Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes
Abstract
Background Arabidopsis, 7-transmembrane Regulator of G signaling protein 1 (AtRGS1) modulates canonical G protein signaling by promoting the inactive state of heterotrimeric G protein complex on the plasma membrane. It is known that plant leucine-rich repeat receptor-like kinases (LRR RLKs) phosphorylate AtRGS1 in vitro but little is known about the in vivo interaction, molecular dynamics, or the cellular consequences of this interaction. Methods Therefore, a subset of the known RLKs that phosphorylate AtRGS1 were selected for elucidation, namely, BAK1, BIR1, FLS2. Several microscopies for both static and dynamic protein-protein interactions were used to follow in vivo interactions between the RLKs and AtRGS1 after the presentation of the Pathogen-associated Molecular Pattern, Flagellin 22 (Flg22). These microscopies included FoÈrster Resonance Energy Transfer, Bimolecular Fluoresence Complementation, and Cross Number and Brightness fluorescence Correlation Spectroscopy. In addition, reactive oxygen species and calcium changes in living cells were quantitated using luminometry and R-GECO1 microscopy. Results The LRR RLKs BAK1 and BIR1, interact with AtRGS1 at the plasma membrane. The RLK ligand flg22 sets BAK1 in motion toward AtRGS1 and BIR1 away, both returning to the baseline orientations by 10 minutes. The C-terminal tail of AtRGS1 is important for the interaction with BAK1 and for themore »
- Authors:
-
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology; Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Pharmacology
- Publication Date:
- Research Org.:
- University of North Carolina, Chapel Hill, NC (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1362033
- Grant/Contract Number:
- FG02-05ER15671; R01GM065989; MCB-0718202
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 2; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Tunc-Ozdemir, Meral, and Jones, Alan M. Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes. United States: N. p., 2017.
Web. doi:10.1371/journal.pone.0171854.
Tunc-Ozdemir, Meral, & Jones, Alan M. Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes. United States. https://doi.org/10.1371/journal.pone.0171854
Tunc-Ozdemir, Meral, and Jones, Alan M. Fri .
"Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes". United States. https://doi.org/10.1371/journal.pone.0171854. https://www.osti.gov/servlets/purl/1362033.
@article{osti_1362033,
title = {Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes},
author = {Tunc-Ozdemir, Meral and Jones, Alan M.},
abstractNote = {Background Arabidopsis, 7-transmembrane Regulator of G signaling protein 1 (AtRGS1) modulates canonical G protein signaling by promoting the inactive state of heterotrimeric G protein complex on the plasma membrane. It is known that plant leucine-rich repeat receptor-like kinases (LRR RLKs) phosphorylate AtRGS1 in vitro but little is known about the in vivo interaction, molecular dynamics, or the cellular consequences of this interaction. Methods Therefore, a subset of the known RLKs that phosphorylate AtRGS1 were selected for elucidation, namely, BAK1, BIR1, FLS2. Several microscopies for both static and dynamic protein-protein interactions were used to follow in vivo interactions between the RLKs and AtRGS1 after the presentation of the Pathogen-associated Molecular Pattern, Flagellin 22 (Flg22). These microscopies included FoÈrster Resonance Energy Transfer, Bimolecular Fluoresence Complementation, and Cross Number and Brightness fluorescence Correlation Spectroscopy. In addition, reactive oxygen species and calcium changes in living cells were quantitated using luminometry and R-GECO1 microscopy. Results The LRR RLKs BAK1 and BIR1, interact with AtRGS1 at the plasma membrane. The RLK ligand flg22 sets BAK1 in motion toward AtRGS1 and BIR1 away, both returning to the baseline orientations by 10 minutes. The C-terminal tail of AtRGS1 is important for the interaction with BAK1 and for the tempo of the AtRGS1/BIR1 dynamics. This window of time corresponds to the flg22-induced transient production of reactive oxygen species and calcium release which are both attenuated in the rgs1 and the bak1 null mutants. Conclusions A temporal model of these interactions is proposed. flg22 binding induces nearly instantaneous dimerization between FLS2 and BAK1. Phosphorylated BAK1 interacts with and enables AtRGS1 to move away from BIR1 and AtRGS1 becomes phosphorylated leading to its endocytosis thus leading to de-repression by permitting AtGPA1 to exchange GDP for GTP. Finally, the G protein complex becomes dissociated thus AGB1 interacts with its effector proteins leading to changes in reactive oxygen species and calcium.},
doi = {10.1371/journal.pone.0171854},
journal = {PLoS ONE},
number = 2,
volume = 12,
place = {United States},
year = {Fri Feb 10 00:00:00 EST 2017},
month = {Fri Feb 10 00:00:00 EST 2017}
}
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Correction
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Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis
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