Substrate specificity determinants of class III nucleotidyl cyclases

FEBS J. 2016 Oct;283(20):3723-3738. doi: 10.1111/febs.13837. Epub 2016 Sep 9.

Abstract

The two second messengers in signalling, cyclic AMP and cyclic GMP, are produced by adenylyl and guanylyl cyclases respectively. Recognition and discrimination of the substrates ATP and GTP by the nucleotidyl cyclases are vital in these reactions. Various apo-, substrate- or inhibitor-bound forms of adenylyl cyclase (AC) structures from transmembrane and soluble ACs have revealed the catalytic mechanism of ATP cyclization reaction. Previously reported structures of guanylyl cyclases represent ligand-free forms and inactive open states of the enzymes and thus do not provide information regarding the exact mode of substrate binding. The structures we present here of the cyclase homology domain of a class III AC from Mycobacterium avium (Ma1120) and its mutant in complex with ATP and GTP in the presence of calcium ion, provide the structural basis for substrate selection by the nucleotidyl cyclases at the atomic level. Precise nature of the enzyme-substrate interactions, novel modes of substrate binding and the ability of the binding pocket to accommodate diverse conformations of the substrates have been revealed by the present crystallographic analysis. This is the first report to provide structures of both the nucleotide substrates bound to a nucleotidyl cyclase.

Database: Coordinates and structure factors have been deposited in the Protein Data Bank with accession numbers: 5D15 (Ma1120CHD +ATP.Ca2+ ), 5D0E (Ma1120CHD +GTP.Ca2+ ), 5D0H (Ma1120CHD (KDA→EGY)+ATP.Ca2+ ), 5D0G (Ma1120CHD (KDA→EGY)+GTP.Ca2+ ).

Enzymes: Adenylyl cyclase (EC number: 4.6.1.1).

Keywords: cAMP; cGMP; X-ray crystallography; adenylyl cyclase; guanylyl cyclase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Adenylyl Cyclases / chemistry
  • Adenylyl Cyclases / genetics
  • Adenylyl Cyclases / metabolism*
  • Amino Acid Substitution
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Calcium / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • Guanosine Triphosphate / metabolism
  • Guanylate Cyclase / chemistry
  • Guanylate Cyclase / genetics
  • Guanylate Cyclase / metabolism
  • Kinetics
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Mycobacterium avium / enzymology
  • Mycobacterium avium / genetics
  • Protein Domains
  • Static Electricity
  • Substrate Specificity

Substances

  • Bacterial Proteins
  • Mutant Proteins
  • Guanosine Triphosphate
  • Adenosine Triphosphate
  • Adenylyl Cyclases
  • adenylate cyclase 3
  • Guanylate Cyclase
  • Calcium