Structural Insights into Arl1-Mediated Targeting of the Arf-GEF BIG1 to the trans-Golgi

Cell Reports

Volumn 16, Issue 3, 2016, Pages 839-850

  Galindo, Antonio ^a   Soler, Nicolas ^a   McLaughlin, Stephen H ^a   Yu, Minmin ^a   Williams, Roger L ^a   Munro, Sean ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CYCLOPHILIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MEMBRANE PROTEIN; PROTEIN BIG1; PROTEIN BIG2; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR RELATED PROTEINS; ARFGEF1 PROTEIN, HUMAN; ARFGEF2 PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; GOLGI MEMBRANE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; GOLGI COMPLEX; HELA CELL LINE; METABOLISM; PROTEIN DOMAIN; TUMOR CELL LINE;

ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; AMINO ACID SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CYCLOPHILINS; DIMERIZATION; GOLGI APPARATUS; GTP PHOSPHOHYDROLASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; PROTEIN DOMAINS; SEQUENCE ALIGNMENT;

EID: 84978431839     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.022     Document Type: Article

References (60)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. Anders, N., Nielsen, M., Keicher, J., Stierhof, Y.D., Furutani, M., Tasaka, M., Skriver, K., Jürgens, G., Membrane association of the Arabidopsis ARF exchange factor GNOM involves interaction of conserved domains. Plant Cell 20 (2008), 142–151.
3. Andrade, M.A., Petosa, C., O'Donoghue, S.I., Müller, C.W., Bork, P., Comparison of ARM and HEAT protein repeats. J. Mol. Biol. 309 (2001), 1–18.
4. Barr, F.A., Review series: Rab GTPases and membrane identity: causal or inconsequential?. J. Cell Biol. 202 (2013), 191–199.
5. Belov, G.A., Kovtunovych, G., Jackson, C.L., Ehrenfeld, E., Poliovirus replication requires the N-terminus but not the catalytic Sec7 domain of ArfGEF GBF1. Cell. Microbiol. 12 (2010), 1463–1479.
6. Bhatt, J.M., Viktorova, E.G., Busby, T., Wyrozumska, P., Newman, L.E., Lin, H., Lee, E., Wright, J., Belov, G.A., Kahn, R.A., Sztul, E., Oligomerization of the Sec7 domain Arf guanine nucleotide exchange factor GBF1 is dispensable for Golgi localization and function but regulates degradation. Am. J. Physiol. Cell Physiol. 310 (2016), C456–C469.
7. Bui, Q.T., Golinelli-Cohen, M.P., Jackson, C.L., Large Arf1 guanine nucleotide exchange factors: evolution, domain structure, and roles in membrane trafficking and human disease. Mol. Genet. Genomics 282 (2009), 329–350.
8. Chavrier, P., Ménétrey, J., Toward a structural understanding of arf family:effector specificity. Structure 18 (2010), 1552–1558.
9. Cherfils, J., Arf GTPases and their effectors: assembling multivalent membrane-binding platforms. Curr. Opin. Struct. Biol. 29 (2014), 67–76.
10. Cherfils, J., Ménétrey, J., Mathieu, M., Le Bras, G., Robineau, S., Béraud-Dufour, S., Antonny, B., Chardin, P., Structure of the Sec7 domain of the Arf exchange factor ARNO. Nature 392 (1998), 101–105.
11. Christis, C., Munro, S., The small G protein Arl1 directs the trans-Golgi-specific targeting of the Arf1 exchange factors BIG1 and BIG2. J. Cell Biol. 196 (2012), 327–335.
12. De la Mora-Rey, T., Guenther, B.D., Finzel, B.C., The structure of the TOG-like domain of Drosophila melanogaster Mast/Orbit. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69 (2013), 723–729.
13. Donaldson, J.G., Jackson, C.L., ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12 (2011), 362–375.
14. Efe, J.A., Plattner, F., Hulo, N., Kressler, D., Emr, S.D., Deloche, O., Yeast Mon2p is a highly conserved protein that functions in the cytoplasm-to-vacuole transport pathway and is required for Golgi homeostasis. J. Cell Sci. 118 (2005), 4751–4764.
15. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
16. Gillingham, A.K., Munro, S., The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23 (2007), 579–611.
17. Gillingham, A.K., Pfeifer, A.C., Munro, S., CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol. Biol. Cell 13 (2002), 3761–3774.
18. Gillingham, A.K., Whyte, J.R.C., Panic, B., Munro, S., Mon2, a relative of large Arf exchange factors, recruits Dop1 to the Golgi apparatus. J. Biol. Chem. 281 (2006), 2273–2280.
19. Grebe, M., Gadea, J., Steinmann, T., Kientz, M., Rahfeld, J.U., Salchert, K., Koncz, C., Jürgens, G., A conserved domain of the arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding. Plant Cell 12 (2000), 343–356.
20. Hanzal-Bayer, M., Renault, L., Roversi, P., Wittinghofer, A., Hillig, R.C., The complex of Arl2-GTP and PDE delta: from structure to function. EMBO J. 21 (2002), 2095–2106.
21. Hildebrand, A., Remmert, M., Biegert, A., Söding, J., Fast and accurate automatic structure prediction with HHpred. Proteins 77:Suppl 9 (2009), 128–132.
22. Hutagalung, A.H., Novick, P.J., Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91 (2011), 119–149.
23. Jackson, C.L., Bouvet, S., Arfs at a glance. J. Cell Sci. 127 (2014), 4103–4109.
24. Jones, S., Jedd, G., Kahn, R.A., Franzusoff, A., Bartolini, F., Segev, N., Genetic interactions in yeast between Ypt GTPases and Arf guanine nucleotide exchangers. Genetics 152 (1999), 1543–1556.
25. Kabsch, W., Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 133–144.
26. Khan, A.R., Ménétrey, J., Structural biology of Arf and Rab GTPases’ effector recruitment and specificity. Structure 21 (2013), 1284–1297.
27. Klausner, R.D., Donaldson, J.G., Lippincott-Schwartz, J., Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116 (1992), 1071–1080.
28. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T., Ben-Tal, N., ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33 (2005), W299–W302.
29. Li, H., Wei, S., Cheng, K., Gounko, N.V., Ericksen, R.E., Xu, A., Hong, W., Han, W., BIG3 inhibits insulin granule biogenesis and insulin secretion. EMBO Rep. 15 (2014), 714–722.
30. Lu, L., Horstmann, H., Ng, C., Hong, W., Regulation of Golgi structure and function by ARF-like protein 1 (Arl1). J. Cell Sci. 114 (2001), 4543–4555.
31. Man, Z., Kondo, Y., Koga, H., Umino, H., Nakayama, K., Shin, H.W., Arfaptins are localized to the trans-Golgi by interaction with Arl1, but not Arfs. J. Biol. Chem. 286 (2011), 11569–11578.
32. Mansour, S.J., Skaug, J., Zhao, X.H., Giordano, J., Scherer, S.W., Melançon, P., p200 ARF-GEP1: a Golgi-localized guanine nucleotide exchange protein whose Sec7 domain is targeted by the drug brefeldin A. Proc. Natl. Acad. Sci. USA 96 (1999), 7968–7973.
33. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Cryst. 40 (2007), 658–674.
34. McDonold, C.M., Fromme, J.C., Four GTPases differentially regulate the Sec7 Arf-GEF to direct traffic at the trans-golgi network. Dev. Cell 30 (2014), 759–767.
35. Mizuno-Yamasaki, E., Rivera-Molina, F., Novick, P., GTPase networks in membrane traffic. Annu. Rev. Biochem. 81 (2012), 637–659.
36. Monetta, P., Slavin, I., Romero, N., Alvarez, C., Rab1b interacts with GBF1 and modulates both ARF1 dynamics and COPI association. Mol. Biol. Cell 18 (2007), 2400–2410.
37. Mossessova, E., Gulbis, J.M., Goldberg, J., Structure of the guanine nucleotide exchange factor Sec7 domain of human arno and analysis of the interaction with ARF GTPase. Cell 92 (1998), 415–423.
38. Mouratou, B., Biou, V., Joubert, A., Cohen, J., Shields, D.J., Geldner, N., Jürgens, G., Melançon, P., Cherfils, J., The domain architecture of large guanine nucleotide exchange factors for the small GTP-binding protein Arf. BMC Genomics, 6, 2005, 20.
39. Nakamura, K., Man, Z., Xie, Y., Hanai, A., Makyio, H., Kawasaki, M., Kato, R., Shin, H.W., Nakayama, K., Wakatsuki, S., Structural basis for membrane binding specificity of the Bin/Amphiphysin/Rvs (BAR) domain of Arfaptin-2 determined by Arl1 GTPase. J. Biol. Chem. 287 (2012), 25478–25489.
40. O'Neal, C.J., Jobling, M.G., Holmes, R.K., Hol, W.G.J., Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309 (2005), 1093–1096.
41. Paczkowski, J.E., Richardson, B.C., Fromme, J.C., Cargo adaptors: structures illuminate mechanisms regulating vesicle biogenesis. Trends Cell Biol. 25 (2015), 408–416.
42. Panic, B., Perisic, O., Veprintsev, D.B., Williams, R.L., Munro, S., Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol. Cell 12 (2003), 863–874.
43. Panic, B., Whyte, J.R., Munro, S., The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus. Curr. Biol. 13 (2003), 405–410.
44. Pasqualato, S., Renault, L., Cherfils, J., Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for ‘front-back’ communication. EMBO Rep. 3 (2002), 1035–1041.
45. Perica, T., Kondo, Y., Tiwari, S.P., McLaughlin, S.H., Kemplen, K.R., Zhang, X., Steward, A., Reuter, N., Clarke, J., Teichmann, S.A., Evolution of oligomeric state through allosteric pathways that mimic ligand binding. Science, 346, 2014, 1254346.
46. Powell, H.R., Johnson, O., Leslie, A.G., Autoindexing diffraction images with iMosflm. Acta Crystallogr. D Biol. Crystallogr. 69 (2013), 1195–1203.
47. Ramaen, O., Joubert, A., Simister, P., Belgareh-Touzé, N., Olivares-Sanchez, M.C., Zeeh, J.C., Chantalat, S., Golinelli-Cohen, M.P., Jackson, C.L., Biou, V., Cherfils, J., Interactions between conserved domains within homodimers in the BIG1, BIG2, and GBF1 Arf guanine nucleotide exchange factors. J. Biol. Chem. 282 (2007), 28834–28842.
48. Recacha, R., Boulet, A., Jollivet, F., Monier, S., Houdusse, A., Goud, B., Khan, A.R., Structural basis for recruitment of Rab6-interacting protein 1 to Golgi via a RUN domain. Structure 17 (2009), 21–30.
49. Richardson, B.C., McDonold, C.M., Fromme, J.C., The Sec7 Arf-GEF is recruited to the trans-Golgi network by positive feedback. Dev. Cell 22 (2012), 799–810.
50. Richardson, B.C., Halaby, S.L., Gustafson, M.A., Fromme, J.C., The Sec7 N-terminal regulatory domains facilitate membrane-proximal activation of the Arf1 GTPase. eLife, 5, 2016, e12411.
51. Sáenz, J.B., Sun, W.J., Chang, J.W., Li, J., Bursulaya, B., Gray, N.S., Haslam, D.B., Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat. Chem. Biol. 5 (2009), 157–165.
52. Sheen, V.L., Ganesh, V.S., Topcu, M., Sebire, G., Bodell, A., Hill, R.S., Grant, P.E., Shugart, Y.Y., Imitola, J., Khoury, S.J., et al. Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat. Genet. 36 (2004), 69–76.
53. Shiba, T., Kawasaki, M., Takatsu, H., Nogi, T., Matsugaki, N., Igarashi, N., Suzuki, M., Kato, R., Nakayama, K., Wakatsuki, S., Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport. Nat. Struct. Biol. 10 (2003), 386–393.
54. 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. 274 (1999), 12308–12315.
55. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 235–242.
56. Wong, M., Munro, S., Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science, 346, 2014, 1256898.
57. Wright, J., Kahn, R.A., Sztul, E., Regulating the large Sec7 ARF guanine nucleotide exchange factors: the when, where and how of activation. Cell. Mol. Life Sci. 71 (2014), 3419–3438.
58. Wu, M., Lu, L., Hong, W., Song, H., Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1. Nat. Struct. Mol. Biol. 11 (2004), 86–94.
59. Zhang, T., Li, S., Zhang, Y., Zhong, C., Lai, Z., Ding, J., Crystal structure of the ARL2-GTP-BART complex reveals a novel recognition and binding mode of small GTPase with effector. Structure 17 (2009), 602–610.
60. Zhao, X., Lasell, T.K.R., Melançon, 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 13 (2002), 119–133.