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

Paczkowski JE, Fromme JC
Dev Cell 30 610-24 (2014)
Cited: 23 times
EuropePMC logo PMID: 25203211

Abstract

Cargo adaptor subunits of vesicle coat protein complexes sort transmembrane proteins to distinct membrane compartments in eukaryotic cells. The exomer complex is the only cargo adaptor known to sort proteins at the trans-Golgi network into secretory vesicles. Exomer function is regulated by the Arf1 GTPase, a master regulator of trafficking at the Golgi. We report the structure of exomer bound to two copies of Arf1. Exomer interacts with each Arf1 molecule via two surfaces, one of which is a noncanonical interface that regulates GTP hydrolysis. The structure uncovers an unexpected membrane-proximal hydrophobic element that exomer uses in cooperation with Arf1 to remodel membranes. Given the constrained motion of the exomer hinge region, we envision that exomer dynamically positions multiple membrane insertion elements to drive membrane fission. In contrast to other known cargo adaptors, exomer therefore couples two functions, cargo sorting and membrane fission, into a single complex.

Articles - 4q66 mentioned but not cited (2)

  1. Structural basis for membrane binding and remodeling by the exomer secretory vesicle cargo adaptor. Paczkowski JE, Fromme JC. Dev Cell 30 610-624 (2014)
  2. Near-atomic structures of the BBSome reveal the basis for BBSome activation and binding to GPCR cargoes. Yang S, Bahl K, Chou HT, Woodsmith J, Stelzl U, Walz T, Nachury MV. Elife 9 e55954 (2020)


Reviews citing this publication (6)

  1. Direct trafficking pathways from the Golgi apparatus to the plasma membrane. Stalder D, Gershlick DC. Semin Cell Dev Biol 107 112-125 (2020)
  2. Cargo adaptors: structures illuminate mechanisms regulating vesicle biogenesis. Paczkowski JE, Richardson BC, Fromme JC. Trends Cell Biol 25 408-416 (2015)
  3. Arf GTPases and their effectors: assembling multivalent membrane-binding platforms. Cherfils J. Curr Opin Struct Biol 29 67-76 (2014)
  4. The Road not Taken: Less Traveled Roads from the TGN to the Plasma Membrane. Spang A. Membranes (Basel) 5 84-98 (2015)
  5. Chitin Synthesis in Yeast: A Matter of Trafficking. Sánchez N, Roncero C. Int J Mol Sci 23 12251 (2022)
  6. Induction of membrane curvature by proteins involved in Golgi trafficking. Makowski SL, Kuna RS, Field SJ. Adv Biol Regul 75 100661 (2020)

Articles citing this publication (15)

  1. A novel physiological role for ARF1 in the formation of bidirectional tubules from the Golgi. Bottanelli F, Kilian N, Ernst AM, Rivera-Molina F, Schroeder LK, Kromann EB, Lessard MD, Erdmann RS, Schepartz A, Baddeley D, Bewersdorf J, Toomre D, Rothman JE. Mol Biol Cell 28 1676-1687 (2017)
  2. The Molecular Architecture of Native BBSome Obtained by an Integrated Structural Approach. Chou HT, Apelt L, Farrell DP, White SR, Woodsmith J, Svetlov V, Goldstein JS, Nager AR, Li Z, Muller J, Dollfus H, Nudler E, Stelzl U, DiMaio F, Nachury MV, Walz T. Structure 27 1384-1394.e4 (2019)
  3. Traffic Through the Trans-Golgi Network and the Endosomal System Requires Collaboration Between Exomer and Clathrin Adaptors in Fission Yeast. Hoya M, Yanguas F, Moro S, Prescianotto-Baschong C, Doncel C, de León N, Curto MÁ, Spang A, Valdivieso MH. Genetics 205 673-690 (2017)
  4. Dynamic assembly of the exomer secretory vesicle cargo adaptor subunits. Huranova M, Muruganandam G, Weiss M, Spang A. EMBO Rep 17 202-219 (2016)
  5. A Screen for Membrane Fission Catalysts Identifies the ATPase EHD1. Kamerkar SC, Roy K, Bhattacharyya S, Pucadyil TJ. Biochemistry 58 65-71 (2019)
  6. A lipid-managing program maintains a stout Spitzenkörper. Peñalva MA. Mol Microbiol 97 1-6 (2015)
  7. Exomer complex regulates protein traffic at the TGN through differential interactions with cargos and clathrin adaptor complexes. Anton-Plagaro C, Sanchez N, Valle R, Mulet JM, Duncan MC, Roncero C. FASEB J 35 e21615 (2021)
  8. Involvement of the exomer complex in the polarized transport of Ena1 required for Saccharomyces cerevisiae survival against toxic cations. Anton C, Zanolari B, Arcones I, Wang C, Mulet JM, Spang A, Roncero C. Mol Biol Cell 28 3672-3685 (2017)
  9. Membrane-Deformation Ability of ANKHD1 Is Involved in the Early Endosome Enlargement. Kitamata M, Hanawa-Suetsugu K, Maruyama K, Suetsugu S. iScience 17 101-118 (2019)
  10. Evolutionary cell biology traces the rise of the exomer complex in Fungi from an ancient eukaryotic component. Ramirez-Macias I, Barlow LD, Anton C, Spang A, Roncero C, Dacks JB. Sci Rep 8 11154 (2018)
  11. The Functional Specialization of Exomer as a Cargo Adaptor During the Evolution of Fungi. Anton C, Taubas JV, Roncero C. Genetics 208 1483-1498 (2018)
  12. Analysis of Arf1 GTPase-Dependent Membrane Binding and Remodeling Using the Exomer Secretory Vesicle Cargo Adaptor. Paczkowski JE, Fromme JC. Methods Mol Biol 1496 41-53 (2016)
  13. Exomer Is Part of a Hub Where Polarized Secretion and Ionic Stress Connect. Moro S, Moscoso-Romero E, Poddar A, Mulet JM, Perez P, Chen Q, Valdivieso MH. Front Microbiol 12 708354 (2021)
  14. Genome doubling enabled the expansion of yeast vesicle traffic pathways. Purkanti R, Thattai M. Sci Rep 12 11213 (2022)
  15. Kinetics of Arf1 inactivation regulates Golgi organisation and function in non-adherent fibroblasts. B R R, Shah N, Joshi P, Madhusudan MS, Balasubramanian N. Biol Open 12 bio059669 (2023)


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