Structural basis for cyclic-nucleotide selectivity and cGMP-selective activation of PKG i

Structure

Volumn 22, Issue 1, 2014, Pages 116-124

  Huang, Gilbert Y ^a   Kim, Jeong Joo ^a   Reger, Albert S ^a   Lorenz, Robin ^b   Moon, Eui Whan ^a   Zhao, Chi ^c   Casteel, Darren E ^d   Bertinetti, Daniela ^b   Vanschouwen, Bryan ^e   Selvaratnam, Rajeevan ^e   Pflugrath, James W ^f   Sankaran, Banumathi ^g   Melacini, Giuseppe ^e   Herberg, Friedrich W ^b   Kim, Choel ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF KASSEL   (Germany)

^c RICE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e MCMASTER UNIVERSITY   (Canada)

^f RIGAKU CORPORATION   (Japan)

^g LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC NUCLEOTIDE; GUANINE; CYCLIC AMP BINDING PROTEIN; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; HUMAN CELL; HYDROGEN BOND; MUTAGENESIS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; AORTA ANEURYSM; CAPPING PHENOMENON; DIMERIZATION; EC50; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; HEART; SCANNING ELECTRON MICROSCOPY; SMOOTH MUSCLE CONTRACTION; UNITED STATES;

AMINO ACID SEQUENCE; ARGININE; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYCLIC AMP; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; ESCHERICHIA COLI; GENE EXPRESSION; HEK293 CELLS; HUMANS; KINETICS; LEUCINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; THERMODYNAMICS;

EID: 84891859938     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.09.021     Document Type: Article

References (43)

1. P.V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, M. Mustyakimov, T.C. Terwilliger, A. Urzhumtsev, P.H. Zwart, and P.D. Adams Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr. D Biol. Crystallogr. 68 2012 352 367
2. V. Alverdi, H. Mazon, C. Versluis, W. Hemrika, G. Esposito, R. van den Heuvel, A. Scholten, and A.J. Heck cGMP-binding prepares PKG for substrate binding by disclosing the C-terminal domain J. Mol. Biol. 375 2008 1380 1393
3. A. Bahrami, A.H. Assadi, J.L. Markley, and H.R. Eghbalnia Probabilistic interaction network of evidence algorithm and its application to complete labeling of peak lists from protein NMR spectroscopy PLoS Comput. Biol. 5 2009 e1000307
4. J.A. Beavo, and L.L. Brunton Cyclic nucleotide research - still expanding after half a century Nat. Rev. Mol. Cell Biol. 3 2002 710 718
5. H.M. Berman, L.F. Ten Eyck, D.S. Goodsell, N.M. Haste, A. Kornev, and S.S. Taylor The cAMP binding domain: an ancient signaling module Proc. Natl. Acad. Sci. USA 102 2005 45 50
6. T.I. Brelidze, A.E. Carlson, B. Sankaran, and W.N. Zagotta Structure of the carboxy-terminal region of a KCNH channel Nature 481 2012 530 533
7. E. Brickman, L. Soll, and J. Beckwith Genetic characterization of mutations which affect catabolite-sensitive operons in Escherichia coli, including deletions of the gene for adenyl cyclase J. Bacteriol. 116 1973 582 587
8. K. Büssow, C. Scheich, V. Sievert, U. Harttig, J. Schultz, B. Simon, P. Bork, H. Lehrach, and U. Heinemann Structural genomics of human proteins - target selection and generation of a public catalogue of expression clones Microb. Cell Fact. 4 2005 21
9. T.L. Cornwell, E. Arnold, N.J. Boerth, and T.M. Lincoln Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP Am. J. Physiol. 267 1994 C1405 C1413
10. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
11. T.C. Diller, Madhusudan, N.H. Xuong, and S.S. Taylor Molecular basis for regulatory subunit diversity in cAMP-dependent protein kinase: crystal structure of the type II beta regulatory subunit Structure 9 2001 73 82
12. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
13. S.H. Francis, and J.D. Corbin Cyclic nucleotide-dependent protein kinases: intracellular receptors for cAMP and cGMP action Crit. Rev. Clin. Lab. Sci. 36 1999 275 328
14. S.H. Francis, J.L. Busch, J.D. Corbin, and D. Sibley cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action Pharmacol. Rev. 62 2010 525 563
15. T.D. Goddard, and D.G. Kneller SPARKY-NMR Assignment and Integration Software 2006 University of California San Francisco
16. D.C. Guo, E. Regalado, D.E. Casteel, R.L. Santos-Cortez, L. Gong, J.J. Kim, S. Dyack, S.G. Horne, G. Chang, and G. Jondeau et al. Recurrent gain-of-function mutation in PRKG1 causes thoracic aortic aneurysms and acute aortic dissections Am. J. Hum. Genet. 2013 10.1016/j.ajhg.2013.06.019 Published online July 30, 2013
17. M.H. Huang, P.R. Knight 3rd, and J.L. Izzo Jr. Ca2+-induced Ca2+ release involved in positive inotropic effect mediated by CGRP in ventricular myocytes Am. J. Physiol. 276 1999 R259 R264
18. H. Jiang, J.L. Colbran, S.H. Francis, and J.D. Corbin Direct evidence for cross-activation of cGMP-dependent protein kinase by cAMP in pig coronary arteries J. Biol. Chem. 267 1992 1015 1019
19. B. Johnsson, S. Löfås, and G. Lindquist Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors Anal. Biochem. 198 1991 268 277
20. J.J. Kim, D.E. Casteel, G. Huang, T.H. Kwon, R.K. Ren, P. Zwart, J.J. Headd, N.G. Brown, D.C. Chow, T. Palzkill, and C. Kim Co-crystal structures of PKG Iβ (92-227) with cGMP and cAMP reveal the molecular details of cyclic-nucleotide binding PLoS ONE 6 2011 e18413
21. P. Komalavilas, and T.M. Lincoln Phosphorylation of the inositol 1,4,5-trisphosphate receptor. Cyclic GMP-dependent protein kinase mediates cAMP and cGMP dependent phosphorylation in the intact rat aorta J. Biol. Chem. 271 1996 21933 21938
22. G. Langer, S.X. Cohen, V.S. Lamzin, and A. Perrakis Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3 2008 1171 1179
23. J.H. Lee, S. Li, T. Liu, S. Hsu, C. Kim, V.L. Woods Jr., and D.E. Casteel The amino terminus of cGMP-dependent protein kinase Iβ increases the dynamics of the protein's cGMP-binding pockets Int. J. Mass Spectrom. 302 2011 44 52
24. M.J. Marques-Carvalho, N. Sahoo, F.W. Muskett, R.S. Vieira-Pires, G. Gabant, M. Cadene, R. Schönherr, and J.H. Morais-Cabral Structural, biochemical, and functional characterization of the cyclic nucleotide binding homology domain from the mouse EAG1 potassium channel J. Mol. Biol. 423 2012 34 46
25. W. Minor, M. Cymborowski, Z. Otwinowski, and M. Chruszcz HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. D Biol. Crystallogr. 62 2006 859 866
26. D. Moll, A. Prinz, F. Gesellchen, S. Drewianka, B. Zimmermann, and F.W. Herberg Biomolecular interaction analysis in functional proteomics J. Neural Transm. 113 2006 1015 1032
27. B.W. Osborne, J. Wu, C.J. McFarland, C.K. Nickl, B. Sankaran, D.E. Casteel, V.L. Woods Jr., A.P. Kornev, S.S. Taylor, and W.R. Dostmann Crystal structure of cGMP-dependent protein kinase reveals novel site of interchain communication Structure 19 2011 1317 1327
28. L.R. Pearce, D. Komander, and D.R. Alessi The nuts and bolts of AGC protein kinases Nat. Rev. Mol. Cell Biol. 11 2010 9 22
29. D. Pellegrino, S. Shiva, T. Angelone, M.T. Gladwin, and B. Tota Nitrite exerts potent negative inotropy in the isolated heart via eNOS-independent nitric oxide generation and cGMP-PKG pathway activation Biochim. Biophys. Acta 1787 2009 818 827
30. A. Pfeifer, P. Klatt, S. Massberg, L. Ny, M. Sausbier, C. Hirneiss, G.X. Wang, M. Korth, A. Aszódi, and K.E. Andersson et al. Defective smooth muscle regulation in cGMP kinase I-deficient mice EMBO J. 17 1998 3045 3051
31. B. Ponsioen, J. Zhao, J. Riedl, F. Zwartkruis, G. van der Krogt, M. Zaccolo, W.H. Moolenaar, J.L. Bos, and K. Jalink Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator EMBO Rep. 5 2004 1176 1180
32. M.C. Puljung, and W.N. Zagotta A secondary structural transition in the C-helix promotes gating of cyclic nucleotide-regulated ion channels J. Biol. Chem. 288 2013 12944 12956
33. R.B. Reed, M. Sandberg, T. Jahnsen, S.M. Lohmann, S.H. Francis, and J.D. Corbin Fast and slow cyclic nucleotide-dissociation sites in cAMP-dependent protein kinase are transposed in type Ibeta cGMP-dependent protein kinase J. Biol. Chem. 271 1996 17570 17575
34. H. Rehmann, A. Wittinghofer, and J.L. Bos Capturing cyclic nucleotides in action: snapshots from crystallographic studies Nat. Rev. Mol. Cell Biol. 8 2007 63 73
35. P. Ruth, W. Landgraf, A. Keilbach, B. May, C. Egleme, and F. Hofmann The activation of expressed cGMP-dependent protein kinase isozymes I alpha and I beta is determined by the different amino-termini Eur. J. Biochem. 202 1991 1339 1344
36. J. Schlossmann, and F. Hofmann cGMP-dependent protein kinases in drug discovery Drug Discov. Today 10 2005 627 634
37. J.A. Smith, R.B. Reed, S.H. Francis, K. Grimes, and J.D. Corbin Distinguishing the roles of the two different cGMP-binding sites for modulating phosphorylation of exogenous substrate (heterophosphorylation) and autophosphorylation of cGMP-dependent protein kinase J. Biol. Chem. 275 2000 154 158
38. Y. Su, W.R. Dostmann, F.W. Herberg, K. Durick, N.H. Xuong, L. Ten Eyck, S.S. Taylor, and K.I. Varughese Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains Science 269 1995 807 813
39. J.W. Taraska, M.C. Puljung, N.B. Olivier, G.E. Flynn, and W.N. Zagotta Mapping the structure and conformational movements of proteins with transition metal ion FRET Nat. Methods 6 2009 532 537
40. T.C. Terwilliger, P.D. Adams, R.J. Read, A.J. McCoy, N.W. Moriarty, R.W. Grosse-Kunstleve, P.V. Afonine, P.H. Zwart, and L.W. Hung Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Acta Crystallogr. D Biol. Crystallogr. 65 2009 582 601
41. B. Trivedi, and R.H. Kramer Real-time patch-cram detection of intracellular cGMP reveals long-term suppression of responses to NO and muscarinic agonists Neuron 21 1998 895 906
42. M.E. Wall, S.H. Francis, J.D. Corbin, K. Grimes, R. Richie-Jannetta, J. Kotera, B.A. Macdonald, R.R. Gibson, and J. Trewhella Mechanisms associated with cGMP binding and activation of cGMP-dependent protein kinase Proc. Natl. Acad. Sci. USA 100 2003 2380 2385
43. J. Wu, S. Brown, N.H. Xuong, and S.S. Taylor RIalpha subunit of PKA: a cAMP-free structure reveals a hydrophobic capping mechanism for docking cAMP into site B Structure 12 2004 1057 1065