2j59 Citations

Structural basis for ARF1-mediated recruitment of ARHGAP21 to Golgi membranes.

Abstract

ARHGAP21 is a Rho family GTPase-activating protein (RhoGAP) that controls the Arp2/3 complex and F-actin dynamics at the Golgi complex by regulating the activity of the small GTPase Cdc42. ARHGAP21 is recruited to the Golgi by binding to another small GTPase, ARF1. Here, we present the crystal structure of the activated GTP-bound form of ARF1 in a complex with the Arf-binding domain (ArfBD) of ARHGAP21 at 2.1 A resolution. We show that ArfBD comprises a PH domain adjoining a C-terminal alpha helix, and that ARF1 interacts with both of these structural motifs through its switch regions and triggers structural rearrangement of the PH domain. We used site-directed mutagenesis to confirm that both the PH domain and the helical motif are essential for the binding of ArfBD to ARF1 and for its recruitment to the Golgi. Our data demonstrate that two well-known small GTPase-binding motifs, the PH domain and the alpha helical motif, can combine to create a novel mode of binding to Arfs.

Articles - 2j59 mentioned but not cited (11)

  1. Dynamic structure of membrane-anchored Arf*GTP. Liu Y, Kahn RA, Prestegard JH. Nat Struct Mol Biol 17 876-881 (2010)
  2. FRODOCK: a new approach for fast rotational protein-protein docking. Garzon JI, Lopéz-Blanco JR, Pons C, Kovacs J, Abagyan R, Fernandez-Recio J, Chacon P. Bioinformatics 25 2544-2551 (2009)
  3. Structural basis of selective ubiquitination of TRF1 by SCFFbx4. Zeng Z, Wang W, Yang Y, Chen Y, Yang X, Diehl JA, Liu X, Lei M. Dev Cell 18 214-225 (2010)
  4. Interaction of Fapp1 with Arf1 and PI4P at a membrane surface: an example of coincidence detection. Liu Y, Kahn RA, Prestegard JH. Structure 22 421-430 (2014)
  5. CONS-COCOMAPS: a novel tool to measure and visualize the conservation of inter-residue contacts in multiple docking solutions. Vangone A, Oliva R, Cavallo L. BMC Bioinformatics 13 Suppl 4 S19 (2012)
  6. Protein Interaction Z Score Assessment (PIZSA): an empirical scoring scheme for evaluation of protein-protein interactions. Roy AA, Dhawanjewar AS, Sharma P, Singh G, Madhusudhan MS. Nucleic Acids Res 47 W331-W337 (2019)
  7. Structure of Plasmodium falciparum ADP-ribosylation factor 1. Cook WJ, Smith CD, Senkovich O, Holder AA, Chattopadhyay D. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 1426-1431 (2010)
  8. The Glo3 GAP crystal structure supports the molecular niche model for ArfGAPs in COPI coats. Xie B, Jung C, Chandra M, Engel A, Kendall AK, Jackson LP. Adv Biol Regul 79 100781 (2021)
  9. Classification of heterodimer interfaces using docking models and construction of scoring functions for the complex structure prediction. Tsuchiya Y, Kanamori E, Nakamura H, Kinoshita K. Adv Appl Bioinform Chem 2 79-100 (2009)
  10. A Structural Network Analysis of Neuronal ArhGAP21/23 Interactors by Computational Modeling. Kouchi Z, Kojima M. ACS Omega 8 19249-19264 (2023)
  11. ARF1 prevents aberrant type I interferon induction by regulating STING activation and recycling. Hirschenberger M, Lepelley A, Rupp U, Klute S, Hunszinger V, Koepke L, Merold V, Didry-Barca B, Wondany F, Bergner T, Moreau T, Rodero MP, Rösler R, Wiese S, Volpi S, Gattorno M, Papa R, Lynch SA, Haug MG, Houge G, Wigby KM, Sprague J, Lenberg J, Read C, Walther P, Michaelis J, Kirchhoff F, de Oliveira Mann CC, Crow YJ, Sparrer KMJ. Nat Commun 14 6770 (2023)


Reviews citing this publication (12)

  1. Regulation of small GTPases by GEFs, GAPs, and GDIs. Cherfils J, Zeghouf M. Physiol Rev 93 269-309 (2013)
  2. The small G proteins of the Arf family and their regulators. Gillingham AK, Munro S. Annu Rev Cell Dev Biol 23 579-611 (2007)
  3. Protein-protein docking tested in blind predictions: the CAPRI experiment. Janin J. Mol Biosyst 6 2351-2362 (2010)
  4. Protein-protein docking dealing with the unknown. Moreira IS, Fernandes PA, Ramos MJ. J Comput Chem 31 317-342 (2010)
  5. GTPases involved in vesicular trafficking: structures and mechanisms. Itzen A, Goody RS. Semin Cell Dev Biol 22 48-56 (2011)
  6. Structures of Ras superfamily effector complexes: What have we learnt in two decades? Mott HR, Owen D. Crit Rev Biochem Mol Biol 50 85-133 (2015)
  7. Arf GTPases and their effectors: assembling multivalent membrane-binding platforms. Cherfils J. Curr Opin Struct Biol 29 67-76 (2014)
  8. Structural biology of Arf and Rab GTPases' effector recruitment and specificity. Khan AR, Ménétrey J. Structure 21 1284-1297 (2013)
  9. Actin acting at the Golgi. Egea G, Serra-Peinado C, Salcedo-Sicilia L, Gutiérrez-Martínez E. Histochem Cell Biol 140 347-360 (2013)
  10. Toward a structural understanding of arf family:effector specificity. Chavrier P, Ménétrey J. Structure 18 1552-1558 (2010)
  11. ARHGAP21 as a master regulator of multiple cellular processes. Rosa LRO, Soares GM, Silveira LR, Boschero AC, Barbosa-Sampaio HCL. J Cell Physiol 233 8477-8481 (2018)
  12. The Arf family GTPases: Regulation of vesicle biogenesis and beyond. Li FL, Guan KL. Bioessays 45 e2200214 (2023)

Articles citing this publication (52)

  1. HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. de Vries SJ, van Dijk AD, Krzeminski M, van Dijk M, Thureau A, Hsu V, Wassenaar T, Bonvin AM. Proteins 69 726-733 (2007)
  2. Docking and scoring protein complexes: CAPRI 3rd Edition. Lensink MF, Méndez R, Wodak SJ. Proteins 69 704-718 (2007)
  3. ARF6 Interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Montagnac G, Sibarita JB, Loubéry S, Daviet L, Romao M, Raposo G, Chavrier P. Curr Biol 19 184-195 (2009)
  4. Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. DiNitto JP, Delprato A, Gabe Lee MT, Cronin TC, Huang S, Guilherme A, Czech MP, Lambright DG. Mol Cell 28 569-583 (2007)
  5. ClusPro: performance in CAPRI rounds 6-11 and the new server. Comeau SR, Kozakov D, Brenke R, Shen Y, Beglov D, Vajda S. Proteins 69 781-785 (2007)
  6. Kinetic studies of the Arf activator Arno on model membranes in the presence of Arf effectors suggest control by a positive feedback loop. Stalder D, Barelli H, Gautier R, Macia E, Jackson CL, Antonny B. J Biol Chem 286 3873-3883 (2011)
  7. Molecular basis of phosphatidylinositol 4-phosphate and ARF1 GTPase recognition by the FAPP1 pleckstrin homology (PH) domain. He J, Scott JL, Heroux A, Roy S, Lenoir M, Overduin M, Stahelin RV, Kutateladze TG. J Biol Chem 286 18650-18657 (2011)
  8. The structural basis of Arf effector specificity: the crystal structure of ARF6 in a complex with JIP4. Isabet T, Montagnac G, Regazzoni K, Raynal B, El Khadali F, England P, Franco M, Chavrier P, Houdusse A, Ménétrey J. EMBO J 28 2835-2845 (2009)
  9. Blind predictions of protein interfaces by docking calculations in CAPRI. Lensink MF, Wodak SJ. Proteins 78 3085-3095 (2010)
  10. Transport of influenza virus neuraminidase (NA) to host cell surface is regulated by ARHGAP21 and Cdc42 proteins. Wang S, Li H, Chen Y, Wei H, Gao GF, Liu H, Huang S, Chen JL. J Biol Chem 287 9804-9816 (2012)
  11. The performance of ZDOCK and ZRANK in rounds 6-11 of CAPRI. Wiehe K, Pierce B, Tong WW, Hwang H, Mintseris J, Weng Z. Proteins 69 719-725 (2007)
  12. β-Arrestin 1 inhibits the GTPase-activating protein function of ARHGAP21, promoting activation of RhoA following angiotensin II type 1A receptor stimulation. Anthony DF, Sin YY, Vadrevu S, Advant N, Day JP, Byrne AM, Lynch MJ, Milligan G, Houslay MD, Baillie GS. Mol Cell Biol 31 1066-1075 (2011)
  13. Decoupling of activation and effector binding underlies ARF6 priming of fast endocytic recycling. Montagnac G, de Forges H, Smythe E, Gueudry C, Romao M, Salamero J, Chavrier P. Curr Biol 21 574-579 (2011)
  14. The small G protein Arl1 directs the trans-Golgi-specific targeting of the Arf1 exchange factors BIG1 and BIG2. Christis C, Munro S. J Cell Biol 196 327-335 (2012)
  15. Implicit flexibility in protein docking: cross-docking and local refinement. Król M, Chaleil RA, Tournier AL, Bates PA. Proteins 69 750-757 (2007)
  16. Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis. Makyio H, Ohgi M, Takei T, Takahashi S, Takatsu H, Katoh Y, Hanai A, Ueda T, Kanaho Y, Xie Y, Shin HW, Kamikubo H, Kataoka M, Kawasaki M, Kato R, Wakatsuki S, Nakayama K. EMBO J 31 2590-2603 (2012)
  17. Retrograde Shiga toxin trafficking is regulated by ARHGAP21 and Cdc42. Hehnly H, Longhini KM, Chen JL, Stamnes M. Mol Biol Cell 20 4303-4312 (2009)
  18. Cdc42 regulates microtubule-dependent Golgi positioning. Hehnly H, Xu W, Chen JL, Stamnes M. Traffic 11 1067-1078 (2010)
  19. Structural basis for membrane recruitment and allosteric activation of cytohesin family Arf GTPase exchange factors. Malaby AW, van den Berg B, Lambright DG. Proc Natl Acad Sci U S A 110 14213-14218 (2013)
  20. ARAP1 regulates EGF receptor trafficking and signalling. Daniele T, Di Tullio G, Santoro M, Turacchio G, De Matteis MA. Traffic 9 2221-2235 (2008)
  21. Congress The third CAPRI assessment meeting Toronto, Canada, April 20-21, 2007. Janin J, Wodak S. Structure 15 755-759 (2007)
  22. Blood fluke exploitation of non-cognate CD4+ T cell help to facilitate parasite development. Lamb EW, Walls CD, Pesce JT, Riner DK, Maynard SK, Crow ET, Wynn TA, Schaefer BC, Davies SJ. PLoS Pathog 6 e1000892 (2010)
  23. Neutralization of the membrane protein Nogo-A enhances growth and reactive sprouting in established organotypic hippocampal slice cultures. Craveiro LM, Hakkoum D, Weinmann O, Montani L, Stoppini L, Schwab ME. Eur J Neurosci 28 1808-1824 (2008)
  24. Structural insights into the small G-protein Arl13B and implications for Joubert syndrome. Miertzschke M, Koerner C, Spoerner M, Wittinghofer A. Biochem J 457 301-311 (2014)
  25. ARF1-mediated actin polymerization produces movement of artificial vesicles. Heuvingh J, Franco M, Chavrier P, Sykes C. Proc Natl Acad Sci U S A 104 16928-16933 (2007)
  26. Podosome assembly is controlled by the GTPase ARF1 and its nucleotide exchange factor ARNO. Rafiq NB, Lieu ZZ, Jiang T, Yu CH, Matsudaira P, Jones GE, Bershadsky AD. J Cell Biol 216 181-197 (2017)
  27. Membrane and Protein Interactions of the Pleckstrin Homology Domain Superfamily. Lenoir M, Kufareva I, Abagyan R, Overduin M. Membranes (Basel) 5 646-663 (2015)
  28. Protein-protein docking in CAPRI using ATTRACT to account for global and local flexibility. May A, Zacharias M. Proteins 69 774-780 (2007)
  29. Prediction and scoring of docking poses with pyDock. Grosdidier S, Pons C, Solernou A, Fernández-Recio J. Proteins 69 852-858 (2007)
  30. RosettaDock in CAPRI rounds 6-12. Wang C, Schueler-Furman O, Andre I, London N, Fleishman SJ, Bradley P, Qian B, Baker D. Proteins 69 758-763 (2007)
  31. Identification of Laying-Related SNP Markers in Geese Using RAD Sequencing. Yu S, Chu W, Zhang L, Han H, Zhao R, Wu W, Zhu J, Dodson MV, Wei W, Liu H, Chen J. PLoS One 10 e0131572 (2015)
  32. CLN3 deficient cells display defects in the ARF1-Cdc42 pathway and actin-dependent events. Schultz ML, Tecedor L, Stein CS, Stamnes MA, Davidson BL. PLoS One 9 e96647 (2014)
  33. Assessing the energy landscape of CAPRI targets by FunHunt. London N, Schueler-Furman O. Proteins 69 809-815 (2007)
  34. Autoregulation of Sec7 Arf-GEF activity and localization by positive feedback. Richardson BC, Fromme JC. Small GTPases 3 240-243 (2012)
  35. Combining interface core and whole interface descriptors in postscan processing of protein-protein docking models. Kowalsman N, Eisenstein M. Proteins 77 297-318 (2009)
  36. Brefeldin A-inhibited ADP-ribosylation factor activator BIG2 regulates cell migration via integrin β1 cycling and actin remodeling. Shen X, Li CC, Aponte AM, Shen RF, Billings EM, Moss J, Vaughan M. Proc Natl Acad Sci U S A 109 14464-14469 (2012)
  37. Rosetta in CAPRI rounds 13-19. Fleishman SJ, Corn JE, Strauch EM, Whitehead TA, Andre I, Thompson J, Havranek JJ, Das R, Bradley P, Baker D. Proteins 78 3212-3218 (2010)
  38. The targets of CAPRI rounds 6-12. Janin J. Proteins 69 699-703 (2007)
  39. The SKE-DOCK server and human teams based on a combined method of shape complementarity and free energy estimation. Terashi G, Takeda-Shitaka M, Kanou K, Iwadate M, Takaya D, Umeyama H. Proteins 69 866-872 (2007)
  40. SOFTDOCK application to protein-protein interaction benchmark and CAPRI. Li N, Sun Z, Jiang F. Proteins 69 801-808 (2007)
  41. Docking with PIPER and refinement with SDU in rounds 6-11 of CAPRI. Shen Y, Brenke R, Kozakov D, Comeau SR, Beglov D, Vajda S. Proteins 69 734-742 (2007)
  42. Light on the structural communication in Ras GTPases. Raimondi F, Felline A, Portella G, Orozco M, Fanelli F. J Biomol Struct Dyn 31 142-157 (2013)
  43. The weak complex between RhoGAP protein ARHGAP22 and signal regulatory protein 14-3-3 has 1:2 stoichiometry and a single peptide binding mode. Hu SH, Whitten AE, King GJ, Jones A, Rowland AF, James DE, Martin JL. PLoS One 7 e41731 (2012)
  44. MiR-199a Inhibits Secondary Envelopment of Herpes Simplex Virus-1 Through the Downregulation of Cdc42-specific GTPase Activating Protein Localized in Golgi Apparatus. Kobayashi K, Suemasa F, Sagara H, Nakamura S, Ino Y, Kobayashi K, Hiramatsu H, Haraguchi T, Kurokawa K, Todo T, Nakano A, Iba H. Sci Rep 7 6650 (2017)
  45. A filter enhanced sampling and combinatorial scoring study for protein docking in CAPRI. Gong XQ, Chang S, Zhang QH, Li CH, Shen LZ, Ma XH, Wang MH, Liu B, He HQ, Chen WZ, Wang CX. Proteins 69 859-865 (2007)
  46. Acidic groups docked to well defined wetted pockets at the core of the binding interface: a tale of scoring and missing protein interactions in CAPRI. Bueno M, Camacho CJ. Proteins 69 786-792 (2007)
  47. Protein-protein docking: progress in CAPRI rounds 6-12 using a combination of methods: the introduction of steered solvated molecular dynamics. Heifetz A, Pal S, Smith GR. Proteins 69 816-822 (2007)
  48. RNA-seq analysis identifies cytoskeletal structural genes and pathways for meat quality in beef. Leal-Gutiérrez JD, Elzo MA, Carr C, Mateescu RG. PLoS One 15 e0240895 (2020)
  49. ARHGAP21 prevents abnormal insulin release through actin rearrangement in pancreatic islets from neonatal mice. Ferreira SM, Santos GJ, Rezende LF, Gonçalves LM, Santos-Silva JC, Bigarella CL, Carneiro EM, Saad ST, Boschero AC, Barbosa-Sampaio HC. Life Sci 127 53-58 (2015)
  50. An Arf1 GTPase mutant with different responses to GEF inhibitors. Flisiak S, Zeeh JC, Guibert B, Cherfils J, Zeghouf M. Biochem Biophys Res Commun 377 156-160 (2008)
  51. Dominant ARF3 variants disrupt Golgi integrity and cause a neurodevelopmental disorder recapitulated in zebrafish. Fasano G, Muto V, Radio FC, Venditti M, Mosaddeghzadeh N, Coppola S, Paradisi G, Zara E, Bazgir F, Ziegler A, Chillemi G, Bertuccini L, Tinari A, Vetro A, Pantaleoni F, Pizzi S, Conti LA, Petrini S, Bruselles A, Prandi IG, Mancini C, Chandramouli B, Barth M, Bris C, Milani D, Selicorni A, Macchiaiolo M, Gonfiantini MV, Bartuli A, Mariani R, Curry CJ, Guerrini R, Slavotinek A, Iascone M, Dallapiccola B, Ahmadian MR, Lauri A, Tartaglia M. Nat Commun 13 6841 (2022)
  52. Structural insights into regulation of CNNM-TRPM7 divalent cation uptake by the small GTPase ARL15. Mahbub L, Kozlov G, Zong P, Lee EL, Tetteh S, Nethramangalath T, Knorn C, Jiang J, Shahsavan A, Yue L, Runnels L, Gehring K. Elife 12 e86129 (2023)


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