Engineering of an artificial light-modulated potassium channel

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Caro, Lydia N ^a,b,c,d   Moreau, Christophe J ^a,b,c   Estrada Mondragón, Argel ^a,b,c   Ernst, Oliver P ^d   Vivaudou, Michel ^a,b,c  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b CEA GRENOBLE   (France)

^c UNIV GRENOBLE ALPES   (France)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

11 CIS RETINAL; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HYBRID PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; OPSIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KIR3.1; RETINAL; RHODOPSIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONTROLLED STUDY; ILLUMINATION; NONHUMAN; OOCYTE; PHOTOSTIMULATION; PROTEIN ANALYSIS; PROTEIN ENGINEERING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VOLTAGE CLAMP; XENOPUS;

ANIMALS; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; LIGHT; OOCYTES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN ENGINEERING; RECOMBINANT FUSION PROTEINS; RHODOPSIN; XENOPUS LAEVIS;

EID: 84865171826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043766     Document Type: Article

References (52)

1. Li J, Edwards PC, Burghammer M, Villa C, Schertler GF, ((2004)) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343:: 1409--38.
2. Okada T, Sugihara M, Bondar AN, Elstner M, Entel P, et al. ((2004)) The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J Mol Biol 342:: 571--83.
3. Salom D, Lodowski DT, Stenkamp RE, Le Trong I, Golczak M, et al. ((2006)) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci U S A 103:: 16123--8.
4. Choe HW, Kim YJ, Park JH, Morizumi T, Pai EF, et al. ((2011)) Crystal structure of metarhodopsin II. Nature 471:: 651--5.
5. Standfuss J, Edwards PC, D'Antona A, Fransen M, Xie G, et al. ((2011)) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471:: 656--60.
6. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, et al. ((2000)) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289:: 739--45.
7. Park JH, Scheerer P, Hofmann KP, Choe HW, Ernst OP, ((2008)) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454:: 183--7.
8. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, et al. ((2008)) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455:: 497--502.
9. Deupi X, Edwards P, Singhal A, Nickle B, Oprian D, et al. ((2012)) Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc Natl Acad Sci U S A 109:: 119--24.
10. Sui JL, Chan K, Langan MN, Vivaudou M, Logothetis DE, ((1999)) G protein gated potassium channels. Adv Second Messenger Phosphoprotein Res 33:: 179--201.
11. Chan KW, Sui JL, Vivaudou M, Logothetis DE, ((1996)) Control of channel activity through a unique amino acid residue of a G protein-gated inwardly rectifying K+ channel subunit. Proc Natl Acad Sci U S A 93:: 14193--8.
12. Vivaudou M, Chan KW, Sui JL, Jan LY, Reuveny E, et al. ((1997)) Probing the G-protein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J Biol Chem 272:: 31553--60.
13. Lim NF, Dascal N, Labarca C, Davidson N, Lester HA, ((1995)) A G protein-gated K channel is activated via beta 2-adrenergic receptors and G beta gamma subunits in Xenopus oocytes. J Gen Physiol 105:: 421--39.
14. McAllister SD, Griffin G, Satin LS, Abood ME, ((1999)) Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a xenopus oocyte expression system. J Pharmacol Exp Ther 291:: 618--26.
15. Madani N, Kozak SL, Kavanaugh MP, Kabat D, ((1998)) gp120 envelope glycoproteins of human immunodeficiency viruses competitively antagonize signaling by coreceptors CXCR4 and CCR5. Proc Natl Acad Sci U S A 95:: 8005--10.
16. Werner P, Hussy N, Buell G, Jones KA, North RA, ((1996)) D2, D3, and D4 dopamine receptors couple to G protein-regulated potassium channels in Xenopus oocytes. Mol Pharmacol 49:: 656--61.
17. Sahlholm K, Nilsson J, Marcellino D, Fuxe K, Arhem P, ((2007)) The human histamine H3 receptor couples to GIRK channels in Xenopus oocytes. Eur J Pharmacol 567:: 206--10.
18. Saugstad JA, Segerson TP, Westbrook GL, ((1996)) Metabotropic glutamate receptors activate G-protein-coupled inwardly rectifying potassium channels in Xenopus oocytes. J Neurosci 16:: 5979--85.
19. Khorana HG, Knox BE, Nasi E, Swanson R, Thompson DA, ((1988)) Expression of a bovine rhodopsin gene in Xenopus oocytes: demonstration of light-dependent ionic currents. Proc Natl Acad Sci U S A 85:: 7917--21.
20. Knox BE, Khorana HG, Nasi E, ((1993)) Light-induced currents in Xenopus oocytes expressing bovine rhodopsin. J Physiol 466:: 157--72.
21. Moreau CJ, Dupuis JP, Revilloud J, Arumugam K, Vivaudou M, ((2008)) Coupling ion channels to receptors for biomolecule sensing. Nat Nanotechnol 3:: 620--5.
22. Caro LN, Moreau CJ, Revilloud J, Vivaudou M, ((2011)) ß2-Adrenergic ion-channel coupled receptors as conformational motion detectors. PloS ONE 6:: e18226.
23. Caro LN, Moreau CJ, Estrada-Mondragon A, Revilloud J, Vivaudou M, ((2012)) Ion-Channel Coupled Receptors: New Tools for the Study of Receptors and Channels. Biophys J 102:: 539a.
24. Piechnick R, Ritter E, Hildebrand PW, Ernst OP, Scheerer P, et al. ((2012)) Effect of channel mutations on the uptake and release of the retinal ligand in opsin. Proc Natl Acad Sci U S A 109:: 5247--52.
25. Orsini F, Santacroce M, Arosio P, Castagna M, Lenardi C, et al. ((2009)) Intermittent contact mode AFM investigation of native plasma membrane of Xenopus laevis oocyte. Eur Biophys J 38:: 903--10.
26. Ernst OP, Gramse V, Kolbe M, Hofmann KP, Heck M, ((2007)) Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit. Proc Natl Acad Sci U S A 104:: 10859--64.
27. Bayburt TH, Leitz AJ, Xie G, Oprian DD, Sligar SG, ((2007)) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J Biol Chem 282:: 14875--81.
28. Banerjee S, Huber T, Sakmar TP, ((2008)) Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles. J Mol Biol 377:: 1067--81.
29. Whorton MR, Jastrzebska B, Park PS, Fotiadis D, Engel A, et al. ((2008)) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283:: 4387--94.
30. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, et al. ((2003)) Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421:: 127--8.
31. Palczewski K, ((2006)) G protein-coupled receptor rhodopsin. Annu Rev Biochem 75:: 743--67.
32. Govardovskii VI, Korenyak DA, Shukolyukov SA, Zueva LV, ((2009)) Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal. Mol Vis 15:: 1717--29.
33. Terakita A, Yamashita T, Nimbari N, Kojima D, Shichida Y, ((2002)) Functional interaction between bovine rhodopsin and G protein transducin. J Biol Chem 277:: 40--6.
34. Li X, Gutierrez DV, Hanson MG, Han J, Mark MD, et al. ((2005)) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A 102:: 17816--21.
35. Mangmool S, Kurose H, ((2011)) G(i/o) Protein-Dependent and-Independent Actions of Pertussis Toxin (PTX). Toxins 3:: 884--99.
36. Moreau C, Prost AL, Dérand R, Vivaudou M, ((2005)) SUR, ABC proteins targeted by KATP channel openers. J Mol Cell Cardiol 38:: 951--63.
37. Hosy E, Dupuis JP, Vivaudou M, ((2010)) Impact of disease-causing SUR1 mutations on the KATP channel subunit interface probed with a rhodamine protection assay. J Biol Chem 285:: 3084--91.
38. Bornancin F, Franco M, Bigay J, Chabre M, ((1992)) Functional modifications of transducin induced by cholera or pertussis-toxin-catalyzed ADP-ribosylation. Eur J Biochem 210:: 33--44.
39. Franke RR, König B, Sakmar TP, Khorana HG, Hofmann KP, ((1990)) Rhodopsin mutants that bind but fail to activate transducin. Science 250:: 123--5.
40. Franke RR, Sakmar TP, Graham RM, Khorana HG, ((1992)) Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin. J Biol Chem 267:: 14767--74.
41. Bünemann M, Frank M, Lohse MJ, ((2003)) Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc Natl Acad Sci U S A 100:: 16077--82.
42. Lambert NA, ((2008)) Dissociation of heterotrimeric G proteins in cells. Sci Signal 1:: re5.
43. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, et al. ((2011)) Structure of a nanobody-stabilized active state of the ß(2) adrenoceptor. Nature 469:: 175--80.
44. Xu F, Wu H, Katritch V, Han GW, Jacobson KA, et al. ((2011)) Structure of an agonist-bound human A2A adenosine receptor. Science 332:: 322--7.
45. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, et al. ((2011)) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474:: 521--5.
46. Farrens DL, Altenbach C, Yang K, Hubbell WL, Khorana HG, ((1996)) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274:: 768--70.
47. Altenbach C, Kusnetzow AK, Ernst OP, Hofmann KP, Hubbell WL, ((2008)) High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation. Proc Natl Acad Sci U S A 105:: 7439--44.
48. Lin YW, MacMullen C, Ganguly A, Stanley CA, Shyng SL, ((2006)) A novel KCNJ11 mutation associated with congenital hyperinsulinism reduces the intrinsic open probability of beta-cell ATP-sensitive potassium channels. J Biol Chem 281:: 3006--12.
49. Nichols CG, ((2006)) KATP channels as molecular sensors of cellular metabolism. Nature 440:: 470--6.
50. Sakmar TP, Franke RR, Khorana HG, ((1989)) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci U S A 86:: 8309--13.
51. Chan KW, Zhang H, Logothetis DE, ((2003)) N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J 22:: 3833--43.
52. Knowles A, Priestley A, ((1978)) The preparation of 11-cis-retinal. Vision Res 18:: 115--6.