Analysis of endocytic pathways in Drosophila cells reveals a conserved role for GBF1 in internalization via GEECs

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Gupta, Gagan D ^a,b   Swetha, M G ^a   Kumari, Sudha ^a   Lakshminarayan, Ramya ^a   Dey, Gautam ^a   Mayor, Satyajit ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b Chromous Biotech Pvt Ltd   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHOLESTEROL; DYNAMIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN CDC42; PROTEIN GARZ; PROTEIN GBF1; RAC1 PROTEIN; RHO FACTOR; UNCLASSIFIED DRUG; G BOX BINDING FACTOR; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL LABELING; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; INSECT CELL; INTERNALIZATION; NONHUMAN; PINOCYTOSIS; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; TRANSPORT KINETICS; ANIMAL; CYTOLOGY; GENETICS; METABOLISM;

MAMMALIA;

ANIMALS; DROSOPHILA; ENDOCYTOSIS; G-BOX BINDING FACTORS; GREEN FLUORESCENT PROTEINS; RNA INTERFERENCE;

EID: 69849095344     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006768     Document Type: Article

References (64)

1. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422: 37-44.
2. Benmerah A, Lamaze C (2007) Clathrin-coated pits: vive la difference? Traffic 8: 970-982.
3. Mayor S, Pagano RE (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8: 603-612.
4. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2: 411-423.
5. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, et al. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168: 465-476.
6. Gauthier NC, Monzo P, Kaddai V, Doye A, Ricci V, et al. (2005) Helicobacter pylori VacA cytotoxin: a probe for a clathrin-independent and Cdc42-dependent pinocytic pathway routed to late endosomes. Mol Biol Cell 16: 4852-4866.
7. Sharma P, Varma R, Sarasij RC, IraGousset K, et al. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-589.
8. Chadda R, Howes MT, Plowman SJ, Hancock JF, Parton RG, et al. (2007) Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8: 702-717.
9. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, et al. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135: 1085-1097.
10. Kumari S, Mayor S (2008) ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 10: 30-41.
11. Dubois T, Chavrier P (2005) [ARHGAP10, a novel RhoGAP at the cross-road between ARF1 and Cdc42 pathways, regulates Arp2/3 complex and actin dynamics on Golgi membranes]. Med Sci (Paris) 21: 692-694.
12. Donaldson JG, Jackson CL (2000) Regulators and effectors of the ARF GTPases. Curr Opin Cell Biol 12: 475-482.
13. Cox R, Mason-Gamer RJ, Jackson CL, Segev N (2004) Phylogenetic analysis of Sec7-domain-containing Arf nucleotide exchangers. Mol Biol Cell 15: 1487-1505.
14. Mouratou B, Biou V, Joubert A, Cohen J, Shields DJ, et al. (2005) The domain architecture of large guanine nucleotide exchange factors for the small GTP-binding protein Arf. BMC Genomics 6: 20.
15. Szul T, Grabski R, Lyons S, Morohashi Y, Shestopal S, et al. (2007) Dissecting the role of the ARF guanine nucleotide exchange factor GBF1 in Golgi biogenesis and protein trafficking. J Cell Sci 120: 3929-3940.
16. Manolea F, Claude A, Chun J, Rosas J, Melancon 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.
17. Mossessova E, Corpina RA, Goldberg J (2003) Crystal structure of ARF1*Sec7 complexed with Brefeldin A and its implications for the guanine nucleotide exchange mechanism. Mol Cell 12: 1403-1411.
18. Renault L, Guibert B, Cherfils J (2003) Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 426: 525-530.
19. Guha A, Sriram V, Krishnan KS, Mayor S (2003) Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J Cell Sci 116: 3373-3386.
20. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, et al. (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci U S A 97: 6499-6503.
21. Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, et al. (2000) Comparative genomics of the eukaryotes. Science 287: 2204-2215.
22. Koke JA, Yang M, Henner DJ, Volwerk JJ, Griffith OH (1991) High-level expression in Escherichia coli and rapid purification of phosphatidylinositol-specific phospholipase C from Bacillus cereus and Bacillus thuringiensis. Protein Expr Purif 2: 51-58.
23. Marois E, Mahmoud A, Eaton S (2006) The endocytic pathway and formation of the Wingless morphogen gradient. Development 133: 307-317.
24. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
25. Greco V, Hannus M, Eaton S (2001) Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106: 633-645.
26. Yanagawa S, Lee JS, Ishimoto A (1998) Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to wingless signaling. J Biol Chem 273: 32353-32359.
27. Abrams JM, Lux A, Steller H, Krieger M (1992) Macrophages in Drosophila embryos and L2 cells exhibit scavenger receptor-mediated endocytosis. Proc Natl Acad Sci U S A 89: 10375-10379.
28. Haberland ME, Fogelman AM (1985) Scavenger receptor-mediated recognition of maleyl bovine plasma albumin and the demaleylated protein in human monocyte macrophages. Proc Natl Acad Sci U S A 82: 2693-2697.
29. Mayor S, Sabharanjak S, Maxfield FR (1998) Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J 17: 4626-4638.
30. Chatterjee S, Mayor S (2001) The GPI-anchor and protein sorting. Cell Mol Life Sci 58: 1969-1987.
31. Sriram V, Krishnan KS, Mayor S (2003) deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. J Cell Biol 161: 593-607.
32. Johnson LS, Dunn KW, Pytowski B, McGraw TE (1993) Endosome acidification and receptor trafficking: bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif. Mol Biol Cell 4: 1251-1266.
33. Cham BE, Knowles BR (1976) A solvent system for delipidation of plasma or serum without protein precipitation. J Lipid Res 17: 176-181.
34. Dunn KW, Maxfield FR (1992) Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J Cell Biol 117: 301-310.
35. Schneider I (1972) Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27: 353-365.
36. Biyasheva A, Svitkina T, Kunda P, Baum B, Borisy G (2004) Cascade pathway of filopodia formation downstream of SCAR. J Cell Sci 117: 837-848.
37. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117.
38. Kalia M, Kumari S, Chadda R, Hill MM, Parton RG, et al. (2006) Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/ phosphatidylinositol-3′-kinase-dependent machinery. Mol Biol Cell 17: 3689-3704.
39. Van Hoof D, Rodenburg KW, Van der Horst DJ (2005) Receptor-mediated endocytosis and intracellular trafficking of lipoproteins and transferrin in insect cells. Insect Biochem Mol Biol 35: 117-128.
40. Yamashiro DJ, Maxfield FR (1987) Kinetics of endosome acidification in mutant and wild-type Chinese hamster ovary cells. J Cell Biol 105: 2713-2721.
41. Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5: 121-132.
42. Luzio JP, Pryor PR, Gray SR, Gratian MJ, Piper RC, et al. (2005) Membrane traffic to and from lysosomes. Biochem Soc Symp. pp 77-86.
43. Kochubey O, Majumdar A, Klingauf J (2006) Imaging clathrin dynamics in Drosophila melanogaster hemocytes reveals a role for actin in vesicle fission. Traffic 7: 1614-1627.
44. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
45. Silberkang M, Havel CM, Friend DS, McCarthy BJ, Watson JA (1983) Isoprene synthesis in isolated embryonic Drosophila cells. I. Sterol-deficient eukaryotic cells. J Biol Chem 258: 8503-8511.
46. Szul T, Garcia-Mata R, Brandon E, Shestopal S, Alvarez C, et al. (2005) Dissection of membrane dynamics of the ARF-guanine nucleotide exchange factor GBF1. Traffic 6: 374-385.
47. Niu TK, Pfeifer AC, Lippincott-Schwartz J, Jackson CL (2005) Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol Biol Cell 16: 1213-1222.
48. Chun J, Shapovalova Z, Dejgaard SY, Presley JF, Melancon P (2008) Characterization of class I and II ADP-ribosylation factors (Arfs) in live cells: GDP-bound class II Arfs associate with the ER-Golgi intermediate compartment independently of GBF1. Mol Biol Cell 19: 3488-3500.
49. Korolchuk VI, Schutz MM, Gomez-Llorente C, Rocha J, Lansu NR, et al. (2007) Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J Cell Sci 120: 4367-4376.
50. Hao M, Maxfield FR (2000) Characterization of rapid membrane internalization and recycling. J Biol Chem 275: 15279-15286.
51. Klausner RD, Van Renswoude J, Ashwell G, Kempf C, Schechter AN, et al. (1983) Receptor-mediated endocytosis of transferrin in K562 cells. J Biol Chem 258: 4715-4724.
52. Iacopetta BJ, Morgan EH (1983) The kinetics of transferrin endocytosis and iron uptake from transferrin in rabbit reticulocytes. J Biol Chem 258: 9108-9115.
53. Swanson JA (2008) Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9: 639-649.
54. Claude A, Zhao BP, Kuziemsky CE, Dahan S, Berger SJ, et al. (1999) GBF1: A novel Golgi-associated BFA-resistant guanine nucleotide exchange factor that displays specificity for ADP-ribosylation factor 5. J Cell Biol 146: 71-84.
55. Teh OK, Moore I (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448: 493-496.
56. Stroschein-Stevenson SL, Foley E, O'Farrell PH, Johnson AD (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 4: e4.
57. Cheng LW, Viala JP, Stuurman N, Wiedemann U, Vale RD, et al. (2005) Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen. Proc Natl Acad Sci U S A 102: 13646-13651.
58. Agaisse H, Burrack LS, Philips JA, Rubin EJ, Perrimon N, et al. (2005) Genomewide RNAi screen for host factors required for intracellular bacterial infection. Science 309: 1248-1251.
59. Wessels E, Duijsings D, Niu TK, Neumann S, Oorschot VM, et al. (2006) A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1. Dev Cell 11: 191-201.
60. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, et al. (2007) Imaging Poliovirus Entry in Live Cells. PLoS Biol 5: e183.
61. Beller M, Sztalryd C, Southall N, Bell M, Jackle H, et al. (2008) COPI complex is a regulator of lipid homeostasis. PLoS Biol 6: e292.
62. Guo Y, Walther TC, Rao M, Stuurman N, Goshima G, et al. (2008) Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453: 657-661.
63. Thiele C, Spandl J (2008) Cell biology of lipid droplets. Curr Opin Cell Biol 20: 378-385.
64. Miller S, Krijnse-Locker J (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6: 363-374.