Mechanism and evolution of the Zn-fingernail required for interaction of VARP with VPS29.
Cryoelectron Microscopy
Cysteine
/ chemistry
Evolution, Molecular
GTPase-Activating Proteins
/ chemistry
Guanine Nucleotide Exchange Factors
/ chemistry
HeLa Cells
Humans
Magnetic Resonance Spectroscopy
Models, Molecular
Multiprotein Complexes
/ chemistry
Protein Conformation
Vesicular Transport Proteins
/ chemistry
Zinc
/ metabolism
Zinc Fingers
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
06 10 2020
06 10 2020
Historique:
received:
28
01
2020
accepted:
08
09
2020
entrez:
7
10
2020
pubmed:
8
10
2020
medline:
30
10
2020
Statut:
epublish
Résumé
VARP and TBC1D5 are accessory/regulatory proteins of retromer-mediated retrograde trafficking from endosomes. Using an NMR/X-ray approach, we determined the structure of the complex between retromer subunit VPS29 and a 12 residue, four-cysteine/Zn
Identifiants
pubmed: 33024112
doi: 10.1038/s41467-020-18773-2
pii: 10.1038/s41467-020-18773-2
pmc: PMC7539009
doi:
Substances chimiques
ANKRD27 protein, human
0
GTPase-Activating Proteins
0
Guanine Nucleotide Exchange Factors
0
Multiprotein Complexes
0
TBC1D5 protein, human
0
VPS29 protein, human
0
Vesicular Transport Proteins
0
Zinc
J41CSQ7QDS
Cysteine
K848JZ4886
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5031Subventions
Organisme : Medical Research Council
ID : MC_U105178934
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 090909/Z/09/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : U105178934
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R009015/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM119525
Pays : United States
Références
Burd, C. & Cullen, P. J. Retromer: a master conductor of endosome sorting. Cold Spring Harb. Perspect. Biol. 6, a016774 (2014).
pubmed: 24492709
pmcid: 3941235
doi: 10.1101/cshperspect.a016774
Chen, K. E., Healy, M. D. & Collins, B. M. Towards a molecular understanding of endosomal trafficking by Retromer and Retriever. Traffic 20, 465–478 (2019).
pubmed: 30993794
doi: 10.1111/tra.12649
pmcid: 30993794
Seaman, M. N. The retromer complex - endosomal protein recycling and beyond. J. Cell Sci. 125, 4693–4702 (2012).
pubmed: 23148298
pmcid: 3517092
doi: 10.1242/jcs.103440
Trousdale, C. & Kim, K. Retromer: Structure, function, and roles in mammalian disease. Eur. J. Cell Biol. 94, 513–521 (2015).
pubmed: 26220253
doi: 10.1016/j.ejcb.2015.07.002
pmcid: 26220253
Koumandou, V. L. et al. Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 124, 1496–1509 (2011).
pubmed: 21502137
pmcid: 3078816
doi: 10.1242/jcs.081596
Lee, J. J., Radice, G., Perkins, C. P. & Costantini, F. Identification and characterization of a novel, evolutionarily conserved gene disrupted by the murine H beta 58 embryonic lethal transgene insertion. Development 115, 277–288 (1992).
pubmed: 1638986
pmcid: 1638986
Radice, G., Lee, J. J. & Costantini, F. H beta 58, an insertional mutation affecting early postimplantation development of the mouse embryo. Development 111, 801–811 (1991).
pubmed: 1879343
pmcid: 1879343
Reitz, C. Retromer dysfunction and neurodegenerative disease. Curr. Genomics 19, 279–288 (2018).
pubmed: 29755290
pmcid: 5930449
doi: 10.2174/1389202919666171024122809
Harterink, M. et al. A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat. Cell Biol. 13, 914–923 (2011).
pubmed: 21725319
pmcid: 4052212
doi: 10.1038/ncb2281
Rojas, R., Kametaka, S., Haft, C. R. & Bonifacino, J. S. Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol. Cell Biol. 27, 1112–1124 (2007).
pubmed: 17101778
doi: 10.1128/MCB.00156-06
pmcid: 17101778
Temkin, P. et al. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 715–721 (2011).
pubmed: 21602791
pmcid: 3113693
doi: 10.1038/ncb2252
Wassmer, T. et al. A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J. Cell Sci. 120, 45–54 (2007).
pubmed: 17148574
doi: 10.1242/jcs.03302
pmcid: 17148574
Gomez, T. S. & Billadeau, D. D. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699–711 (2009).
pubmed: 19922874
pmcid: 2803077
doi: 10.1016/j.devcel.2009.09.009
Harbour, M. E. et al. The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703–3717 (2010).
pubmed: 20923837
pmcid: 2964111
doi: 10.1242/jcs.071472
Jimenez-Orgaz, A. et al. Control of RAB7 activity and localization through the retromer-TBC1D5 complex enables RAB7-dependent mitophagy. EMBO J. 37, 235–254 (2018).
pubmed: 29158324
doi: 10.15252/embj.201797128
pmcid: 29158324
Seaman, M. N., Harbour, M. E., Tattersall, D., Read, E. & Bright, N. Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 122, 2371–2382 (2009).
pubmed: 19531583
pmcid: 2704877
doi: 10.1242/jcs.048686
Shi, A. et al. Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J. 28, 3290–3302 (2009).
pubmed: 19763082
pmcid: 2776105
doi: 10.1038/emboj.2009.272
Zhang, J. et al. Rabankyrin-5 interacts with EHD1 and Vps26 to regulate endocytic trafficking and retromer function. Traffic 13, 745–757 (2012).
pubmed: 22284051
pmcid: 3613124
doi: 10.1111/j.1600-0854.2012.01334.x
Hesketh, G. G. et al. VARP is recruited on to endosomes by direct interaction with retromer, where together they function in export to the cell surface. Dev. Cell 29, 591–606 (2014).
pubmed: 24856514
pmcid: 4059916
doi: 10.1016/j.devcel.2014.04.010
McGough, I. J. et al. Identification of molecular heterogeneity in SNX27-retromer-mediated endosome-to-plasma-membrane recycling. J. Cell Sci. 127, 4940–4953 (2014).
pubmed: 25278552
pmcid: 4231307
doi: 10.1242/jcs.156299
Burgo, A. et al. Role of Varp, a Rab21 exchange factor and TI-VAMP/VAMP7 partner, in neurite growth. EMBO Rep. 10, 1117–1124 (2009).
pubmed: 19745841
pmcid: 2759737
doi: 10.1038/embor.2009.186
Schafer, I. B. et al. The binding of Varp to VAMP7 traps VAMP7 in a closed, fusogenically inactive conformation. Nat. Struct. Mol. Biol. 19, 1300–1309 (2012).
pubmed: 23104059
pmcid: 3605791
doi: 10.1038/nsmb.2414
Tamura, K. et al. Varp is a novel Rab32/38-binding protein that regulates Tyrp1 trafficking in melanocytes. Mol. Biol. Cell 20, 2900–2908 (2009).
pubmed: 19403694
pmcid: 2695797
doi: 10.1091/mbc.e08-12-1161
Zhang, X., He, X., Fu, X. Y. & Chang, Z. Varp is a Rab21 guanine nucleotide exchange factor and regulates endosome dynamics. J. Cell Sci. 119, 1053–1062 (2006).
pubmed: 16525121
doi: 10.1242/jcs.02810
pmcid: 16525121
Burgo, A. et al. A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev. Cell 23, 166–180 (2012).
pubmed: 22705394
doi: 10.1016/j.devcel.2012.04.019
pmcid: 22705394
Linding, R., Russell, R. B., Neduva, V. & Gibson, T. J. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701–3708 (2003).
pubmed: 12824398
pmcid: 169197
doi: 10.1093/nar/gkg519
Collins, B. M., Skinner, C. F., Watson, P. J., Seaman, M. N. & Owen, D. J. Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat. Struct. Mol. Biol. 12, 594–602 (2005).
pubmed: 15965486
doi: 10.1038/nsmb954
pmcid: 15965486
Eustermann, S. et al. Structural basis of detection and signaling of DNA single-strand breaks by human PARP-1. Mol. Cell 60, 742–754 (2015).
pubmed: 26626479
pmcid: 4678113
doi: 10.1016/j.molcel.2015.10.032
Gobl, C., Madl, T., Simon, B. & Sattler, M. NMR approaches for structural analysis of multidomain proteins and complexes in solution. Prog. Nucl. Magn. Reson Spectrosc. 80, 26–63 (2014).
pubmed: 24924266
doi: 10.1016/j.pnmrs.2014.05.003
pmcid: 24924266
Mackereth, C. D. et al. Multi-domain conformational selection underlies pre-mRNA splicing regulation by U2AF. Nature 475, 408–411 (2011).
pubmed: 21753750
doi: 10.1038/nature10171
pmcid: 21753750
Wishart, D. S. & Sykes, B. D. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 4, 171–180 (1994).
pubmed: 8019132
doi: 10.1007/BF00175245
pmcid: 8019132
Harbour, M. E. & Seaman, M. N. Evolutionary variations of VPS29, and their implications for the heteropentameric model of retromer. Commun. Integr. Biol. 4, 619–622 (2011).
pubmed: 22046480
pmcid: 3204146
doi: 10.4161/cib.16855
Krissinel, E. Stock-based detection of protein oligomeric states in jsPISA. Nucleic Acids Res. 43, W314–W319 (2015).
pubmed: 25908787
pmcid: 4489313
doi: 10.1093/nar/gkv314
Andreini, C., Bertini, I. & Cavallaro, G. Minimal functional sites allow a classification of zinc sites in proteins. PLoS ONE 6, e26325 (2011).
pubmed: 22043316
pmcid: 3197139
doi: 10.1371/journal.pone.0026325
Kluska, K., Adamczyk, J. & Krezel, A. Metal binding properties of zinc fingers with a naturally altered metal binding site. Metallomics 10, 248–263 (2018).
pubmed: 29230465
doi: 10.1039/C7MT00256D
pmcid: 29230465
Medina, A. et al. ALEPH: a network-oriented approach for the generation of fragment-based libraries and for structure interpretation. Acta Crystallogr. D. Struct. Biol. 76, 193–208 (2020).
pubmed: 32133985
pmcid: 7057218
doi: 10.1107/S2059798320001679
Steinberg, F. et al. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15, 461–471 (2013).
pubmed: 23563491
pmcid: 4052425
doi: 10.1038/ncb2721
Seaman, M. N. J., Mukadam, A. S. & Breusegem, S. Y. Inhibition of TBC1D5 activates Rab7a and can enhance the function of the retromer cargo-selective complex. J. Cell Sci. 131, 217398 (2018).
de Beer, T. et al. Molecular mechanism of NPF recognition by EH domains. Nat. Struct. Biol. 7, 1018–1022 (2000).
pubmed: 11062555
doi: 10.1038/80924
pmcid: 11062555
Edeling, M. A., Smith, C. & Owen, D. Life of a clathrin coat: insights from clathrin and AP structures. Nat. Rev. Mol. Cell Biol. 7, 32–44 (2006).
pubmed: 16493411
doi: 10.1038/nrm1786
pmcid: 16493411
Mukhopadhyay, A., Pan, X., Lambright, D. G. & Tissenbaum, H. A. An endocytic pathway as a target of tubby for regulation of fat storage. EMBO Rep. 8, 931–938 (2007).
pubmed: 17762880
pmcid: 2002550
doi: 10.1038/sj.embor.7401055
Barlocher, K. et al. Structural insights into Legionella RidL-Vps29 retromer subunit interaction reveal displacement of the regulator TBC1D5. Nat. Commun. 8, 1543 (2017).
pubmed: 29146912
pmcid: 5691146
doi: 10.1038/s41467-017-01512-5
Jia, D. et al. Structural and mechanistic insights into regulation of the retromer coat by TBC1d5. Nat. Commun. 7, 13305 (2016).
pubmed: 27827364
pmcid: 5105194
doi: 10.1038/ncomms13305
Romano-Moreno, M. et al. Molecular mechanism for the subversion of the retromer coat by the Legionella effector RidL. Proc. Natl Acad. Sci. USA 114, E11151–E11160 (2017).
pubmed: 29229824
doi: 10.1073/pnas.1715361115
pmcid: 29229824
Yao, J. et al. Mechanism of inhibition of retromer transport by the bacterial effector RidL. Proc. Natl Acad. Sci. USA 115, E1446–E1454 (2018).
pubmed: 29386389
doi: 10.1073/pnas.1717383115
pmcid: 29386389
Haft, C. R. et al. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11, 4105–4116 (2000).
pubmed: 11102511
pmcid: 15060
doi: 10.1091/mbc.11.12.4105
Kovtun, O. et al. Structure of the membrane-assembled retromer coat determined by cryo-electron tomography. Nature 561, 561–564 (2018).
pubmed: 30224749
pmcid: 6173284
doi: 10.1038/s41586-018-0526-z
Kendall, A. K. et al. Mammalian retromer is an adaptable scaffold for cargo sorting from endosomes. Structure 28, 393–405 e394 (2020).
pubmed: 32027819
pmcid: 7145723
doi: 10.1016/j.str.2020.01.009
Lucas, M. et al. Structural mechanism for cargo recognition by the retromer complex. Cell 167, 1623–1635.e1614 (2016).
pubmed: 27889239
pmcid: 5147500
doi: 10.1016/j.cell.2016.10.056
Norwood, S. J. et al. Assembly and solution structure of the core retromer protein complex. Traffic 12, 56–71 (2011).
pubmed: 20875039
doi: 10.1111/j.1600-0854.2010.01124.x
pmcid: 20875039
Dennis, M. K. et al. BLOC-1 and BLOC-3 regulate VAMP7 cycling to and from melanosomes via distinct tubular transport carriers. J. Cell Biol. 214, 293–308 (2016).
pubmed: 27482051
pmcid: 4970331
doi: 10.1083/jcb.201605090
Itzhak, D. N., Tyanova, S., Cox, J. & Borner, G. H. Global, quantitative and dynamic mapping of protein subcellular localization. Elife 5, e16950 (2016).
pubmed: 27278775
pmcid: 4959882
doi: 10.7554/eLife.16950
Roy, S., Leidal, A. M., Ye, J., Ronen, S. M. & Debnath, J. Autophagy-dependent shuttling of TBC1D5 controls plasma membrane translocation of GLUT1 and glucose uptake. Mol. Cell 67, 84–95 e85 (2017).
pubmed: 28602638
pmcid: 5522182
doi: 10.1016/j.molcel.2017.05.020
Ye, H. et al. Retromer subunit, VPS29, regulates synaptic transmission and is required for endolysosomal function in the aging brain. Elife 9, e51977 (2020).
pubmed: 32286230
pmcid: 7182434
doi: 10.7554/eLife.51977
Gabernet-Castello, C., O’Reilly, A. J., Dacks, J. B. & Field, M. C. Evolution of Tre-2/Bub2/Cdc16 (TBC) Rab GTPase-activating proteins. Mol. Biol. Cell 24, 1574–1583 (2013).
pubmed: 23485563
pmcid: 3655817
doi: 10.1091/mbc.e12-07-0557
Herman, E. K., Ali, M., Field, M. C. & Dacks, J. B. Regulation of early endosomes across eukaryotes: evolution and functional homology of Vps9 proteins. Traffic 19, 546–563 (2018).
pubmed: 29603841
pmcid: 6032885
doi: 10.1111/tra.12570
Elias, M., Brighouse, A., Gabernet-Castello, C., Field, M. C. & Dacks, J. B. Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J. Cell Sci. 125, 2500–2508 (2012).
pubmed: 22366452
pmcid: 3383260
doi: 10.1242/jcs.101378
Kloepper, T. H., Kienle, C. N. & Fasshauer, D. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18, 3463–3471 (2007).
pubmed: 17596510
pmcid: 1951749
doi: 10.1091/mbc.e07-03-0193
Vedovato, M., Rossi, V., Dacks, J. B. & Filippini, F. Comparative analysis of plant genomes allows the definition of the “Phytolongins”: a novel non-SNARE longin domain protein family. BMC Genomics 10, 510 (2009).
pubmed: 19889231
pmcid: 2779197
doi: 10.1186/1471-2164-10-510
Bean, B. D. et al. Rab5-family guanine nucleotide exchange factors bind retromer and promote its recruitment to endosomes. Mol. Biol. Cell 26, 1119–1128 (2015).
pubmed: 25609093
pmcid: 4357511
doi: 10.1091/mbc.E14-08-1281
Goody, R. S., Rak, A. & Alexandrov, K. The structural and mechanistic basis for recycling of Rab proteins between membrane compartments. Cell Mol. Life Sci. 62, 1657–1670 (2005).
pubmed: 15924270
doi: 10.1007/s00018-005-4486-8
pmcid: 15924270
Simpson, J. C. et al. A role for the small GTPase Rab21 in the early endocytic pathway. J. Cell Sci. 117, 6297–6311 (2004).
pubmed: 15561770
doi: 10.1242/jcs.01560
pmcid: 15561770
Stenmark, H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513–525 (2009).
pubmed: 19603039
doi: 10.1038/nrm2728
pmcid: 19603039
Vranken, W. F. et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687–696 (2005).
pubmed: 15815974
doi: 10.1002/prot.20449
pmcid: 15815974
Schwieters, C. D., Kuszewski, J. J., Tjandra, N. & Clore, G. M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson 160, 65–73 (2003).
pubmed: 12565051
doi: 10.1016/S1090-7807(02)00014-9
pmcid: 12565051
Hierro, A. et al. Functional architecture of the retromer cargo-recognition complex. Nature 449, 1063–1067 (2007).
pubmed: 17891154
pmcid: 2377034
doi: 10.1038/nature06216
Swarbrick, J. D. et al. VPS29 is not an active metallo-phosphatase but is a rigid scaffold required for retromer interaction with accessory proteins. PLoS ONE 6, e20420 (2011).
pubmed: 21629666
pmcid: 3101248
doi: 10.1371/journal.pone.0020420
Kuszewski, J., Gronenborn, A. M. & Clore, G. M. Improving the quality of NMR and crystallographic protein structures by means of a conformational database potential derived from structure databases. Protein Sci. 5, 1067–1080 (1996).
pubmed: 8762138
pmcid: 2143426
doi: 10.1002/pro.5560050609
Hommel, U., Harvey, T. S., Driscoll, P. C. & Campbell, I. D. Human epidermal growth factor. High resolution solution structure and comparison with human transforming growth factor alpha. J. Mol. Biol. 227, 271–282 (1992).
pubmed: 1522591
doi: 10.1016/0022-2836(92)90697-I
pmcid: 1522591
Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. & Thornton, J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477–486 (1996).
pubmed: 9008363
doi: 10.1007/BF00228148
pmcid: 9008363
Diamond, R. Coordinate-based cluster analysis. Acta Crystallogr. D. Biol. Crystallogr. 51, 127–135 (1995).
pubmed: 15299312
doi: 10.1107/S0907444994010723
pmcid: 15299312
Bright, N. A., Davis, L. J. & Luzio, J. P. Endolysosomes are the principal intracellular sites of acid hydrolase activity. Curr. Biol. 26, 2233–2245 (2016).
pubmed: 27498570
pmcid: 5026700
doi: 10.1016/j.cub.2016.06.046
Eddy, S. R. A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol. 4, e1000069 (2008).
pubmed: 18516236
pmcid: 2396288
doi: 10.1371/journal.pcbi.1000069
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
pmcid: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Marchler-Bauer, A. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225–D229 (2011).
pubmed: 21109532
doi: 10.1093/nar/gkq1189
pmcid: 21109532
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 15034147
doi: 10.1093/nar/gkh340