Co-Crystal Structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the Molecular Details of Cyclic-Nucleotide Binding
Abstract
Background: Cyclic GMP-dependent protein kinases (PKGs) are central mediators of the NO-cGMP signaling pathway and phosphorylate downstream substrates that are crucial for regulating smooth muscle tone, platelet activation, nociception and memory formation. As one of the main receptors for cGMP, PKGs mediate most of the effects of cGMP elevating drugs, such as nitric oxide-releasing agents and phosphodiesterase inhibitors which are used for the treatment of angina pectoris and erectile dysfunction, respectively. Methodology/Principal Findings: We have investigated the mechanism of cyclic nucleotide binding to PKG by determining crystal structures of the amino-terminal cyclic nucleotide-binding domain (CNBD-A) of human PKG I bound to either cGMP or cAMP. We also determined the structure of CNBD-A in the absence of bound nucleotide. The crystal structures of CNBD-A with bound cAMP or cGMP reveal that cAMP binds in either syn or anti configurations whereas cGMP binds only in a syn configuration, with a conserved threonine residue anchoring both cyclic phosphate and guanine moieties. The structure of CNBD-A in the absence of bound cyclic nucleotide was similar to that of the cyclic nucleotide bound structures. Surprisingly, isothermal titration calorimetry experiments demonstrated that CNBD-A binds both cGMP and cAMP with a relatively high affinity, showing an approximatelymore »
- Authors:
-
- Baylor Univ., Houston, TX (United States). College of Medicine. Dept. of Pharmacology
- Univ. of California, San Diego, La Jolla, CA (United States). Dept. of Medicine
- Baylor Univ., Houston, TX (United States). College of Medicine. The Verna and Marrs McLean Dept. of Biochemistry and Molecular Biology
- Rice Univ., Houston, TX (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). The Berkeley Center for Structural Biology
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Computational Crystallography Initiative
- Baylor Univ., Houston, TX (United States). College of Medicine. Dept. of Pharmacology; Baylor Univ., Houston, TX (United States). College of Medicine. The Verna and Marrs McLean Dept. of Biochemistry and Molecular Biology; Baylor Univ., Houston, TX (United States). College of Medicine. Dept. of Molecular Virology and Microbiology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)
- OSTI Identifier:
- 1629608
- Grant/Contract Number:
- AC02-05CH11231; K22-CA124517
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Kim, Jeong Joo, Casteel, Darren E., Huang, Gilbert, Kwon, Taek Hun, Ren, Ronnie Kuo, Zwart, Peter, Headd, Jeffrey J., Brown, Nicholas Gene, Chow, Dar-Chone, Palzkill, Timothy, and Kim, Choel. Co-Crystal Structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the Molecular Details of Cyclic-Nucleotide Binding. United States: N. p., 2011.
Web. doi:10.1371/journal.pone.0018413.
Kim, Jeong Joo, Casteel, Darren E., Huang, Gilbert, Kwon, Taek Hun, Ren, Ronnie Kuo, Zwart, Peter, Headd, Jeffrey J., Brown, Nicholas Gene, Chow, Dar-Chone, Palzkill, Timothy, & Kim, Choel. Co-Crystal Structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the Molecular Details of Cyclic-Nucleotide Binding. United States. https://doi.org/10.1371/journal.pone.0018413
Kim, Jeong Joo, Casteel, Darren E., Huang, Gilbert, Kwon, Taek Hun, Ren, Ronnie Kuo, Zwart, Peter, Headd, Jeffrey J., Brown, Nicholas Gene, Chow, Dar-Chone, Palzkill, Timothy, and Kim, Choel. Tue .
"Co-Crystal Structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the Molecular Details of Cyclic-Nucleotide Binding". United States. https://doi.org/10.1371/journal.pone.0018413. https://www.osti.gov/servlets/purl/1629608.
@article{osti_1629608,
title = {Co-Crystal Structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the Molecular Details of Cyclic-Nucleotide Binding},
author = {Kim, Jeong Joo and Casteel, Darren E. and Huang, Gilbert and Kwon, Taek Hun and Ren, Ronnie Kuo and Zwart, Peter and Headd, Jeffrey J. and Brown, Nicholas Gene and Chow, Dar-Chone and Palzkill, Timothy and Kim, Choel},
abstractNote = {Background: Cyclic GMP-dependent protein kinases (PKGs) are central mediators of the NO-cGMP signaling pathway and phosphorylate downstream substrates that are crucial for regulating smooth muscle tone, platelet activation, nociception and memory formation. As one of the main receptors for cGMP, PKGs mediate most of the effects of cGMP elevating drugs, such as nitric oxide-releasing agents and phosphodiesterase inhibitors which are used for the treatment of angina pectoris and erectile dysfunction, respectively. Methodology/Principal Findings: We have investigated the mechanism of cyclic nucleotide binding to PKG by determining crystal structures of the amino-terminal cyclic nucleotide-binding domain (CNBD-A) of human PKG I bound to either cGMP or cAMP. We also determined the structure of CNBD-A in the absence of bound nucleotide. The crystal structures of CNBD-A with bound cAMP or cGMP reveal that cAMP binds in either syn or anti configurations whereas cGMP binds only in a syn configuration, with a conserved threonine residue anchoring both cyclic phosphate and guanine moieties. The structure of CNBD-A in the absence of bound cyclic nucleotide was similar to that of the cyclic nucleotide bound structures. Surprisingly, isothermal titration calorimetry experiments demonstrated that CNBD-A binds both cGMP and cAMP with a relatively high affinity, showing an approximately two-fold preference for cGMP. Conclusions/Significance: Our findings suggest that CNBD-A binds cGMP in the syn conformation through its interaction with Thr193 and an unusual cis-peptide forming residues Leu172 and Cys173. Although these studies provide the first structural insights into cyclic nucleotide binding to PKG, our ITC results show only a two-fold preference for cGMP, indicating that other domains are required for the previously reported cyclic nucleotide selectivity.},
doi = {10.1371/journal.pone.0018413},
journal = {PLoS ONE},
number = 4,
volume = 6,
place = {United States},
year = {Tue Apr 19 00:00:00 EDT 2011},
month = {Tue Apr 19 00:00:00 EDT 2011}
}
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