Activation of the Hetero-octameric ATP Phosphoribosyl Transferase through Subunit Interface Rearrangement by a tRNA Synthetase Paralog

Champagne, Karen S.; Larrabee, Yuna C.; Doublié, Sylvie; Francklyn, Christopher S.

doi:10.1074/jbc.m505041200

Cited by 34 publications

(102 citation statements)

References 47 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The long and short form ATP-PRTs differ in quaternary structure and mechanism of allostery, although they share a common catalytic core [4,5,12,13]. …”

Section: Discussionmentioning

confidence: 99%

“…Extensive bioinformatic analysis has indicated that HisG S is homologous to the periplasmicbinding proteins and is likely to be the phylogenetically older form of ATP-PRT [12]. HisG S has approximately 25% sequence identity to HisG L , consists of two domains comparable to domains I and II of HisG L , and is devoid of the regulatory ACT domain [12,13]. Previous reports have indicated that HisG S is catalytically inactive on its own and association with a second protein, HisZ, is required to form a functional ATP-PRT [3,13,14].…”

mentioning

confidence: 99%

“…histidine [12,13,15]. Despite the structural similarity between a single chain of HisG S and HisG L , the short form and long form ATP-PRTs differ in their quaternary structure.…”

mentioning

confidence: 99%

“…The long form ATP-PRT is homo-hexameric while the short form exists as a hetero-octameric complex (HisZG S ) [4,16]. X-ray crystal structures of HisG L from Mycobacterium tuberculosis (PDB 1NH7, 1NH8), Escherichia coli (PDB 1H3D, 1Q1K), and HisZG S from Lactococcus lactis (PDB 1Z7M, 1Z7N), and Thermotoga maritima (PDB 1USY) have been reported [4,5,12,13].…”

mentioning

confidence: 99%

See 3 more Smart Citations

Independent catalysis of the short form HisG from Lactococcus lactis

et al. 2016

View full text Add to dashboard Cite

Edited by Michael IbbaATP-phosphoribosyltransferase (ATP-PRT) catalyses the first step of histidine biosynthesis. Two different forms of ATP-PRT have been described; the homo-hexameric long form, and the hetero-octameric short form. Lactococcus lactis possesses the short form ATP-PRT comprising four subunits of HisG S , the catalytic subunit, and four subunits of HisZ, a histidyl-tRNA synthetase paralogue. Previous studies have suggested that HisG S requires HisZ for catalysis. Here, we reveal that the dimeric HisG S does display ATP-PRT activity in the absence of HisZ. This result reflects the evolutionary relationship between the long and short form ATP-PRT, which acquired allosteric inhibition and enhanced catalysis via two divergent strategies.

show abstract

“…The long and short form ATP-PRTs differ in quaternary structure and mechanism of allostery, although they share a common catalytic core [4,5,12,13]. …”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

“…histidine [12,13,15]. Despite the structural similarity between a single chain of HisG S and HisG L , the short form and long form ATP-PRTs differ in their quaternary structure.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Independent catalysis of the short form HisG from Lactococcus lactis

et al. 2016

View full text Add to dashboard Cite

show abstract

“…22 Likewise, while mesophilic and thermophilic ATPPRT's have been characterised, 11,12 no psychrophilic example has been reported.…”

mentioning

confidence: 99%

Kinetics and Structure of a Cold-Adapted Hetero-Octameric ATP Phosphoribosyltransferase

Stroek

Talbot²,

Glok³

et al. 2017

Biochemistry

112

View full text Add to dashboard Cite

ATP-phosphoribosyltransferase (ATPPRT) catalyses the first step in histidine biosynthesis, the condensation of ATP and 5-phospho--D-ribosyl-1-pyrophosphate to generate N 1 -(5-phospho--D-ribosyl)-ATP and inorganic pyrophosphate. The enzyme is allosterically inhibited by histidine. Two forms of ATPPRT, encoded by the hisG gene, exist in nature, depending on the species. The long form, HisGL, is a single polypeptide chain with catalytic and regulatory domains. The short form, HisGS, lacks a regulatory domain, and cannot bind histidine. HisGS instead is found in complex with a regulatory protein, HisZ, constituting the ATPPRT holoenzyme. HisZ triggers HisGS catalytic activity while rendering it sensitive to allosteric inhibition by histidine. Until recently, HisGS was thought to be catalytically inactive without HisZ. Here, recombinant HisGS and HisZ from the psychrophilic bacterium Psychrobacter arcticus were independently overexpressed and purified. The crystal structure of P. arcticus ATPPRT was solved at 2.34-Å resolution, revealing an equimolar HisGS-HisZ hetero-octamer. Steady-state kinetics indicate that both ATPPRT holoenzyme and HisGS are catalytically active. Surprisingly, HisZ confers only a modest 2-to 4-fold increase in kcat.Reaction profiles for both enzymes are indistinguishable by 31 P-NMR, indicating that the same reaction is catalysed. Temperature dependence of kcat shows deviation from Arrhenius behaviour at 308 K with the holoenzyme. Interestingly, such deviation is detected only at 313 K with HisGS. Thermal denaturation by CD spectroscopy resulted in Tm's of 312 K and 316 K for HisZ and HisGS, respectively, suggesting that HisZ renders the ATPPRT complex more thermolabile. This is the first characterisation of a psychrophilic ATPPRT. 4Adenosine 5ʹ-triphosphate phosphoribosyltransferase (ATPPRT) (EC 2.4.2.17) catalyses the reversible Mg 2+ -dependent reaction between adenosine 5ʹ-triphosphate (ATP) and(PR-ATP) and inorganic pyrophosphate (PPi) (Scheme 1), the first step in histidine biosynthesis. 1 The chemical equilibrium of the reaction strongly favours reactants, 2 and the enzyme is allosterically inhibited by histidine. 1 In addition to being a model for understanding allostery, 2-4 ATPPRT is of biotechnological interest as a tool for histidine production, provided that histidine feedback inhibition can be overcome. [5][6][7] Two forms of ATPPRT, encoded by the hisG gene, are found in nature. Fungi, plants, and most bacteria possess a long, homo-hexameric protein, HisGL, each subunit consisting of two domains that make up the catalytic core and a C-terminal regulatory domain that mediates feedback inhibition by histidine. 8 Some bacteria and archaea have a short version of the protein, HisGS, which lacks the C-terminal regulatory domain and is insensitive to histidine. In these organisms, a catalytically inactive regulatory protein, HisZ, the product of the hisZ gene, is present. 9 HisZ, which shares a common ancestry with histidyl-tRNA synthetase (HisRS), binds HisGS to form ...

show abstract

Aminoacyl tRNASynthetases, Chemistry of

Nawaz

Martinis

2008

Wiley Encyclopedia of Chemical Biology

View full text Add to dashboard Cite

Aminoacyl‐tRNA synthetases (aaRSs) compose a family of essential enzymes that attach amino acids covalently to tRNA molecules during protein synthesis. Some aaRSs possess a hydrolytic amino acid editing function to ensure the fidelity of protein synthesis. In addition, aminoacylation can occur by indirect pathways that rely on mischarged tRNA intermediates and enzymes other than aaRSs. Throughout evolution, structural and functional divergence of aaRSs has yielded diverse secondary roles. Likewise, aaRS‐like proteins with either sequence or structural similarities to synthetases exhibit functions that may or may not be related to aminoacylation. Many of these diverse aaRSs and aaRS‐like proteins have been capitalized on by the microbial world and by medical research as targets for therapeutic agents such as antibiotics.

show abstract

Activation of the Hetero-octameric ATP Phosphoribosyl Transferase through Subunit Interface Rearrangement by a tRNA Synthetase Paralog

Cited by 34 publications

References 47 publications

Independent catalysis of the short form HisG from Lactococcus lactis

Independent catalysis of the short form HisG from Lactococcus lactis

Kinetics and Structure of a Cold-Adapted Hetero-Octameric ATP Phosphoribosyltransferase

Aminoacyl tRNASynthetases, Chemistry of

Contact Info

Product

Resources

About