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The structure of Escherichia coli ATP-phosphoribosyltransferase: identification of substrate binding sites and mode of AMP inhibition.

Lohkamp B, McDermott G, Campbell SA, Coggins JR, Lapthorn AJ
J Mol Biol 336 131-44 (2004)
Cited: 33 times
EuropePMC logo PMID: 14741209

Abstract

ATP-phosphoribosyltransferase (ATP-PRT), the first enzyme of the histidine pathway, is a complex allosterically regulated enzyme, which controls the flow of intermediates through this biosynthetic pathway. The crystal structures of Escherichia coli ATP-PRT have been solved in complex with the inhibitor AMP at 2.7A and with product PR-ATP at 2.9A (the ribosyl-triphosphate could not be resolved). On the basis of binding of AMP and PR-ATP and comparison with type I PRTs, the PRPP and parts of the ATP-binding site are identified. These structures clearly identify the AMP as binding in the 5-phosphoribosyl-alpha-1-pyrophosphate (PRPP)-binding site, with the adenosine ring occupying the ATP-binding site. Comparison with the recently solved Mycobacterium tuberculosis ATP-PRT structures indicates that histidine is solely responsible for the large conformational changes observed between the hexameric forms of the enzyme. The role of oligomerisation in inhibition and the structural basis for the synergistic inhibition by histidine and AMP are discussed.

Reviews - 1q1k mentioned but not cited (1)

  1. Insight into de-regulation of amino acid feedback inhibition: a focus on structure analysis method. Naz S, Liu P, Farooq U, Ma H. Microb Cell Fact 22 161 (2023)

Articles - 1q1k mentioned but not cited (2)

  1. Discovery of novel nitrobenzothiazole inhibitors for Mycobacterium tuberculosis ATP phosphoribosyl transferase (HisG) through virtual screening. Cho Y, Ioerger TR, Sacchettini JC. J Med Chem 51 5984-5992 (2008)
  2. Uncoupling conformational states from activity in an allosteric enzyme. Pisco JP, de Chiara C, Pacholarz KJ, Garza-Garcia A, Ogrodowicz RW, Walker PA, Barran PE, Smerdon SJ, de Carvalho LPS. Nat Commun 8 203 (2017)


Reviews citing this publication (7)

  1. Cyclic di-AMP: another second messenger enters the fray. Corrigan RM, Gründling A. Nat Rev Microbiol 11 513-524 (2013)
  2. Direct binding targets of the stringent response alarmone (p)ppGpp. Kanjee U, Ogata K, Houry WA. Mol Microbiol 85 1029-1043 (2012)
  3. Phosphoribosyl Diphosphate (PRPP): Biosynthesis, Enzymology, Utilization, and Metabolic Significance. Hove-Jensen B, Andersen KR, Kilstrup M, Martinussen J, Switzer RL, Willemoës M. Microbiol Mol Biol Rev 81 e00040-16 (2017)
  4. Histidine biosynthesis, its regulation and biotechnological application in Corynebacterium glutamicum. Kulis-Horn RK, Persicke M, Kalinowski J. Microb Biotechnol 7 5-25 (2014)
  5. Maximizing efficiency of rumen microbial protein production. Hackmann TJ, Firkins JL. Front Microbiol 6 465 (2015)
  6. From cyanobacteria to plants: conservation of PII functions during plastid evolution. Chellamuthu VR, Alva V, Forchhammer K. Planta 237 451-462 (2013)
  7. Phosphoribosyltransferases and Their Roles in Plant Development and Abiotic Stress Response. Liu Y, Wu P, Li B, Wang W, Zhu B. Int J Mol Sci 24 11828 (2023)

Articles citing this publication (23)

  1. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Gründling A. Proc Natl Acad Sci U S A 110 9084-9089 (2013)
  2. Biosynthesis of Histidine. Winkler ME, Ramos-Montañez S. EcoSal Plus 3 (2009)
  3. Activation of the hetero-octameric ATP phosphoribosyl transferase through subunit interface rearrangement by a tRNA synthetase paralog. Champagne KS, Sissler M, Larrabee Y, Doublié S, Francklyn CS. J Biol Chem 280 34096-34104 (2005)
  4. Substrate recognition by the hetero-octameric ATP phosphoribosyltransferase from Lactococcus lactis. Champagne KS, Piscitelli E, Francklyn CS. Biochemistry 45 14933-14943 (2006)
  5. Regulation of the hetero-octameric ATP phosphoribosyl transferase complex from Thermotoga maritima by a tRNA synthetase-like subunit. Vega MC, Zou P, Fernandez FJ, Murphy GE, Sterner R, Popov A, Wilmanns M. Mol Microbiol 55 675-686 (2005)
  6. Relative contributions of nine genes in the pathway of histidine biosynthesis to the control of free histidine concentrations in Arabidopsis thaliana. Rees JD, Ingle RA, Smith JA. Plant Biotechnol J 7 499-511 (2009)
  7. Campylobacter jejuni adenosine triphosphate phosphoribosyltransferase is an active hexamer that is allosterically controlled by the twisting of a regulatory tail. Mittelstädt G, Moggré GJ, Panjikar S, Nazmi AR, Parker EJ. Protein Sci 25 1492-1506 (2016)
  8. The evolution of histidine biosynthesis in archaea: insights into the his genes structure and organization in LUCA. Fondi M, Emiliani G, Liò P, Gribaldo S, Fani R. J Mol Evol 69 512-526 (2009)
  9. Transition State Analysis of Adenosine Triphosphate Phosphoribosyltransferase. Moggré GJ, Poulin MB, Tyler PC, Schramm VL, Parker EJ. ACS Chem Biol 12 2662-2670 (2017)
  10. A dimeric catalytic core relates the short and long forms of ATP-phosphoribosyltransferase. Mittelstädt G, Jiao W, Livingstone EK, Moggré GJ, Nazmi AR, Parker EJ. Biochem J 475 247-260 (2018)
  11. Alterations in the two globular domains or in the connecting alpha-helix of bacterial ribosomal protein L9 induces +1 frameshifts. Leipuviene R, Björk GR. J Bacteriol 189 7024-7031 (2007)
  12. Letter Independent catalysis of the short form HisG from Lactococcus lactis. Livingstone EK, Mittelstädt G, Given FM, Parker EJ. FEBS Lett 590 2603-2610 (2016)
  13. Inverted Regulation of Multidrug Efflux Pumps, Acid Resistance, and Porins in Benzoate-Evolved Escherichia coli K-12. Moore JP, Li H, Engmann ML, Bischof KM, Kunka KS, Harris ME, Tancredi AC, Ditmars FS, Basting PJ, George NS, Bhagwat AA, Slonczewski JL. Appl Environ Microbiol 85 e00966-19 (2019)
  14. Letter Inference from proteobacterial operons shows piecewise organization: a reply to Price et al. Fani R, Brilli M, Liò P. J Mol Evol 63 577-580 (2006)
  15. Allosteric Activation Shifts the Rate-Limiting Step in a Short-Form ATP Phosphoribosyltransferase. Fisher G, Thomson CM, Stroek R, Czekster CM, Hirschi JS, da Silva RG. Biochemistry 57 4357-4367 (2018)
  16. Histidine Regulates Seed Oil Deposition through Abscisic Acid Biosynthesis and β-Oxidation. Ma H, Wang S. Plant Physiol 172 848-857 (2016)
  17. Two ATP phosphoribosyltransferase isozymes of Geobacter sulfurreducens contribute to growth in the presence or absence of histidine and under nitrogen fixation conditions. Aklujkar M. Can J Microbiol 57 547-558 (2011)
  18. ATP phosphoribosyltransferase from symbiont Entomomyces delphacidicola invovled in histidine biosynthesis of Nilaparvata lugens (Stål). Wan PJ, Tang YH, Yuan SY, Wang WX, Lai FX, Yu XP, Fu Q. Amino Acids 48 2605-2617 (2016)
  19. Hinge Twists and Population Shifts Deliver Regulated Catalysis for ATP-PRT in Histidine Biosynthesis. Jiao W, Mittelstädt G, Moggré GJ, Parker EJ. Biophys J 116 1887-1897 (2019)
  20. Crystal structure of a hypothetical protein, TTHA0829 from Thermus thermophilus HB8, composed of cystathionine-β-synthase (CBS) and aspartate-kinase chorismate-mutase tyrA (ACT) domains. Nakabayashi M, Shibata N, Ishido-Nakai E, Kanagawa M, Iio Y, Komori H, Ueda Y, Nakagawa N, Kuramitsu S, Higuchi Y. Extremophiles 20 275-282 (2016)
  21. Guarding the gateway to histidine biosynthesis in plants: Medicago truncatula ATP-phosphoribosyltransferase in relaxed and tense states. Ruszkowski M. Biochem J 475 2681-2697 (2018)
  22. Crystal Structure, Steady-State, and Pre-Steady-State Kinetics of Acinetobacter baumannii ATP Phosphoribosyltransferase. Read BJ, Cadzow AF, Alphey MS, Mitchell JBO, da Silva RG. Biochemistry 63 230-240 (2024)
  23. Multifactorial interaction of selenium, iron, xylose, and glycine on cordycepin metabolism in Cordyceps militaris. Zhao B, Zhang Y, Zhang S, Hu T, Guo Y. Appl Microbiol Biotechnol 107 7403-7416 (2023)


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