Conformational biosensors reveal GPCR signalling from endosomes
Conformation-specific antibodies capable of monitoring the activation state of a G-protein-coupled seven-transmembrane receptor, the β 2 -adrenoceptor, reveals receptor and G-protein activation not only in the plasma membrane, but also in the endosome. Adrenoceptor signalling linked to endosomes It...
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| Published in | Nature (London) Vol. 495; no. 7442; pp. 534 - 538 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
28.03.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Conformation-specific antibodies capable of monitoring the activation state of a G-protein-coupled seven-transmembrane receptor, the β
2
-adrenoceptor, reveals receptor and G-protein activation not only in the plasma membrane, but also in the endosome.
Adrenoceptor signalling linked to endosomes
It is widely assumed that G-protein-linked signalling occurs only at the plasma membrane. In this study, Mark von Zastrow and colleagues use conformation-specific single-chain antibodies to directly probe the activation of the β2-adrenoceptor, which is a prototypical G-protein-coupled receptor, and its cognate G protein, G
s
, in living cells. They show that classical or canonical G-protein-linked signalling occurs from endosomes as well as from the plasma membrane.
A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution
1
. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins
2
,
3
, or GPCR activation elicits a discrete form of persistent G protein signalling
4
,
5
,
6
,
7
,
8
,
9
, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response
10
. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformation-specific single-domain antibodies (nanobodies) to directly probe activation of the β
2
-adrenoceptor, a prototypical GPCR
11
, and its cognate G protein, G
s
(ref.
12
), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosome membrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change
in vivo
. |
|---|---|
| AbstractList | Conformation-specific antibodies capable of monitoring the activation state of a G-protein-coupled seven-transmembrane receptor, the β
2
-adrenoceptor, reveals receptor and G-protein activation not only in the plasma membrane, but also in the endosome.
Adrenoceptor signalling linked to endosomes
It is widely assumed that G-protein-linked signalling occurs only at the plasma membrane. In this study, Mark von Zastrow and colleagues use conformation-specific single-chain antibodies to directly probe the activation of the β2-adrenoceptor, which is a prototypical G-protein-coupled receptor, and its cognate G protein, G
s
, in living cells. They show that classical or canonical G-protein-linked signalling occurs from endosomes as well as from the plasma membrane.
A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution
1
. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins
2
,
3
, or GPCR activation elicits a discrete form of persistent G protein signalling
4
,
5
,
6
,
7
,
8
,
9
, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response
10
. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformation-specific single-domain antibodies (nanobodies) to directly probe activation of the β
2
-adrenoceptor, a prototypical GPCR
11
, and its cognate G protein, G
s
(ref.
12
), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosome membrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change
in vivo
. A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins, or GPCR activation elicits a discrete form of persistent G protein signalling, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformation-specific single-domain antibodies (nanobodies) to directly probe activation of the β2-adrenoceptor, a prototypical GPCR, and its cognate G protein, Gs (ref. 12), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosome membrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change in vivo.A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins, or GPCR activation elicits a discrete form of persistent G protein signalling, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformation-specific single-domain antibodies (nanobodies) to directly probe activation of the β2-adrenoceptor, a prototypical GPCR, and its cognate G protein, Gs (ref. 12), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosome membrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change in vivo. A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins, or GPCR activation elicits a discrete form of persistent G protein signalling, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformation-specific single-domain antibodies (nanobodies) to directly probe activation of the β2-adrenoceptor, a prototypical GPCR, and its cognate G protein, Gs (ref. 12), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosome membrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change in vivo. A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G proteins is confined to the plasma membrane. Evidence supporting this traditional view is based on analytical methods that provide limited or no subcellular resolution1. It has been subsequently proposed that signalling by internalized GPCRs is restricted to G-protein-independent mechanisms such as scaffolding by arrestins, or GPCR activation elicits a discrete formof persistent G protein signalling, or that internalized GPCRs can indeed contribute to the acute G-protein-mediated response10. Evidence supporting these various latter hypotheses is indirect or subject to alternative interpretation, and it remains unknown if endosome-localized GPCRs are even present in an active form. Here we describe the application of conformationspecific single-domain antibodies (nanobodies) to directly probe activation of the b2-adrenoceptor, a prototypical GPCR11, and its cognate G protein, Gs (ref. 12), in living mammalian cells. We show that the adrenergic agonist isoprenaline promotes receptor and G protein activation in the plasma membrane as expected, but also in the early endosomemembrane, and that internalized receptors contribute to the overall cellular cyclic AMP response within several minutes after agonist application. These findings provide direct support for the hypothesis that canonical GPCR signalling occurs from endosomes as well as the plasma membrane, and suggest a versatile strategy for probing dynamic conformational change in vivo. [PUBLICATION ABSTRACT] |
| Audience | Academic |
| Author | Tomshine, Jon R. Tomshine, Jin C. Huang, Bo Mahoney, Jacob P. von Zastrow, Mark Irannejad, Roshanak Sunahara, Roger K. Chevalier, Michael Rasmussen, Søren G. F. Steyaert, Jan El-Samad, Hana |
| Author_xml | – sequence: 1 givenname: Roshanak surname: Irannejad fullname: Irannejad, Roshanak organization: Department of Psychiatry, University of California – sequence: 2 givenname: Jin C. surname: Tomshine fullname: Tomshine, Jin C. organization: Department of Psychiatry, University of California – sequence: 3 givenname: Jon R. surname: Tomshine fullname: Tomshine, Jon R. organization: Department of Psychiatry, University of California – sequence: 4 givenname: Michael surname: Chevalier fullname: Chevalier, Michael organization: Department of Biochemistry & Biophysics, University of California – sequence: 5 givenname: Jacob P. surname: Mahoney fullname: Mahoney, Jacob P. organization: Department of Pharmacology, University of Michigan Medical School – sequence: 6 givenname: Jan surname: Steyaert fullname: Steyaert, Jan organization: Department of Molecular and Cellular Interactions, Vrije Universiteit Brussel, B-1050 Brussels, Belgium, Structural Biology Research Centre, VIB, B-1050 Brussels, Belgium – sequence: 7 givenname: Søren G. F. surname: Rasmussen fullname: Rasmussen, Søren G. F. organization: Department of Neuroscience and Pharmacology, The Panum Institute, University of Copenhagen, 2200 Copenhagen N, Denmark – sequence: 8 givenname: Roger K. surname: Sunahara fullname: Sunahara, Roger K. organization: Department of Pharmacology, University of Michigan Medical School – sequence: 9 givenname: Hana surname: El-Samad fullname: El-Samad, Hana organization: Department of Biochemistry & Biophysics, University of California – sequence: 10 givenname: Bo surname: Huang fullname: Huang, Bo organization: Department of Biochemistry & Biophysics, University of California, Department of Pharmaceutical Chemistry, University of California – sequence: 11 givenname: Mark surname: von Zastrow fullname: von Zastrow, Mark email: Mark.VonZastrow@ucsf.edu organization: Department of Psychiatry, University of California, Department of Cellular & Molecular Pharmacology, University of California |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23515162$$D View this record in MEDLINE/PubMed |
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| CODEN | NATUAS |
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| ContentType | Journal Article |
| Copyright | Springer Nature Limited 2013 COPYRIGHT 2013 Nature Publishing Group Copyright Nature Publishing Group Mar 28, 2013 |
| Copyright_xml | – notice: Springer Nature Limited 2013 – notice: COPYRIGHT 2013 Nature Publishing Group – notice: Copyright Nature Publishing Group Mar 28, 2013 |
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| Snippet | Conformation-specific antibodies capable of monitoring the activation state of a G-protein-coupled seven-transmembrane receptor, the β
2
-adrenoceptor, reveals... A long-held tenet of molecular pharmacology is that canonical signal transduction mediated by G-protein-coupled receptor (GPCR) coupling to heterotrimeric G... |
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| SubjectTerms | 631/80/86/2363 Adrenergic beta-2 Receptor Agonists - pharmacology Biosensing Techniques - methods Biosensors Cell Membrane - chemistry Cell Membrane - metabolism Clathrin-Coated Vesicles Cyclic AMP - metabolism Cytoplasm Dopamine Endocytosis Endosomes - chemistry Endosomes - metabolism Green Fluorescent Proteins - analysis Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism GTP-Binding Protein alpha Subunits, Gs - metabolism HEK293 Cells Humanities and Social Sciences Humans Hypotheses Isoproterenol - pharmacology letter Ligands (Biochemistry) Models, Biological multidisciplinary Pharmacology Phosphorylation Plasma Protein Conformation Proteins Receptors, Adrenergic, beta-2 - chemistry Receptors, Adrenergic, beta-2 - immunology Receptors, Adrenergic, beta-2 - metabolism Recruitment Science Signal Transduction Single-Domain Antibodies - genetics Single-Domain Antibodies - immunology |
| Title | Conformational biosensors reveal GPCR signalling from endosomes |
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