VPS26 Moonlights as a β-Arrestin-like Adapter for a 7-Transmembrane RGS Protein in Arabidopsis thaliana

Lou, Fei; Zhou, Wenbin; Tunc-Ozdemir, Meral; Yang, Jing; Velazhahan, Vaithish; Tate, Christopher G.; Jones, Alan M.

doi:10.1021/acs.biochem.4c00361

VPS26 Moonlights as a β-Arrestin-like Adapter for a 7-Transmembrane RGS Protein in Arabidopsis thaliana

Journal Article · Mon Oct 28 00:00:00 EDT 2024 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.4c00361· OSTI ID:2475196

Lou, Fei ^[1]; Zhou, Wenbin ^[1]; Tunc-Ozdemir, Meral ^[1]; Yang, Jing ^[1]; Velazhahan, Vaithish ^[2]; ^[3]; ^[1]

University of North Carolina at Chapel Hill, NC (United States)
MRC Laboratory of Molecular Biology, Cambridge (United Kingdom); University of Cambridge (United Kingdom)
MRC Laboratory of Molecular Biology, Cambridge (United Kingdom)

Extracellular signals perceived by 7-transmembrane (7TM)-spanning receptors initiate desensitization that involves the removal of these receptors from the plasma membrane. Agonist binding often evokes phosphorylation in the flexible C-terminal region and/or intracellular loop 3 of many 7TM G-protein-coupled receptors in animal cells, which consequently recruits a cytoplasmic intermediate adaptor, β-arrestin, resulting in clathrin-mediated endocytosis (CME) and downstream signaling such as transcriptional changes. Some 7TM receptors undergo CME without recruiting β-arrestin, but it is not clear how. Arrestins are not encoded in the Arabidopsis thaliana genome, yet Arabidopsis cells have a well-characterized signal-induced CME of a 7TM protein, designated Regulator of G Signaling 1 (AtRGS1). Here we show that a component of the retromer complex, Vacuolar Protein Sorting-Associated 26 (VPS26), binds the phosphorylated C-terminal region of AtRGS1 as a VPS26A/B heterodimer to form a complex that is required for downstream signaling. We propose that VPS26 moonlights as an arrestin-like adaptor in the CME of AtRGS1.

View Journal Article

Research Organization:: University of North Carolina at Chapel Hill, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: FG02-05ER15671

OSTI ID:: 2475196

Alternate ID(s):: OSTI ID: 2478058

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 22 Vol. 63; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (62)

Invited review: Activation of G proteins by GTP and the mechanism of Gα‐catalyzed GTP hydrolysis Sprang, Stephen R. Biopolymers, Vol. 105, Issue 8 https://doi.org/10.1002/bip.22836	journal	May 2016
Studying molecular interactions via capillary electrophoresis and microscale thermophoresis: A review Asmari, Mufarreh; Michalcová, Lenka; Ibrahim, Adel Ehab ELECTROPHORESIS, Vol. 44, Issue 13-14 https://doi.org/10.1002/elps.202200275	journal	April 2023
Proteomic applications of automated GPCR classification Davies, Matthew N.; Gloriam, David E.; Secker, Andrew PROTEOMICS, Vol. 7, Issue 16 https://doi.org/10.1002/pmic.200700093	journal	August 2007
Standard protocol for mass photometry experiments Wu, Di; Piszczek, Grzegorz European Biophysics Journal, Vol. 50, Issue 3-4 https://doi.org/10.1007/s00249-021-01513-9	journal	March 2021
Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit Fu, Yan; Lim, Sungmin; Urano, Daisuke Cell, Vol. 156, Issue 5 https://doi.org/10.1016/j.cell.2014.01.013	journal	February 2014
How GPCR Phosphorylation Patterns Orchestrate Arrestin-Mediated Signaling Latorraca, Naomi R.; Masureel, Matthieu; Hollingsworth, Scott A. Cell, Vol. 183, Issue 7 https://doi.org/10.1016/j.cell.2020.11.014	journal	December 2020
GPCR desensitization: Acute and prolonged phases Rajagopal, Sudarshan; Shenoy, Sudha K. Cellular Signalling, Vol. 41 https://doi.org/10.1016/j.cellsig.2017.01.024	journal	January 2018
d -Glucose sensing by a plasma membrane regulator of G signaling protein, At RGS1 Grigston, Jeffrey C.; Osuna, Daniel; Scheible, Wolf-Rüdiger FEBS Letters, Vol. 582, Issue 25-26 https://doi.org/10.1016/j.febslet.2008.08.038	journal	September 2008
G protein–coupled receptor interactions with arrestins and GPCR kinases: The unresolved issue of signal bias Chen, Qiuyan; Tesmer, John J. G. Journal of Biological Chemistry, Vol. 298, Issue 9 https://doi.org/10.1016/j.jbc.2022.102279	journal	September 2022
Phosphorylation Dynamics in a flg22-Induced, G Protein–Dependent Network Reveals the AtRGS1 Phosphatase Watkins, Justin M.; Montes, Christian; Clark, Natalie M. Molecular & Cellular Proteomics, Vol. 23, Issue 2 https://doi.org/10.1016/j.mcpro.2023.100705	journal	February 2024
How bacteria overcome flagellin pattern recognition in plants Sanguankiattichai, Nattapong; Buscaill, Pierre; Preston, Gail M. Current Opinion in Plant Biology, Vol. 67 https://doi.org/10.1016/j.pbi.2022.102224	journal	June 2022
New insights into GPCR coupling and dimerisation from cryo-EM structures Gusach, Anastasiia; García-Nafría, Javier; Tate, Christopher G. Current Opinion in Structural Biology, Vol. 80 https://doi.org/10.1016/j.sbi.2023.102574	journal	June 2023
Structural Basis of Arrestin-Dependent Signal Transduction Chen, Qiuyan; Iverson, Tina M.; Gurevich, Vsevolod V. Trends in Biochemical Sciences, Vol. 43, Issue 6 https://doi.org/10.1016/j.tibs.2018.03.005	journal	June 2018
β-arrestin-mediated receptor trafficking and signal transduction Shenoy, Sudha K.; Lefkowitz, Robert J. Trends in Pharmacological Sciences, Vol. 32, Issue 9 https://doi.org/10.1016/j.tips.2011.05.002	journal	September 2011
Chemical Synthesis of a Full-Length G-Protein-Coupled Receptor β₂-Adrenergic Receptor with Defined Modification Patterns at the C-Terminus Li, Yulei; Heng, Jie; Sun, Demeng Journal of the American Chemical Society, Vol. 143, Issue 42 https://doi.org/10.1021/jacs.1c07369	journal	October 2021
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke Nature, Vol. 448, Issue 7152 https://doi.org/10.1038/nature05999	journal	July 2007
Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis Urano, Daisuke; Phan, Nguyen; Jones, Janice C. Nature Cell Biology, Vol. 14, Issue 10 https://doi.org/10.1038/ncb2568	journal	September 2012
CCC- and WASH-mediated endosomal sorting of LDLR is required for normal clearance of circulating LDL Bartuzi, Paulina; Billadeau, Daniel D.; Favier, Robert Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10961	journal	March 2016
The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain Shi, Hang; Rojas, Raul; Bonifacino, Juan S. Nature Structural & Molecular Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nsmb1103	journal	May 2006
Ligand-triggered de-repression of Arabidopsis heterotrimeric G proteins coupled to immune receptor kinases Liang, Xiangxiu; Ma, Miaomiao; Zhou, Zhaoyang Cell Research, Vol. 28, Issue 5 https://doi.org/10.1038/s41422-018-0027-5	journal	March 2018
Molecular identification of a BAR domain-containing coat complex for endosomal recycling of transmembrane proteins Simonetti, Boris; Paul, Blessy; Chaudhari, Karina Nature Cell Biology, Vol. 21, Issue 10 https://doi.org/10.1038/s41556-019-0393-3	journal	October 2019
Molecular basis of β-arrestin coupling to formoterol-bound β1-adrenoceptor Lee, Yang; Warne, Tony; Nehmé, Rony Nature, Vol. 583, Issue 7818 https://doi.org/10.1038/s41586-020-2419-1	journal	June 2020
Structure of the class D GPCR Ste2 dimer coupled to two G proteins Velazhahan, Vaithish; Ma, Ning; Pándy-Szekeres, Gáspár Nature, Vol. 589, Issue 7840 https://doi.org/10.1038/s41586-020-2994-1	journal	December 2020
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Tail engagement of arrestin at the glucagon receptor Chen, Kun; Zhang, Chenhui; Lin, Shuling Nature, Vol. 620, Issue 7975 https://doi.org/10.1038/s41586-023-06420-x	journal	August 2023
Disruption of endocytosis through chemical inhibition of clathrin heavy chain function Dejonghe, Wim; Sharma, Isha; Denoo, Bram Nature Chemical Biology, Vol. 15, Issue 6 https://doi.org/10.1038/s41589-019-0262-1	journal	April 2019
The power and pitfalls of AlphaFold2 for structure prediction beyond rigid globular proteins Agarwal, Vinayak; McShan, Andrew C. Nature Chemical Biology, Vol. 20, Issue 8 https://doi.org/10.1038/s41589-024-01638-w	journal	June 2024
A structural biology community assessment of AlphaFold2 applications Akdel, Mehmet; Pires, Douglas E. V.; Pardo, Eduard Porta Nature Structural & Molecular Biology, Vol. 29, Issue 11 https://doi.org/10.1038/s41594-022-00849-w	journal	November 2022
Visualizing the GPCR Network: Classification and Evolution Hu, Geng-Ming; Mai, Te-Lun; Chen, Chi-Ming Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-15707-9	journal	November 2017
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling Johnston, C. A.; Taylor, J. P.; Gao, Y. Proceedings of the National Academy of Sciences, Vol. 104, Issue 44 https://doi.org/10.1073/pnas.0704751104	journal	October 2007
A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer Gallon, Matthew; Clairfeuille, Thomas; Steinberg, Florian Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1410552111	journal	August 2014
Buried ionizable networks are an ancient hallmark of G protein-coupled receptor activation Isom, Daniel G.; Dohlman, Henrik G. Proceedings of the National Academy of Sciences, Vol. 112, Issue 18 https://doi.org/10.1073/pnas.1417888112	journal	April 2015
Functional Reconstitution of an Atypical G Protein Heterotrimer and Regulator of G Protein Signaling Protein (RGS1) from Arabidopsis thaliana Jones, Janice C.; Temple, Brenda R. S.; Jones, Alan M. Journal of Biological Chemistry, Vol. 286, Issue 15 https://doi.org/10.1074/jbc.M110.190355	journal	February 2011
Tyrosine phosphorylation switching of a G protein Li, Bo; Tunc-Ozdemir, Meral; Urano, Daisuke Journal of Biological Chemistry, Vol. 293, Issue 13 https://doi.org/10.1074/jbc.RA117.000163	journal	March 2018
An atypical heterotrimeric Gα protein has substantially reduced nucleotide binding but retains nucleotide-independent interactions with its cognate RGS protein and Gβγ dimer Lou, Fei; Abramyan, Tigran M.; Jia, Haiyan Journal of Biomolecular Structure and Dynamics, Vol. 38, Issue 17 https://doi.org/10.1080/07391102.2019.1704879	journal	December 2019
Receptor Recycling by Retromer Carosi, Julian M.; Denton, Donna; Kumar, Sharad Molecular and Cellular Biology, Vol. 43, Issue 7 https://doi.org/10.1080/10985549.2023.2222053	journal	June 2023
GPCRdb in 2021: integrating GPCR sequence, structure and function Kooistra, Albert J.; Mordalski, Stefan; Pándy-Szekeres, Gáspár Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1080	journal	December 2020
Cargo Recognition in Clathrin-Mediated Endocytosis Traub, L. M.; Bonifacino, J. S. Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 11 https://doi.org/10.1101/cshperspect.a016790	journal	November 2013
“Round Up the Usual Suspects”: A Comment on Nonexistent Plant G Protein-Coupled Receptors Urano, Daisuke; Jones, Alan M. Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.212324	journal	January 2013
Structure of Vps26B and Mapping of its Interaction with the Retromer Protein Complex Collins, Brett M.; Norwood, Suzanne J.; Kerr, Markus C. Traffic, Vol. 9, Issue 3 https://doi.org/10.1111/j.1600-0854.2007.00688.x	journal	December 2007
Nudge‐nudge, WNK‐WNK (kinases), say no more? Cao‐Pham, Anh H.; Urano, Daisuke; Ross‐Elliott, Timothy J. New Phytologist, Vol. 220, Issue 1 https://doi.org/10.1111/nph.15276	journal	June 2018
The Diverse Roles of Arrestin Scaffolds in G Protein–Coupled Receptor Signaling Peterson, Yuri K.; Luttrell, Louis M. Pharmacological Reviews, Vol. 69, Issue 3 https://doi.org/10.1124/pr.116.013367	journal	April 2017
Architecture and mechanism of metazoan retromer:SNX3 tubular coat assembly Leneva, Natalya; Kovtun, Oleksiy; Morado, Dustin R. Science Advances, Vol. 7, Issue 13 https://doi.org/10.1126/sciadv.abf8598	journal	March 2021
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation Chen, J. -G. Science, Vol. 301, Issue 5640 https://doi.org/10.1126/science.1087790	journal	September 2003
High-Resolution Crystal Structure of an Engineered Human 2-Adrenergic G Protein-Coupled Receptor Cherezov, V.; Rosenbaum, D. M.; Hanson, M. A. Science, Vol. 318, Issue 5854 https://doi.org/10.1126/science.1150577	journal	October 2007
Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex Sun, Y.; Li, L.; Macho, A. P. Science, Vol. 342, Issue 6158 https://doi.org/10.1126/science.1243825	journal	October 2013
Noncanonical scaffolding of G _αi and β-arrestin by G protein–coupled receptors Smith, Jeffrey S.; Pack, Thomas F.; Inoue, Asuka Science, Vol. 371, Issue 6534 https://doi.org/10.1126/science.aay1833	journal	March 2021
AlphaFold2 structures guide prospective ligand discovery Lyu, Jiankun; Kapolka, Nicholas; Gumpper, Ryan Science, Vol. 384, Issue 6702 https://doi.org/10.1126/science.adn6354	journal	June 2024
The Crystal Structure of a Self-Activating G Protein Subunit Reveals Its Distinct Mechanism of Signal Initiation Jones, J. C.; Duffy, J. W.; Machius, M. Science Signaling, Vol. 4, Issue 159 https://doi.org/10.1126/scisignal.2001446	journal	February 2011
Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom Urano, Daisuke; Maruta, Natsumi; Trusov, Yuri Science Signaling, Vol. 9, Issue 446 https://doi.org/10.1126/scisignal.aaf9558	journal	September 2016
Differential regulation of G protein signaling in Arabidopsis through two distinct pathways that internalize AtRGS1 Watkins, Justin M.; Ross-Elliott, Timothy J.; Shan, Xiaoyi Science Signaling, Vol. 14, Issue 695 https://doi.org/10.1126/scisignal.abe4090	journal	August 2021
G Protein–Coupled Receptor Sorting to Endosomes and Lysosomes Marchese, Adriano; Paing, May M.; Temple, Brenda R. S. Annual Review of Pharmacology and Toxicology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.pharmtox.48.113006.094646	journal	February 2008
Regulation of GPCRs by Endocytic Membrane Trafficking and Its Potential Implications Hanyaloglu, Aylin C.; Zastrow, Mark von Annual Review of Pharmacology and Toxicology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.pharmtox.48.113006.094830	journal	February 2008
G protein-coupled receptor signaling: transducers and effectors Jiang, Haoran; Galtes, Daniella; Wang, Jialu American Journal of Physiology-Cell Physiology, Vol. 323, Issue 3 https://doi.org/10.1152/ajpcell.00210.2022	journal	September 2022
On the origins of arrestin and rhodopsin Alvarez, Carlos E. BMC Evolutionary Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2148-8-222	journal	January 2008
QR code model: a new possibility for GPCR phosphorylation recognition Chen, Hao; Zhang, Suli; Zhang, Xi Cell Communication and Signaling, Vol. 20, Issue 1 https://doi.org/10.1186/s12964-022-00832-4	journal	March 2022
Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes Tunc-Ozdemir, Meral; Jones, Alan M. PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171854	journal	February 2017
PRODIGY: A Contact-based Predictor of Binding Affinity in Protein-protein Complexes Vangone, Anna; Bonvin, Alexandre BIO-PROTOCOL, Vol. 7, Issue 3 https://doi.org/10.21769/BioProtoc.2124	journal	January 2017
The F238L Point Mutation in the Cannabinoid Type 1 Receptor Enhances Basal Endocytosis via Lipid Rafts Wickert, Melanie; Hildick, Keri L.; Baillie, Gemma L. Frontiers in Molecular Neuroscience, Vol. 11 https://doi.org/10.3389/fnmol.2018.00230	journal	July 2018
GPCR Signaling Regulation: The Role of GRKs and Arrestins Gurevich, Vsevolod V.; Gurevich, Eugenia V. Frontiers in Pharmacology, Vol. 10 https://doi.org/10.3389/fphar.2019.00125	journal	February 2019
Diversity of retromer-mediated vesicular trafficking pathways in plants Jha, Suryatapa Ghosh; Larson, Emily R. Frontiers in Plant Science, Vol. 14 https://doi.org/10.3389/fpls.2023.1184047	journal	June 2023
Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy Clark, Natalie M.; Hinde, Elizabeth; Winter, Cara M. eLife, Vol. 5 https://doi.org/10.7554/eLife.14770	journal	June 2016

Similar Records

VPS26 Moonlights as an Arrestin-like Adapter for a 7-transmembrane RGS 2 protein in Arabidopsis thaliana

Technical Report · Mon Mar 06 23:00:00 EST 2023 · OSTI ID:1959926

Differential regulation of G protein signaling in Arabidopsis through two distinct pathways that internalize AtRGS1

Journal Article · Mon Aug 09 20:00:00 EDT 2021 · Science Signaling · OSTI ID:1812769

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Genetics
Monomers
Oligomers
Peptides and proteins
Receptors

VPS26 Moonlights as a β-Arrestin-like Adapter for a 7-Transmembrane RGS Protein in Arabidopsis thaliana

Citation Formats

References (62)

Similar Records

Related Subjects