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Review Article

The dynamic determinants of reaction specificity in the IMPDH/GMPR family of (β/α)8 barrel enzymes

Pages 250-263 | Received 01 Oct 2011, Accepted 09 Jan 2012, Published online: 15 Feb 2012

References

  • Anantharaman V, Aravind L, Koonin EV. 2003. Emergence of diverse biochemical activities in evolutionarily conserved structural scaffolds of proteins. Curr Opin Chem Biol 7:12–20.
  • Andrews SC, Guest JR. 1988. Nucleotide sequence of the gene encoding the GMP reductase of Escherichia coli K12. Biochem J 255:35–43.
  • Bateman A. 1997. The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem Sci 22:12–13.
  • Bowne SJ, Sullivan LS, Mortimer SE, Hedstrom L, Zhu J, Spellicy CJ, Gire AI, Hughbanks-Wheaton D, Birch DG, Lewis RA, Heckenlively JR, Daiger SP. 2006. Spectrum and frequency of mutations in IMPDH1 associated with autosomal dominant retinitis pigmentosa and leber congenital amaurosis. Invest Ophthalmol Vis Sci 47:34–42.
  • Brox LW, Hampton A. 1968. Inactivation of guanosine 5′-phosphate reductase by 6-chloro-, 6-mercapto-, and 2-amino-6-mercapto-9-β-D-ribofuranosylpurine 5′-phosphates. Biochemistry 7:398–406.
  • Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UC, Besteiro S, Sicheritz-Ponten T, Noel CJ, Dacks JB, Foster PG, Simillion C, Van dePeer Y, Miranda-Saavedra D, Barton GJ, Westrop GD, Müller S, Dessi D, Fiori PL, Ren Q, Paulsen I, Zhang H, Bastida-Corcuera FD, Simoes-Barbosa A, Brown MT, Hayes RD, Mukherjee M, Okumura CY, Schneider R, Smith AJ, Vanacova S, Villalvazo M, Haas BJ, Pertea M, Feldblyum TV, Utterback TR, Shu CL, Osoegawa K, de Jong PJ, Hrdy I, Horvathova L, Zubacova Z, Dolezal P, Malik SB, Logsdon JM Jr, Henze K, Gupta A, Wang CC, Dunne RL, Upcroft JA, Upcroft P, White O, Salzberg SL, Tang P, Chiu CH, Lee YS, Embley TM, Coombs GH, Mottram JC, Tachezy J, Fraser-Liggett CM, Johnson PJ. 2007. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212.
  • Carr SF, Papp E, Wu JC, Natsumeda Y. 1993. Characterization of human type I and type II IMP dehydrogenases. J Biol Chem 268:27286–27290.
  • Chen L, Pankiewicz KW. 2007. Recent development of IMP dehydrogenase inhibitors for the treatment of cancer. Curr Opin Drug Discov Devel 10:403–412.
  • Cornuel JF, Moraillon A, Guéron M. 2002. Participation of yeast inosine 5′-monophosphate dehydrogenase in an in vitro complex with a fragment of the C-rich telomeric strand. Biochimie 84:279–289.
  • Deng Y, Wang Z, Ying K, Gu S, Ji C, Huang Y, Gu X, Wang Y, Xu Y, Li Y, Xie Y, Mao Y. 2002. NADPH-dependent GMP reductase isoenzyme of human (GMPR2). Expression, purification, and kinetic properties. Int J Biochem Cell Biol 34:1035–1050.
  • Digits JA, Hedstrom L. 1999. Kinetic mechanism of Tritrichomonas foetus inosine 5′-monophosphate dehydrogenase. Biochemistry 38:2295–2306.
  • Digits JA, Hedstrom L. 2000. Drug selectivity is determined by coupling across the NAD+ site of IMP dehydrogenase. Biochemistry 39:1771–1777.
  • Eppler RK, Komor RS, Huynh J, Dordick JS, Reimer JA, Clark DS. 2006. Water dynamics and salt-activation of enzymes in organic media: mechanistic implications revealed by NMR spectroscopy. Proc Natl Acad Sci USA 103:5706–5710.
  • Fonstein M, Kogan Y, Osterman A, Overbeek R, Vonstein V. 2003. Fellowship for the Interpretation of Genomes (FIG), The SEED http://theseed.uchicago.edu/FIG/index. cgi accessed June 11, 2011.
  • Gan L, Petsko GA, Hedstrom L. 2002. Crystal structure of a ternary complex of Tritrichomonas foetus inosine 5′-monophosphate dehydrogenase: NAD+ orients the active site loop for catalysis. Biochemistry 41:13309–13317.
  • Gan L, Seyedsayamdost MR, Shuto S, Matsuda A, Petsko GA, Hedstrom L. 2003. The immunosuppressive agent mizoribine monophosphate forms a transition state analogue complex with inosine monophosphate dehydrogenase. Biochemistry 42:857–863.
  • Gerlt JA, Raushel FM. 2003. Evolution of function in (β/α)8-barrel enzymes. Curr Opin Chem Biol 7:252–264.
  • Glasner ME, Gerlt JA, Babbitt PC. 2006. Evolution of enzyme superfamilies. Curr Opin Chem Biol 10:492–497.
  • Gollapalli DR, Macpherson IS, Liechti G, Gorla SK, Goldberg JB, Hedstrom L. 2010. Structural determinants of inhibitor selectivity in prokaryotic IMP dehydrogenases. Chem Biol 17:1084–1091.
  • Guillén Schlippe YV, Hedstrom L. 2005. Is Arg418 the catalytic base required for the hydrolysis step of the IMP dehydrogenase reaction? Biochemistry 44:11700–11707.
  • Guillén Schlippe YV, Hedstrom L. 2005a. Guanidine derivatives rescue the Arg418Ala mutation of Tritrichomonas foetus IMP dehydrogenase. Biochemistry 44:16695–16700.
  • Guillén Schlippe YV, Hedstrom L. 2005b. A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch Biochem Biophys 433:266–278.
  • Guillén Schlippe YV, Riera TV, Seyedsayamdost MR, Hedstrom L. 2004. Substitution of the conserved Arg-Tyr dyad selectively disrupts the hydrolysis phase of the IMP dehydrogenase reaction. Biochemistry 43:4511–4521.
  • Gunter JH, Thomas EC, Lengefeld N, Kruger SJ, Worton L, Gardiner EM, Jones A, Barnett NL, Whitehead JP. 2008. Characterisation of inosine monophosphate dehydrogenase expression during retinal development: differences between variants and isoforms. Int J Biochem Cell Biol 40:1716–1728.
  • Hansen AK, Moran NA. 2011. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci USA 108:2849–2854.
  • Hansen BG, Sun XE, Genee HJ, Kaas CS, Nielsen JB, Mortensen UH, Frisvad JC, Hedstrom L. 2011. Adaptive evolution of drug targets in producer and non-producer organisms. Biochem J 441:219–226.
  • Hedstrom L. 2009. IMP dehydrogenase: structure, mechanism, and inhibition. Chem Rev 109:2903–2928.
  • Hedstrom L, Gan L. 2006. IMP dehydrogenase: structural schizophrenia and an unusual base. Curr Opin Chem Biol 10:520–525.
  • Hedstrom L, Liechti G, Goldberg JB, Gollapalli DR. 2011. The antibiotic potential of prokaryotic IMP dehydrogenase inhibitors. Curr Med Chem 18:1909–1918.
  • Heyde E, Nagabhushanam A, Vonarx M, Morrison JF. 1976. Studies on inosine monophosphate dehydrogenase. Steady state kinetics. Biochim Biophys Acta 429:645–660.
  • Holmes EW, Pehlke DM, Kelley WN. 1974. Human IMP dehydrogenase. Kinetics and regulatory properties. Biochim Biophys Acta 364:209–217.
  • Ignoul S, Eggermont J. 2005. CBS domains: structure, function, and pathology in human proteins. Am J Physiol, Cell Physiol 289:C1369–C1378.
  • Jackson RC, Weber G, Morris HP. 1975. IMP dehydrogenase, an enzyme linked with proliferation and malignancy. Nature 256:331–333.
  • Jämsen J, Tuominen H, Salminen A, Belogurov GA, Magretova NN, Baykov AA, Lahti R. 2007. A CBS domain-containing pyrophosphatase of Moorella thermoacetica is regulated by adenine nucleotides. Biochem J 408:327–333.
  • Janosík M, Kery V, Gaustadnes M, Maclean KN, Kraus JP. 2001. Regulation of human cystathionine β-synthase by s-adenosyl-l-methionine: evidence for two catalytically active conformations involving an autoinhibitory domain in the C-terminal region. Biochemistry 40:10625–10633.
  • Jentsch TJ. 2008. CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol Biol 43:3–36.
  • Ji R, Brune A. 2006. Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78:267–283.
  • Josephine HR, Ravichandran KR, Hedstrom L. 2010. The Cys319 loop modulates the transition between dehydrogenase and hydrolase conformations in inosine 5′-monophosphate dehydrogenase. Biochemistry 49:10674–10681.
  • Kerr KM, Cahoon M, Bosco DA, Hedstrom L. 2000. Monovalent cation activation in Escherichia coli inosine 5′-monophosphate dehydrogenase. Arch Biochem Biophys 375:131–137.
  • Kessler AI, Gots JS. 1985. Regulation of guaC expression in Escherichia coli. J Bacteriol 164:1288–1293.
  • Kim HS, Mittenthal JE, Caetano-Anollés G. 2006. MANET: tracing evolution of protein architecture in metabolic networks. BMC Bioinformatics 7:351.
  • Köhler GA, Gong X, Bentink S, Theiss S, Pagani GM, Agabian N, Hedstrom L. 2005. The functional basis of mycophenolic acid resistance in Candida albicans IMP dehydrogenase. J Biol Chem 280:11295–11302.
  • Kuehner JN, Brow DA. 2008. Regulation of a eukaryotic gene by GTP-dependent start site selection and transcription attenuation. Mol Cell 31:201–211.
  • Li J, Wei Z, Zheng M, Gu X, Deng Y, Qiu R, Chen F, Ji C, Gong W, Xie Y, Mao Y. 2006. Crystal structure of human guanosine monophosphate reductase 2 (GMPR2) in complex with GMP. J Mol Biol 355:980–988.
  • Link JO, Straub K. 1996. Trapping of an IMP dehydrogenase-substrate covalent interemediate by mycophenolic acid. J Am Chem Soc 118:2091–2092.
  • Liu YC, Li F, Handler J, Huang CR, Xiang Y, Neretti N, Sedivy JM, Zeller KI, Dang CV. 2008. Global regulation of nucleotide biosynthetic genes by c-Myc. PLoS ONE 3:e2722.
  • Lo Conte L, Brenner SE, Hubbard TJ, Chothia C, Murzin AG. 2002. SCOP database in 2002: refinements accommodate structural genomics. Nucleic Acids Res 30:264–267.
  • Looker DL, Marr JJ, Berens RL. 1986. Mechanisms of action of pyrazolopyrimidines in Leishmania donovani. J Biol Chem 261:9412–9415.
  • Mackenzie JJ, Sorensen LB. 1973. Guanosine 5′-phosphate reductase of human erythrocytes. Biochim Biophys Acta 327:282–294.
  • Macpherson IS, Kirubakaran S, Gorla SK, Riera TV, D’Aquino JA, Zhang M, Cuny GD, Hedstrom L. 2010. The structural basis of Cryptosporidium - specific IMP dehydrogenase inhibitor selectivity. J Am Chem Soc 132:1230–1231.
  • Mager J, Magasanik B. 1960. Guanosine 5′-phosphate reductase and its role in the interconversion of purine nucleotides. J Biol Chem 235:1474–1478.
  • Martinelli LK, Ducati RG, Rosado LA, Breda A, Selbach BP, Santos DS, Basso LA. 2011. Recombinant Escherichia coli GMP reductase: kinetic, catalytic and chemical mechanisms, and thermodynamics of enzyme-ligand binary complex formation. Mol Biosyst 7:1289–1305.
  • McLean JE, Hamaguchi N, Belenky P, Mortimer SE, Stanton M, Hedstrom L. 2004. Inosine 5′-monophosphate dehydrogenase binds nucleic acids in vitro and in vivo. Biochem J 379:243–251.
  • Min D, Josephine HR, Li H, Lakner C, Macpherson IS, Naylor GJ, Swofford D, Hedstrom L, Yang W. 2008. An enzymatic atavist revealed in dual pathways for water activation. PLoS Biol 6:e206.
  • Minegishi S, Mayr H. 2003. How constant are Ritchie’s “constant selectivity relationships”? A general reactivity scale for n-, pi-, and sigma-nucleophiles. J Am Chem Soc 125:286–295.
  • Moffat KG, Mackinnon G. 1985. Cloning of the Escherichia coli K-12 guaC gene following its transposition into the RP4::Mu cointegrate. Gene 40:141–143.
  • Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML. 2007. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926.
  • Mortimer SE, Hedstrom L. 2005. Autosomal dominant retinitis pigmentosa mutations in inosine 5′-monophosphate dehydrogenase type I disrupt nucleic acid binding. Biochem J 390:41–47.
  • Mortimer SE, Xu D, McGrew D, Hamaguchi N, Lim HC, Bowne SJ, Daiger SP, Hedstrom L. 2008. IMP dehydrogenase type 1 associates with polyribosomes translating rhodopsin mRNA. J Biol Chem 283:36354–36360.
  • Musa-Aziz R, Chen LM, Pelletier MF, Boron WF. 2009. Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 106:5406–5411.
  • Nagano N, Orengo CA, Thornton JM. 2002. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol 321:741–765.
  • Nair V, Shu Q. 2007. Inosine monophosphate dehydrogenase as a probe in antiviral drug discovery. Antivir Chem Chemother 18:245–258.
  • Nimmesgern E, Black J, Futer O, Fulghum JR, Chambers SP, Brummel CL, Raybuck SA, Sintchak MD. 1999. Biochemical analysis of the modular enzyme inosine 5′-monophosphate dehydrogenase. Protein Expr Purif 17:282–289.
  • Oláh E, Kökény S, Papp J, Bozsik A, Keszei M. 2006. Modulation of cancer pathways by inhibitors of guanylate metabolism. Adv Enzyme Regul 46:176–190.
  • Orengo CA, Michie AD, Jones S, Jones DT, Swindells MB, Thornton JM. 1997. CATH–a hierarchic classification of protein domain structures. Structure 5:1093–1108.
  • Pankiewicz KW, Patterson SE, Black PL, Jayaram HN, Risal D, Goldstein BM, Stuyver LJ, Schinazi RF. 2004. Cofactor mimics as selective inhibitors of NAD-dependent inosine monophosphate dehydrogenase (IMPDH)–the major therapeutic target. Curr Med Chem 11:887–900.
  • Park JH, Ahn SH. 2010. IMP dehydrogenase is recruited to the transcription complex through serine 2 phosphorylation of RNA polymerase II. Biochem Biophys Res Commun 392:588–592.
  • Patton GC, Stenmark P, Gollapalli DR, Sevastik R, Kursula P, Flodin S, Schuler H, Swales CT, Eklund H, Himo F, Nordlund P, Hedstrom L. 2011. Cofactor mobility determines reaction outcome in the IMPDH and GMPR (β/α)8 barrel enzymes. Nat Chem Biol 7:950–958.
  • Pimkin M, Markham GD. 2008. The CBS subdomain of inosine 5′-monophosphate dehydrogenase regulates purine nucleotide turnover. Mol Microbiol 68:342–359.
  • Pimkin M, Pimkina J, Markham GD. 2009. A regulatory role of the Bateman domain of IMP dehydrogenase in adenylate nucleotide biosynthesis. J Biol Chem 284:7960–7969.
  • Prosise GL, Luecke H. 2003. Crystal structures of Tritrichomonas foetus inosine monophosphate dehydrogenase in complex with substrate, cofactor and analogs: a structural basis for the random-in ordered-out kinetic mechanism. J Mol Biol 326:517–527.
  • Prosise GL, Wu JZ, Luecke H. 2002. Crystal structure of Tritrichomonas foetus inosine monophosphate dehydrogenase in complex with the inhibitor ribavirin monophosphate reveals a catalysis-dependent ion-binding site. J Biol Chem 277:50654–50659.
  • Ratcliffe AJ. 2006. Inosine 5′-monophosphate dehydrogenase inhibitors for the treatment of autoimmune diseases. Curr Opin Drug Discov Devel 9:595–605.
  • Renart MF, Renart J, Sillero MA, Sillero A. 1976a. Guanosine monophosphate reductase from Artemia salina: inhibition by xanthosine monophosphate and activation by diguanosine tetraphosphate. Biochemistry 15:4962–4966.
  • Renart MF, Renart J, Sillero MAG, Sillero A. 1976b. Guanosine monphosphate dehydrogenase from Artemia salina: inhibition by xanthosine monophosphate and activation by diguanosine tetraphosphate. Biochemistry 15:4962–4966.
  • Rhodes MM, Réblová K, Sponer J, Walter NG. 2006. Trapped water molecules are essential to structural dynamics and function of a ribozyme. Proc Natl Acad Sci USA 103:13380–13385.
  • Riera TV, Wang W, Josephine HR, Hedstrom L. 2008. A kinetic alignment of orthologous inosine-5′-monophosphate dehydrogenases. Biochemistry 47:8689–8696.
  • Riera TV, Zheng L, Josephine HR, Min D, Yang W, Hedstrom L. 2011. Allosteric activation via kinetic control: potassium accelerates a conformational change in IMP dehydrogenase. Biochemistry 50:8508–8518.
  • Salvatore D, Bartha T, Larsen PR. 1998. The guanosine monophosphate reductase gene is conserved in rats and its expression increases rapidly in brown adipose tissue during cold exposure. J Biol Chem 273:31092–31096.
  • Scott JW, Hawley SA, Green KA, Anis M, Stewart G, Scullion GA, Norman DG, Hardie DG. 2004. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113:274–284.
  • Sintchak MD, Fleming MA, Futer O, Raybuck SA, Chambers SP, Caron PR, Murcko MA, Wilson KP. 1996. Structure and mechanism of inosine monophosphate dehydrogenase in complex with the immunosuppressant mycophenolic acid. Cell 85:921–930.
  • Snyder FF, Henderson JF, Kim SC, Paterson AR, Brox LW. 1973. Purine nucleotide metabolism and nucleotide pool sizes in synchronized lymphoma L5178Y cells. Cancer Res 33:2425–2430.
  • Soskine M, Tawfik DS. 2010. Mutational effects and the evolution of new protein functions. Nat Rev Genet 11:572–582.
  • Spector T, Jones TE. 1982. Guanosine 5′-monophosphate reductase from Leishmania donovani. A possible chemotherapeutic target. Biochem Pharmacol 31:3891–3897.
  • Spector T, Jones TE, LaFon SW, Nelson DJ, Berens RL, Marr JJ. 1984. Monophosphates of formycin B and allopurinol riboside. Interactions with leishmanial and mammalian succino-AMP synthetase and GMP reductase. Biochem Pharmacol 33:1611–1617.
  • Spector T, Jones TE, Miller RL. 1979. Reaction mechanism and specificity of human GMP reductase. Substrates, inhibitors, activators, and inactivators. J Biol Chem 254:2308–2315.
  • Spellicy CJ, Daiger SP, Sullivan LS, Zhu J, Liu Q, Pierce EA, Bowne SJ. 2007. Characterization of retinal inosine monophosphate dehydrogenase 1 in several mammalian species. Mol Vis 13:1866–1872.
  • Stephens RW, Whittaker VK. 1973. Calf thymus GMP reductase: control by XMP. Biochem Biophys Res Commun 53:975–981.
  • Thomas MS, Drabble WT. 1984. Molecular cloning and characterisation of the gua regulatory region of Escherichia coli K12. Mol Gen Genet 195:238–245.
  • van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernández JM, Jiménez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Morán F, Moya A. 2003. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA 100:581–586.
  • Wang W, Hedstrom L. 1997. Kinetic mechanism of human inosine 5′-monophosphate dehydrogenase type II: random addition of substrates and ordered release of products. Biochemistry 36:8479–8483.
  • Weber G, Nakamura H, Natsumeda Y, Szekeres T, Nagai M. 1992. Regulation of GTP biosynthesis. Adv Enzyme Regul 32:57–69.
  • Wise EL, Rayment I. 2004. Understanding the importance of protein structure to nature’s routes for divergent evolution in TIM barrel enzymes. Acc Chem Res 37:149–158.
  • Xiang B, Taylor JC, Markham GD. 1996. Monovalent cation activation and kinetic mechanism of inosine 5′-monophosphate dehydrogenase. J Biol Chem 271:1435–1440.
  • Zahnle K, Schaefer L, Fegley B. 2010. Earth’s earliest atmospheres. Cold Spring Harb Perspect Biol 2:a004895.
  • Zalatan JG, Herschlag D. 2009. The far reaches of enzymology. Nat Chem Biol 5:516–520.
  • Zhang J, Zhang W, Zou D, Chen G, Wan T, Zhang M, Cao X. 2003. Cloning and functional characterization of GMPR2, a novel human guanosine monophosphate reductase, which promotes the monocytic differentiation of HL-60 leukemia cells. J Cancer Res Clin Oncol 129:76–83.
  • Zhang R, Evans G, Rotella F, Westbrook E, Huberman E, Joachimiak A, Collart FR. 1999. Differential signatures of bacterial and mammalian IMP dehydrogenase enzymes. Curr Med Chem 6:537–543.

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