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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 2835-45 (2009)
Cited: 53 times
EuropePMC logo PMID: 19644450

Abstract

The JNK-interacting proteins, JIP3 and JIP4, are specific effectors of the small GTP-binding protein ARF6. The interaction of ARF6-GTP with the second leucine zipper (LZII) domains of JIP3/JIP4 regulates the binding of JIPs to kinesin-1 and dynactin. Here, we report the crystal structure of ARF6-GTP bound to the JIP4-LZII at 1.9 A resolution. The complex is a heterotetramer with dyad symmetry arranged in an ARF6-(JIP4)(2)-ARF6 configuration. Comparison of the ARF6-JIP4 interface with the equivalent region of ARF1 shows the structural basis of JIP4's specificity for ARF6. Using site-directed mutagenesis and surface plasmon resonance, we further show that non-conserved residues at the switch region borders are the key structural determinants of JIP4 specificity. A structure-derived model of the association of the ARF6-JIP3/JIP4 complex with membranes shows that the JIP4-LZII coiled-coil should lie along the membrane to prevent steric hindrances, resulting in only one ARF6 molecule bound. Such a heterotrimeric complex gives insights to better understand the ARF6-mediated motor switch regulatory function.

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  1. Arf6 as a therapeutic target: Structure, mechanism, and inhibitors. Sun D, Guo Y, Tang P, Li H, Chen L. Acta Pharm Sin B 13 4089-4104 (2023)

Articles - 2w83 mentioned but not cited (10)

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  5. ARF6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. Eva R, Crisp S, Marland JR, Norman JC, Kanamarlapudi V, ffrench-Constant C, Fawcett JW. J Neurosci 32 10352-10364 (2012)
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  7. Congress Survey of the 2009 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 24 892-914 (2011)
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  17. 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)
  18. The scaffold protein JIP3 functions as a downstream effector of the small GTPase ARF6 to regulate neurite morphogenesis of cortical neurons. Suzuki A, Arikawa C, Kuwahara Y, Itoh K, Watanabe M, Watanabe H, Suzuki T, Funakoshi Y, Hasegawa H, Kanaho Y. FEBS Lett 584 2801-2806 (2010)
  19. Syd/JIP3 and JNK signaling are required for myonuclear positioning and muscle function. Schulman VK, Folker ES, Rosen JN, Baylies MK. PLoS Genet 10 e1004880 (2014)
  20. Strengths and weaknesses of data-driven docking in critical assessment of prediction of interactions. de Vries SJ, Melquiond AS, Kastritis PL, Karaca E, Bordogna A, van Dijk M, Rodrigues JP, Bonvin AM. Proteins 78 3242-3249 (2010)
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  23. Structural characterization of the RH1-LZI tandem of JIP3/4 highlights RH1 domains as a cytoskeletal motor-binding motif. Vilela F, Velours C, Chenon M, Aumont-Nicaise M, Campanacci V, Thureau A, Pylypenko O, Andreani J, Llinas P, Ménétrey J. Sci Rep 9 16036 (2019)
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  25. CAPRI targets T29-T42: proving ground for new docking procedures. Eisenstein M, Ben-Shimon A, Frankenstein Z, Kowalsman N. Proteins 78 3174-3181 (2010)
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  28. Rab10 regulates the sorting of internalised TrkB for retrograde axonal transport. Lazo OM, Schiavo G. Elife 12 e81532 (2023)
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  30. Novel modulation factor quantifies the role of water molecules in protein interactions. Bueno M, Temiz NA, Camacho CJ. Proteins 78 3226-3234 (2010)
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  32. Loss of MAPK8IP3 Affects Endocytosis in Neurons. Snead AM, Gowrishankar S. Front Cell Neurosci 16 828071 (2022)


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