The FGD homologue EXC-5 regulates apical trafficking in C. elegans tubules

Developmental Biology

Volumn 359, Issue 1, 2011, Pages 59-72

  Mattingly, Brendan C ^a   Buechner, Matthew ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

CDC42; Charcot Marie Tooth Syndrome; EEA1; Endosome recycling; FGD; Rab; RME 1

Indexed keywords

CELL PROTEIN; PROTEIN CDC42; PROTEIN EXC 5; RAC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL STRUCTURE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; EXC 5 GENE; FLUORESCENCE ANALYSIS; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENOTYPE; HEREDITARY MOTOR SENSORY NEUROPATHY; MARKER GENE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT;

CAENORHABDITIS ELEGANS; METAZOA; NEMATODA;

EID: 80053580018     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.08.011     Document Type: Article

References (72)

1. Azzedine H., Bolino A., Taieb T., Birouk N., Di Duca M., Bouhouche A., Benamou S., Mrabet A., Hammadouche T., Chkili T., Gouider R., Ravazzolo R., Brice A., Laporte J., LeGuern E. Mutations in MTMR13, a new pseudophosphatase homologue of MTMR2 and Sbf1, in two families with an autosomal recessive demyelinating form of Charcot-Marie-Tooth disease associated with early-onset glaucoma. Am. J. Hum. Genet. 2003, 72:1141-1153.
2. Balklava Z., Pant S., Fares H., Grant B.D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 2007, 9:1066-1073.
3. Berry K.L., Bulow H.E., Hall D.H., Hobert O. A C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 2003, 302:2134-2137.
4. Bolino A., Muglia M., Conforti F.L., LeGuern E., Salih M.A., Georgiou D.M., Christodoulou K., Hausmanowa-Petrusewicz I., Mandich P., Schenone A., Gambardella A., Bono F., Quattrone A., Devoto M., Monaco A.P. Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2. Nat. Genet. 2000, 25:17-19.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992, 70:715-728.
7. Buechner M. Tubes and the single C. elegans excretory cell. Trends Cell Biol. 2002, 12:479-484.
8. Buechner M., Hall D.H., Bhatt H., Hedgecock E.M. Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol. 1999, 214:227-241.
9. Chavrier P., Parton R.G., Hauri H.P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 1990, 62:317-329.
10. Chen C.C., Schweinsberg P.J., Vashist S., Mareiniss D.P., Lambie E.J., Grant B.D. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 2006, 17:1286-1297.
11. Chitwood M.B., Chitwood B.G. The excretory system. Introduction to Nematology 1974, 126-135. University Park Press, Baltimore, Maryland. B.G. Chitwood, M.G. Chitwood (Eds.).
12. Delague V., Jacquier A., Hamadouche T., Poitelon Y., Baudot C., Boccaccio I., Chouery E., Chaouch M., Kassouri N., Jabbour R., Grid D., Megarbane A., Haase G., Levy N. Mutations in FGD4 encoding the Rho GDP/GTP exchange factor FRABIN cause autosomal recessive Charcot-Marie-Tooth type 4H. Am. J. Hum. Genet. 2007, 81:1-16.
13. Egorov M.V., Capestrano M., Vorontsova O.A., Di Pentima A., Egorova A.V., Mariggio S., Ayala M.I., Tete S., Gorski J.L., Luini A., Buccione R., Polishchuk R.S. Faciogenital dysplasia protein (FGD1) regulates export of cargo proteins from the golgi complex via Cdc42 activation. Mol. Biol. Cell 2009, 20:2413-2427.
14. Estrada L., Caron E., Gorski J.L. Fgd1, the Cdc42 guanine nucleotide exchange factor responsible for faciogenital dysplasia, is localized to the subcortical actin cytoskeleton and Golgi membrane. Hum. Mol. Genet. 2001, 10:485-495.
15. Fujita M., Hawkinson D., King K.V., Hall D.H., Sakamoto H., Buechner M. The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Dev. Biol. 2003, 256:290-301.
16. Gao J., Estrada L., Cho S., Ellis R.E., Gorski J.L. The Caenorhabditis elegans homolog of FGD1, the human Cdc42 GEF gene responsible for faciogenital dysplasia, is critical for excretory cell morphogenesis. Hum. Mol. Genet. 2001, 10:3049-3062.
17. Gaullier J.M., Simonsen A., D'Arrigo A., Bremnes B., Stenmark H., Aasland R. FYVE fingers bind PtdIns(3)P. Nature 1998, 394:432-433.
18. Gettner S.N., Kenyon C., Reichardt L.F. Characterization of βpat-3 heterodimers, a family of essential integrin receptors in C. elegans. J. Cell Biol. 1995, 129:1127-1141.
19. Gobel V., Barrett P.L., Hall D.H., Fleming J.T. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 2004, 6:865-873.
20. Graham T.R., Kozlov M.M. Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 2010, 22:430-436.
21. Grant B.D., Donaldson J.G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 2009, 10:597-608.
22. Hahn-Windgassen A., Van Gilst M.R. The Caenorhabditis elegans HNF4alpha Homolog, NHR-31, mediates excretory tube growth and function through coordinate regulation of the vacuolar ATPase. PLoS Genet. 2009, 5:e1000553.
23. Harris K.P., Tepass U. Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J. Cell Biol. 2008, 183:1129-1143.
24. Harris K.P., Tepass U. Cdc42 and vesicle trafficking in polarized cells. Traffic 2010, 11:1272-1279.
25. Harris P.C., Torres V.E. Polycystic kidney disease. Annu. Rev. Med. 2008, 183:1129-1143.
26. Hedgecock E.M., Culotti J.G., Hall D.H., Stern B.D. Genetics of cell and axon migrations in Caenorhabditis elegans. Development 1987, 100:365-382.
27. Hermann G.J., Schroeder L.K., Hieb C.A., Kershner A.M., Rabbitts B.M., Fonarev P., Grant B.D., Priess J.R. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell 2005, 16:3273-3288.
28. Hisamoto N., Moriguchi T., Urushiyama S., Mitani S., Shibuya H., Matsumoto K. Caenorhabditis elegans WNK-STE20 pathway regulates tube formation by modulating ClC channel activity. EMBO Rep. 2008, 9:70-75.
29. Huber C., Martensson A., Bokoch G.M., Nemazee D., Gavin A.L. FGD2, a CDC42-specific exchange factor expressed by antigen-presenting cells, localizes to early endosomes and active membrane ruffles. J. Biol. Chem. 2008, 283:34002-34012.
30. Kesavan G., Sand F.W., Greiner T.U., Johansson J.K., Kobberup S., Wu X., Brakebusch C., Semb H. Cdc42-mediated tubulogenesis controls cell specification. Cell 2009, 139:791-801.
31. Kjer-Nielsen L., Teasdale R.D., van Vliet C., Gleeson P.A. A novel Golgi-localisation domain shared by a class of coiled-coil peripheral membrane proteins. Curr. Biol. 1999, 9:385-388.
32. Kumfer K.T., Cook S.J., Squirrell J.M., Eliceiri K.W., Peel N., O'Connell K.F., White J.G. CGEF-1 and CHIN-1 regulate CDC-42 activity during asymmetric division in the Caenorhabditis elegans embryo. Mol. Biol. Cell 2010, 21:266-277.
33. 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.
34. Liegeois S., Benedetto A., Michaux G., Belliard G., Labouesse M. Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 2007, 175:709-724.
35. Lubarsky B., Krasnow M.A. Tube morphogenesis: making and shaping biological tubes. Cell 2003, 112:19-28.
36. Luschnig S., Batz T., Armbruster K., Krasnow M.A. Serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 2006, 16:186-194.
37. Martin-Belmonte F., Mostov K. Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 2008, 20:227-234.
38. Mattingly, B., 2011. EXC-5 controls intracellular trafficking in order to maintain the structure of the C. elegans excretory canal. Ph.D. Thesis, University of Kansas.
39. McCaffrey L.M., Macara I.G. The Par3/aPKC interaction is essential for end bud remodeling and progenitor differentiation during mammary gland morphogenesis. Genes Dev. 2009, 23:1450-1460.
40. Moore R.H., Millman E.E., Alpizar-Foster E., Dai W., Knoll B.J. Rab11 regulates the recycling and lysosome targeting of beta2-adrenergic receptors. J. Cell Sci. 2004, 117:3107-3117.
41. Mu F.T., Callaghan J.M., Steele-Mortimer O., Stenmark H., Parton R.G., Campbell P.L., McCluskey J., Yeo J.P., Tock E.P., Toh B.H. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J. Biol. Chem. 1995, 270:13503-13511.
42. Munro S., Nichols B.J. The GRIP domain - a novel Golgi-targeting domain found in several coiled-coil proteins. Curr. Biol. 1999, 9:377-380.
43. Naslavsky N., Caplan S. C-terminal EH-domain-containing proteins: consensus for a role in endocytic trafficking, EH?. J. Cell Sci. 2005, 118:4093-4101.
44. Nelson F.K., Riddle D.L. Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J. Exp. Zool. 1984, 231:45-56.
45. Nelson F.K., Albert P.S., Riddle D.S. Fine structure of the Caenorhabditis elegans secretory-excretory system. J. Ultrastruct. Res. 1983, 82:156-171.
46. Oka T., Toyomura T., Honjo K., Wada Y., Futai M. Four subunit a isoforms of Caenorhabditis elegans vacuolar H+-ATPase. Cell-specific expression during development. J. Biol. Chem. 2001, 276:33079-33085.
47. Olson M.F., Pasteris N.G., Gorski J.L., Hall A. Faciogenital dysplasia protein (FGD1) and Vav, two related proteins required for normal embryonic development, are upstream regulators of Rho GTPases. Curr. Biol. 1996, 6:1628-1633.
48. Ono Y., Nakanishi H., Nishimura M., Kakizaki M., Takahashi K., Miyahara M., Satoh-Horikawa K., Mandai K., Takai Y. Two actions of frabin: direct activation of Cdc42 and indirect activation of Rac. Oncogene 2000, 19:3050-3058.
49. Pant S., Sharma M., Patel K., Caplan S., Carr C.M., Grant B.D. AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat. Cell Biol. 2009, 11:1399-1410.
50. Pasteris N.G., Cadle A., Logie L.J., Porteous M.E., Schwartz C.E., Stevenson R.E., Glover T.W., Wilroy R.S., Gorski J.L. Isolation and characterization of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell 1994, 79:669-678.
51. Praitis V., Casey E., Collar D., Austin J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 2001, 157:1217-1226.
52. Praitis V., Ciccone E., Austin J. SMA-1 spectrin has essential roles in epithelial cell sheet morphogenesis in C. elegans. Dev. Biol. 2005, 283:157-170.
53. Ren M., Xu G., Zeng J., De Lemos-Chiarandini C., Adesnik M., Sabatini D.D. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6187-6192.
54. Roberts R.C., Peden A.A., Buss F., Bright N.A., Latouche M., Reilly M.M., Kendrick-Jones J., Luzio J.P. Mistargeting of SH3TC2 away from the recycling endosome causes Charcot-Marie-Tooth disease type 4C. Hum. Mol. Genet. 2010, 19:1009-1018.
55. Rodriguez-Fraticelli A.E., Vergarajauregui S., Eastburn D.J., Datta A., Alonso M.A., Mostov K., Martin-Belmonte F. The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis. J. Cell Biol. 2010, 189:725-738.
56. Rojas R., Ruiz W.G., Leung S.M., Jou T.S., Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 2001, 12:2257-2274.
57. Rondanino C., Rojas R., Ruiz W.G., Wang E., Hughey R.P., Dunn K.W., Apodaca G. RhoB-dependent modulation of postendocytic traffic in polarized Madin-Darby canine kidney cells. Traffic 2007, 8:932-949.
58. Schink K.O., Bolker M. Coordination of cytokinesis and cell separation by endosomal targeting of a Cdc42-specific guanine nucleotide exchange factor in Ustilago maydis. Mol. Biol. Cell 2009, 20:1081-1088.
59. Senderek J., Bergmann C., Weber S., Ketelsen U.P., Schorle H., Rudnik-Schoneborn S., Buttner R., Buchheim E., Zerres K. Mutation of the SBF2 gene, encoding a novel member of the myotubularin family, in Charcot-Marie-Tooth neuropathy type 4B2/11p15. Hum. Mol. Genet. 2003, 12:349-356.
60. Sharma M., Naslavsky N., Caplan S. A role for EHD4 in the regulation of early endosomal transport. Traffic 2008, 9:995-1018.
61. Shi A., Pant S., Balklava Z., Chen C.C., Figueroa V., Grant B.D. A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport. Curr. Biol. 2007, 17:1913-1924.
62. Shioi G., Shoji M., Nakamura M., Ishihara T., Katsura I., Fujisawa H., Takagi S. Mutations affecting nerve attachment of Caenorhabditis elegans. Genetics 2001, 157:1611-1622.
63. Stendel C., Roos A., Deconinck T., Pereira J., Castagner F., Niemann A., Kirschner J., Korinthenberg R., Ketelsen U.P., Battaloglu E., Parman Y., Nicholson G., Ouvrier R., Seeger J., De Jonghe P., Weis J., Kruttgen A., Rudnik-Schoneborn S., Bergmann C., Suter U., Zerres K., Timmerman V., Relvas J.B., Senderek J. Peripheral nerve demyelination caused by a mutant Rho GTPase guanine nucleotide exchange factor, frabin/FGD4. Am. J. Hum. Genet. 2007, 81:158-164.
64. Stendel C., Roos A., Kleine H., Arnaud E., Ozcelik M., Sidiropoulos P.N., Zenker J., Schupfer F., Lehmann U., Sobota R.M., Litchfield D.W., Luscher B., Chrast R., Suter U., Senderek J. SH3TC2, a protein mutant in Charcot-Marie-Tooth neuropathy, links peripheral nerve myelination to endosomal recycling. Brain 2010, 133:2462-2474.
65. Stenmark H., Parton R.G., Steele-Mortimer O., Lutcke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 1994, 13:1287-1296.
66. Stringham E.G., Schmidt K.L. Navigating the cell. Cell Adh. Migr. 2009, 3:342-346.
67. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
68. Suzuki N., Buechner M., Nishiwaki K., Hall D.H., Nakanishi H., Takai Y., Hisamoto N., Matsumoto K. A putative GDP-GTP exchange factor is required for development of the excretory cell in Caenorhabditis elegans. EMBO Rep. 2001, 2:530-535.
69. Teramoto T., Sternick L.A., Kage-Nakadai E., Sajjadi S., Siembida J., Mitani S., Iwasaki K., Lambie E.J. Magnesium excretion in C. elegans requires the activity of the GTL-2 TRPM channel. PLoS One 2010, 5:e9589.
70. Tong X., Buechner M. CRIP homologues maintain apical cytoskeleton to regulate tubule size in C. elegans. Dev. Biol. 2008, 317:225-233.
71. Whitehead I.P., Abe K., Gorski J.L., Der C.J. CDC42 and FGD1 cause distinct signaling and transforming activities. Mol. Cell. Biol. 1998, 18:4689-4697.
72. Yandell M.D., Edgar L.G., Wood W.B. Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:1381-1385.