., Rohatgi, R., Lebensohn, A. M., Le Ma, Li, J, Gygi, S. P and Kirschner, M. W. (2004). Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118, 203-216.
35. Horne-Badovinac, S. and Bilder, D. (2005). Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev. Dyn. 232, 559-574.
36. Huckaba, T. M., Gennerich, A., Wilhelm, J. E., Chishti, A. H. and Vale, R. D. (2011). Kinesin-73 is a processive motor that localizes to Rab5-containing organelles. J. Biol. Chem. 286, 7457-7467.
37. Icking, A., Matt, S., Opitz, N., Wiesenthal, A., Müller-Esterl, W. and Schilling, K. (2005). NOSTRIN functions as a homotrimeric adaptor protein facilitating internalization of eNOS. J. Cell Sci. 118, 5059-5069.
38. Itoh, T. and De Camilli, P. (2006). BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912.
39. Kessels, M. M. and Qualmann, B. (2002). Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 21, 6083-6094.
40. Koch, D., Westermann, M., Kessels, M. M. and Qualmann, B. (2012a). Ultrastructural freeze-fracture immunolabeling identifies plasma membranelocalized syndapin II as a crucial factor in shaping caveolae. Histochem. Cell Biol. 138, 215-230.
41. Koch, N., Dharmalingam, E., Westermann, M., Qualmann, B., Thomas, U. and Kessels, M. M. (2012b). Abp1 utilizes the Arp2/3 complex activator Scar/WAVE in bristle development. J. Cell Sci. 125, 3578-3589.
42. Kovacevic, I., Hu, J., Siehoff-Icking, A., Opitz, N., Griffin, A., Perkins, A. C., Munn, A. L., Müller-Esterl, W., Popp, R., Fleming, I. et al. (2012). The F-BAR protein NOSTRIN participates in FGF signal transduction and vascular development. EMBO J. 31, 3309-3322.
43. Krasnow, R. E. and Adler, P. N. (1994). A single frizzled protein has a dual function in tissue polarity. Development 120, 1883-1893.
44. Lammel, U., Bechtold, M., Risse, B., Berh, D., Fleige, A., Bunse, I., Jiang, X., Klämbt, C. and Bogdan, S. (2014). The Drosophila FHOD1-like formin Knittrig acts through Rok to promote stress fiber formation and directed macrophage migration during the cellular immune response. Development 141, 1366-1380.
45. Leibfried, A., Fricke, R., Morgan, M. J., Bogdan, S. and Bellaiche, Y. (2008). Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr. Biol. 18, 1639-1648.
46. Ló pez-Schier, H. and St Johnston, D. (2001). Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15, 1393-1405.
47. Lupas, A. (1996). Prediction and analysis of coiled-coil structures. Methods Enzymol. 266, 513-525.
48. McCaffrey, R., St Johnston, D. and González-Reyes, A. (2006). A novel mutant phenotype implicates dicephalic in cyst formation in the Drosophila ovary. Dev. Dyn. 235, 908-917.
49. McMahon, H. T. and Gallop, J. L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596.
50. Nahm, M., Long, A. A., Paik, S. K., Kim, S., Bae, Y. C., Broadie, K. and Lee, S. (2010). The Cdc42-selective GAP rich regulates postsynaptic development and retrograde BMP transsynaptic signaling. J. Cell Biol. 191, 661-675.
51. Parks, A. L., Cook, K. R., Belvin, M., Dompe, N. A., Fawcett, R., Huppert, K., Tan, L. R., Winter, C. G., Bogart, K. P., Deal, J. E. et al. (2004). Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288-292.
52. Qualmann, B., Roos, J., DiGregorio, P. J. and Kelly, R. B. (1999). Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol. Biol. Cell 10, 501-513.
53. Qualmann, B., Koch, D. and Kessels, M. M. (2011). Let's go bananas: revisiting the endocytic BAR code. EMBO J. 30, 3501-3515.
54. Roberts-Galbraith, R. H., Chen, J.-S., Wang, J. and Gould, K. L. (2009). The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 184, 113-127.
55. Robinson, D. N. and Cooley, L. (1997). Genetic analysis of the actin cytoskeleton in the Drosophila ovary. Annu. Rev. Cell Dev. Biol. 13, 147-170.
56. Sander, M., Squarr, A. J., Risse, B., Jiang, X. and Bogdan, S. (2013). Drosophila pupal macrophages - a versatile tool for combined ex vivo and in vivo imaging of actin dynamics at high resolution. Eur. J. Cell Biol. 92, 349-354.
57. Sato, K., Nishida, K. M., Shibuya, A., Siomi, M. C. and Siomi, H. (2011). Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev. 25, 2361-2373.
58. Schneider, K., Seemann, E., Liebmann, L., Ahuja, R., Koch, D., Westermann, M., Hübner, C. A., Kessels, M. M. and Qualmann, B. (2014). ProSAP1 and membrane nanodomain-associated syndapin I promote postsynapse formation and function. J. Cell Biol. 205, 197-215.
59. Shimada, Y., Yonemura, S., Ohkura, H., Strutt, D. and Uemura, T. (2006). Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev. Cell 10, 209-222.
60. Shimada, A., Niwa, H., Tsujita, K., Suetsugu, S., Nitta, K., Hanawa-Suetsugu, K., Akasaka, R., Nishino, Y., Toyama, M., Chen, L. et al. (2007). Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772.
61. Strutt, D. I. (2002). The asymmetric subcellular localisation of components of the planar polarity pathway. Semin. Cell Dev. Biol. 13, 225-231.
62. Suetsugu, S. (2010). The proposed functions of membrane curvatures mediated by the BAR domain superfamily proteins. J. Biochem. 148, 1-12.
63. Suetsugu, S. and Gautreau, A. (2012). Synergistic BAR-NPF interactions in actin-driven membrane remodeling. Trends Cell Biol. 22, 141-150.
64. Tanentzapf, G., Smith, C., McGlade, J. and Tepass, U. (2000). Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J. Cell Biol. 151, 891-904.
65. Theiss, C., Neuhaus, A., Schliebs, W. and Erdmann, R. (2012). TubStain: a universal peptide-tool to label microtubules. Histochem. Cell Biol. 138, 531-540.
66. Tsujita, K., Suetsugu, S., Sasaki, N., Furutani, M., Oikawa, T. and Takenawa, T. (2006). Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279.
67. Turner, C. M. and Adler, P. N. (1995). Morphogenesis of Drosophila pupal wings in vitro. Mech. Dev. 52, 247-255.
68. Turner, C. M. and Adler, P. N. (1998). Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila. Mech. Dev. 70, 181-192.
69. Vachias, C., Couderc, J.-L. and Grammont, M. (2010). A two-step Notchdependant mechanism controls the selection of the polar cell pair in Drosophila oogenesis. Development 137, 2703-2711.
70. Xu, J., Lan, L., Bogard, N., Mattione, C. and Cohen, R. S. (2011). Rab11 is required for epithelial cell viability, terminal differentiation, and suppression of tumor-like growth in the Drosophila egg chamber. PLoS ONE 6, e20180.
71. Yan, S., Lv, Z., Winterhoff, M., Wenzl, C., Zobel, T., Faix, J., Bogdan, S. and Grosshans, J. (2013). The F-BAR protein Cip4/Toca-1 antagonizes the formin Diaphanous in membrane stabilization and compartmentalization. J. Cell Sci. 126, 1796-1805.
72. Zimmermann, K., Opitz, N., Dedio, J., Renne, C., Muller-Esterl, W. and Oess, S. (2002). NOSTRIN: a protein modulating nitric oxide release and subcellular distribution of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA 99, 17167-17172.
73. Zobel, T. and Bogdan, S. (2013). A high resolution view of the fly actin cytoskeleton lacking a functional WAVE complex. J. Microsc. 251, 224-231.