Literature DB >> 34260394

Proton-gated coincidence detection is a common feature of GPCR signaling.

Nicholas J Kapolka1, Jacob B Rowe1, Geoffrey J Taghon1, William M Morgan1, Corin R O'Shea1, Daniel G Isom2,3,4.   

Abstract

The evolutionary expansion of G protein-coupled receptors (GPCRs) has produced a rich diversity of transmembrane sensors for many physical and chemical signals. In humans alone, over 800 GPCRs detect stimuli such as light, hormones, and metabolites to guide cellular decision-making primarily using intracellular G protein signaling networks. This diversity is further enriched by GPCRs that function as molecular sensors capable of discerning multiple inputs to transduce cues encoded in complex, context-dependent signals. Here, we show that many GPCRs are coincidence detectors that couple proton (H+) binding to GPCR signaling. Using a panel of 28 receptors covering 280 individual GPCR-Gα coupling combinations, we show that H+ gating both positively and negatively modulates GPCR signaling. Notably, these observations extend to all modes of GPCR pharmacology including ligand efficacy, potency, and cooperativity. Additionally, we show that GPCR antagonism and constitutive activity are regulated by H+ gating and report the discovery of an acid sensor, the adenosine A2a receptor, which can be activated solely by acidic pH. Together, these findings establish a paradigm for GPCR signaling, biology, and pharmacology applicable to acidified microenvironments such as endosomes, synapses, tumors, and ischemic vasculature.

Entities:  

Keywords:  Boolean; GPCR; acidosis; coincidence detection; proton gating

Mesh:

Substances:

Year:  2021        PMID: 34260394      PMCID: PMC8285908          DOI: 10.1073/pnas.2100171118

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  28 in total

1.  CRISPR-addressable yeast strains with applications in human G protein-coupled receptor profiling and synthetic biology.

Authors:  Jacob B Rowe; Geoffrey J Taghon; Nicholas J Kapolka; William M Morgan; Daniel G Isom
Journal:  J Biol Chem       Date:  2020-05-01       Impact factor: 5.157

2.  Pheromone signaling mechanisms in yeast: a prototypical sex machine.

Authors:  Yuqi Wang; Henrik G Dohlman
Journal:  Science       Date:  2004-11-26       Impact factor: 47.728

3.  Endocytosis of Ligand-Activated Sphingosine 1-Phosphate Receptor 1 Mediated by the Clathrin-Pathway.

Authors:  Patrick M Reeves; Yuan-Lin Kang; Tom Kirchhausen
Journal:  Traffic       Date:  2015-12-09       Impact factor: 6.215

4.  Protons as second messenger regulators of G protein signaling.

Authors:  Daniel G Isom; Vishwajith Sridharan; Rachael Baker; Sarah T Clement; David M Smalley; Henrik G Dohlman
Journal:  Mol Cell       Date:  2013-08-15       Impact factor: 17.970

5.  Coincidence Detection of Membrane Stretch and Extracellular pH by the Proton-Sensing Receptor OGR1 (GPR68).

Authors:  Wei-Chun Wei; Fabio Bianchi; Yang-Kao Wang; Ming-Jer Tang; Hua Ye; Maike D Glitsch
Journal:  Curr Biol       Date:  2018-11-21       Impact factor: 10.834

6.  TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor.

Authors:  Ju-Qiang Wang; Junko Kon; Chihiro Mogi; Masayuki Tobo; Alatangaole Damirin; Koichi Sato; Mayumi Komachi; Enkhzol Malchinkhuu; Naoya Murata; Takao Kimura; Atsushi Kuwabara; Kaori Wakamatsu; Hideki Koizumi; Toshimitsu Uede; Gozoh Tsujimoto; Hitoshi Kurose; Takashi Sato; Akihiro Harada; Norihiko Misawa; Hideaki Tomura; Fumikazu Okajima
Journal:  J Biol Chem       Date:  2004-08-23       Impact factor: 5.157

7.  Noncanonical control of vasopressin receptor type 2 signaling by retromer and arrestin.

Authors:  Timothy N Feinstein; Naofumi Yui; Matthew J Webber; Vanessa L Wehbi; Hilary P Stevenson; J Darwin King; Kenneth R Hallows; Dennis Brown; Richard Bouley; Jean-Pierre Vilardaga
Journal:  J Biol Chem       Date:  2013-08-09       Impact factor: 5.157

8.  Proton-sensing G-protein-coupled receptors.

Authors:  Marie-Gabrielle Ludwig; Miroslava Vanek; Danilo Guerini; Jürg A Gasser; Carol E Jones; Uwe Junker; Hans Hofstetter; Romain M Wolf; Klaus Seuwen
Journal:  Nature       Date:  2003-09-04       Impact factor: 49.962

9.  HCAR3: an underexplored metabolite sensor.

Authors:  Nicholas J Kapolka; Daniel G Isom
Journal:  Nat Rev Drug Discov       Date:  2020-11       Impact factor: 112.288

10.  Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding.

Authors:  Christian Frantz; Gabriela Barreiro; Laura Dominguez; Xiaoming Chen; Robert Eddy; John Condeelis; Mark J S Kelly; Matthew P Jacobson; Diane L Barber
Journal:  J Cell Biol       Date:  2008-11-24       Impact factor: 10.539

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  3 in total

1.  Serotonin G Protein-Coupled Receptor-Based Biosensing Modalities in Yeast.

Authors:  Bettina Lengger; Emma E Hoch-Schneider; Christina N Jensen; Tadas Jakočiu Nas; Anja A Petersen; Thomas M Frimurer; Emil D Jensen; Michael K Jensen
Journal:  ACS Sens       Date:  2022-04-22       Impact factor: 9.618

Review 2.  Physiological relevance of proton-activated GPCRs.

Authors:  Pedro H Imenez Silva; Carsten A Wagner
Journal:  Pflugers Arch       Date:  2022-03-05       Impact factor: 3.657

3.  Screening microbially produced Δ9-tetrahydrocannabinol using a yeast biosensor workflow.

Authors:  William M Shaw; Yunfeng Zhang; Xinyu Lu; Ahmad S Khalil; Graham Ladds; Xiaozhou Luo; Tom Ellis
Journal:  Nat Commun       Date:  2022-09-20       Impact factor: 17.694

  3 in total

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