LG186: An Inhibitor of GBF1 Function that Causes Golgi Disassembly in Human and Canine Cells

Traffic

Volumn 11, Issue 12, 2010, Pages 1537-1551

  Boal, Frédéric ^a   Guetzoyan, Lucie ^b,c   Sessions, Richard B ^d   Zeghouf, Mahel ^e   Spooner, Robert A ^b   Lord, J Michael ^b   Cherfils, Jacqueline ^e   Clarkson, Guy J ^c   Roberts, Lynne M ^b   Stephens, David J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

Arf GEF; GBF1; Golgi; Vesicle transport

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; BREFELDIN A; EXO 2; GOLGI BREFELDIN A RESISTANCE FACTOR 1; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; LG 186; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOENGINEERING; CELL ASSAY; CELL STRAIN; CELL TYPE; CELL VACUOLE; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SECRETORY PATHWAY;

ADP-RIBOSYLATION FACTOR 1; AMINO ACID SEQUENCE; ANIMALS; BENZALDEHYDES; BREFELDIN A; CELL LINE; DOGS; GOLGI APPARATUS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; HYDRAZONES; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PYRIDINES; PYRIMIDINES; QUINOLINES;

EID: 78349274356     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01122.x     Document Type: Article

References (46)

1. Schekman R. Merging cultures in the study of membrane traffic. Nat Cell Biol 2004;6:483-486.
2. Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 1991;67:601-616.
3. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, Klausner RD. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 1989;56:801-813.
4. Klausner RD, Donaldson JG, Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 1992;116:1071-1080.
5. Donaldson JG, Lippincott-Schwartz J, Bloom GS, Kreis TE, Klausner RD. Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action. J Cell Biol 1990;111:2295-2306.
6. Orci L, Tagaya M, Amherdt M, Perrelet A, Donaldson JG, Lippincott-Schwartz J, Klausner RD, Rothman JE. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae. Cell 1991;64:1183-1195.
7. Helms JB, Rothman JE. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 1992;360:352-354.
8. Donaldson JG, Finazzi D, Klausner RD. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 1992;360:350-352.
9. Wood SA, Park JE, Brown WJ. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 1991;67:591-600.
10. Renault L, Guibert B, Cherfils J. Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 2003;426:525-530.
11. Pommier Y, Cherfils J. Interfacial inhibition of macromolecular interactions: nature's paradigm for drug discovery. Trends Pharmacol Sci 2005;26:138-145.
12. Garcia-Mata R, Szul T, Alvarez C, Sztul E. ADP-ribosylation factor/ COPI-dependent events at the endoplasmic reticulum-Golgi interface are regulated by the guanine nucleotide exchange factor GBF1. Mol Biol Cell 2003;14:2250-2261.
13. Zhao X, Lasell TK, Melancon P. Localization of large ADP-ribosylation factor-guanine nucleotide exchange factors to different Golgi compartments: evidence for distinct functions in protein traffic. Mol Biol Cell 2002;13:119-133.
14. Togawa A, Morinaga N, Ogasawara M, Moss J, Vaughan M. Purification and cloning of a brefeldin A-inhibited guanine nucleotide-exchange protein for ADP-ribosylation factors. J Biol Chem 1999;274:12308-12315.
15. Ishizaki R, Shin HW, Mitsuhashi H, Nakayama K. Redundant roles of BIG2 and BIG1, guanine-nucleotide exchange factors for ADP-ribosylation factors in membrane traffic between the trans-Golgi network and endosomes. Mol Biol Cell 2008;19:2650-2660.
16. Islam A, Shen X, Hiroi T, Moss J, Vaughan M, Levine SJ. The brefeldin A-inhibited guanine nucleotide-exchange protein, BIG2, regulates the constitutive release of TNFR1 exosome-like vesicles. J Biol Chem 2007;282:9591-9599.
17. Shin HW, Morinaga N, Noda M, Nakayama K. BIG2, a guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity. Mol Biol Cell 2004;15:5283-5294.
18. Hunziker W, Whitney JA, Mellman I. Selective inhibition of transcytosis by brefeldin A in MDCK cells. Cell 1991;67:617-627.
19. Niu TK, Pfeifer AC, Lippincott-Schwartz J, Jackson CL. Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol Biol Cell 2005;16:1213-1222.
20. Peyroche A, Antonny B, Robineau S, Acker J, Cherfils J, Jackson CL. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol Cell 1999;3:275-285.
21. Saenz JB, Sun WJ, Chang JW, Li J, Bursulaya B, Gray NS, Haslam DB. Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat Chem Biol 2009;5:157-165.
22. Bryant DM, Mostov KE. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 2008;9:887-901.
23. Toye AM. Defective kidney anion-exchanger 1 (AE1, Band 3) trafficking in dominant distal renal tubular acidosis (dRTA). Biochem Soc Symp 2005;72:47-63.
24. Feng Y, Jadhav AP, Rodighiero C, Fujinaga Y, Kirchhausen T, Lencer WI. Retrograde transport of cholera toxin from the plasma membrane to the endoplasmic reticulum requires the trans-Golgi network but not the Golgi apparatus in Exo2-treated cells. EMBO Rep 2004;5:596-601.
25. Spooner RA, Watson P, Smith DC, Boal F, Amessou M, Johannes L, Clarkson GJ, Lord JM, Stephens DJ, Roberts LM. The secretion inhibitor Exo2 perturbs trafficking of Shiga toxin between endosomes and the trans-Golgi network. Biochem J 2008;414:471-484.
26. *Sec7 complexed with Brefeldin A and its implications for the guanine nucleotide exchange mechanism. Mol Cell 2003;12:1403-1411.
27. Zhao X, Claude A, Chun J, Shields DJ, Presley JF, Melancon P. GBF1, a cis-Golgi and VTCs-localized ARF-GEF, is implicated in ER-to-Golgi protein traffic. J Cell Sci 2006;119:3743-3753.
28. Szul T, Garcia-Mata R, Brandon E, Shestopal S, Alvarez C, Sztul E. Dissection of membrane dynamics of the ARF-guanine nucleotide exchange factor GBF1. Traffic 2005;6:374-385.
29. Cavenagh MM, Whitney JA, Carroll K, Zhang C, Boman AL, Rosenwald AG, Mellman I, Kahn RA. Intracellular distribution of Arf proteins in mammalian cells. Arf6 is uniquely localized to the plasma membrane. J Biol Chem 1996;271:21767-21774.
30. Viaud J, Zeghouf M, Barelli H, Zeeh JC, Padilla A, Guibert B, Chardin P, Royer CA, Cherfils J, Chavanieu A. Structure-based discovery of an inhibitor of Arf activation by Sec7 domains through targeting of protein-protein complexes. Proc Natl Acad Sci U S A 2007;104:10370-10375.
31. Zeeh JC, Zeghouf M, Grauffel C, Guibert B, Martin E, Dejaegere A, Cherfils J. Dual specificity of the interfacial inhibitor brefeldin a for arf proteins and sec7 domains. J Biol Chem 2006;281:11805-11814.
32. Boal F, Stephens DJ. Specific functions of BIG1, and BIG2 in endomembrane organization. PLOS One 2010;5(3):e9898.
33. Manolea F, Claude A, Chun J, Rosas J, Melancon P. 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 2008;19:523-535.
34. Claude A, Zhao BP, Kuziemsky CE, Dahan S, Berger SJ, Yan JP, Armold AD, Sullivan EM, Melancon P. GBF1: a novel Golgi-associated BFA-resistant guanine nucleotide exchange factor that displays specificity for ADP-ribosylation factor 5. J Cell Biol 1999;146:71-84.
35. Prydz K, Hansen SH, Sandvig K, Van Deurs B. Effects of brefeldin A on endocytosis, transcytosis and transport to the Golgi complex in polarized MDCK cells. J Cell Biol 1992;119:259-272.
36. Sandvig K, Prydz K, Hansen SH, Van Deurs B. Ricin transport in brefeldin A-treated cells: correlation between Golgi structure and toxic effect. J Cell Biol 1991;115:971-981.
37. Boal F, Stephens DJ. Specific functions of BIG1 and BIG2 in endomembrane organization. PLoS One 2010;5:e9898.
38. Waters ML. Aromatic interactions in peptides: impact on structure and function. Biopolymers 2004;76:435-445.
39. Mossessova E, Gulbis JM, Goldberg J. Structure of the guanine nucleotide exchange factor Sec7 domain of human arno and analysis of the interaction with ARF GTPase. Cell 1998;92:415-423.
40. Arkin MR, Wells JA. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 2004;3:301-317.
41. Shinotsuka C, Yoshida Y, Kawamoto K, Takatsu H, Nakayama K. Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation. J Biol Chem 2002;277:9468-9473.
42. Hirst J, Seaman MN, Buschow SI, Robinson MS. The role of cargo proteins in GGA recruitment. Traffic 2007;8:594-604.
43. Ramaen O, Joubert A, Simister P, Belgareh-Touze N, Olivares-Sanchez MC, Zeeh JC, Chantalat S, Golinelli-Cohen MP, Jackson CL, Biou V, Cherfils J. Interactions between conserved domains within homodimers in the BIG1, BIG2, and GBF1 Arf guanine nucleotide exchange factors. J Biol Chem 2007;282:28834-28842.
44. Townley AK, Feng Y, Schmidt K, Carter DA, Porter R, Verkade P, Stephens DJ. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J Cell Sci 2008;121:3025-3034.
45. Palmer KJ, Hughes H, Stephens DJ. Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol Biol Cell 2009;20:2885-2899.
46. Citterio C, Jones HD, Pacheco-Rodriguez G, Islam A, Moss J, Vaughan M. Effect of protein kinase A on accumulation of brefeldin A-inhibited guanine nucleotide-exchange protein 1 (BIG1) in HepG2 cell nuclei. Proc Natl Acad Sci U S A 2006;103:2683-2688.