The ArfGEF GBF-1 Is Required for ER Structure, Secretion and Endocytic Transport in C. elegans

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Ackema, Karin B ^a   Sauder, Ursula ^a   Solinger, Jachen A ^a   Spang, Anne ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; CELL PROTEIN; GBF 1 PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; GBF-1 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MATURATION; CELL STRUCTURE; CELL TRANSPORT; CELLULAR SECRETION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GBF 1 GENE; GENE; INTESTINE EPITHELIUM CELL; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; ANIMAL; CELL CULTURE; CYTOLOGY; ENDOCYTOSIS; EPITHELIUM CELL; GENETICS; INTESTINE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INTESTINES; OOCYTES; RNA INTERFERENCE;

EID: 84879222721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067076     Document Type: Article

References (53)

1. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A, (2010) Identification of the switch in early-to-late endosome transition. Cell 141: 497-508.
2. Morinaga N, Tsai SC, Moss J, Vaughan M, (1996) Isolation of a brefeldin A-inhibited guanine nucleotide-exchange protein for ADP ribosylation factor (ARF) 1 and ARF3 that contains a Sec7-like domain. Proceedings of the National Academy of Sciences of the United States of America 93: 12856-12860.
3. Sato K, Sato M, Audhya A, Oegema K, Schweinsberg P, et al. (2006) Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol Biol Cell 17: 3085-3094.
4. Peyroche A, Paris S, Jackson CL, (1996) Nucleotide exchange on ARF mediated by yeast Gea1 protein. Nature 384: 479-481.
5. Spang A, Herrmann JM, Hamamoto S, Schekman R, (2001) The ADP ribosylation factor-nucleotide exchange factors Gea1p and Gea2p have overlapping, but not redundant functions in retrograde transport from the Golgi to the endoplasmic reticulum. Mol Biol Cell 12: 1035-1045.
6. Peyroche A, Courbeyrette R, Rambourg A, Jackson CL, (2001) The ARF exchange factors Gea1p and Gea2p regulate Golgi structure and function in yeast. Journal of cell science 114: 2241-2253.
7. Sáenz JB, Sun WJ, Chang JW, Li J, Bursulaya B, et al. (2009) Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat Chem Biol 5: 157-165.
8. García-Mata R, Szul T, Alvarez C, Sztul E, (2003) ADP-ribosylation factor/COPI-dependent events at the endoplasmic reticulum-Golgi interface are regulated by the guanine nucleotide exchange factor GBF1. Mol Biol Cell 14: 2250-2261.
9. Zhao X, Claude A, Chun J, Shields DJ, Presley JF, et al. (2006) GBF1, a cis-Golgi and VTCs-localized ARF-GEF, is implicated in ER-to-Golgi protein traffic. J Cell Sci 119: 3743-3753.
10. Manolea F, Claude A, Chun J, Rosas J, Melançon P, (2008) Distinct functions for Arf guanine nucleotide exchange factors at the Golgi complex: GBF1 and BIGs are required for assembly and maintenance of the Golgi stack and trans-Golgi network, respectively. Mol Biol Cell 19: 523-535.
11. Zhao X, Lasell TK, Melancon P, (2002) Localization of large ADP-ribosylation factor-guanine nucleotide exchange factors to different Golgi compartments: evidence for distinct functions in protein traffic. Mol Biol Cell 13: 119-133.
12. Szul T, Burgess J, Jeon M, Zinn K, Marques G, et al. (2011) The Garz Sec7 domain guanine nucleotide exchange factor for Arf regulates salivary gland development in Drosophila. Cellular logistics 1: 69-76.
13. Armbruster K, Luschnig S, (2012) The Drosophila Sec7 domain guanine nucleotide exchange factor protein Gartenzwerg localizes at the cis-Golgi and is essential for epithelial tube expansion. J Cell Sci 125: 1318-1328.
14. Wang S, Meyer H, Ochoa-Espinosa A, Buchwald U, Onel S, et al. (2012) GBF1 (Gartenzwerg)-dependent secretion is required for Drosophila tubulogenesis. Journal of cell science 125: 461-472.
15. Kumari S, Mayor S, (2008) ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 10: 30-41.
16. Gupta GD, Swetha MG, Kumari S, Lakshminarayan R, Dey G, et al. (2009) Analysis of endocytic pathways in Drosophila cells reveals a conserved role for GBF1 in internalization via GEECs. PLoS One 4: e6768.
17. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
18. Bembenek JN, Richie CT, Squirrell JM, Campbell JM, Eliceiri KW, et al. (2007) Cortical granule exocytosis in C. elegans is regulated by cell cycle components including separase. Development 134: 3837-3848.
19. Sato M, Grant BD, Harada A, Sato K, (2008) Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J Cell Sci 121: 3177-3186.
20. Poteryaev D, Squirrell JM, Campbell JM, White JG, Spang A (2005) Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Mol Biol Cell 16: 2139-2153. Epub 2005 Feb 2116.
21. Frederick RL, McCaffery JM, Cunningham KW, Okamoto K, Shaw JM, (2004) Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J Cell Biol 167: 87-98.
22. Balklava Z, Pant S, Fares H, Grant BD, (2007) Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 9: 1066-1073.
23. Grant B, Hirsh D, (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
24. Esaki M, Liu Y, Glick BS, (2006) The budding yeast Pichia pastoris has a novel Sec23p homolog. FEBS Lett 580: 5215-5221.
25. Schmutz C, Stevens J, Spang A, (2007) Functions of the novel RhoGAP proteins RGA-3 and RGA-4 in the germ line and in the early embryo of C. elegans. Development 134: 3495-3505.
26. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR, (2008) Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol Biol 9: 9.
27. Ahringer J, ed (2006) Reverse genetics In: Ambros V, editor: The C. elegans Research Community, Wormbook.
28. Franzusoff A, Redding K, Crosby J, Fuller RS, Schekman R, (1991) Localization of components involved in protein transport and processing through the yeast Golgi apparatus. The Journal of cell biology 112: 27-37.
29. 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.
30. Shaham S (2006) Wormbook: Methods in Cell Biology. In: Ambros V, editor: WormBook, ed. The C. elegans Research Community.
31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome biology 3: RESEARCH0034.
32. Shi A, Sun L, Banerjee R, Tobin M, Zhang Y, et al. (2009) Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. The EMBO journal 28: 3290-3302.
33. Hadwiger G, Dour S, Arur S, Fox P, Nonet ML, (2010) A monoclonal antibody toolkit for C. elegans. PLoS One 5: e10161.
34. Witte K, Schuh AL, Hegermann J, Sarkeshik A, Mayers JR, et al. (2011) TFG-1 function in protein secretion and oncogenesis. Nat Cell Biol 13: 550-558.
35. Bianchi L, Driscoll M (2006) Culture of embryonic C.elegans cells for electrophysiological and pharmalogical analyses. In: Schafer WJ, editor: The C. elegans Research Community, Wormbook.
36. Trzebiatowska A, Topf U, Sauder U, Drabikowski K, Chiquet-Ehrismann R, (2008) Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol Biol Cell 19: 3898-3908.
37. Grant BD, Sato M (2006) Intracellular trafficking. WormBook: 1-9.
38. Andrews R, Ahringer J, (2007) Asymmetry of early endosome distribution in C. elegans embryos. PLoS One 2: e493.
39. Kondylis V, Rabouille C, (2009) The Golgi apparatus: lessons from Drosophila. FEBS Lett 583: 3827-3838.
40. Herpers B, Rabouille C, (2004) mRNA localization and ER-based protein sorting mechanisms dictate the use of transitional endoplasmic reticulum-golgi units involved in gurken transport in Drosophila oocytes. Molecular biology of the cell 15: 5306-5317.
41. Rossanese OW, Soderholm J, Bevis BJ, Sears IB, O'Connor J, et al. (1999) Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J Cell Biol 145: 69-81.
42. Page AP, Johnstone IL (2007) The cuticle. WormBook: 1-15.
43. Roberts B, Clucas C, Johnstone IL, (2003) Loss of SEC-23 in Caenorhabditis elegans causes defects in oogenesis, morphogenesis, and extracellular matrix secretion. Mol Biol Cell 14: 4414-4426.
44. Schierenberg E, Junkersdorf B (1992) The role of eggshell and underlying vitelline membrane for normal pattern formation in the early C. elegans embryo. Roux's Archives of Developmental Biology: 10-16.
45. Johnston WL, Krizus A, Dennis JW, (2006) The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. elegans embryo. BMC Biol 4: 35.
46. Gu F, Gruenberg J, (2000) ARF1 regulates pH-dependent COP functions in the early endocytic pathway. The Journal of biological chemistry 275: 8154-8160.
47. Johnson D, Nehrke K, (2010) Mitochondrial fragmentation leads to intracellular acidification in Caenorhabditis elegans and mammalian cells. Mol Biol Cell 21: 2191-2201.
48. Ben-Tekaya H, Kahn RA, Hauri HP, (2010) ADP ribosylation factors 1 and 4 and group VIA phospholipase A(2) regulate morphology and intraorganellar traffic in the endoplasmic reticulum-Golgi intermediate compartment. Molecular biology of the cell 21: 4130-4140.
49. Faure J, Stalder R, Borel C, Sobo K, Piguet V, et al. (2004) ARF1 regulates Nef-induced CD4 degradation. Current biology: CB 14: 1056-1064.
50. Wolff NA, Lee WK, Thevenod F, (2011) Role of Arf1 in endosomal trafficking of protein-metal complexes and cadmium-metallothionein-1 toxicity in kidney proximal tubule cells. Toxicology letters 203: 210-218.
51. Tang L, Fares H, Zhao X, Du W, Liu BF, (2012) Different endocytic functions of AGEF-1 in C. elegans coelomocytes. Biochim Biophys Acta 1820: 829-840.
52. Natarajan P, Liu K, Patil DV, Sciorra VA, Jackson CL, et al. (2009) Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 11: 1421-1426.
53. Achstetter T, Franzusoff A, Field C, Schekman R, (1988) SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus. J Biol Chem 263: 11711-11717.