Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-Monophosphate
Abstract
Cyclic nucleotide phosphodiesterases (PDEs) decompose second messengers cAMP and cGMP that play critical roles in many physiological processes. PDE1 of Saccharomyces cerevisiae has been subcloned and expressed in Escherichia coli. Recombinant yPDE1 has a KM of 110 μM and a kcat of 16.9 s⁻¹ for cAMP and a KM of 105 μM and a kcat of 11.8 s₅⁻¹ for cGMP. Thus, the specificity constant (kcat/KMcAMP)/(kcat/KMcGMP) of 1.4 indicates a dual specificity of yPDE1 for hydrolysis of both cAMP and cGMP. The crystal structures of unliganded yPDE1 and its complex with GMP at 1.31 Å resolution reveal a new structural folding that is different from those of human PDEs but is partially similar to that of some other metalloenzymes such as metallo-β-lactamase. In spite of their different structures and divalent metals, yPDE1 and human PDEs may share a common mechanism for hydrolysis of cAMP and cGMP.
- Authors:
-
- Beijing Technology and Business Univ., Beijing (China); Univ. of North Carolina, Chapel Hill, NC (United States)
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Univ. of North Carolina, Chapel Hill, NC (United States); Sun Yat-Sen Univ., Guangzhou (China)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Sun Yat-Sen Univ., Guangzhou (China)
- Beijing Technology and Business Univ., Beijing (China)
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
- OSTI Identifier:
- 1179586
- Resource Type:
- Published Article
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Name: Biochemistry Journal Volume: 53 Journal Issue: 30; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Tian, Yuanyuan, Cui, Wenjun, Huang, Manna, Robinson, Howard, Wan, Yiqian, Wang, Yousheng, and Ke, Hengming. Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-Monophosphate. United States: N. p., 2014.
Web. doi:10.1021/bi500406h.
Tian, Yuanyuan, Cui, Wenjun, Huang, Manna, Robinson, Howard, Wan, Yiqian, Wang, Yousheng, & Ke, Hengming. Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-Monophosphate. United States. https://doi.org/10.1021/bi500406h
Tian, Yuanyuan, Cui, Wenjun, Huang, Manna, Robinson, Howard, Wan, Yiqian, Wang, Yousheng, and Ke, Hengming. Tue .
"Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-Monophosphate". United States. https://doi.org/10.1021/bi500406h.
@article{osti_1179586,
title = {Dual specificity and novel structural folding of yeast phosphodiesterase-1 for hydrolysis of second messengers cyclic adenosine and guanosine 3',5'-Monophosphate},
author = {Tian, Yuanyuan and Cui, Wenjun and Huang, Manna and Robinson, Howard and Wan, Yiqian and Wang, Yousheng and Ke, Hengming},
abstractNote = {Cyclic nucleotide phosphodiesterases (PDEs) decompose second messengers cAMP and cGMP that play critical roles in many physiological processes. PDE1 of Saccharomyces cerevisiae has been subcloned and expressed in Escherichia coli. Recombinant yPDE1 has a KM of 110 μM and a kcat of 16.9 s⁻¹ for cAMP and a KM of 105 μM and a kcat of 11.8 s₅⁻¹ for cGMP. Thus, the specificity constant (kcat/KMcAMP)/(kcat/KMcGMP) of 1.4 indicates a dual specificity of yPDE1 for hydrolysis of both cAMP and cGMP. The crystal structures of unliganded yPDE1 and its complex with GMP at 1.31 Å resolution reveal a new structural folding that is different from those of human PDEs but is partially similar to that of some other metalloenzymes such as metallo-β-lactamase. In spite of their different structures and divalent metals, yPDE1 and human PDEs may share a common mechanism for hydrolysis of cAMP and cGMP.},
doi = {10.1021/bi500406h},
journal = {Biochemistry},
number = 30,
volume = 53,
place = {United States},
year = {Tue Aug 05 00:00:00 EDT 2014},
month = {Tue Aug 05 00:00:00 EDT 2014}
}
https://doi.org/10.1021/bi500406h
Web of Science
Works referenced in this record:
The Gα Protein Gpa2 Controls Yeast Differentiation by Interacting with Kelch Repeat Proteins that Mimic Gβ Subunits
journal, July 2002
- Harashima, Toshiaki; Heitman, Joseph
- Molecular Cell, Vol. 10, Issue 1
Role of Ca 2+ /Calmodulin-Stimulated Cyclic Nucleotide Phosphodiesterase 1 in Mediating Cardiomyocyte Hypertrophy
journal, November 2009
- Miller, Clint L.; Oikawa, Masayoshi; Cai, Yujun
- Circulation Research, Vol. 105, Issue 10
Correlation of Internal Torsional Motion with Overall Molecular Motion in Crystals
journal, October 1998
- Schomaker, V.; Trueblood, K. N.
- Acta Crystallographica Section B Structural Science, Vol. 54, Issue 5
The zinc-containing high Km cyclic nucleotide phosphodiesterase of bakers' yeast.
journal, March 1983
- Londesborough, J.; Suoranta, K.
- Journal of Biological Chemistry, Vol. 258, Issue 5
Overexpression of PDE2 or SSD1-V in Saccharomyces cerevisiae W303-1A strain renders it ethanol-tolerant
journal, March 2012
- Avrahami-Moyal, Liat; Braun, Sergei; Engelberg, David
- FEMS Yeast Research, Vol. 12, Issue 4
Isolation and characterization of a previously undetected human cAMP phosphodiesterase by complementation of cAMP phosphodiesterase-deficient Saccharomyces cerevisiae
journal, June 1993
- Michaeli, T.; Bloom, T. J.; Martins, T.
- Journal of Biological Chemistry, Vol. 268, Issue 17
The pH and temperature dependence of the activity of the high Km cyclic nucleotide phosphodiesterase of bakers' yeast.
journal, October 1980
- Londesborough, J.; Lukkari, T. M.
- Journal of Biological Chemistry, Vol. 255, Issue 19
Purification of intact and nicked forms of a zinc-containing, Mg2+-dependent, low Km cyclic AMP phosphodiesterase from bakers' yeast.
journal, June 1984
- Suoranta, K.; Londesborough, J.
- Journal of Biological Chemistry, Vol. 259, Issue 11
Phosphodiesterase 5 inhibitors: current status and potential applications
journal, September 2002
- Rotella, David P.
- Nature Reviews Drug Discovery, Vol. 1, Issue 9
The PDE1 -encoded Low-Affinity Phosphodiesterase in the Yeast Saccharomyces cerevisiae Has a Specific Function in Controlling Agonist-induced cAMP Signaling
journal, January 1999
- Ma, Pingsheng; Wera, Stefaan; Van Dijck, Patrick
- Molecular Biology of the Cell, Vol. 10, Issue 1
A Candida albicans cyclic nucleotide phosphodiesterase: cloning and expression in Saccharomyces cerevisiae and biochemical characterization of the recombinant enzyme
journal, July 1994
- Hoyer, L. L.; Cieslinski, L. B.; Mclaughlin, M. M.
- Microbiology, Vol. 140, Issue 7
The specificity of yeast low-Km cyclic AMP phosphodiesterase towards free bivalent metal ions and the diastereoisomers of cyclic adenosine phosphorothioate
journal, March 1985
- Suoranta, K.; Londesborough, J.
- Biochemical Journal, Vol. 226, Issue 3
Stereochemistry of hydrolysis of adenosine 3‘:5‘-cyclic phosphorothioate by the cyclic phosphodiesterase from beef heart.
journal, October 1979
- Burgers, P. M.; Eckstein, F.; Hunneman, D. H.
- Journal of Biological Chemistry, Vol. 254, Issue 20
The Crystal Structure of AMP-Bound PDE4 Suggests a Mechanism for Phosphodiesterase Catalysis † , ‡
journal, November 2003
- Huai, Qing; Colicelli, John; Ke, Hengming
- Biochemistry, Vol. 42, Issue 45
Sildenafil Citrate Therapy for Pulmonary Arterial Hypertension
journal, November 2005
- Galiè, Nazzareno; Ghofrani, Hossein A.; Torbicki, Adam
- New England Journal of Medicine, Vol. 353, Issue 20
The effect of cAMP and cGMP on the activity and substrate specificity of protein kinase A from methylotrophic yeast Pichia pastoris.
journal, December 2003
- Frajnt, Magdalena; Cytryńska, Małgorzata; Jakubowicz, Teresa
- Acta Biochimica Polonica, Vol. 50, Issue 4
Recent Advances in Zinc Enzymology
journal, January 1996
- Lipscomb, William N.; Sträter, Norbert
- Chemical Reviews, Vol. 96, Issue 7
Biochemistry and Physiology of Cyclic Nucleotide Phosphodiesterases: Essential Components in Cyclic Nucleotide Signaling
journal, June 2007
- Conti, Marco; Beavo, Joseph
- Annual Review of Biochemistry, Vol. 76, Issue 1
Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae.
journal, December 1986
- Sass, P.; Field, J.; Nikawa, J.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 24
Multiple Elements Jointly Determine Inhibitor Selectivity of Cyclic Nucleotide Phosphodiesterases 4 and 7
journal, September 2005
- Wang, Huanchen; Liu, Yudong; Chen, Yuxiang
- Journal of Biological Chemistry, Vol. 280, Issue 35
Deletion of the high-affinity cAMP phosphodiesterase encoded by PDE2 affects stress responses and virulence in Candida albicans
journal, August 2007
- Wilson, Duncan; Tutulan-Cunita, Andreea; Jung, WonHee
- Molecular Microbiology, Vol. 65, Issue 4
Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily
journal, December 2007
- Bebrone, Carine
- Biochemical Pharmacology, Vol. 74, Issue 12
Improved methods for building protein models in electron density maps and the location of errors in these models
journal, March 1991
- Jones, T. A.; Zou, J. Y.; Cowan, S. W.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119
Crystal Structures of Phosphodiesterases and Implications on Substrate Specificity and Inhibitor Selectivity
journal, February 2007
- Ke, Hengming; Wang, Huanchen
- Current Topics in Medicinal Chemistry, Vol. 7, Issue 4
The cAMP phosphodiesterase encoded by CaPDE2 is required for hyphal development in Candida albicans
journal, October 2003
- Jung, Won Hee; Stateva, Lubomira I.
- Microbiology, Vol. 149, Issue 10
cAMP and cGMP Signaling Cross-Talk: Role of Phosphodiesterases and Implications for Cardiac Pathophysiology
journal, June 2007
- Zaccolo, Manuela; Movsesian, Matthew A.
- Circulation Research, Vol. 100, Issue 11
Phosphodiesterases in the CNS: targets for drug development
journal, August 2006
- Menniti, Frank S.; Faraci, W. Stephen; Schmidt, Christopher J.
- Nature Reviews Drug Discovery, Vol. 5, Issue 8
Characterization of a cyclic nucleotide phosphodiesterase-deficient mutant in yeast.
journal, March 1983
- Uno, I.; Matsumoto, K.; Ishikawa, T.
- Journal of Biological Chemistry, Vol. 258, Issue 6
Phosphodiesterase-4 inhibitors for asthma and chronic obstructive pulmonary disease
journal, January 2005
- Lipworth, Brian J.
- The Lancet, Vol. 365, Issue 9454
RAS/Cyclic AMP and Transcription Factor Msn2 Regulate Mating and Mating-Type Switching in the Yeast Kluyveromyces lactis
journal, November 2011
- Barsoum, E.; Rajaei, N.; Åström, S. U.
- Eukaryotic Cell, Vol. 10, Issue 11
Increased high-affinity phosphodiesterase PDE2 gene expression in germ tubes counteracts CAP1-dependent synthesis of cyclic AMP, limits hypha production and promotes virulence of Candida albicans: Regulation of cAMP signalling and virulence of C. albicans
journal, August 2003
- Bahn, Yong-Sun; Staab, Janet; Sundstrom, Paula
- Molecular Microbiology, Vol. 50, Issue 2
Candida albicans Pde1p and Gpa2p comprise a regulatory module mediating agonist-induced cAMP signalling and environmental adaptation
journal, September 2010
- Wilson, Duncan; Fiori, Alessandro; Brucker, Katrijn De
- Fungal Genetics and Biology, Vol. 47, Issue 9
The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras–cyclic AMP pathway in stress responses
journal, February 2005
- Park, Jong-In; Grant, Chris M.; Dawes, Ian W.
- Biochemical and Biophysical Research Communications, Vol. 327, Issue 1
Cyclic Nucleotide Phosphodiesterases: Molecular Regulation to Clinical Use
journal, September 2006
- Bender, Andrew T.; Beavo, Joseph A.
- Pharmacological Reviews, Vol. 58, Issue 3
cAMP-Dependent Signaling as a Core Component of the Mammalian Circadian Pacemaker
journal, May 2008
- O'Neill, J. S.; Maywood, E. S.; Chesham, J. E.
- Science, Vol. 320, Issue 5878
Deletion ofPDE2, the gene encoding the high-affinity cAMP phosphodiesterase, results in changes of the cell wall and membrane inCandida albicans
journal, January 2005
- Jung, Won Hee; Warn, Peter; Ragni, Enrico
- Yeast, Vol. 22, Issue 4
DaliLite workbench for protein structure comparison
journal, June 2000
- Holm, L.; Park, J.
- Bioinformatics, Vol. 16, Issue 6
Overview of PDEs and Their Regulation
journal, February 2007
- Omori, Kenji; Kotera, Jun
- Circulation Research, Vol. 100, Issue 3
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
Advances in targeting cyclic nucleotide phosphodiesterases
journal, April 2014
- Maurice, Donald H.; Ke, Hengming; Ahmad, Faiyaz
- Nature Reviews Drug Discovery, Vol. 13, Issue 4
Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast
journal, June 2000
- Thevelein, Johan M.; Cauwenberg, Liesbet; Colombo, Sonia
- Enzyme and Microbial Technology, Vol. 26, Issue 9-10
Structural basis for the catalytic mechanism of human phosphodiesterase 9
journal, August 2008
- Liu, S.; Mansour, M. N.; Dillman, K. S.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 36
Overexpression of the YAP1 , PDE2 , and STB3 genes enhances the tolerance of yeast to oxidative stress induced by 7-chlorotetrazolo[5,1-c]benzo[1,2,4]triazine
journal, September 2012
- Drobna, Eva; Gazdag, Zoltan; Culakova, Hana
- FEMS Yeast Research, Vol. 12, Issue 8