publication . Article . Other literature type . 2019

Crystal structure of jumping spider rhodopsin-1 as a light sensitive GPCR

Varma, Niranjan; Mutt, Eshita; Mühle, Jonas; Panneels, Valérie; Terakita, Akihisa; Deupi, Xavier; Nogly, Przemyslaw; Schertler, Gebhard F. X.; Lesca, Elena;
Open Access English
  • Published: 16 Jul 2019 Journal: Proceedings of the National Academy of Sciences of the United States of America, volume 116, issue 29, pages 14,547-14,556 (issn: 0027-8424, eissn: 1091-6490, Copyright policy)
  • Publisher: National Academy of Sciences
  • Country: Switzerland
Abstract
Significance Photosensitive G protein-coupled receptors (GPCRs) have been used as model systems in the study of class A GPCRs. These are classified into mono- and bistable rhodopsins based on the thermal stability of their active states. Although much is known about monostable rhodopsins, their bistable counterparts remain structurally elusive. The crystal structure of the bistable jumping spider rhodopsin-1 lays the basis in the understanding of molecular mechanistic differences between these 2 subclasses. Furthermore, bistable rhodopsins conform to an “activation-ready” architecture bearing similarities to nonphotosensitive class A GPCRs when compared to monos...
Subjects
free text keywords: Crystallography; Molecular dynamics simulation; GPCRs, G-protein coupled receptors; RHODOPSIN STRUCTURE, PNAS Plus, Biological Sciences, Applied Biological Sciences, rhodopsin, bistability, G protein-coupled receptors, retinal, X-ray crystallography, Crystallography, Molecular dynamics simulation, GPCRs, G-protein coupled receptors, RHODOPSIN STRUCTURE, Multidisciplinary
Funded by
EC| PSI-FELLOW
Project
PSI-FELLOW
International Fellowship Program on Materials & Matter, Energy & Environment, Human Health & Life-Sciences, and Accelerator Technology
  • Funder: European Commission (EC)
  • Project Code: 290605
  • Funding stream: FP7 | SP3 | PEOPLE
,
SNSF| Analyzing protein dynamics in receptor signaling relevant to pharmacology
Project
  • Funder: Swiss National Science Foundation (SNSF)
  • Project Code: 310030B_173335
  • Funding stream: Project funding | Project funding (Div. I-III)
,
SNSF| A three-dimensional movie of the structural changes in a membrane chloride pump revealed by X-ray Free Electron Laser pulses
Project
  • Funder: Swiss National Science Foundation (SNSF)
  • Project Code: PZ00P3_174169
  • Funding stream: Careers | Ambizione
,
EC| X-probe
Project
X-probe
Advanced XFEL and Synchrotron based Probes of Protein Structure and Dynamics
  • Funder: European Commission (EC)
  • Project Code: 637295
  • Funding stream: H2020 | MSCA-ITN-ETN
75 references, page 1 of 5

1 Terakita A., Kawano-Yamashita E., Koyanagi M., Evolution and diversity of opsins. Wiley Interdiscip. Rev. Membr. Transp. Signal.1, 104–111 (2012).

2 Sakmar T. P., Franke R. R., Khorana H. G., Glutamic acid-113 serves as the retinylidene Schiff ba se counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. U.S.A.86, 8309–8313 (1989).2573063 [OpenAIRE] [PubMed]

3 Sakmar T. P., Franke R. R., Khorana H. G., The role of the retinylidene Schiff base counterion in rhodopsin in determining wavelength absorbance and Schiff base pKa. Proc. Natl. Acad. Sci. U.S.A.88, 3079–3083 (1991).2014228 [OpenAIRE] [PubMed]

4 Terakita A., Counterion displacement in the molecular evolution of the rhodopsin family. Nat. Struct. Mol. Biol.11, 284–289 (2004).14981504 [OpenAIRE] [PubMed]

5 Kimata N., Retinal orientation and interactions in rhodopsin reveal a two-stage trigger mechanism for activation. Nat. Commun.7, 12683 (2016).27585742 [OpenAIRE] [PubMed]

6 Palczewski K., G protein-coupled receptor rhodopsin. Annu. Rev. Biochem.75, 743–767 (2006).16756510 [OpenAIRE] [PubMed]

7 Tsukamoto H., Terakita A., Diversity and functional properties of bistable pigments. Photochem. Photobiol. Sci.9, 1435–1443 (2010).20852774 [OpenAIRE] [PubMed]

8 Ehrenberg D., The two-photon reversible reaction of the bistable jumping spider rhodopsin-1. Biophys. J.116, 1248–1258 (2019).30902364 [OpenAIRE] [PubMed]

9 Yan E. C. Y., Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. U.S.A.100, 9262–9267 (2003).12835420 [OpenAIRE] [PubMed]

10 Isberg V., Generic GPCR residue numbers–Aligning topology maps while minding the gaps. Trends Pharmacol. Sci.36, 22–31 (2015).25541108 [OpenAIRE] [PubMed]

11 Ota T., Furutani Y., Terakita A., Shichida Y., Kandori H., Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy. Biochemistry 45, 2845–2851 (2006).16503639 [OpenAIRE] [PubMed]

12 Murakami M., Kouyama T., Crystal structure of squid rhodopsin. Nature 453, 363–367 (2008).18480818 [OpenAIRE] [PubMed]

13 Shimamura T., Crystal structure of squid rhodopsin with intracellularly extended cytoplasmic region. J. Biol. Chem.283, 17753–17756 (2008).18463093 [OpenAIRE] [PubMed]

14 Angel T. E., Chance M. R., Palczewski K., Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A.106, 8555–8560 (2009).19433801 [OpenAIRE] [PubMed]

15 Flock T., Selectivity determinants of GPCR-G-protein binding. Nature 545, 317–322 (2017).28489817 [OpenAIRE] [PubMed]

75 references, page 1 of 5
Abstract
Significance Photosensitive G protein-coupled receptors (GPCRs) have been used as model systems in the study of class A GPCRs. These are classified into mono- and bistable rhodopsins based on the thermal stability of their active states. Although much is known about monostable rhodopsins, their bistable counterparts remain structurally elusive. The crystal structure of the bistable jumping spider rhodopsin-1 lays the basis in the understanding of molecular mechanistic differences between these 2 subclasses. Furthermore, bistable rhodopsins conform to an “activation-ready” architecture bearing similarities to nonphotosensitive class A GPCRs when compared to monos...
Subjects
free text keywords: Crystallography; Molecular dynamics simulation; GPCRs, G-protein coupled receptors; RHODOPSIN STRUCTURE, PNAS Plus, Biological Sciences, Applied Biological Sciences, rhodopsin, bistability, G protein-coupled receptors, retinal, X-ray crystallography, Crystallography, Molecular dynamics simulation, GPCRs, G-protein coupled receptors, RHODOPSIN STRUCTURE, Multidisciplinary
Funded by
EC| PSI-FELLOW
Project
PSI-FELLOW
International Fellowship Program on Materials & Matter, Energy & Environment, Human Health & Life-Sciences, and Accelerator Technology
  • Funder: European Commission (EC)
  • Project Code: 290605
  • Funding stream: FP7 | SP3 | PEOPLE
,
SNSF| Analyzing protein dynamics in receptor signaling relevant to pharmacology
Project
  • Funder: Swiss National Science Foundation (SNSF)
  • Project Code: 310030B_173335
  • Funding stream: Project funding | Project funding (Div. I-III)
,
SNSF| A three-dimensional movie of the structural changes in a membrane chloride pump revealed by X-ray Free Electron Laser pulses
Project
  • Funder: Swiss National Science Foundation (SNSF)
  • Project Code: PZ00P3_174169
  • Funding stream: Careers | Ambizione
,
EC| X-probe
Project
X-probe
Advanced XFEL and Synchrotron based Probes of Protein Structure and Dynamics
  • Funder: European Commission (EC)
  • Project Code: 637295
  • Funding stream: H2020 | MSCA-ITN-ETN
75 references, page 1 of 5

1 Terakita A., Kawano-Yamashita E., Koyanagi M., Evolution and diversity of opsins. Wiley Interdiscip. Rev. Membr. Transp. Signal.1, 104–111 (2012).

2 Sakmar T. P., Franke R. R., Khorana H. G., Glutamic acid-113 serves as the retinylidene Schiff ba se counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. U.S.A.86, 8309–8313 (1989).2573063 [OpenAIRE] [PubMed]

3 Sakmar T. P., Franke R. R., Khorana H. G., The role of the retinylidene Schiff base counterion in rhodopsin in determining wavelength absorbance and Schiff base pKa. Proc. Natl. Acad. Sci. U.S.A.88, 3079–3083 (1991).2014228 [OpenAIRE] [PubMed]

4 Terakita A., Counterion displacement in the molecular evolution of the rhodopsin family. Nat. Struct. Mol. Biol.11, 284–289 (2004).14981504 [OpenAIRE] [PubMed]

5 Kimata N., Retinal orientation and interactions in rhodopsin reveal a two-stage trigger mechanism for activation. Nat. Commun.7, 12683 (2016).27585742 [OpenAIRE] [PubMed]

6 Palczewski K., G protein-coupled receptor rhodopsin. Annu. Rev. Biochem.75, 743–767 (2006).16756510 [OpenAIRE] [PubMed]

7 Tsukamoto H., Terakita A., Diversity and functional properties of bistable pigments. Photochem. Photobiol. Sci.9, 1435–1443 (2010).20852774 [OpenAIRE] [PubMed]

8 Ehrenberg D., The two-photon reversible reaction of the bistable jumping spider rhodopsin-1. Biophys. J.116, 1248–1258 (2019).30902364 [OpenAIRE] [PubMed]

9 Yan E. C. Y., Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. U.S.A.100, 9262–9267 (2003).12835420 [OpenAIRE] [PubMed]

10 Isberg V., Generic GPCR residue numbers–Aligning topology maps while minding the gaps. Trends Pharmacol. Sci.36, 22–31 (2015).25541108 [OpenAIRE] [PubMed]

11 Ota T., Furutani Y., Terakita A., Shichida Y., Kandori H., Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy. Biochemistry 45, 2845–2851 (2006).16503639 [OpenAIRE] [PubMed]

12 Murakami M., Kouyama T., Crystal structure of squid rhodopsin. Nature 453, 363–367 (2008).18480818 [OpenAIRE] [PubMed]

13 Shimamura T., Crystal structure of squid rhodopsin with intracellularly extended cytoplasmic region. J. Biol. Chem.283, 17753–17756 (2008).18463093 [OpenAIRE] [PubMed]

14 Angel T. E., Chance M. R., Palczewski K., Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A.106, 8555–8560 (2009).19433801 [OpenAIRE] [PubMed]

15 Flock T., Selectivity determinants of GPCR-G-protein binding. Nature 545, 317–322 (2017).28489817 [OpenAIRE] [PubMed]

75 references, page 1 of 5
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