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Molecular mechanism of ubiquitin recognition by GGA3 GAT domain.

Kawasaki M, Shiba T, Shiba Y, Yamaguchi Y, Matsugaki N, Igarashi N, Suzuki M, Kato R, Kato K, Nakayama K, Wakatsuki S
Genes Cells 10 639-54 (2005)
Cited: 30 times
EuropePMC logo PMID: 15966896

Abstract

GGA (Golgi-localizing, gamma-adaptin ear domain homology, ARF-binding) proteins, which constitute a family of clathrin coat adaptor proteins, have recently been shown to be involved in the ubiquitin-dependent sorting of receptors, through the interaction between the C-terminal three-helix-bundle of the GAT (GGA and Tom1) domain (C-GAT) and ubiquitin. We report here the crystal structure of human GGA3 C-GAT in complex with ubiquitin. A hydrophobic patch on C-GAT helices alpha1 and alpha2 forms a binding site for the hydrophobic Ile44 surface of ubiquitin. Two distinct orientations of ubiquitin Arg42 determine the shape and the charge distribution of ubiquitin Ile44 surface, leading to two different binding modes. Biochemical and NMR data strongly suggest another hydrophobic binding site on C-GAT helices alpha2 and alpha3, opposite to the first binding site, also binds ubiquitin although weakly. The double-sided ubiquitin binding provides the GAT domain with higher efficiency in recognizing ubiquitinated receptors for lysosomal receptor degradation.

Reviews - 1wr6 mentioned but not cited (2)

  1. Ubiquitin-dependent sorting in endocytosis. Piper RC, Dikic I, Lukacs GL. Cold Spring Harb Perspect Biol 6 (2014)
  2. Structure of Golgi transport proteins. Kümmel D, Reinisch KM. Cold Spring Harb Perspect Biol 3 (2011)


Reviews citing this publication (9)

  1. Ubiquitin-binding domains - from structures to functions. Dikic I, Wakatsuki S, Walters KJ. Nat. Rev. Mol. Cell Biol. 10 659-671 (2009)
  2. Ubiquitin-binding domains. Hurley JH, Lee S, Prag G. Biochem. J. 399 361-372 (2006)
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  4. Governance of endocytic trafficking and signaling by reversible ubiquitylation. Clague MJ, Liu H, Urbé S. Dev. Cell 23 457-467 (2012)
  5. Survey of the year 2005 commercial optical biosensor literature. Rich RL, Myszka DG. J. Mol. Recognit. 19 478-534 (2006)
  6. Membrane recruitment of effector proteins by Arf and Rab GTPases. Kawasaki M, Nakayama K, Wakatsuki S. Curr. Opin. Struct. Biol. 15 681-689 (2005)
  7. Cargo adaptors: structures illuminate mechanisms regulating vesicle biogenesis. Paczkowski JE, Richardson BC, Fromme JC. Trends Cell Biol. 25 408-416 (2015)
  8. The emerging role of VHS domain-containing Tom1, Tom1L1 and Tom1L2 in membrane trafficking. Wang T, Liu NS, Seet LF, Hong W. Traffic 11 1119-1128 (2010)
  9. Ubiquitin and its binding domains. Randles L, Walters KJ. Front Biosci (Landmark Ed) 17 2140-2157 (2012)

Articles citing this publication (19)

  1. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Penengo L, Mapelli M, Murachelli AG, Confalonieri S, Magri L, Musacchio A, Di Fiore PP, Polo S, Schneider TR. Cell 124 1183-1195 (2006)
  2. Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Hirano S, Kawasaki M, Ura H, Kato R, Raiborg C, Stenmark H, Wakatsuki S. Nat. Struct. Mol. Biol. 13 272-277 (2006)
  3. PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Wang J, Sun HQ, Macia E, Kirchhausen T, Watson H, Bonifacino JS, Yin HL. Mol. Biol. Cell 18 2646-2655 (2007)
  4. Ubiquitin regulates GGA3-mediated degradation of BACE1. Kang EL, Cameron AN, Piazza F, Walker KR, Tesco G. J. Biol. Chem. 285 24108-24119 (2010)
  5. Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. Pak Y, Glowacka WK, Bruce MC, Pham N, Rotin D. J. Cell Biol. 175 631-645 (2006)
  6. The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, Hummer G, Bonifacino JS, Hurley JH. Dev. Cell 12 973-986 (2007)
  7. Solution structure and dynamics of Ufm1, a ubiquitin-fold modifier 1. Sasakawa H, Sakata E, Yamaguchi Y, Komatsu M, Tatsumi K, Kominami E, Tanaka K, Kato K. Biochem. Biophys. Res. Commun. 343 21-26 (2006)
  8. Gga2 mediates sequential ubiquitin-independent and ubiquitin-dependent steps in the trafficking of ARN1 from the trans-Golgi network to the vacuole. Deng Y, Guo Y, Watson H, Au WC, Shakoury-Elizeh M, Basrai MA, Bonifacino JS, Philpott CC. J. Biol. Chem. 284 23830-23841 (2009)
  9. BACE1 protein endocytosis and trafficking are differentially regulated by ubiquitination at lysine 501 and the Di-leucine motif in the carboxyl terminus. Kang EL, Biscaro B, Piazza F, Tesco G. J. Biol. Chem. 287 42867-42880 (2012)
  10. Structural basis for recognition of ubiquitinated cargo by Tom1-GAT domain. Akutsu M, Kawasaki M, Katoh Y, Shiba T, Yamaguchi Y, Kato R, Kato K, Nakayama K, Wakatsuki S. FEBS Lett. 579 5385-5391 (2005)
  11. Monoubiquitylation of GGA3 by hVPS18 regulates its ubiquitin-binding ability. Yogosawa S, Kawasaki M, Wakatsuki S, Kominami E, Shiba Y, Nakayama K, Kohsaka S, Akazawa C. Biochem. Biophys. Res. Commun. 350 82-90 (2006)
  12. Geometric similarities of protein-protein interfaces at atomic resolution are only observed within homologous families: an exhaustive structural classification study. Kinjo AR, Nakamura H. J. Mol. Biol. 399 526-540 (2010)
  13. Defects in cellular sorting and retroviral assembly induced by GGA overexpression. Joshi A, Nagashima K, Freed EO. BMC Cell Biol. 10 72 (2009)
  14. The Endosome-associated Deubiquitinating Enzyme USP8 Regulates BACE1 Enzyme Ubiquitination and Degradation. Yeates EF, Tesco G. J. Biol. Chem. 291 15753-15766 (2016)
  15. Protein-spanning water networks and implications for prediction of protein-protein interactions mediated through hydrophobic effects. Cui D, Ou S, Patel S. Proteins 82 3312-3326 (2014)
  16. Comment Two new structures of Ub-receptor complexes. U2. Alam SL, Sundquist WI. Nat. Struct. Mol. Biol. 13 186-188 (2006)
  17. Ubiquitin fragments: their known biological activities and putative roles. Pasikowski P, Cydzik M, Kluczyk A, Stefanowicz P, Szewczuk Z. Biomol Concepts 1 67-83 (2010)
  18. The Habc domain of syntaxin 3 is a ubiquitin binding domain. Giovannone AJ, Reales E, Bhattaram P, Nackeeran S, Monahan AB, Syed R, Weimbs T. Sci Rep 10 21350 (2020)
  19. Up-regulated GGA3 promotes non-small cell lung cancer proliferation by regulating TrkA receptor. Jiang BG, Zhou YR. Transl Cancer Res 8 2543-2551 (2019)


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