Exocyst subunits Exo70 and Exo84 cooperate with small GTPases to regulate behavior and endocytic trafficking in C. elegans

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Jiu, Yaming ^a   Jin, Congyu ^b   Liu, Yanbo ^a   Holmberg, Carina I ^b   Jäntti, Jussi ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; GUANOSINE TRIPHOSPHATASE; CAENORHABDITIS ELEGANS PROTEIN; EXOC 8 PROTEIN, C ELEGANS; EXOC-8 PROTEIN, C ELEGANS; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; DEVELOPMENT; DOWN REGULATION; ENDOCYTIC TRAFFICKING; EXO70 GENE; EXO84 GENE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; INTESTINE EPITHELIUM CELL; MUTANT; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAB 10 GENE; REGULATORY MECHANISM; RNA INTERFERENCE; UPREGULATION; ENDOCYTOSIS; EXOCYTOSIS; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

CAENORHABDITIS ELEGANS;

CAENORHABDITIS ELEGANS PROTEINS; ENDOCYTOSIS; EXOCYTOSIS; MONOMERIC GTP-BINDING PROTEINS; MUTATION; RNA INTERFERENCE; VESICULAR TRANSPORT PROTEINS;

EID: 84863296670     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032077     Document Type: Article

References (62)

1. He B, Guo W, (2009) The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21: 537-542.
2. Hsu SC, TerBush D, Abraham M, Guo W, (2004) The exocyst complex in polarized exocytosis. Int Rev Cytol 233: 243-265.
3. Munson M, Novick P, (2006) The exocyst defrocked, a framework of rods revealed. Nat Struct Mol Biol 13: 577-581.
4. St Johnston D, Ahringer J, (2010) Cell polarity in eggs and epithelia: parallels and diversity. Cell 141: 757-774.
5. Hsu SC, Ting AE, Hazuka CD, Davanger S, Kenny JW, et al. (1996) The mammalian brain rsec6/8 complex. Neuron 17: 1209-1219.
6. TerBush DR, Maurice T, Roth D, Novick P, (1996) The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15: 6483-6494.
7. Bowser R, Novick P, (1991) Sec15 protein, an essential component of the exocytotic apparatus, is associated with the plasma membrane and with a soluble 19.5S particle. J Cell Biol 112: 1117-1131.
8. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, et al. (1998) Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93: 731-740.
9. Yeaman C, Grindstaff KK, Wright JR, Nelson WJ, (2001) Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells. J Cell Biol 155: 593-604.
10. Kang J, Shin D, Yu JR, Lee J, (2009) Lats kinase is involved in the intestinal apical membrane integrity in the nematode Caenorhabditis elegans. Development 136: 2705-2715.
11. Rogers KK, Wilson PD, Snyder RW, Zhang X, Guo W, et al. (2004) The exocyst localizes to the primary cilium in MDCK cells. Biochem Biophys Res Commun 319: 138-143.
12. Hutagalung AH, Novick PJ, (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119-149.
13. Wu H, Rossi G, Brennwald P, (2008) The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol 18: 397-404.
14. Finger FP, Hughes TE, Novick P, (1998) Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92: 559-571.
15. Guo W, Roth D, Walch-Solimena C, Novick P, (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18: 1071-1080.
16. Guo W, Tamanoi F, Novick P, (2001) Spatial regulation of the exocyst complex by Rho1 GTPase. Nat Cell Biol 3: 353-360.
17. Wu H, Turner C, Gardner J, Temple B, Brennwald P, (2010) The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol Biol Cell 21: 430-442.
18. Robinson NG, Guo L, Imai J, Toh EA, Matsui Y, et al. (1999) Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol Cell Biol 19: 3580-3587.
19. Adamo JE, Rossi G, Brennwald P, (1999) The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol Biol Cell 10: 4121-4133.
20. Brymora A, Valova VA, Larsen MR, Roufogalis BD, Robinson PJ, (2001) The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J Biol Chem 276: 29792-29797.
21. Chen XW, Leto D, Xiao J, Goss J, Wang Q, et al. (2011) Exocyst function is regulated by effector phosphorylation. Nat Cell Biol 13: 580-588.
22. Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, et al. (2002) The exocyst is a Ral effector complex. Nat Cell Biol 4: 66-72.
23. Sugihara K, Asano S, Tanaka K, Iwamatsu A, Okawa K, et al. (2002) The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat Cell Biol 4: 73-78.
24. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, et al. (2007) High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 5: e237.
25. Inglis PN, Ou G, Leroux MR, Scholey JM, (2007) The sensory cilia of Caenorhabditis elegans. WormBook pp. 1-22.
26. Wicks SR, de Vries CJ, van Luenen HG, Plasterk RH, (2000) CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev Biol 221: 295-307.
27. Bryant DM, Datta A, Rodriguez-Fraticelli AE, Peranen J, Martin-Belmonte F, et al. (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12: 1035-1045.
28. Camonis JH, White MA, (2005) Ral GTPases: corrupting the exocyst in cancer cells. Trends Cell Biol 15: 327-332.
29. Moskalenko S, Tong C, Rosse C, Mirey G, Formstecher E, et al. (2003) Ral GTPases regulate exocyst assembly through dual subunit interactions. J Biol Chem 278: 51743-51748.
30. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12: 1317-1319.
31. McGhee JD, (2007) The C. elegans intestine. WormBook pp. 1-36.
32. Leung B, Hermann GJ, Priess JR, (1999) Organogenesis of the Caenorhabditis elegans intestine. Dev Biol 216: 114-134.
33. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, et al. (2006) RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17: 1286-1297.
34. Babbey CM, Bacallao RL, Dunn KW, (2010) Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 299: F495-506.
35. Glodowski DR, Chen CC, Schaefer H, Grant BD, Rongo C, (2007) RAB-10 regulates glutamate receptor recycling in a cholesterol-dependent endocytosis pathway. Mol Biol Cell 18: 4387-4396.
36. Naslavsky N, Weigert R, Donaldson JG, (2004) Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 15: 3542-3552.
37. Ishikawa H, Marshall WF, (2011) Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12: 222-234.
38. Scholey JM, (2008) Intraflagellar transport motors in cilia: moving along the cell's antenna. J Cell Biol 180: 23-29.
39. Das A, Guo W, (2011) Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol 21: 383-386.
40. Zuo X, Guo W, Lipschutz JH, (2009) The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol Biol Cell 20: 2522-2529.
41. Zhang X, Bi E, Novick P, Du L, Kozminski KG, et al. (2001) Cdc42 interacts with the exocyst and regulates polarized secretion. J Biol Chem 276: 46745-46750.
42. Inoue M, Chang L, Hwang J, Chiang SH, Saltiel AR, (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422: 629-633.
43. Henry L, Sheff DR, (2008) Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol Biol Cell 19: 2059-2068.
44. Ishikura S, Bilan PJ, Klip A, (2007) Rabs 8A and 14 are targets of the insulin-regulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem Biophys Res Commun 353: 1074-1079.
45. Frische EW, Pellis-van Berkel W, van Haaften G, Cuppen E, Plasterk RH, et al. (2007) RAP-1 and the RAL-1/exocyst pathway coordinate hypodermal cell organization in Caenorhabditis elegans. EMBO J 26: 5083-5092.
46. Han M, Sternberg PW, (1990) let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. Cell 63: 921-931.
47. Hirotsu T, Saeki S, Yamamoto M, Iino Y, (2000) The Ras-MAPK pathway is important for olfaction in Caenorhabditis elegans. Nature 404: 289-293.
48. Masuda ES, Luo Y, Young C, Shen M, Rossi AB, et al. (2000) Rab37 is a novel mast cell specific GTPase localized to secretory granules. FEBS Lett 470: 61-64.
49. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
50. Honjoh S, Yamamoto T, Uno M, Nishida E, (2009) Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans. Nature 457: 726-730.
51. Tatebe H, Morigasaki S, Murayama S, Zeng CT, Shiozaki K, (2010) Rab-family GTPase regulates TOR complex 2 signaling in fission yeast. Curr Biol 20: 1975-1982.
52. Michaux G, Dyer CE, Nightingale TD, Gallaud E, Nurrish S, et al. (2011) A role for Rab10 in von Willebrand factor release discovered by an AP-1 interactor screen in C. elegans. J Thromb Haemost 9: 392-401.
53. Lipschutz JH, Guo W, O'Brien LE, Nguyen YH, Novick P, et al. (2000) Exocyst is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol Biol Cell 11: 4259-4275.
54. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
55. Koelle MR, Horvitz HR, (1996) EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-125.
56. Ishihara T, Iino Y, Mohri A, Mori I, Gengyo-Ando K, et al. (2002) HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109: 639-649.
57. Jiu YM, Yue Y, Yang S, Liu L, Yu JW, et al. (2010) Insulin-like signaling pathway functions in integrative response to an olfactory and a gustatory stimuli in Caenorhabditis elegans. Protein Cell 1: 75-81.
58. Lackner MR, Nurrish SJ, Kaplan JM, (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335-346.
59. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330.
60. Mello C, Fire A, (1995) DNA transformation. Methods Cell Biol 48: 451-482.
61. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970.
62. Yu Y, Wang L, Jiu Y, Zhan Y, Liu L, et al. (2011) HID-1 is a novel player in the regulation of neuropeptide sorting. Biochem J 434: 383-390.