Structural Basis for Plexin Activation and Regulation

Neuron

Volumn 91, Issue 3, 2016, Pages 548-560

  Kong, Youxin ^a   Janssen, Bert J C ^a,d   Malinauskas, Tomas ^a   Vangoor, Vamshidhar R ^b   Coles, Charlotte H ^a,e   Kaufmann, Rainer ^a,c   Ni, Tao ^a   Gilbert, Robert J C ^a   Padilla Parra, Sergi ^a   Pasterkamp, R Jeroen ^b   Jones, E Yvonne ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UTRECHT UNIVERSITY   (Netherlands)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

autoinhibition; axon guidance; semaphorin signaling; structure function

Indexed keywords

PLEXIN; PLEXIN A1; PLEXIN A2; PLEXIN A4; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; NERVE PROTEIN; PLXNA1 PROTEIN, MOUSE; PLXNA2 PROTEIN, MOUSE; PLXNA4 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ELECTRON MICROSCOPY; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GRANULE CELL; GROWTH CONE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ANIMALS; MICE; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; PROTEIN MULTIMERIZATION; RECEPTORS, CELL SURFACE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84991098169     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.06.018     Document Type: Article

References (46)

1. Andermatt, I., Wilson, N.H., Bergmann, T., Mauti, O., Gesemann, M., Sockanathan, S., Stoeckli, E.T., Semaphorin 6B acts as a receptor in post-crossing commissural axon guidance. Development 141 (2014), 3709–3720.
2. Antipenko, A., Himanen, J.-P., van Leyen, K., Nardi-Dei, V., Lesniak, J., Barton, W.A., Rajashankar, K.R., Lu, M., Hoemme, C., Püschel, A.W., Nikolov, D.B., Structure of the semaphorin-3A receptor binding module. Neuron 39 (2003), 589–598.
3. Aricescu, A.R., Lu, W., Jones, E.Y., A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 1243–1250.
4. Atanasova, M., Whitty, A., Understanding cytokine and growth factor receptor activation mechanisms. Crit. Rev. Biochem. Mol. Biol. 47 (2012), 502–530.
5. Bashaw, G.J., Klein, R., Signaling from axon guidance receptors. Cold Spring Harb. Perspect. Biol., 2, 2010, a001941.
6. Booth, D.S., Avila-Sakar, A., Cheng, Y., Visualizing proteins and macromolecular complexes by negative stain em: from grid preparation to image acquisition. J. Vis. Exp., 2011, 10.3791/3227.
7. Brookes, E., Cao, W., Demeler, B., A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur. Biophys. J. 39 (2010), 405–414.
8. Brown, P.H., Balbo, A., Schuck, P., Characterizing Protein-Protein Interactions by Sedimentation Velocity Analytical Ultracentrifugation. 2001, John Wiley & Sons, Inc., Hoboken, NJ, USA.
9. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
10. Evans, P.R., An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 282–292.
11. Flanagan, J.F. 4th, Namy, O., Brierley, I., Gilbert, R.J.C., Direct observation of distinct A/P hybrid-state tRNAs in translocating ribosomes. Structure 18 (2010), 257–264.
12. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., Leith, A., SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996), 190–199.
13. Haklai-Topper, L., Mlechkovich, G., Savariego, D., Gokhman, I., Yaron, A., Cis interaction between Semaphorin6A and Plexin-A4 modulates the repulsive response to Sema6A. EMBO J. 29 (2010), 2635–2645.
14. Janssen, B.J.C., Robinson, R.A., Pérez-Brangulí, F., Bell, C.H., Mitchell, K.J., Siebold, C., Jones, E.Y., Structural basis of semaphorin-plexin signalling. Nature 467 (2010), 1118–1122.
15. Janssen, B.J.C., Malinauskas, T., Weir, G.A., Cader, M.Z., Siebold, C., Jones, E.Y., Neuropilins lock secreted semaphorins onto plexins in a ternary signaling complex. Nat. Struct. Mol. Biol. 19 (2012), 1293–1299.
16. Jongbloets, B.C., Pasterkamp, R.J., Semaphorin signalling during development. Development 141 (2014), 3292–3297.
17. Kolodkin, A.L., Tessier-Lavigne, M., Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol., 3, 2011, a001727.
18. Langmuir, I., THE ADSORPTION OF GASES ON PLANE SURFACES OF GLASS, MICA AND PLATINUM. J. Am. Chem. Soc. 40 (1918), 1361–1403.
19. Leray, A., Padilla-Parra, S., Roul, J., Héliot, L., Tramier, M., Spatio-Temporal Quantification of FRET in living cells by fast time-domain FLIM: a comparative study of non-fitting methods [corrected]. PLoS ONE, 8, 2013, e69335.
20. Leslie, A.G.W., The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 48–57.
21. Liu, H., Juo, Z.S., Shim, A.H.-R., Focia, P.J., Chen, X., Garcia, K.C., He, X., Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. Cell 142 (2010), 749–761.
22. Marita, M., Wang, Y., Kaliszewski, M.J., Skinner, K.C., Comar, W.D., Shi, X., Dasari, P., Zhang, X., Smith, A.W., Class A Plexins Are Organized as Preformed Inactive Dimers on the Cell Surface. Biophys. J. 109 (2015), 1937–1945.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Cryst. 40 (2007), 658–674.
24. Murshudov, G.N., Skubák, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 355–367.
25. Nicholls, R.A., Long, F., Murshudov, G.N., Low-resolution refinement tools in REFMAC5. Acta Crystallogr. D Biol. Crystallogr. 68 (2012), 404–417.
26. Nogi, T., Yasui, N., Mihara, E., Matsunaga, Y., Noda, M., Yamashita, N., Toyofuku, T., Uchiyama, S., Goshima, Y., Kumanogoh, A., Takagi, J., Structural basis for semaphorin signalling through the plexin receptor. Nature 467 (2010), 1123–1127.
27. Padilla-Parra, S., Audugé, N., Coppey-Moisan, M., Tramier, M., Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells. Biophys. J. 95 (2008), 2976–2988.
28. Padilla-Parra, S., Audugé, N., Tramier, M., Coppey-Moisan, M., Time-domain fluorescence lifetime imaging microscopy: a quantitative method to follow transient protein-protein interactions in living cells. Cold Spring Harb. Protoc. 2015 (2015), 508–521.
29. Pasterkamp, R.J., Getting neural circuits into shape with semaphorins. Nat. Rev. Neurosci. 13 (2012), 605–618.
30. Reeves, P.J., Callewaert, N., Contreras, R., Khorana, H.G., Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. USA 99 (2002), 13419–13424.
31. Schuck, P., Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78 (2000), 1606–1619.
32. Siebold, C., Jones, E.Y., Structural insights into semaphorins and their receptors. Semin. Cell Dev. Biol. 24 (2013), 139–145.
33. Sun, L.O., Jiang, Z., Rivlin-Etzion, M., Hand, R., Brady, C.M., Matsuoka, R.L., Yau, K.-W., Feller, M.B., Kolodkin, A.L., On and off retinal circuit assembly by divergent molecular mechanisms. Science, 342, 2013 1241974–1241974.
34. Suto, F., Murakami, Y., Nakamura, F., Goshima, Y., Fujisawa, H., Identification and characterization of a novel mouse plexin, plexin-A4. Mech. Dev. 120 (2003), 385–396.
35. Suto, F., Tsuboi, M., Kamiya, H., Mizuno, H., Kiyama, Y., Komai, S., Shimizu, M., Sanbo, M., Yagi, T., Hiromi, Y., et al. Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 53 (2007), 535–547.
36. Takahashi, T., Strittmatter, S.M., Plexina1 autoinhibition by the plexin sema domain. Neuron 29 (2001), 429–439.
37. Tang, G., Peng, L., Baldwin, P.R., Mann, D.S., Jiang, W., Rees, I., Ludtke, S.J., EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157 (2007), 38–46.
38. Van Battum, E.Y., Gunput, R.-A.F., Lemstra, S., Groen, E.J.N., Yu, K.L., Adolfs, Y., Zhou, Y., Hoogenraad, C.C., Yoshida, Y., Schachner, M., et al. The intracellular redox protein MICAL-1 regulates the development of hippocampal mossy fibre connections. Nat. Commun., 5, 2014, 4317.
39. van Erp, S., van den Heuvel, D.M.A., Fujita, Y., Robinson, R.A., Hellemons, A.J.C.G.M., Adolfs, Y., Van Battum, E.Y., Blokhuis, A.M., Kuijpers, M., Demmers, J.A.A., et al. Lrig2 Negatively Regulates Ectodomain Shedding of Axon Guidance Receptors by ADAM Proteases. Dev. Cell 35 (2015), 537–552.
40. Van Heel, M., Keegstra, W., IMAGIC: A fast, flexible and friendly image analysis software system. Ultramicroscopy 7 (1981), 113–129.
41. Wang, Y., He, H., Srivastava, N., Vikarunnessa, S., Chen, Y.B., Jiang, J., Cowan, C.W., Zhang, X., Plexins are GTPase-activating proteins for Rap and are activated by induced dimerization. Sci. Signal., 5, 2012 ra6–ra6.
42. Wang, Y., Pascoe, H.G., Brautigam, C.A., He, H., Zhang, X., Structural basis for activation and non-canonical catalysis of the Rap GTPase activating protein domain of plexin. eLife, 2, 2013 e01279–e01279.
43. Wu, Y., Vendome, J., Shapiro, L., Ben-Shaul, A., Honig, B., Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 475 (2011), 510–513.
44. Yamada, H., Padilla-Parra, S., Park, S.-J., Itoh, T., Chaineau, M., Monaldi, I., Cremona, O., Benfenati, F., De Camilli, P., Coppey-Moisan, M., et al. Dynamic interaction of amphiphysin with N-WASP regulates actin assembly. J. Biol. Chem. 284 (2009), 34244–34256.
45. Yogev, S., Shen, K., Cellular and molecular mechanisms of synaptic specificity. Annu. Rev. Cell Dev. Biol. 30 (2014), 417–437.
46. Zhao, Y., Ren, J., Padilla-Parra, S., Fry, E.E., Stuart, D.I., Lysosome sorting of β-glucocerebrosidase by LIMP-2 is targeted by the mannose 6-phosphate receptor. Nat. Commun., 5, 2014, 4321.