Functional Role of Arrestin-1 Residues Interacting with Unphosphorylated Rhodopsin Elements
Abstract
:1. Introduction
2. Results
2.1. β-Strand VI
2.2. The C-Loop
2.3. Back Loop Residues That Contact Rhodopsin in the Structure
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Mutagenesis and Plasmid Construction
4.3. Direct Binding Assay
4.4. Data Analysis and Statistics
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Gurevich, V.V.; Gurevich, E.V. The molecular acrobatics of arrestin activation. Trends Pharmacol. Sci. 2004, 25, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V.; Benovic, J.L. Cell-free expression of visual arrestin. Truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J. Biol. Chem. 1992, 267, 21919–21923. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V.; Benovic, J.L. Visual arrestin interaction with rhodopsin: Sequential multisite binding ensures strict selectivity towards light-activated phosphorylated rhodopsin. J. Biol. Chem. 1993, 268, 11628–11638. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V.; Benovic, J.L. Visual arrestin binding to rhodopsin: Diverse functional roles of positively charged residues within the phosphorylation-recignition region of arrestin. J. Biol. Chem. 1995, 270, 6010–6016. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V.; Benovic, J.L. Mechanism of phosphorylation-recognition by visual arrestin and the transition of arrestin into a high affinity binding state. Mol. Pharmacol. 1997, 51, 161–169. [Google Scholar] [CrossRef]
- Gray-Keller, M.P.; Detwiler, P.B.; Benovic, J.L.; Gurevich, V.V. Arrestin with a single amino acid substitution quenches light-activated rhodopsin in a phosphorylation-independent fasion. Biochemistry 1997, 36, 7058–7063. [Google Scholar] [CrossRef]
- Gurevich, V.V.; Pals-Rylaarsdam, R.; Benovic, J.L.; Hosey, M.M.; Onorato, J.J. Agonist-receptor-arrestin, an alternative ternary complex with high agonist affinity. J. Biol. Chem. 1997, 272, 28849–28852. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Schubert, C.; Climaco, G.C.; Gurevich, Y.V.; Velez, M.-G.; Gurevich, V.V. An additional phosphate-binding element in arrestin molecule: Implications for the mechanism of arrestin activation. J. Biol. Chem. 2000, 275, 41049–41057. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Zheng, C.; May, M.B.; Karnam, P.C.; Gurevich, E.V.; Gurevich, V.V. Lysine in the lariat loop of arrestins does not serve as phosphate sensor. J. Neurochem. 2021, 156, 435–444. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Paz, C.L.; Schubert, C.; Hirsch, J.A.; Sigler, P.B.; Gurevich, V.V. How does arrestin respond to the phosphorylated state of rhodopsin? J. Biol. Chem. 1999, 274, 11451–11454. [Google Scholar] [CrossRef]
- Zhou, X.E.; He, Y.; de Waal, P.W.; Gao, X.; Kang, Y.; Van Eps, N.; Yin, Y.; Pal, K.; Goswami, D.; White, T.A.; et al. Identification of Phosphorylation Codes for Arrestin Recruitment by G protein-Coupled Receptors. Cell 2017, 170, 457–469. [Google Scholar] [CrossRef] [PubMed]
- Pan, L.; Gurevich, E.V.; Gurevich, V.V. The nature of the arrestin x receptor complex determines the ultimate fate of the internalized receptor. J. Biol. Chem. 2003, 278, 11623–11632. [Google Scholar] [CrossRef] [PubMed]
- Kovoor, A.; Celver, J.; Abdryashitov, R.I.; Chavkin, C.; Gurevich, V.V. Targeted construction of phosphorylation-independent b-arrestin mutants with constitutive activity in cells. J. Biol. Chem. 1999, 274, 6831–6834. [Google Scholar] [CrossRef] [PubMed]
- Celver, J.; Vishnivetskiy, S.A.; Chavkin, C.; Gurevich, V.V. Conservation of the phosphate-sensitive elements in the arrestin family of proteins. J. Biol. Chem. 2002, 277, 9043–9048. [Google Scholar] [CrossRef]
- Hirsch, J.A.; Schubert, C.; Gurevich, V.V.; Sigler, P.B. The 2.8 A crystal structure of visual arrestin: A model for arrestin’s regulation. Cell 1999, 97, 257–269. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Huh, E.K.; Gurevich, E.V.; Gurevich, V.V. The finger loop as an activation sensor in arrestin. J. Neurochem. 2021, 157, 1138–1152. [Google Scholar] [CrossRef]
- Chen, Q.; Perry, N.A.; Vishnivetskiy, S.A.; Berndt, S.; Gilbert, N.C.; Zhuo, Y.; Singh, P.K.; Tholen, J.; Ohi, M.D.; Gurevich, E.V.; et al. Structural basis of arrestin-3 activation and signaling. Nat. Commun. 2017, 8, 1427. [Google Scholar] [CrossRef]
- Zheng, C.; Tholen, J.; Gurevich, V.V. Critical role of the finger loop in arrestin binding to the receptors. PLoS ONE 2019, 14, e0213792. [Google Scholar] [CrossRef]
- Peterhans, C.; Lally, C.C.; Ostermaier, M.K.; Sommer, M.E.; Standfuss, J. Functional map of arrestin binding to phosphorylated opsin, with and without agonist. Sci. Rep. 2016, 6, 28686. [Google Scholar] [CrossRef]
- Ostermaier, M.K.; Peterhans, C.; Jaussi, R.; Deupi, X.; Standfuss, J. Functional map of arrestin-1 at single amino acid resolution. Proc. Natl. Acad. Sci. USA 2014, 111, 1825–1830. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Huh, E.K.; Karnam, P.C.; Oviedo, S.; Gurevich, E.V.; Gurevich, V.V. The Role of arrestin-1 middle loop in rhodopsin binding. Int. J. Mol. Sci. 2022, 23, 13887. [Google Scholar] [CrossRef] [PubMed]
- Kang, Y.; Zhou, X.E.; Gao, X.; He, Y.; Liu, W.; Ishchenko, A.; Barty, A.; White, T.A.; Yefanov, O.; Han, G.W.; et al. Crystal structure of rhodopsin bound to arrestin determined by femtosecond X-ray laser. Nature 2015, 523, 561–567. [Google Scholar] [CrossRef] [PubMed]
- Yin, W.; Li, Z.; Jin, M.; Yin, Y.L.; de Waal, P.W.; Pal, K.; Yin, Y.; Gao, X.; He, Y.; Gao, J.; et al. A complex structure of arrestin-2 bound to a G protein-coupled receptor. Cell Res. 2019, 29, 971–983. [Google Scholar] [CrossRef] [PubMed]
- Staus, D.P.; Hu, H.; Robertson, M.J.; Kleinhenz, A.L.W.; Wingler, L.M.; Capel, W.D.; Latorraca, N.R.; Lefkowitz, R.J.; Skiniotis, G. Structure of the M2 muscarinic receptor-β-arrestin complex in a lipid nanodisc. Nature 2020, 579, 297–302. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.; Warne, T.; Nehmé, R.; Pandey, S.; Dwivedi-Agnihotri, H.; Chaturvedi, M.; Edwards, P.C.; García-Nafría, J.; Leslie, A.G.W.; Shukla, A.K.; et al. Molecular basis of β-arrestin coupling to formoterol-bound β(1)-adrenoceptor. Nature 2020, 583, 862–866. [Google Scholar] [CrossRef]
- Huang, W.; Masureel, M.; Qianhui, Q.; Janetzko, J.; Inoue, A.; Kato, H.E.; Robertson, M.J.; Nguyen, K.C.; Glenn, J.S.; Skiniotis, G.; et al. Structure of the neurotensin receptor 1 in complex with β-arrestin 1. Nature 2020, 579, 303–308. [Google Scholar] [CrossRef]
- Bous, J.; Fouillen, A.; Orcel, H.; Trapani, S.; Cong, X.; Fontanel, S.; Saint-Paul, J.; Lai-Kee-Him, J.; Urbach, S.; Sibille, N.; et al. Structure of the vasopressin hormone-V2 receptor-β-arrestin1 ternary complex. Sci. Adv. 2022, 8, eabo7761. [Google Scholar] [CrossRef]
- Cao, C.; Barros-Álvarez, X.; Zhang, S.; Kim, K.; Dämgen, M.A.; Panova, O.; Suomivuori, C.M.; Fay, J.F.; Zhong, X.; Krumm, B.E.; et al. Signaling snapshots of a serotonin receptor activated by the prototypical psychedelic LSD. Neuron 2022, 110, 3154–3167. [Google Scholar] [CrossRef]
- Palczewski, K.; Buczyłko, J.; Imami, N.R.; McDowell, J.H.; Hargrave, P.A. Role of the carboxyl-terminal region of arrestin in binding to phosphorylated rhodopsin. J. Biol. Chem. 1991, 266, 15334–15339. [Google Scholar] [CrossRef]
- Kim, M.; Vishnivetskiy, S.A.; Van Eps, N.; Alexander, N.S.; Cleghorn, W.M.; Zhan, X.; Hanson, S.M.; Morizumi, T.; Ernst, O.P.; Meiler, J.; et al. Conformation of receptor-bound visual arrestin. Proc. Nat. Acad. Sci. USA 2012, 109, 18407–18412. [Google Scholar] [CrossRef]
- Hanson, S.M.; Francis, D.J.; Vishnivetskiy, S.A.; Kolobova, E.A.; Hubbell, W.L.; Klug, C.S.; Gurevich, V.V. Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc. Natl. Acad. Sci. USA 2006, 103, 4900–4905. [Google Scholar] [CrossRef] [PubMed]
- Vishnivetskiy, S.A.; Francis, D.J.; Van Eps, N.; Kim, M.; Hanson, S.M.; Klug, C.S.; Hubbell, W.L.; Gurevich, V.V. The role of arrestin alpha-helix I in receptor binding. J. Mol. Biol. 2010, 395, 42–54. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V. The selectivity of visual arrestin for light-activated phosphorhodopsin is controlled by multiple nonredundant mechanisms. J. Biol. Chem. 1998, 273, 15501–15506. [Google Scholar] [CrossRef] [PubMed]
- Vishnivetskiy, S.A.; Gimenez, L.E.; Francis, D.J.; Hanson, S.M.; Hubbell, W.L.; Klug, C.S.; Gurevich, V.V. Few residues within an extensive binding interface drive receptor interaction and determine the specificity of arrestin proteins. J. Biol. Chem. 2011, 286, 24288–24299. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Hosey, M.M.; Benovic, J.L.; Gurevich, V.V. Mapping the arrestin-receptor interface: Structural elements responsible for receptor specificity of arrestin proteins. J. Biol. Chem. 2004, 279, 1262–1268. [Google Scholar] [CrossRef]
- Indrischek, H.; Prohaska, S.J.; Gurevich, V.V.; Gurevich, E.V.; Stadler, P.F. Uncovering missing pieces: Duplication and deletion history of arrestins in deuterostomes. BMC Evol. Biol. 2017, 17, 163. [Google Scholar] [CrossRef]
- Gurevich, V.V.; Dion, S.B.; Onorato, J.J.; Ptasienski, J.; Kim, C.M.; Sterne-Marr, R.; Hosey, M.M.; Benovic, J.L. Arrestin interaction with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, b2-adrenergic, and m2 muscarinic cholinergic receptors. J. Biol. Chem. 1995, 270, 720–731. [Google Scholar] [CrossRef]
- Jacobson, S.G.; Kemp, C.M.; Cideciyan, A.V.; Macke, J.P.; Sung, C.H.; Nathans, J. Phenotypes of stop codon and splice site rhodopsin mutations causing retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 1994, 35, 2521–2534. [Google Scholar]
- Concepcion, F.; Chen, J. Q344ter mutation causes mislocalization of rhodopsin molecules that are catalytically active: A mouse model of Q344ter-induced retinal degeneration. PLoS ONE 2010, 5, e10904. [Google Scholar] [CrossRef]
- Khani, S.C.; Nielsen, L.; Vogt, T.M. Biochemical evidence for pathogenicity of rhodopsin kinase mutations correlated with the oguchi form of congenital stationary night blindness. Proc. Natl. Acad. Sci. USA 1998, 95, 2824–2827. [Google Scholar] [CrossRef]
- Cideciyan, A.V.; Zhao, X.; Nielsen, L.; Khani, S.C.; Jacobson, S.G.; Palczewski, K. Null mutation in the rhodopsin kinase gene slows recovery kinetics of rod and cone phototransduction in man. Proc. Natl. Acad. Sci. USA 1998, 95, 328–333. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, S.; Sippel, K.C.; Berson, E.L.; Dryja, T.P. Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat. Genet. 1997, 15, 175–178. [Google Scholar] [CrossRef] [PubMed]
- Gurevich, V.V. Use of bacteriophage RNA polymerase in RNA synthesis. Methods Enzymol. 1996, 275, 382–397. [Google Scholar] [PubMed]
- Vishnivetskiy, S.A.; Lee, R.J.; Zhou, X.E.; Franz, A.; Xu, Q.; Xu, H.E.; Gurevich, V.V. Functional role of the three conserved cysteines in the N domain of visual arrestin-1. J. Biol. Chem. 2017, 292, 12496–12502. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Chen, Q.; Palazzo, M.C.; Brooks, E.K.; Altenbach, C.; Iverson, T.M.; Hubbell, W.L.; Gurevich, V.V. Engineering visual arrestin-1 with special functional characteristics. J. Biol. Chem. 2013, 288, 11741–11750. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Sullivan, L.S.; Bowne, S.J.; Daiger, S.P.; Gurevich, E.V.; Gurevich, V.V. Molecular Defects of the Disease-Causing Human Arrestin-1 C147F Mutant. Invest. Ophthalmol. Vis. Sci. 2018, 59, 13–20. [Google Scholar] [CrossRef]
- Gurevich, V.V.; Benovic, J.L. Arrestin: Mutagenesis, expression, purification, and functional characterization. Methods Enzymol. 2000, 315, 422–437. [Google Scholar]
- Lee, K.B.; Ptasienski, J.A.; Pals-Rylaarsdam, R.; Gurevich, V.V.; Hosey, M.M. Arrestin binding to the M2 muscarinic acetylcholine receptor is precluded by an inhibitory element in the third intracellular loop of the receptor. J. Biol. Chem. 2000, 275, 9284–9289. [Google Scholar] [CrossRef]
- Vishnivetskiy, S.A.; Baameur, F.; Findley, K.R.; Gurevich, V.V. Critical role of the central 139-loop in stability and binding selectivity of arrestin-1. J. Biol. Chem. 2013, 288, 11741–11750. [Google Scholar] [CrossRef]
- Zhuo, Y.; Vishnivetskiy, S.A.; Zhan, X.; Gurevich, V.V.; Klug, C.S. Identification of receptor binding-induced conformational changes in non-visual arrestins. J. Biol. Chem. 2014, 289, 20991–21002. [Google Scholar] [CrossRef]
- Zhuang, T.; Chen, Q.; Cho, M.-K.; Vishnivetskiy, S.A.; Iverson, T.I.; Gurevich, V.V.; Hubbell, W.L. Involvement of Distinct Arrestin-1 Elements in Binding to Different Functional Forms of Rhodopsin. Proc. Nat. Acad. Sci. USA 2013, 110, 942–947. [Google Scholar] [CrossRef] [PubMed]
- Böttke, T.; Ernicke, S.; Serfling, R.; Ihling, C.; Burda, E.; Gurevich, V.V.; Sinz, A.; Coin, I. Exploring GPCR-arrestin interfaces with genetically encoded crosslinkers. EMBO Rep. 2020, 21, e50437. [Google Scholar] [CrossRef] [PubMed]
- Aydin, Y.; Böttke, T.; Lam, J.H.; Ernicke, S.; Fortmann, A.; Tretbar, M.; Zarzycka, B.; Gurevich, V.V.; Katritch, V.; Coin, I. Structural details of a class B GPCR-arrestin complex revealed by genetically encoded crosslinkers in living cells. Nat. Commun. 2023, 14, 1151. [Google Scholar] [CrossRef] [PubMed]
Mutation | WT/P-Rh* | WT/Rh* | Tr/P-Rh* | Tr/Rh* |
---|---|---|---|---|
D82A | ↑ *** | ↓ * | ||
D82R | ↑ *** | ↑ *** | ↓ *** | ↓ * |
L83A | ↑ ** | ↓↓ *** | ||
Y84A | ↑ * | |||
Y84F | ||||
F85A | ↑ *** | |||
S86A | ↑ * | |||
Q87A | ↑ ** | ↑ *** | ||
V88A | ↓ *** | ↓ ** | ||
Q89A | ↑ * | ↓ *** | ↓ *** | |
L249A | ↓ * | ↓ ** | ↑ *** | ↓ *** |
Y250A | ↓ * | ↓ *** | ↑ ** | ↓ *** |
S251A | ↓ *** | ↓ ** | ||
D253A | ↓ *** | ↓ *** | ||
D253R | ↓ *** | ↑ *** | ||
Y254A | ↓ * | |||
Y254F | ||||
R291A | ↑ *** | ↑ *** | ↑ ** | ↑ *** |
R291E | ↑ * | ↑ *** | ||
T319A | ||||
T319E | ↓ *** | ↓ *** | ↑ ** | ↑ *** |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Vishnivetskiy, S.A.; Weinstein, L.D.; Zheng, C.; Gurevich, E.V.; Gurevich, V.V. Functional Role of Arrestin-1 Residues Interacting with Unphosphorylated Rhodopsin Elements. Int. J. Mol. Sci. 2023, 24, 8903. https://doi.org/10.3390/ijms24108903
Vishnivetskiy SA, Weinstein LD, Zheng C, Gurevich EV, Gurevich VV. Functional Role of Arrestin-1 Residues Interacting with Unphosphorylated Rhodopsin Elements. International Journal of Molecular Sciences. 2023; 24(10):8903. https://doi.org/10.3390/ijms24108903
Chicago/Turabian StyleVishnivetskiy, Sergey A., Liana D. Weinstein, Chen Zheng, Eugenia V. Gurevich, and Vsevolod V. Gurevich. 2023. "Functional Role of Arrestin-1 Residues Interacting with Unphosphorylated Rhodopsin Elements" International Journal of Molecular Sciences 24, no. 10: 8903. https://doi.org/10.3390/ijms24108903