Structure of a Pancreatic ATP-Sensitive Potassium Channel

Cell

Volumn 168, Issue 1-2, 2017, Pages 101-110.e10

  Li, Ningning ^a   Wu, Jing Xiang ^a   Ding, Dian ^a   Cheng, Jiaxuan ^b   Gao, Ning ^b   Chen, Lei ^a  

^a PEKING UNIVERSITY   (China)

^b TSINGHUA UNIVERSITY   (China)

Author keywords

ABCC; glibenclamide; KATP; Kir; PIP2; sulfonylurea; SUR

Indexed keywords

ABC TRANSPORTER; ADENOSINE DIPHOSPHATE MAGNESIUM; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; GLIBENCLAMIDE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SULFONYLUREA RECEPTOR 1; HYDROLASE; INWARDLY RECTIFYING POTASSIUM CHANNEL; MULTIDRUG RESISTANCE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; SULFONYLUREA RECEPTOR;

ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; MOUSE; MUS MUSCULUS; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STOICHIOMETRY; SYRIAN HAMSTER; ANIMAL; CHEMISTRY; MAMMAL; MESOCRICETUS; METABOLISM; MOLECULAR MODEL;

ANIMALS; CRYOELECTRON MICROSCOPY; HUMANS; HYDROLASES; KATP CHANNELS; MAMMALS; MESOCRICETUS; MICE; MODELS, MOLECULAR; P-GLYCOPROTEINS; PHOSPHOINOSITIDE PHOSPHOLIPASE C; POTASSIUM CHANNELS, INWARDLY RECTIFYING; SULFONYLUREA RECEPTORS;

EID: 85009170650     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.12.028     Document Type: Article

References (56)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. Aguilar-Bryan, L., Nichols, C.G., Wechsler, S.W., Clement, J.P. 4th, Boyd, A.E. 3rd, González, G., Herrera-Sosa, H., Nguy, K., Bryan, J., Nelson, D.A., Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268 (1995), 423–426.
3. Aguilar-Bryan, L., Clement, J.P. 4th, Gonzalez, G., Kunjilwar, K., Babenko, A., Bryan, J., Toward understanding the assembly and structure of KATP channels. Physiol. Rev. 78 (1998), 227–245.
4. Aittoniemi, J., Fotinou, C., Craig, T.J., de Wet, H., Proks, P., Ashcroft, F.M., Review. SUR1: a unique ATP-binding cassette protein that functions as an ion channel regulator. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 257–267.
5. Aller, S.G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P.M., Trinh, Y.T., Zhang, Q., Urbatsch, I.L., Chang, G., Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323 (2009), 1718–1722.
6. Antcliff, J.F., Haider, S., Proks, P., Sansom, M.S., Ashcroft, F.M., Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit. EMBO J. 24 (2005), 229–239.
7. Ashcroft, F.M., K(ATP) channels and insulin secretion: a key role in health and disease. Biochem. Soc. Trans. 34 (2006), 243–246.
8. Ashfield, R., Gribble, F.M., Ashcroft, S.J., Ashcroft, F.M., Identification of the high-affinity tolbutamide site on the SUR1 subunit of the K(ATP) channel. Diabetes 48 (1999), 1341–1347.
9. Babenko, A.P., Bryan, J., Sur domains that associate with and gate KATP pores define a novel gatekeeper. J. Biol. Chem. 278 (2003), 41577–41580.
10. Babenko, A.P., Gonzalez, G., Bryan, J., The tolbutamide site of SUR1 and a mechanism for its functional coupling to K(ATP) channel closure. FEBS Lett. 459 (1999), 367–376.
11. Bai, X.C., Rajendra, E., Yang, G., Shi, Y., Scheres, S.H., Sampling the conformational space of the catalytic subunit of human γ-secretase. eLife, 4, 2015, e11182.
12. Baukrowitz, T., Schulte, U., Oliver, D., Herlitze, S., Krauter, T., Tucker, S.J., Ruppersberg, J.P., Fakler, B., PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282 (1998), 1141–1144.
13. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Gallo Cassarino, T., Bertoni, M., Bordoli, L., Schwede, T., SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42 (2014), W252–258.
14. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
15. Flagg, T.P., Enkvetchakul, D., Koster, J.C., Nichols, C.G., Muscle KATP channels: recent insights to energy sensing and myoprotection. Physiol. Rev. 90 (2010), 799–829.
16. Goehring, A., Lee, C.H., Wang, K.H., Michel, J.C., Claxton, D.P., Baconguis, I., Althoff, T., Fischer, S., Garcia, K.C., Gouaux, E., Screening and large-scale expression of membrane proteins in mammalian cells for structural studies. Nat. Protoc. 9 (2014), 2574–2585.
17. Hambrock, A., Löffler-Walz, C., Quast, U., Glibenclamide binding to sulphonylurea receptor subtypes: dependence on adenine nucleotides. Br. J. Pharmacol. 136 (2002), 995–1004.
18. Hansen, S.B., Tao, X., MacKinnon, R., Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477 (2011), 495–498.
19. Hopf, T.A., Colwell, L.J., Sheridan, R., Rost, B., Sander, C., Marks, D.S., Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149 (2012), 1607–1621.
20. Inagaki, N., Gonoi, T., Clement, J.P., Wang, C.Z., Aguilar-Bryan, L., Bryan, J., Seino, S., A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels. Neuron 16 (1996), 1011–1017.
21. Jin, M.S., Oldham, M.L., Zhang, Q., Chen, J., Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 490 (2012), 566–569.
22. Kawate, T., Gouaux, E., Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14 (2006), 673–681.
23. Kimanius, D., Forsberg, B.O., Scheres, S.H., Lindahl, E., Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife, 5, 2016, e18722.
24. Koster, J.C., Sha, Q., Nichols, C.G., Sulfonylurea and K(+)-channel opener sensitivity of K(ATP) channels. Functional coupling of Kir6.2 and SUR1 subunits. J. Gen. Physiol. 114 (1999), 203–213.
25. Krauter, T., Ruppersberg, J.P., Baukrowitz, T., Phospholipids as modulators of K(ATP) channels: distinct mechanisms for control of sensitivity to sulphonylureas, K(+) channel openers, and ATP. Mol. Pharmacol. 59 (2001), 1086–1093.
26. Kucukelbir, A., Sigworth, F.J., Tagare, H.D., Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11 (2014), 63–65.
27. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A., Cheng, Y., Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10 (2013), 584–590.
28. Li, J., Jaimes, K.F., Aller, S.G., Refined structures of mouse P-glycoprotein. Protein Sci. 23 (2014), 34–46.
29. Locher, K.P., Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat. Struct. Mol. Biol. 23 (2016), 487–493.
30. Mikhailov, M.V., Mikhailova, E.A., Ashcroft, S.J., Molecular structure of the glibenclamide binding site of the beta-cell K(ATP) channel. FEBS Lett. 499 (2001), 154–160.
31. Mikhailov, M.V., Campbell, J.D., de Wet, H., Shimomura, K., Zadek, B., Collins, R.F., Sansom, M.S., Ford, R.C., Ashcroft, F.M., 3-D structural and functional characterization of the purified KATP channel complex Kir6.2-SUR1. EMBO J. 24 (2005), 4166–4175.
32. Nichols, C.G., KATP channels as molecular sensors of cellular metabolism. Nature 440 (2006), 470–476.
33. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
34. Pratt, E.B., Tewson, P., Bruederle, C.E., Skach, W.R., Shyng, S.L., N-terminal transmembrane domain of SUR1 controls gating of Kir6.2 by modulating channel sensitivity to PIP2. J. Gen. Physiol. 137 (2011), 299–314.
35. Pratt, E.B., Zhou, Q., Gay, J.W., Shyng, S.L., Engineered interaction between SUR1 and Kir6.2 that enhances ATP sensitivity in KATP channels. J. Gen. Physiol. 140 (2012), 175–187.
36. Quan, Y., Barszczyk, A., Feng, Z.P., Sun, H.S., Current understanding of K ATP channels in neonatal diseases: focus on insulin secretion disorders. Acta Pharmacol. Sin. 32 (2011), 765–780.
37. Reimann, F., Tucker, S.J., Proks, P., Ashcroft, F.M., Involvement of the n-terminus of Kir6.2 in coupling to the sulphonylurea receptor. J. Physiol. 518 (1999), 325–336.
38. Ribalet, B., John, S.A., Weiss, J.N., Molecular basis for Kir6.2 channel inhibition by adenine nucleotides. Biophys. J. 84 (2003), 266–276.
39. Rohou, A., Grigorieff, N., CTFFIND4: Fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192 (2015), 216–221.
40. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
41. Schwappach, B., Zerangue, N., Jan, Y.N., Jan, L.Y., Molecular basis for K(ATP) assembly: transmembrane interactions mediate association of a K+ channel with an ABC transporter. Neuron 26 (2000), 155–167.
42. Seino, S., ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu. Rev. Physiol. 61 (1999), 337–362.
43. Shaikh, T.R., Gao, H., Baxter, W.T., Asturias, F.J., Boisset, N., Leith, A., Frank, J., SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 3 (2008), 1941–1974.
44. Shimomura, K., Girard, C.A., Proks, P., Nazim, J., Lippiat, J.D., Cerutti, F., Lorini, R., Ellard, S., Hattersley, A.T., Barbetti, F., Ashcroft, F.M., Mutations at the same residue (R50) of Kir6.2 (KCNJ11) that cause neonatal diabetes produce different functional effects. Diabetes 55 (2006), 1705–1712.
45. Shyng, S.L., Nichols, C.G., Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282 (1998), 1138–1141.
46. Tucker, S.J., Gribble, F.M., Zhao, C., Trapp, S., Ashcroft, F.M., Truncation of Kir6.2 produces ATP-sensitive K+ channels in the absence of the sulphonylurea receptor. Nature 387 (1997), 179–183.
47. Vedovato, N., Ashcroft, F.M., Puljung, M.C., The nucleotide-binding sites of SUR1: a mechanistic model. Biophys. J. 109 (2015), 2452–2460.
48. Vila-Carriles, W.H., Zhao, G., Bryan, J., Defining a binding pocket for sulfonylureas in ATP-sensitive potassium channels. FASEB J. 21 (2007), 18–25.
49. Virág, L., Furukawa, T., Hiraoka, M., Modulation of the effect of glibenclamide on KATP channels by ATP and ADP. Mol. Cell. Biochem. 119 (1993), 209–215.
50. Whorton, M.R., MacKinnon, R., Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147 (2011), 199–208.
51. Whorton, M.R., MacKinnon, R., X-ray structure of the mammalian GIRK2-βγ G-protein complex. Nature 498 (2013), 190–197.
52. Woo, S.K., Kwon, M.S., Ivanov, A., Gerzanich, V., Simard, J.M., The sulfonylurea receptor 1 (Sur1)-transient receptor potential melastatin 4 (Trpm4) channel. J. Biol. Chem. 288 (2013), 3655–3667.
53. Zerangue, N., Schwappach, B., Jan, Y.N., Jan, L.Y., A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22 (1999), 537–548.
54. Zhang, Z., Chen, J., Atomic structure of the cystic fibrosis transmembrane conductance regulator. Cell 167 (2016), 1586–1597.
55. Zheng, S., Palovcak, E., Armache, J.-P., Cheng, Y., Agard, D., Anisotropic correction of beam-induced motion for improved single-particle electron cryo-microscopy. bioRxiv, 2016, 10.1101/061960.
56. Zhou, M., Li, Y., Hu, Q., Bai, X.C., Huang, W., Yan, C., Scheres, S.H., Shi, Y., Atomic structure of the apoptosome: mechanism of cytochrome c- and dATP-mediated activation of Apaf-1. Genes Dev. 29 (2015), 2349–2361.