Structural basis for membrane binding and remodeling by the exomer secretory vesicle cargo adaptor

Developmental Cell

Volumn 30, Issue 5, 2014, Pages 610-624

  Paczkowski, Jon E ^a   Fromme, J Christopher ^a  

^a School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CARRIER PROTEIN; EXOMER; GUANOSINE TRIPHOSPHATE; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE INSERTION SEQUENCE; HINGE REGION; HYDROLYSIS; HYDROPHOBICITY; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE FISSION; MEMBRANE REMODELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SECRETORY VESICLE; SURFACE PROPERTY; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GOLGI COMPLEX; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TRANS GOLGI NETWORK; X RAY CRYSTALLOGRAPHY;

EUKARYOTA;

ADP-RIBOSYLATION FACTOR 1; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, FUNGAL; GOLGI APPARATUS; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECRETORY VESICLES; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-GOLGI NETWORK;

EID: 84908609418     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.07.014     Document Type: Article

References (65)

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. 2010, 66:213-221.
2. Agrawal N.J., Nukpezah J., Radhakrishnan R. Minimal mesoscale model for protein-mediated vesiculation in clathrin-dependent endocytosis. PLoS Comput. Biol. 2010, 6:e1000926.
3. Bard F., Malhotra V. The formation of TGN-to-plasma-membrane transport carriers. Annu. Rev. Cell Dev. Biol. 2006, 22:439-455.
4. Barfield R.M., Fromme J.C., Schekman R. The exomer coat complex transports Fus1p to the plasma membrane via a novel plasma membrane sorting signal in yeast. Mol. Biol. Cell 2009, 20:4985-4996.
5. Bi X., Corpina R.A., Goldberg J. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 2002, 419:271-277.
6. Bi X., Mancias J.D., Goldberg J. Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev. Cell 2007, 13:635-645.
7. Bonifacino J.S. Adaptor proteins involved in polarized sorting. J.Cell Biol. 2014, 204:7-17.
8. Bonifacino J.S., Glick B.S. The mechanisms of vesicle budding and fusion. Cell 2004, 116:153-166.
9. Bonifacino J.S., Lippincott-Schwartz J. Coat proteins: shaping membrane transport. Nat. Rev. Mol. Cell Biol. 2003, 4:409-414.
10. Boucrot E., Pick A., Çamdere G., Liska N., Evergren E., McMahon H.T., Kozlov M.M. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 2012, 149:124-136.
11. Campelo F., Malhotra V. Membrane fission: the biogenesis of transport carriers. Annu. Rev. Biochem. 2012, 81:407-427.
12. Campelo F., Fabrikant G., McMahon H.T., Kozlov M.M. Modeling membrane shaping by proteins: focus on EHD2 and N-BAR domains. FEBS Lett. 2010, 584:1830-1839.
13. Collins B.M., McCoy A.J., Kent H.M., Evans P.R., Owen D.J. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002, 109:523-535.
14. Cruz-Garcia D., Ortega-Bellido M., Scarpa M., Villeneuve J., Jovic M., Porzner M., Balla T., Seufferlein T., Malhotra V. Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export. EMBO J. 2013, 32:1717-1729.
15. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 2006, 7:347-358.
16. De Matteis M.A., Luini A. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 2008, 9:273-284.
17. 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. 2011, 12:362-375.
18. Drin G., Antonny B. Amphipathic helices and membrane curvature. FEBS Lett. 2010, 584:1840-1847.
19. Drubin D.G., Nelson W.J. Origins of cell polarity. Cell 1996, 84:335-344.
20. Edeling M.A., Mishra S.K., Keyel P.A., Steinhauser A.L., Collins B.M., Roth R., Heuser J.E., Owen D.J., Traub L.M. Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 2006, 10:329-342.
21. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:486-501.
22. Ferguson S.M., De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 2012, 13:75-88.
23. Gehart H., Goginashvili A., Beck R., Morvan J., Erbs E., Formentini I., De Matteis M.A., Schwab Y., Wieland F.T., Ricci R. The BAR domain protein Arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network. Dev. Cell 2012, 23:756-768.
24. Gillingham A.K., Munro S. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 2007, 23:579-611.
25. Ha V.L., Thomas G.M., Stauffer S., Randazzo P.A. Preparation of myristoylated Arf1 and Arf6. Methods Enzymol. 2005, 404:164-174.
26. Heldwein E.E., Macia E., Wang J., Yin H.L., Kirchhausen T., Harrison S.C. Crystal structure of the clathrin adaptor protein 1 core. Proc. Natl. Acad. Sci. USA 2004, 101:14108-14113.
27. Heller H., Schaefer M., Schulten K. Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid crystal phases. J.Phys. Chem. 1993, 97:8343-8360.
28. Herth W., Schnepf E. The fluorochrome, calcofluor white, binds to structural polysaccharide fibrils. Protoplasma 1980, 105:129-133.
29. Hinshaw J.E., Schmid S.L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 1995, 374:190-192.
30. Ismail S.A., Vetter I.R., Sot B., Wittinghofer A. The structure ofan Arf-ArfGAP complex reveals a Ca2+ regulatory mechanism. Cell 2010, 141:812-821.
31. Jackson L.P., Kelly B.T., McCoy A.J., Gaffry T., James L.C., Collins B.M., Höning S., Evans P.R., Owen D.J. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 2010, 141:1220-1229.
32. Khan A.R., Ménétrey J. Structural biology of Arf and Rab GTPases' effector recruitment and specificity. Structure 2013, 21:1284-1297.
33. Klemm R.W., Ejsing C.S., Surma M.A., Kaiser H.J., Gerl M.J., Sampaio J.L., de Robillard Q., Ferguson C., Proszynski T.J., Shevchenko A., Simons K. Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J.Cell Biol. 2009, 185:601-612.
34. Kosaka T., Ikeda K. Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1. J.Cell Biol. 1983, 97:499-507.
35. Kozlovsky Y., Kozlov M.M. Membrane fission: model for intermediate structures. Biophys. J. 2003, 85:85-96.
36. Krauss M., Jia J.Y., Roux A., Beck R., Wieland F.T., De Camilli P., Haucke V. Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J.Biol. Chem. 2008, 283:27717-27723.
37. Lee C., Goldberg J. Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats. Cell 2010, 142:123-132.
38. Lee M.C., Orci L., Hamamoto S., Futai E., Ravazzola M., Schekman R. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 2005, 122:605-617.
39. *GTP. Nat. Struct. Mol. Biol. 2010, 17:876-881.
40. Lundmark R., Doherty G.J., Vallis Y., Peter B.J., McMahon H.T. Arf family GTP loading is activated by, and generates, positive membrane curvature. Biochem. J. 2008, 414:189-194.
41. Malhotra V., Campelo F. PKD regulates membrane fission to generate TGN to cell surface transport carriers. Cold Spring Harb. Perspect. Biol. 2011, 3:1-9.
42. McMahon H.T., Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 2005, 438:590-596.
43. Mossessova E., Bickford L.C., Goldberg J. SNARE selectivity of the COPII coat. Cell 2003, 114:483-495.
44. Novick P., Schekman R. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1979, 76:1858-1862.
45. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
46. Owen D.J., Vallis Y., Noble M.E., Hunter J.B., Dafforn T.R., Evans P.R., McMahon H.T. A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell 1999, 97:805-815.
47. Paczkowski J.E., Richardson B.C., Strassner A.M., Fromme J.C. The exomer cargo adaptor structure reveals a novel GTPase-binding domain. EMBO J. 2012, 31:4191-4203.
48. Ren X., Farías G.G., Canagarajah B.J., Bonifacino J.S., Hurley J.H. Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 2013, 152:755-767.
49. Richardson B.C., Fromme J.C. The exomer cargo adaptor features a flexible hinge domain. Structure 2013, 21:486-492.
50. 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 2012, 22:799-810.
51. Rockenbauch U., Ritz A.M., Sacristan C., Roncero C., Spang A. The complex interactions of Chs5p, the ChAPs, and the cargo Chs3p. Mol. Biol. Cell 2012, 23:4402-4415.
52. Sanchatjate S., Schekman R. Chs5/6 complex: a multiprotein complex that interacts with and conveys chitin synthase III from the trans-Golgi network to the cell surface. Mol. Biol. Cell 2006, 17:4157-4166.
53. Schekman R., Orci L. Coat proteins and vesicle budding. Science 1996, 271:1526-1533.
54. Shaw J.A., Mol P.C., Bowers B., Silverman S.J., Valdivieso M.H., Durán A., Cabib E. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J.Cell Biol. 1991, 114:111-123.
55. 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. 2003, 10:386-393.
56. Shnyrova A.V., Bashkirov P.V., Akimov S.A., Pucadyil T.J., Zimmerberg J., Schmid S.L., Frolov V.A. Geometric catalysis of membrane fission driven by flexible dynamin rings. Science 2013, 339:1433-1436.
57. Suhre K., Sanejouand Y.-H. ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res. 2004, 32(Web Server issue):W610-W614.
58. Trautwein M., Schindler C., Gauss R., Dengjel J., Hartmann E., Spang A. Arf1p, Chs5p and the ChAPs are required for export of specialized cargo from the Golgi. EMBO J. 2006, 25:943-954.
59. Valdivieso M.H., Mol P.C., Shaw J.A., Cabib E., Durán A. CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J.Cell Biol. 1991, 114:101-109.
60. von Blume J., Alleaume A.M., Cantero-Recasens G., Curwin A., Carreras-Sureda A., Zimmermann T., van Galen J., Wakana Y., Valverde M.A., Malhotra V. ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca2+ ATPase SPCA1. Dev. Cell 2011, 20:652-662.
61. Wakana Y., van Galen J., Meissner F., Scarpa M., Polishchuk R.S., Mann M., Malhotra V. A new class of carriers that transport selective cargo from the trans Golgi network to the cell surface. EMBO J. 2012, 31:3976-3990.
62. Wang C.W., Hamamoto S., Orci L., Schekman R. Exomer: A coat complex for transport of select membrane proteins from the trans-Golgi network to the plasma membrane in yeast. J.Cell Biol. 2006, 174:973-983.
63. Wang Q., Navarro M.V., Peng G., Molinelli E., Goh S.L., Judson B.L., Rajashankar K.R., Sondermann H. Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc. Natl. Acad. Sci. USA 2009, 106:12700-12705.
64. Xu P., Baldridge R.D., Chi R.J., Burd C.G., Graham T.R. Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport. J.Cell Biol. 2013, 202:875-886.
65. Yu X., Breitman M., Goldberg J. A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes. Cell 2012, 148:530-542.