A molecular code for endosomal recycling of phosphorylated cargos by the SNX27-retromer complex

Nature Structural and Molecular Biology

Volumn 23, Issue 10, 2016, Pages 921-932

  Clairfeuille, Thomas ^a,d   Mas, Caroline ^a,e   Chan, Audrey S M ^b   Yang, Zhe ^a   Tello Lafoz, Maria ^c   Chandra, Mintu ^a   Widagdo, Jocelyn ^a   Kerr, Markus C ^a   Paul, Blessy ^a   Mérida, Isabel ^c   Teasdale, Rohan D ^a   Pavlos, Nathan J ^b   Anggono, Victor ^a   Collins, Brett M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d GENENTECH INC   (United States)

^e Integrated Structural Biology Grenoble   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SORTING NEXIN; SORTING NEXIN 27; UNCLASSIFIED DRUG; GLUTAMATE RECEPTOR; PROTEIN BINDING; SNX27 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CELL FUNCTION; CELL RECYCLING; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENDOSOME; HUMAN; HUMAN CELL; METABOLITE; MOLECULAR INTERACTION; NERVE CELL PLASTICITY; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; CHEMISTRY; HEK293 CELL LINE; METABOLISM; MOLECULAR DOCKING; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ENDOSOMES; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PDZ DOMAINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN TRANSPORT; RECEPTORS, GLUTAMATE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SORTING NEXINS;

EID: 84990214542     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3290     Document Type: Article

References (68)

1. Kennedy, M.B. Signal-processing machines at the postsynaptic density. Science 290, 750-754 (2000).
2. Zhang, M., Wang, W. Organization of signaling complexes by PDZ-domain scaffold proteins. Acc. Chem. Res. 36, 530-538 (2003).
3. Kim, E., Sheng, M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781 (2004).
4. Hung, A.Y., Sheng, M. PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277, 5699-5702 (2002).
5. Stiffler, M.A. et al. PDZ domain binding selectivity is optimized across the mouse proteome. Science 317, 364-369 (2007).
6. Hall, R.A. et al. The ?2-adrenergic receptor interacts with the Na+/H+-exchanger regulatory factor to control Na+/H+ exchange. Nature 392, 626-630 (1998).
7. Ye, F., Zhang, M. Structures and target recognition modes of PDZ domains: recurring themes and emerging pictures. Biochem. J. 455, 1-14 (2013).
8. Gallon, M. et al. A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc. Natl. Acad. Sci. USA 111, E3604-E3613 (2014).
9. 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).
10. Lauffer, B.E. et al. SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J. Cell Biol. 190, 565-574 (2010).
11. 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).
12. Choy, R.W. et al. Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82, 55-62 (2014).
13. Chan, A.S. et al. Sorting nexin 27 couples PTHR trafficking to retromer for signal regulation in osteoblasts during bone growth. Mol. Biol. Cell 27, 1367-1382 (2016).
14. Balana, B. et al. Mechanism underlying selective regulation of G protein-gated inwardly rectifying potassium channels by the psychostimulant-sensitive sorting nexin 27. Proc. Natl. Acad. Sci. USA 108, 5831-5836 (2011).
15. Lunn, M.L. et al. A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat. Neurosci. 10, 1249-1259 (2007).
16. Hussain, N.K., Diering, G.H., Sole, J., Anggono, V., Huganir, R.L. Sorting Nexin 27 regulates basal and activity-dependent trafficking of AMPARs. Proc. Natl. Acad. Sci. USA 111, 11840-11845 (2014).
17. Loo, L.S., Tang, N., Al-Haddawi, M., Dawe, G.S., Hong, W. A role for sorting nexin 27 in AMPA receptor trafficking. Nat. Commun. 5, 3176 (2014).
18. Wang, X. et al. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down's syndrome. Nat. Med. 19, 473-480 (2013).
19. Joubert, L. et al. New sorting nexin (SNX27) and NHERF specifically interact with the 5-HT4a receptor splice variant: roles in receptor targeting. J. Cell Sci. 117, 5367-5379 (2004).
20. Lee, S., Chang, J., Blackstone, C. FAM21 directs SNX27-retromer cargoes to the plasma membrane by preventing transport to the Golgi apparatus. Nat. Commun. 7, 10939 (2016).
21. Muhammad, A. et al. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and A? accumulation. Proc. Natl. Acad. Sci. USA 105, 7327-7332 (2008).
22. Vilarinõ-Guëll, C. et al. VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 89, 162-167 (2011).
23. Wen, L. et al. VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J. Cell Biol. 195, 765-779 (2011).
24. Zimprich, A. et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am. J. Hum. Genet. 89, 168-175 (2011).
25. Wang, X. et al. Sorting nexin 27 regulates A? production through modulating ?-secretase activity. Cell Rep. 9, 1023-1033 (2014).
26. Damseh, N. et al. A defect in the retromer accessory protein, SNX27, manifests by infantile myoclonic epilepsy and neurodegeneration. Neurogenetics 16, 215-221 (2015).
27. Tsika, E. et al. Parkinson's disease-linked mutations in VPS35 induce dopaminergic neurodegeneration. Hum. Mol. Genet. 23, 4621-4638 (2014).
28. Vardarajan, B.N. et al. Identification of Alzheimer disease-associated variants in genes that regulate retromer function. Neurobiol. Aging 33, 2231.e15-2231.e30 (2012).
29. Rincón, E. et al. Translocation dynamics of sorting nexin 27 in activated T cells. J. Cell Sci. 124, 776-788 (2011).
30. Rincón, E. et al. Proteomics identification of sorting nexin 27 as a diacylglycerol kinase zeta-associated protein: new diacylglycerol kinase roles in endocytic recycling. Mol. Cell. Proteomics 6, 1073-1087 (2007).
31. Sowa, M.E., Bennett, E.J., Gygi, S.P., Harper, J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403 (2009).
32. Okabe, S. Molecular anatomy of the postsynaptic density. Mol. Cell. Neurosci. 34, 503-518 (2007).
33. Wang, J.Q. et al. Roles of subunit phosphorylation in regulating glutamate receptor function. Eur. J. Pharmacol. 728, 183-187 (2014).
34. Lussier, M.P., Sanz-Clemente, A., Roche, K.W. Dynamic regulation of N-methyl-d-aspartate (nmda) and ?-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by posttranslational modifications. J. Biol. Chem. 290, 28596-28603 (2015).
35. Ryan, T.J., Emes, R.D., Grant, S.G., Komiyama, N.H. Evolution of NMDA receptor cytoplasmic interaction domains: implications for organisation of synaptic signalling complexes. BMC Neurosci. 9, 6 (2008).
36. Sakarya, O. et al. Evolutionary expansion and specialization of the PDZ domains. Mol. Biol. Evol. 27, 1058-1069 (2010).
37. Cushing, P.R., Fellows, A., Villone, D., Boisguérin, P., Madden, D.R. The relative binding affinities of PDZ partners for CFTR: a biochemical basis for efficient endocytic recycling. Biochemistry 47, 10084-10098 (2008).
38. Pankow, S. et al. ?F508 CFTR interactome remodelling promotes rescue of cystic fibrosis. Nature 528, 510-516 (2015).
39. Akizu, N. et al. Biallelic mutations in SNX14 cause a syndromic form of cerebellar atrophy and lysosome-autophagosome dysfunction. Nat. Genet. 47, 528-534 (2015).
40. Mas, C. et al. Structural basis for different phosphoinositide specificities of the PX domains of sorting nexins regulating G-protein signaling. J. Biol. Chem. 289, 28554-28568 (2014).
41. Ghai, R. et al. Phox homology band 4.1/ezrin/radixin/moesin-like proteins function as molecular scaffolds that interact with cargo receptors and Ras GTPases. Proc. Natl. Acad. Sci. USA 108, 7763-7768 (2011).
42. Ghai, R. et al. Phosphoinositide binding by the SNX27 FERM domain regulates its localization at the immune synapse of activated T-cells. J. Cell Sci. 128, 553-565 (2015).
43. Ghai, R. et al. Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. Proc. Natl. Acad. Sci. USA 110, E643-E652 (2013).
44. Cao, T.T., Deacon, H.W., Reczek, D., Bretscher, A., von Zastrow, M. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the ?2-adrenergic receptor. Nature 401, 286-290 (1999).
45. Choi, J. et al. Phosphorylation of stargazin by protein kinase A regulates its interaction with PSD-95. J. Biol. Chem. 277, 12359-12363 (2002).
46. Chung, H.J., Huang, Y.H., Lau, L.F., Huganir, R.L. Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. J. Neurosci. 24, 10248-10259 (2004).
47. Chung, H.J., Xia, J., Scannevin, R.H., Zhang, X., Huganir, R.L. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20, 7258-7267 (2000).
48. Cohen, N.A., Brenman, J.E., Snyder, S.H., Bredt, D.S. Binding of the inward rectifier K+ channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17, 759-767 (1996).
49. Sanz-Clemente, A., Matta, J.A., Isaac, J.T., Roche, K.W. Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron 67, 984-996 (2010).
50. Tanemoto, M., Fujita, A., Higashi, K., Kurachi, Y. PSD-95 mediates formation of a functional homomeric Kir5.1 channel in the brain. Neuron 34, 387-397 (2002).
51. Tian, Q.B. et al. Interaction of LDL receptor-related protein 4 (LRP4) with postsynaptic scaffold proteins via its C-terminal PDZ domain-binding motif, and its regulation by Ca/calmodulin-dependent protein kinase II. Eur. J. Neurosci. 23, 2864-2876 (2006).
52. Lee, H.J., Zheng, J.J. PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun. Signal. 8, 8 (2010).
53. Liu, X., Shepherd, T.R., Murray, A.M., Xu, Z., Fuentes, E.J. The structure of the Tiam1 PDZ domain/phospho-syndecan1 complex reveals a ligand conformation that modulates protein dynamics. Structure 21, 342-354 (2013).
54. Nomme, J. et al. Structural basis of a key factor regulating the affinity between the zonula occludens first PDZ domain and claudins. J. Biol. Chem. 290, 16595-16606 (2015).
55. Zhang, N. et al. Phosphorylation of synaptic vesicle protein 2A at Thr84 by casein kinase 1 family kinases controls the specific retrieval of synaptotagmin-1. J. Neurosci. 35, 2492-2507 (2015).
56. Nobles, K.N. et al. Distinct phosphorylation sites on the ?2-adrenergic receptor establish a barcode that encodes differential functions of ?-arrestin. Sci. Signal. 4, ra51 (2011).
57. César-Razquin, A. et al. A call for systematic research on solute carriers. Cell 162, 478-487 (2015).
58. Belotti, E. et al. The human PDZome: a gateway to PSD95-Disc large-zonula occludens (PDZ)-mediated functions. Mol. Cell. Proteomics 12, 2587-2603 (2013).
59. Pim, D., Broniarczyk, J., Bergant, M., Playford, M.P., Banks, L. A novel PDZ domain interaction mediates the binding between human papillomavirus 16 L2 and sorting nexin 27 and modulates virion trafficking. J. Virol. 89, 10145-10155 (2015).
60. Winn, M.D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
61. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
62. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
63. Murshudov, G.N., Vagin, A.A., Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
64. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
65. de Castro, E. et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362-W365 (2006).
66. Santos, T., Carrasco, S., Jones, D.R., Mérida, I., Eguinoa, A. Dynamics of diacylglycerol kinase zeta translocation in living T-cells: study of the structural domain requirements for translocation and activity. J. Biol. Chem. 277, 30300-30309 (2002).
67. Anggono, V. et al. PICK1 interacts with PACSIN to regulate AMPA receptor internalization and cerebellar long-term depression. Proc. Natl. Acad. Sci. USA 110, 13976-13981 (2013).
68. Aubrey, B.J. et al. An inducible lentiviral guide RNA platform enables the identification of tumor-ess ential genes and tumor-promoting mutations in vivo. Cell Rep. 10, 1422-1432 (2015).