Protein Kinase A Catalytic Subunit Primed for Action: Time-Lapse Crystallography of Michaelis Complex Formation

Das, Amit; Gerlits, Oksana; Parks, Jerry M.; Langan, Paul; Kovalevsky, Andrey; Heller, William T.

doi:10.1016/j.str.2015.10.005

Title: Protein Kinase A Catalytic Subunit Primed for Action: Time-Lapse Crystallography of Michaelis Complex Formation

Journal Article · Wed Jan 13 00:00:00 EST 2016 · Structure

DOI:https://doi.org/10.1016/j.str.2015.10.005· OSTI ID:1234755

Das, Amit; Gerlits, Oksana; Parks, Jerry M.; Langan, Paul; Kovalevsky, Andrey; Heller, William T. ^[1]

ORNL

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: DOE - BASIC ENERGY SCIENCES

OSTI ID:: 1234755

Journal Information:: Structure, Vol. 23, Issue (12) ; 12, 2015; ISSN 0969-2126

Publisher:: Elsevier

Country of Publication:: United States

Language:: ENGLISH

References (62)

Divalent metal ions influence catalysis and active-site accessibility in the camp-dependent protein kinase Adams, Joseph A.; Taylor, Susan S. Protein Science, Vol. 2, Issue 12 https://doi.org/10.1002/pro.5560021217	journal	December 1993
Recent developments in the PHENIX software for automated crystallographic structure determination Adams, Paul D.; Gopal, Kreshna; Grosse-Kunstleve, Ralf W. Journal of Synchrotron Radiation, Vol. 11, Issue 1 https://doi.org/10.1107/S0909049503024130	journal	November 2003
Structural Characterization of Protein Kinase A as a Function of Nucleotide Binding Andersen, Mette D.; Shaffer, Jennifer; Jennings, Patricia A. Journal of Biological Chemistry, Vol. 276, Issue 17 https://doi.org/10.1074/jbc.M011543200	journal	April 2001
Phosphoryl Transfer by Protein Kinase A Is Captured in a Crystal Lattice Bastidas, Adam C.; Deal, Michael S.; Steichen, Jon M. Journal of the American Chemical Society, Vol. 135, Issue 12 https://doi.org/10.1021/ja312237q	journal	March 2013
Molecular Features of Product Release for the PKA Catalytic Cycle Bastidas, Adam C.; Wu, Jian; Taylor, Susan S. Biochemistry, Vol. 54, Issue 1 https://doi.org/10.1021/bi500684c	journal	June 2014
Watching the Bacteriophage N4 RNA Polymerase Transcription by Time-dependent Soak-trigger-freeze X-ray Crystallography Basu, Ritwika S.; Murakami, Katsuhiko S. Journal of Biological Chemistry, Vol. 288, Issue 5 https://doi.org/10.1074/jbc.M112.387712	journal	February 2013
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
Mapping Substrate-Induced Conformational Changes in cAMP-Dependent Protein Kinase by Protein Footprinting ^† Cheng, Xiaodong; Shaltiel, Shmuel; Taylor, Susan S. Biochemistry, Vol. 37, Issue 40 https://doi.org/10.1021/bi981057p	journal	October 1998
The role of protein phosphorylation in human health and disease. : Delivered on June 30th 2001 at the FEBS Meeting in Lisbon Cohen, Philip European Journal of Biochemistry, Vol. 268, Issue 19 https://doi.org/10.1046/j.0014-2956.2001.02473.x	journal	October 2001
Nuclear Magnetic Resonance Spectra of Adenosine Di- and Triphosphate Cohn, Mildred; Hughes, Thomas R. Journal of Biological Chemistry, Vol. 237, Issue 1 https://doi.org/10.1016/S0021-9258(18)81382-5	journal	January 1962
Domain movements in protein kinases Cox, Sarah; Radzio-Andzelm, Elzbieta; Taylor, Susan Serota Current Opinion in Structural Biology, Vol. 4, Issue 6 https://doi.org/10.1016/0959-440X(94)90272-0	journal	January 1994
Remarks about protein structure precision Cruickshank, D. W. J. Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 3 https://doi.org/10.1107/S0907444998012645	journal	March 1999
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
X-ray Snapshot of HIV-1 Protease in Action: Observation of Tetrahedral Intermediate and Short Ionic Hydrogen Bond SIHB with Catalytic Aspartate Das, Amit; Mahale, Smita; Prashar, Vishal Journal of the American Chemical Society, Vol. 132, Issue 18 https://doi.org/10.1021/ja100002b	journal	May 2010
Constant pressure molecular dynamics simulation: The Langevin piston method Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470648	journal	September 1995
Role of Phosphate Chain Mobility of MgATP in Completing the 3-Phosphoglycerate Kinase Catalytic Site: Binding, Kinetic, and Crystallographic Studies with ATP and MgATP ^† Flachner, Beáta; Kovári, Zoltán; Varga, Andrea Biochemistry, Vol. 43, Issue 12 https://doi.org/10.1021/bi035022n	journal	March 2004
Insights into the Phosphoryl Transfer Catalyzed by cAMP-Dependent Protein Kinase: An X-ray Crystallographic Study of Complexes with Various Metals and Peptide Substrate SP20 Gerlits, Oksana; Waltman, Mary Jo; Taylor, Susan Biochemistry, Vol. 52, Issue 21 https://doi.org/10.1021/bi400066a	journal	May 2013
Metal-Free cAMP-Dependent Protein Kinase Can Catalyze Phosphoryl Transfer Gerlits, Oksana; Das, Amit; Keshwani, Malik M. Biochemistry, Vol. 53, Issue 19 https://doi.org/10.1021/bi5000965	journal	May 2014
Phosphoryl Transfer Reaction Snapshots in Crystals: INSIGHTS INTO THE MECHANISM OF PROTEIN KINASE A CATALYTIC SUBUNIT Gerlits, Oksana; Tian, Jianhui; Das, Amit Journal of Biological Chemistry, Vol. 290, Issue 25 https://doi.org/10.1074/jbc.M115.643213	journal	April 2015
Protein kinase catalytic domain sequence database: Identification of conserved features of primary structure and classification of family members Hanks, Steven K.; Quinn, Anne Marie Methods in Enzymology https://doi.org/10.1016/0076-6879(91)00126-H	book	January 1991
Role of the Glycine Triad in the ATP-binding Site of cAMP-dependent Protein Kinase Hemmer, Wolfram; McGlone, Maria; Tsigelny, Igor Journal of Biological Chemistry, Vol. 272, Issue 27 https://doi.org/10.1074/jbc.272.27.16946	journal	July 1997
Stereochemical course of the phospho group transfer catalyzed by cAMP-dependent protein kinase Ho, Mengfei.; Bramson, H. Neal.; Hansen, David E. Journal of the American Chemical Society, Vol. 110, Issue 8 https://doi.org/10.1021/ja00216a068	journal	April 1988
Ligand-induced global transitions in the catalytic domain of protein kinase A Hyeon, C.; Jennings, P. A.; Adams, J. A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 9 https://doi.org/10.1073/pnas.0813266106	journal	February 2009
Dynamics of cAMP-Dependent Protein Kinase Johnson, David A.; Akamine, Pearl; Radzio-Andzelm, Elzbieta Chemical Reviews, Vol. 101, Issue 8 https://doi.org/10.1021/cr000226k	journal	August 2001
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
A Transition Path Ensemble Study Reveals a Linchpin Role for Mg ²⁺ during Rate-Limiting ADP Release from Protein Kinase A Khavrutskii, Ilja V.; Grant, Barry; Taylor, Susan S. Biochemistry, Vol. 48, Issue 48 https://doi.org/10.1021/bi901475g	journal	December 2009
PKA-I Holoenzyme Structure Reveals a Mechanism for cAMP-Dependent Activation Kim, Choel; Cheng, Cecilia Y.; Saldanha, S. Adrian Cell, Vol. 130, Issue 6 https://doi.org/10.1016/j.cell.2007.07.018	journal	September 2007
Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase Knighton, D.; Zheng, J.; Ten Eyck, L. Science, Vol. 253, Issue 5018 https://doi.org/10.1126/science.1862343	journal	July 1991
Isotope partitioning in the adenosine 3',5'-monophosphate dependent protein kinase reaction indicates a steady-state random kinetic mechanism Kong, Cheng Te; Cook, Paul F. Biochemistry, Vol. 27, Issue 13 https://doi.org/10.1021/bi00413a032	journal	June 1988
Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Kornev, A. P.; Haste, N. M.; Taylor, S. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 47 https://doi.org/10.1073/pnas.0607656103	journal	November 2006
Low- and room-temperature X-ray structures of protein kinase A ternary complexes shed new light on its activity Kovalevsky, Andrey Y.; Johnson, Hanna; Hanson, B. Leif Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7 https://doi.org/10.1107/S0907444912014886	journal	June 2012
THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal Journal of Computational Chemistry, Vol. 13, Issue 8 https://doi.org/10.1002/jcc.540130812	journal	October 1992
Identification of a Partially Rate-Determining Step in the Catalytic Mechanism of cAMP-Dependent Protein Kinase: A Transient Kinetic Study Using Stopped-Flow Fluorescence Spectroscopy ^† Lew, John; Taylor, Susan S.; Adams, Joseph A. Biochemistry, Vol. 36, Issue 22 https://doi.org/10.1021/bi963164u	journal	June 1997
cAMP-dependent protein kinase: Crystallographic insights into substrate recognition and phosphotransfer Protein Science, Vol. 3, Issue 2 https://doi.org/10.1002/pro.5560030203	journal	February 1994
Crystal structure of a transition state mimic of the catalytic subunit of cAMP-dependent protein kinase Nature Structural Biology, Vol. 9, Issue 4 https://doi.org/10.1038/nsb780	journal	March 2002
Dynamics connect substrate recognition to catalysis in protein kinase A Masterson, Larry R.; Cheng, Cecilia; Yu, Tao Nature Chemical Biology, Vol. 6, Issue 11 https://doi.org/10.1038/nchembio.452	journal	October 2010
Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy Masterson, L. R.; Shi, L.; Metcalfe, E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1102701108	journal	April 2011
Orbital Steering in the Catalytic Power of Enzymes: Small Structural Changes with Large Catalytic Consequences Mesecar, A. D. Science, Vol. 277, Issue 5323 https://doi.org/10.1126/science.277.5323.202	journal	July 1997
Watching DNA polymerase η make a phosphodiester bond Nakamura, Teruya; Zhao, Ye; Yamagata, Yuriko Nature, Vol. 487, Issue 7406 https://doi.org/10.1038/nature11181	journal	July 2012
Crystal Structure of a Polyhistidine-Tagged Recombinant Catalytic Subunit of cAMP-Dependent Protein Kinase Complexed with the Peptide Inhibitor PKI(5−24) and Adenosine Narayana, Narendra; Cox, Sarah; Shaltiel, Shmuel Biochemistry, Vol. 36, Issue 15 https://doi.org/10.1021/bi961947+	journal	April 1997
A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility Narayana, Narendra; Cox, Sarah; Xuong, Nguyen-huu Structure, Vol. 5, Issue 7 https://doi.org/10.1016/S0969-2126(97)00246-3	journal	July 1997
Stability constants for biologically important metal-ligand complexes O'Sullivan, William J.; Smithers, Geoffrey W. Methods in Enzymology https://doi.org/10.1016/0076-6879(79)63014-8	book	January 1979
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
The calculation of the potential of mean force using computer simulations Roux, Benoît Computer Physics Communications, Vol. 91, Issue 1-3 https://doi.org/10.1016/0010-4655(95)00053-I	journal	September 1995
An ATP-Linked Structural Change in Protein Kinase A Precedes Phosphoryl Transfer under Physiological Magnesium Concentrations ^† Shaffer, Jennifer; Adams, Joseph A. Biochemistry, Vol. 38, Issue 17 https://doi.org/10.1021/bi982768q	journal	April 1999
Detection of Conformational Changes along the Kinetic Pathway of Protein Kinase A Using a Catalytic Trapping Technique ^† Shaffer, Jennifer; Adams, Joseph A. Biochemistry, Vol. 38, Issue 37 https://doi.org/10.1021/bi991109q	journal	September 1999
Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A Shaltiel, S.; Cox, S.; Taylor, S. S. Proceedings of the National Academy of Sciences, Vol. 95, Issue 2 https://doi.org/10.1073/pnas.95.2.484	journal	January 1998
Isomeric equilibria in complexes of adenosine 5'-triphosphate with divalent metal ions. Solution structures of M(ATP)2- complexes Sigel, Helmut European Journal of Biochemistry, Vol. 165, Issue 1 https://doi.org/10.1111/j.1432-1033.1987.tb11194.x	journal	May 1987
Electronic Measurements of Single-Molecule Catalysis by cAMP-Dependent Protein Kinase A Sims, Patrick C.; Moody, Issa S.; Choi, Yongki Journal of the American Chemical Society, Vol. 135, Issue 21 https://doi.org/10.1021/ja311604j	journal	May 2013
Interaction of Mg ²⁺ ions with nucleoside triphosphates by phosphorus magnetic resonance spectroscopy Son, Tran-Dinh; Roux, Madeleine; Ellenberger, Michel Nucleic Acids Research, Vol. 2, Issue 7 https://doi.org/10.1093/nar/2.7.1101	journal	January 1975
Synchronous Opening and Closing Motions Are Essential for cAMP-Dependent Protein Kinase A Signaling Srivastava, Atul K.; McDonald, Leanna R.; Cembran, Alessandro Structure, Vol. 22, Issue 12 https://doi.org/10.1016/j.str.2014.09.010	journal	December 2014
Concentration of MgATP2- and other ions in solution. Calculation of the true concentrations of species present in mixtures of associating ions Storer, A. C.; Cornish-Bowden, A. Biochemical Journal, Vol. 159, Issue 1 https://doi.org/10.1042/bj1590001	journal	October 1976
Protein kinases: evolution of dynamic regulatory proteins Taylor, Susan S.; Kornev, Alexandr P. Trends in Biochemical Sciences, Vol. 36, Issue 2 https://doi.org/10.1016/j.tibs.2010.09.006	journal	February 2011
Use of TLS parameters to model anisotropic displacements in macromolecular refinement Winn, M. D.; Isupov, M. N.; Murshudov, G. N. Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 1 https://doi.org/10.1107/S0907444900014736	journal	January 2001
Crystal Structure of a cAMP-dependent Protein Kinase Mutant at 1.26 Å: New Insights into the Catalytic Mechanism Yang, Jie; Ten Eyck, Lynn F.; Xuong, Nguyen-Huu Journal of Molecular Biology, Vol. 336, Issue 2 https://doi.org/10.1016/j.jmb.2003.11.044	journal	February 2004
Autophosphorylation of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli Yonemoto, W.; McGlone, M. L.; Grant, B. Protein Engineering Design and Selection, Vol. 10, Issue 8 https://doi.org/10.1093/protein/10.8.915	journal	August 1997
Chemical mechanism of the adenosine cyclic 3',5'-monophosphate dependent protein kinase from pH studies Yoon, Moon Young; Cook, Paul F. Biochemistry, Vol. 26, Issue 13 https://doi.org/10.1021/bi00387a056	journal	June 1987
Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with magnesium-ATP and peptide inhibitor Zheng, Jianhua; Knighton, Daniel R.; Ten Eyck, Lynn F. Biochemistry, Vol. 32, Issue 9 https://doi.org/10.1021/bi00060a005	journal	March 1993
Is There a Catalytic Base in the Active Site of cAMP-Dependent Protein Kinase? ^† Zhou, Jie; Adams, Joseph A. Biochemistry, Vol. 36, Issue 10 https://doi.org/10.1021/bi9619132	journal	March 1997
Participation of ADP Dissociation in the Rate-Determining Step in cAMP-Dependent Protein Kinase ^† Zhou, Jie; Adams, Joseph A. Biochemistry, Vol. 36, Issue 50 https://doi.org/10.1021/bi971438n	journal	December 1997

Cited By (3)

Globally correlated conformational entropy underlies positive and negative cooperativity in a kinase’s enzymatic cycle Wang, Yingjie; V. S., Manu; Kim, Jonggul Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08655-7	journal	February 2019
Assessing the performance of MM/PBSA and MM/GBSA methods. 9. Prediction reliability of binding affinities and binding poses for protein–peptide complexes Weng, Gaoqi; Wang, Ercheng; Chen, Fu Physical Chemistry Chemical Physics, Vol. 21, Issue 19 https://doi.org/10.1039/c9cp01674k	journal	January 2019
Water-mediated conformational preselection mechanism in substrate binding cooperativity to protein kinase A Setny, Piotr; Wiśniewska, Marta D. Proceedings of the National Academy of Sciences, Vol. 115, Issue 15 https://doi.org/10.1073/pnas.1720024115	journal	March 2018

Similar Records

Protein Kinase A Catalytic Subunit Primed for Action: Time-Lapse Crystallography of Michaelis Complex Formation

Journal Article · Tue Dec 01 00:00:00 EST 2015 · Structure · OSTI ID:1234755

Das, Amit; Gerlits, Oksana; Parks, Jerry M.; +3 more

Functional changes in the properties of the. beta. -adrenoreceptors of pigeon erythrocytes under the action of the catalytic subunit of cAMP-dependent protein kinase

Journal Article · Thu Mar 20 00:00:00 EST 1986 · Biochemistry (Engl. Transl.); (United States) · OSTI ID:1234755

Popov, K M; Bulargina, T V; Severin, E S

Heterologous desensitization of adenylate cyclase from pigeon erythrocytes under the action of the catalytic subunit of cAMP-dependent protein kinase

Journal Article · Fri Sep 20 00:00:00 EDT 1985 · Biochemistry (Engl. Transl.); (United States) · OSTI ID:1234755

Popov, K M; Bulargina, T V; Severin, E S

Title: Protein Kinase A Catalytic Subunit Primed for Action: Time-Lapse Crystallography of Michaelis Complex Formation

Citation Formats

References (62)

Cited By (3)

Similar Records

Related Subjects