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The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase

Journal Article · · BMC Structural Biology (Online)
 [1];  [2];  [2];  [3];  [4]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; DOE/OSTI
  2. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
  3. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Division of Physical Biosciences
  4. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.

Background: Soluble guanylate cyclases generate cyclic GMP when bound to nitric oxide, thereby linking nitric oxide levels to the control of processes such as vascular homeostasis and neurotransmission. The guanylate cyclase catalytic module, for which no structure has been determined at present, is a class III nucleotide cyclase domain that is also found in mammalian membrane-bound guanylate and adenylate cyclases. Results: We have determined the crystal structure of the catalytic domain of a soluble guanylate cyclase from the green algae Chlamydomonas reinhardtii at 2.55 Å resolution, and show that it is a dimeric molecule. Conclusion: Comparison of the structure of the guanylate cyclase domain with the known structures of adenylate cyclases confirms the close similarity in architecture between these two enzymes, as expected from their sequence similarity. The comparison also suggests that the crystallized guanylate cyclase is in an inactive conformation, and the structure provides indications as to how activation might occur. We demonstrate that the two active sites in the dimer exhibit positive cooperativity, with a Hill coefficient of ~1.5. Positive cooperativity has also been observed in the homodimeric mammalian membrane-bound guanylate cyclases. The structure described here provides a reliable model for functional analysis of mammalian guanylate cyclases, which are closely related in sequence.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)
Grant/Contract Number:
AC02-05CH11231; AC03-76SF00098
OSTI ID:
1626558
Journal Information:
BMC Structural Biology (Online), Journal Name: BMC Structural Biology (Online) Journal Issue: 1 Vol. 8; ISSN 1472-6807
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (28)

Structure, mechanism, and regulation of soluble adenylyl cyclases — similarities and differences to transmembrane adenylyl cyclases journal December 2014
A Rhodopsin-Guanylyl Cyclase Gene Fusion Functions in Visual Perception in a Fungus journal June 2014
Interfacial Residues Promote an Optimal Alignment of the Catalytic Center in Human Soluble Guanylate Cyclase: Heterodimerization Is Required but Not Sufficient for Activity journal March 2014
Rhodopsin-cyclases for photocontrol of cGMP/cAMP and 2.3 Å structure of the adenylyl cyclase domain journal May 2018
Probing the Molecular Mechanism of Human Soluble Guanylate Cyclase Activation by NO in vitro and in vivo journal February 2017
Crystal structure of the signaling helix coiled-coil domain of the β1 subunit of the soluble guanylyl cyclase journal January 2010
Guanylyl cyclase sees the light journal January 2008
Fluorescent Fusion Proteins of Soluble Guanylyl Cyclase Indicate Proximity of the Heme Nitric Oxide Domain and Catalytic Domain journal July 2010
Identification of Residues in the Heme Domain of Soluble Guanylyl Cyclase that are Important for Basal and Stimulated Catalytic Activity journal November 2011
Crystal Structures of the Catalytic Domain of Human Soluble Guanylate Cyclase journal March 2013
Crystal Structure of a Ube2S-Ubiquitin Conjugate journal February 2016
Receptor Guanylyl Cyclases in Sensory Processing journal January 2017
Bicarbonate and Ca2+ Sensing Modulators Activate Photoreceptor ROS-GC1 Synergistically journal January 2016
Membrane Guanylate Cyclase catalytic Subdomain: Structure and Linkage with Calcium Sensors and Bicarbonate journal January 2017
Molecular Details of Retinal Guanylyl Cyclase 1/GCAP-2 Interaction journal September 2018
Regulation of soluble guanylate cyclase by matricellular thrombospondins: implications for blood flow journal April 2014
In Search of Enzymes with a Role in 3′, 5′-Cyclic Guanosine Monophosphate Metabolism in Plants journal May 2016
Wedging open a catalytic site journal November 2019
Instability in a coiled‐coil signaling helix is conserved for signal transduction in soluble guanylyl cyclase journal August 2019
Receptor guanylyl cyclase C (GC-C): regulation and signal transduction journal December 2009
Evasion of autophagy mediated by Rickettsia surface protein OmpB is critical for virulence journal October 2019
Structures of soluble guanylate cyclase: implications for regulatory mechanisms and drug development journal January 2014
Allosteric activation of the nitric oxide receptor soluble guanylate cyclase mapped by cryo-electron microscopy posted_content August 2019
Molecular basis for GTP recognition by light‐activated guanylate cyclase Rh GC journal December 2019
The brassinosteroid receptor BRI 1 can generate cGMP enabling cGMP ‐dependent downstream signaling journal June 2017
The soluble guanylate cyclase CYG 12 is required for the acclimation to hypoxia and trophic regimes in Chlamydomonas reinhardtii journal December 2017
The Molecular Pharmacology of G Protein Signaling Then and Now: A Tribute to Alfred G. Gilman journal March 2016
Allosteric activation of the nitric oxide receptor soluble guanylate cyclase mapped by cryo-electron microscopy journal September 2019

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