5emb › Citations

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

Clairfeuille T, Mas C, Chan AS, Yang Z, Tello-Lafoz M, Chandra M, Widagdo J, Kerr MC, Paul B, Mérida I, Teasdale RD, Pavlos NJ, Anggono V, Collins BM
Nat Struct Mol Biol 23 921-932 (2016)
Related entries: 5elq, 5em9, 5ema

Cited: 84 times
EuropePMC logo PMID: 27595347

Abstract

Recycling of internalized receptors from endosomal compartments is essential for the receptors' cell-surface homeostasis. Sorting nexin 27 (SNX27) cooperates with the retromer complex in the recycling of proteins containing type I PSD95-Dlg-ZO1 (PDZ)-binding motifs. Here we define specific acidic amino acid sequences upstream of the PDZ-binding motif required for high-affinity engagement of the human SNX27 PDZ domain. However, a subset of SNX27 ligands, such as the β2 adrenergic receptor and N-methyl-D-aspartate (NMDA) receptor, lack these sequence determinants. Instead, we identified conserved sites of phosphorylation that substitute for acidic residues and dramatically enhance SNX27 interactions. This newly identified mechanism suggests a likely regulatory switch for PDZ interaction and protein transport by the SNX27-retromer complex. Defining this SNX27 binding code allowed us to classify more than 400 potential SNX27 ligands with broad functional implications in signal transduction, neuronal plasticity and metabolite transport.

Reviews - 5emb mentioned but not cited (1)

  1. Toward Understanding the Molecular Role of SNX27/Retromer in Human Health and Disease. Chandra M, Kendall AK, Jackson LP. Front Cell Dev Biol 9 642378 (2021)

Articles - 5emb mentioned but not cited (1)

  1. The oxygen-oxygen distance of water in crystallographic data sets. Palese LL. Data Brief 28 105076 (2020)


Reviews citing this publication (30)

  1. To degrade or not to degrade: mechanisms and significance of endocytic recycling. Cullen PJ, Steinberg F. Nat Rev Mol Cell Biol 19 679-696 (2018)
  2. The enigmatic endosome - sorting the ins and outs of endocytic trafficking. Naslavsky N, Caplan S. J Cell Sci 131 jcs216499 (2018)
  3. GPCR Signaling and Trafficking: The Long and Short of It. Pavlos NJ, Friedman PA. Trends Endocrinol Metab 28 213-226 (2017)
  4. Endosomal receptor trafficking: Retromer and beyond. Wang J, Fedoseienko A, Chen B, Burstein E, Jia D, Billadeau DD. Traffic 19 578-590 (2018)
  5. Regulation of NMDA glutamate receptor functions by the GluN2 subunits. Vieira M, Yong XLH, Roche KW, Anggono V. J Neurochem 154 121-143 (2020)
  6. The emerging role of retromer in neuroprotection. McMillan KJ, Korswagen HC, Cullen PJ. Curr Opin Cell Biol 47 72-82 (2017)
  7. Trafficking in Alzheimer's Disease: Modulation of APP Transport and Processing by the Transmembrane Proteins LRP1, SorLA, SorCS1c, Sortilin, and Calsyntenin. Eggert S, Thomas C, Kins S, Hermey G. Mol Neurobiol 55 5809-5829 (2018)
  8. Barcoding of GPCR trafficking and signaling through the various trafficking roadmaps by compartmentalized signaling networks. Bahouth SW, Nooh MM. Cell Signal 36 42-55 (2017)
  9. Dynamic control of the dopamine transporter in neurotransmission and homeostasis. Bu M, Farrer MJ, Khoshbouei H. NPJ Parkinsons Dis 7 22 (2021)
  10. Mechanisms for Regulating and Organizing Receptor Signaling by Endocytosis. von Zastrow M, Sorkin A. Annu Rev Biochem 90 709-737 (2021)
  11. Emerging Role of Retromer in Modulating Pathogen Growth. Elwell C, Engel J. Trends Microbiol 26 769-780 (2018)
  12. Spatial control of membrane traffic in neuronal dendrites. Radler MR, Suber A, Spiliotis ET. Mol Cell Neurosci 105 103492 (2020)
  13. Endosomal Recycling Defects and Neurodevelopmental Disorders. Saitoh S. Cells 11 148 (2022)
  14. An evolving understanding of sorting signals for endosomal retrieval. Yong X, Mao L, Seaman MNJ, Jia D. iScience 25 104254 (2022)
  15. Interplay Between SNX27 and DAG Metabolism in the Control of Trafficking and Signaling at the IS. González-Mancha N, Mérida I. Int J Mol Sci 21 E4254 (2020)
  16. Noncanonical Sequences Involving NHERF1 Interaction with NPT2A Govern Hormone-Regulated Phosphate Transport: Binding Outside the Box. Mamonova T, Friedman PA. Int J Mol Sci 22 1087 (2021)
  17. Sorting Nexin 27 as a potential target in G protein‑coupled receptor recycling for cancer therapy (Review). Bao Z, Zhou S, Zhou H. Oncol Rep 44 1779-1786 (2020)
  18. The Yin and Yang of GABAergic and Glutamatergic Synaptic Plasticity: Opposites in Balance by Crosstalking Mechanisms. Chapman CA, Nuwer JL, Jacob TC. Front Synaptic Neurosci 14 911020 (2022)
  19. The needs of a synapse-How local organelles serve synaptic proteostasis. Grochowska KM, Andres-Alonso M, Karpova A, Kreutz MR. EMBO J 41 e110057 (2022)
  20. Unveiling the cryo-EM structure of retromer. Chandra M, Kendall AK, Jackson LP. Biochem Soc Trans 48 2261-2272 (2020)
  21. Orchestrating serine/threonine phosphorylation and elucidating downstream effects by short linear motifs. Kliche J, Ivarsson Y. Biochem J 479 1-22 (2022)
  22. SNX-PXA-RGS-PXC Subfamily of SNXs in the Regulation of Receptor-Mediated Signaling and Membrane Trafficking. Amatya B, Lee H, Asico LD, Konkalmatt P, Armando I, Felder RA, Jose PA. Int J Mol Sci 22 2319 (2021)
  23. F-Actin Dynamics in the Regulation of Endosomal Recycling and Immune Synapse Assembly. Capitani N, Baldari CT. Front Cell Dev Biol 9 670882 (2021)
  24. Out of the ESCPE room: Emerging roles of endosomal SNX-BARs in receptor transport and host-pathogen interaction. Simonetti B, Daly JL, Cullen PJ. Traffic 24 234-250 (2023)
  25. In the fast lane: Receptor trafficking during status epilepticus. Naylor DE. Epilepsia Open 8 Suppl 1 S35-S65 (2023)
  26. Retromer dependent changes in cellular homeostasis and Parkinson's disease. Yang Z, Li Z, Teasdale RD. Essays Biochem 65 987-998 (2021)
  27. Cell-specific secretory granule sorting mechanisms: the role of MAGEL2 and retromer in hypothalamic regulated secretion. Štepihar D, Florke Gee RR, Hoyos Sanchez MC, Fon Tacer K. Front Cell Dev Biol 11 1243038 (2023)
  28. Endosomal Sorting Protein SNX27 and Its Emerging Roles in Human Cancers. Deb S, Sun J. Cancers (Basel) 15 70 (2022)
  29. Receptor Recycling by Retromer. Carosi JM, Denton D, Kumar S, Sargeant TJ. Mol Cell Biol 43 317-334 (2023)
  30. The Role of Reversible Phosphorylation of Drosophila Rhodopsin. Smylla TK, Wagner K, Huber A. Int J Mol Sci 23 14674 (2022)

Articles citing this publication (52)

  1. Retriever is a multiprotein complex for retromer-independent endosomal cargo recycling. McNally KE, Faulkner R, Steinberg F, Gallon M, Ghai R, Pim D, Langton P, Pearson N, Danson CM, Nägele H, Morris LL, Singla A, Overlee BL, Heesom KJ, Sessions R, Banks L, Collins BM, Berger I, Billadeau DD, Burstein E, Cullen PJ. Nat Cell Biol 19 1214-1225 (2017)
  2. Structural Mechanism for Cargo Recognition by the Retromer Complex. Lucas M, Gershlick DC, Vidaurrazaga A, Rojas AL, Bonifacino JS, Hierro A. Cell 167 1623-1635.e14 (2016)
  3. Retromer has a selective function in cargo sorting via endosome transport carriers. Cui Y, Carosi JM, Yang Z, Ariotti N, Kerr MC, Parton RG, Sargeant TJ, Teasdale RD. J Cell Biol 218 615-631 (2019)
  4. Mechanism of cargo recognition by retromer-linked SNX-BAR proteins. Yong X, Zhao L, Deng W, Sun H, Zhou X, Mao L, Hu W, Shen X, Sun Q, Billadeau DD, Xue Y, Jia D. PLoS Biol 18 e3000631 (2020)
  5. PTEN Regulates Glucose Transporter Recycling by Impairing SNX27 Retromer Assembly. Shinde SR, Maddika S. Cell Rep 21 1655-1666 (2017)
  6. Architecture and mechanism of metazoan retromer:SNX3 tubular coat assembly. Leneva N, Kovtun O, Morado DR, Briggs JAG, Owen DJ. Sci Adv 7 eabf8598 (2021)
  7. Molecular mechanism for the subversion of the retromer coat by the Legionella effector RidL. Romano-Moreno M, Rojas AL, Williamson CD, Gershlick DC, Lucas M, Isupov MN, Bonifacino JS, Machner MP, Hierro A. Proc Natl Acad Sci U S A 114 E11151-E11160 (2017)
  8. The Dopamine Transporter Recycles via a Retromer-Dependent Postendocytic Mechanism: Tracking Studies Using a Novel Fluorophore-Coupling Approach. Wu S, Fagan RR, Uttamapinant C, Lifshitz LM, Fogarty KE, Ting AY, Melikian HE. J Neurosci 37 9438-9452 (2017)
  9. GGA1 regulates signal-dependent sorting of BACE1 to recycling endosomes, which moderates Aβ production. Toh WH, Chia PZC, Hossain MI, Gleeson PA. Mol Biol Cell 29 191-208 (2018)
  10. Proteome-wide analysis of phospho-regulated PDZ domain interactions. Sundell GN, Arnold R, Ali M, Naksukpaiboon P, Orts J, Güntert P, Chi CN, Ivarsson Y. Mol Syst Biol 14 e8129 (2018)
  11. Mammalian Retromer Is an Adaptable Scaffold for Cargo Sorting from Endosomes. Kendall AK, Xie B, Xu P, Wang J, Burcham R, Frazier MN, Binshtein E, Wei H, Graham TR, Nakagawa T, Jackson LP. Structure 28 393-405.e4 (2020)
  12. Regulation of the endosomal SNX27-retromer by OTULIN. Stangl A, Elliott PR, Pinto-Fernandez A, Bonham S, Harrison L, Schaub A, Kutzner K, Keusekotten K, Pfluger PT, El Oualid F, Kessler BM, Komander D, Krappmann D. Nat Commun 10 4320 (2019)
  13. A Targeted RNAi Screen Identifies Endocytic Trafficking Factors That Control GLP-1 Receptor Signaling in Pancreatic β-Cells. Buenaventura T, Kanda N, Douzenis PC, Jones B, Bloom SR, Chabosseau P, Corrêa IR, Bosco D, Piemonti L, Marchetti P, Johnson PR, Shapiro AMJ, Rutter GA, Tomas A. Diabetes 67 385-399 (2018)
  14. Sorting nexin 27 (SNX27) regulates the trafficking and activity of the glutamine transporter ASCT2. Yang Z, Follett J, Kerr MC, Clairfeuille T, Chandra M, Collins BM, Teasdale RD. J Biol Chem 293 6802-6811 (2018)
  15. Phosphorylation of SNX27 by MAPK11/14 links cellular stress-signaling pathways with endocytic recycling. Mao L, Liao C, Qin J, Gong Y, Zhou Y, Li S, Liu Z, Deng H, Deng W, Sun Q, Mo X, Xue Y, Billadeau DD, Dai L, Li G, Jia D. J Cell Biol 220 e202010048 (2021)
  16. SNX27 suppresses SARS-CoV-2 infection by inhibiting viral lysosome/late endosome entry. Yang B, Jia Y, Meng Y, Xue Y, Liu K, Li Y, Liu S, Li X, Cui K, Shang L, Cheng T, Zhang Z, Hou Y, Yang X, Yan H, Duan L, Tong Z, Wu C, Liu Z, Gao S, Zhuo S, Huang W, Gao GF, Qi J, Shang G. Proc Natl Acad Sci U S A 119 e2117576119 (2022)
  17. SNX27-FERM-SNX1 complex structure rationalizes divergent trafficking pathways by SNX17 and SNX27. Yong X, Zhao L, Hu W, Sun Q, Ham H, Liu Z, Ren J, Zhang Z, Zhou Y, Yang Q, Mo X, Hu J, Billadeau DD, Jia D. Proc Natl Acad Sci U S A 118 e2105510118 (2021)
  18. Mammalian copper homeostasis requires retromer-dependent recycling of the high-affinity copper transporter 1. Curnock R, Cullen PJ. J Cell Sci 133 jcs249201 (2020)
  19. Sorting nexin 27 interactome in T-lymphocytes identifies zona occludens-2 dynamic redistribution at the immune synapse. Tello-Lafoz M, Martínez-Martínez G, Rodríguez-Rodríguez C, Albar JP, Huse M, Gharbi S, Merida I. Traffic 18 491-504 (2017)
  20. Dynamic control of RSK complexes by phosphoswitch-based regulation. Gógl G, Biri-Kovács B, Póti ÁL, Vadászi H, Szeder B, Bodor A, Schlosser G, Ács A, Turiák L, Buday L, Alexa A, Nyitray L, Reményi A. FEBS J 285 46-71 (2018)
  21. Sorting nexin 17 (SNX17) links endosomal sorting to Eps15 homology domain protein 1 (EHD1)-mediated fission machinery. Dhawan K, Naslavsky N, Caplan S. J Biol Chem 295 3837-3850 (2020)
  22. Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting. Evans AJ, Daly JL, Anuar ANK, Simonetti B, Cullen PJ. J Cell Sci 133 jcs246033 (2020)
  23. Cholera toxin inhibits SNX27-retromer-mediated delivery of cargo proteins to the plasma membrane. Singh V, Yang J, Yin J, Cole R, Tse M, Berman DE, Small SA, Petsko G, Donowitz M. J Cell Sci 131 jcs218610 (2018)
  24. Defining the protein and lipid constituents of tubular recycling endosomes. Farmer T, Xie S, Naslavsky N, Stöckli J, James DE, Caplan S. J Biol Chem 296 100190 (2021)
  25. Rewiring of RSK-PDZ Interactome by Linear Motif Phosphorylation. Gógl G, Biri-Kovács B, Durbesson F, Jane P, Nomine Y, Kostmann C, Bilics V, Simon M, Reményi A, Vincentelli R, Trave G, Nyitray L. J Mol Biol 431 1234-1249 (2019)
  26. The human box C/D snoRNA U3 is a miRNA source and miR-U3 regulates expression of sortin nexin 27. Lemus-Diaz N, Ferreira RR, Bohnsack KE, Gruber J, Bohnsack MT. Nucleic Acids Res 48 8074-8089 (2020)
  27. HTLV-1 Tax-1 interacts with SNX27 to regulate cellular localization of the HTLV-1 receptor molecule, GLUT1. Al-Saleem J, Dirksen WP, Martinez MP, Shkriabai N, Kvaratskhelia M, Ratner L, Green PL. PLoS One 14 e0214059 (2019)
  28. Regulation of NMDA receptor trafficking and gating by activity-dependent CaMKIIα phosphorylation of the GluN2A subunit. Yong XLH, Zhang L, Yang L, Chen X, Tan JZA, Yu X, Chandra M, Livingstone E, Widagdo J, Vieira MM, Roche KW, Lynch JW, Keramidas A, Collins BM, Anggono V. Cell Rep 36 109338 (2021)
  29. Retromer Controls Planar Polarity Protein Levels and Asymmetric Localization at Intercellular Junctions. Strutt H, Langton PF, Pearson N, McMillan KJ, Strutt D, Cullen PJ. Curr Biol 29 484-491.e6 (2019)
  30. SARS-CoV-2 spike protein harnesses SNX27-mediated endocytic recycling pathway. Zhao L, Zhong K, Zhao J, Yong X, Tong A, Jia D. MedComm (2020) 2 798-809 (2021)
  31. SNX27-Retromer directly binds ESCPE-1 to transfer cargo proteins during endosomal recycling. Simonetti B, Guo Q, Giménez-Andrés M, Chen KE, Moody ERR, Evans AJ, Chandra M, Danson CM, Williams TA, Collins BM, Cullen PJ. PLoS Biol 20 e3001601 (2022)
  32. SNX27-Mediated Recycling of Neuroligin-2 Regulates Inhibitory Signaling. Halff EF, Szulc BR, Lesept F, Kittler JT. Cell Rep 29 2599-2607.e6 (2019)
  33. SNX27 links DGKζ to the control of transcriptional and metabolic programs in T lymphocytes. Tello-Lafoz M, Rodríguez-Rodríguez C, Kinna G, Loo LS, Hong W, Collins BM, Teasdale RD, Mérida I. Sci Rep 7 16361 (2017)
  34. Kidins220 deficiency causes ventriculomegaly via SNX27-retromer-dependent AQP4 degradation. Del Puerto A, Pose-Utrilla J, Simón-García A, López-Menéndez C, Jiménez AJ, Porlan E, Pajuelo LSM, Cano-García G, Martí-Prado B, Sebastián-Serrano Á, Sánchez-Carralero MP, Cesca F, Schiavo G, Ferrer I, Fariñas I, Campanero MR, Iglesias T. Mol Psychiatry 26 6411-6426 (2021)
  35. Origins of PDZ Binding Specificity. A Computational and Experimental Study Using NHERF1 and the Parathyroid Hormone Receptor. Mamonova T, Zhang Q, Chandra M, Collins BM, Sarfo E, Bu Z, Xiao K, Bisello A, Friedman PA. Biochemistry 56 2584-2593 (2017)
  36. Sorting nexin-27 regulates AMPA receptor trafficking through the synaptic adhesion protein LRFN2. McMillan KJ, Banks PJ, Hellel FL, Carmichael RE, Clairfeuille T, Evans AJ, Heesom KJ, Lewis P, Collins BM, Bashir ZI, Henley JM, Wilkinson KA, Cullen PJ. Elife 10 e59432 (2021)
  37. Eps15 Homology Domain Protein 4 (EHD4) is required for Eps15 Homology Domain Protein 1 (EHD1)-mediated endosomal recruitment and fission. Jones T, Naslavsky N, Caplan S. PLoS One 15 e0239657 (2020)
  38. Sorting Nexin 27 Regulates the Lysosomal Degradation of Aquaporin-2 Protein in the Kidney Collecting Duct. Choi HJ, Jang HJ, Park E, Tingskov SJ, Nørregaard R, Jung HJ, Kwon TH. Cells 9 E1208 (2020)
  39. Biochemical basis for an interaction between SNX27 and the flexible SNX1 N-terminus. Chandra M, Collins BM, Jackson LP. Adv Biol Regul 83 100842 (2022)
  40. De novo macrocyclic peptides for inhibiting, stabilizing, and probing the function of the retromer endosomal trafficking complex. Chen KE, Guo Q, Hill TA, Cui Y, Kendall AK, Yang Z, Hall RJ, Healy MD, Sacharz J, Norwood SJ, Fonseka S, Xie B, Reid RC, Leneva N, Parton RG, Ghai R, Stroud DA, Fairlie DP, Suga H, Jackson LP, Teasdale RD, Passioura T, Collins BM. Sci Adv 7 eabg4007 (2021)
  41. Multisite NHERF1 phosphorylation controls GRK6A regulation of hormone-sensitive phosphate transport. Vistrup-Parry M, Sneddon WB, Bach S, Strømgaard K, Friedman PA, Mamonova T. J Biol Chem 296 100473 (2021)
  42. Interactomic affinity profiling by holdup assay: Acetylation and distal residues impact the PDZome-binding specificity of PTEN phosphatase. Jané P, Gógl G, Kostmann C, Bich G, Girault V, Caillet-Saguy C, Eberling P, Vincentelli R, Wolff N, Travé G, Nominé Y. PLoS One 15 e0244613 (2020)
  43. Structural insights into membrane remodeling by SNX1. Zhang Y, Pang X, Li J, Xu J, Hsu VW, Sun F. Proc Natl Acad Sci U S A 118 e2022614118 (2021)
  44. Phosphorylation-induced changes in the PDZ domain of Dishevelled 3. Jurásek M, Kumar J, Paclíková P, Kumari A, Tripsianes K, Bryja V, Vácha R. Sci Rep 11 1484 (2021)
  45. Sorting Nexin 27 Enables MTOC and Secretory Machinery Translocation to the Immune Synapse. González-Mancha N, Rodríguez-Rodríguez C, Alcover A, Merida I. Front Immunol 12 814570 (2021)
  46. The retromer complex regulates C. elegans development and mammalian ciliogenesis. Xie S, Dierlam C, Smith E, Duran R, Williams A, Davis A, Mathew D, Naslavsky N, Iyer J, Caplan S. J Cell Sci 135 jcs259396 (2022)
  47. Advances and challenges in understanding endosomal sorting and fission. Naslavsky N, Caplan S. FEBS J 290 4187-4195 (2023)
  48. Analysis of the SNARE Stx8 recycling reveals that the retromer-sorting motif has undergone evolutionary divergence. Yanguas F, Valdivieso MH. PLoS Genet 17 e1009463 (2021)
  49. HPV-18E6 Inhibits Interactions between TANC2 and SNX27 in a PBM-Dependent Manner and Promotes Increased Cell Proliferation. Broniarczyk JK, Massimi P, Trejo-Cerro O, Myers MP, Banks L. J Virol 96 e0136522 (2022)
  50. Multifaceted Roles of Retromer in EGFR Trafficking and Signaling Activation. Yang Z, Feng Z, Li Z, Teasdale RD. Cells 11 3358 (2022)
  51. Native holdup (nHU) to measure binding affinities from cell extracts. Zambo B, Morlet B, Negroni L, Trave G, Gogl G. Sci Adv 8 eade3828 (2022)
  52. RNA binding motif protein 45-mediated phosphorylation enhances protein stability of ASCT2 to promote hepatocellular carcinoma progression. Du D, Qin M, Shi L, Liu C, Jiang J, Liao Z, Wang H, Zhang Z, Sun L, Fan H, Liu Z, Yu H, Li H, Peng J, Yuan S, Yang M, Xiong J. Oncogene 42 3127-3141 (2023)


Quick links