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Evidence that two enzyme-derived histidine ligands are sufficient for iron binding and catalysis by factor inhibiting HIF (FIH).

Hewitson KS, Holmes SL, Ehrismann D, Hardy AP, Chowdhury R, Schofield CJ, McDonough MA
J Biol Chem 283 25971-8 (2008)
Cited: 34 times
EuropePMC logo PMID: 18611856

Abstract

A 2-His-1-carboxylate triad of iron binding residues is present in many non-heme iron oxygenases including the Fe(II) and 2-oxoglutarate (2OG)-dependent dioxygenases. Three variants (D201A, D201E, and D201G) of the iron binding Asp-201 residue of an asparaginyl hydroxylase, factor inhibiting HIF (FIH), were made and analyzed. FIH-D201A and FIH-D201E did not catalyze asparaginyl hydroxylation, but in the presence of a reducing agent, they displayed enhanced 2OG turnover when compared with wild-type FIH. Turnover of 2OG by FIH-D201A was significantly stimulated by the addition of HIF-1alpha(786-826) peptide. Like FIH-D201A and D201E, the D201G variant enhanced 2OG turnover but rather unexpectedly catalyzed asparaginyl hydroxylation. Crystal structures of the FIH-D201A and D201G variants in complex with Fe(II)/Zn(II), 2OG, and HIF-1alpha(786-826/788-806) implied that only two FIH-based residues (His-199 and His-279) are required for metal binding. The results indicate that variation of 2OG-dependent dioxygenase iron-ligating residues as a means of functional assignment should be treated with caution. The results are of mechanistic interest in the light of recent biochemical and structural analyses of non-heme iron and 2OG-dependent halogenases that are similar to the FIH-D201A/G variants in that they use only two His-residues to ligate iron.

Articles - 3d8c mentioned but not cited (5)

  1. Evidence that two enzyme-derived histidine ligands are sufficient for iron binding and catalysis by factor inhibiting HIF (FIH). Hewitson KS, Holmes SL, Ehrismann D, Hardy AP, Chowdhury R, Schofield CJ, McDonough MA. J Biol Chem 283 25971-25978 (2008)
  2. Hypoxia inducible factor (HIF) as a model for studying inhibition of protein-protein interactions. Burslem GM, Kyle HF, Nelson A, Edwards TA, Wilson AJ. Chem Sci 8 4188-4202 (2017)
  3. The facial triad in the α-ketoglutarate dependent oxygenase FIH: A role for sterics in linking substrate binding to O2 activation. Hangasky JA, Taabazuing CY, Martin CB, Eron SJ, Knapp MJ. J Inorg Biochem 166 26-33 (2017)
  4. Substrate Promotes Productive Gas Binding in the α-Ketoglutarate-Dependent Oxygenase FIH. Taabazuing CY, Fermann J, Garman S, Knapp MJ. Biochemistry 55 277-286 (2016)
  5. Erratum: Further Correction: Hypoxia inducible factor (HIF) as a model for studying inhibition of protein-protein interactions. Burslem GM, Kyle HF, Nelson A, Edwards TA, Wilson AJ. Chem Sci 9 2008-2009 (2018)


Reviews citing this publication (8)

  1. Inhibition of 2-oxoglutarate dependent oxygenases. Rose NR, McDonough MA, King ON, Kawamura A, Schofield CJ. Chem Soc Rev 40 4364-4397 (2011)
  2. Structural studies on human 2-oxoglutarate dependent oxygenases. McDonough MA, Loenarz C, Chowdhury R, Clifton IJ, Schofield CJ. Curr Opin Struct Biol 20 659-672 (2010)
  3. The HIF pathway and erythrocytosis. Lee FS, Percy MJ. Annu Rev Pathol 6 165-192 (2011)
  4. Structure-function relationships of human JmjC oxygenases-demethylases versus hydroxylases. Markolovic S, Leissing TM, Chowdhury R, Wilkins SE, Lu X, Schofield CJ. Curr Opin Struct Biol 41 62-72 (2016)
  5. Autocatalysed oxidative modifications to 2-oxoglutarate dependent oxygenases. Mantri M, Zhang Z, McDonough MA, Schofield CJ. FEBS J 279 1563-1575 (2012)
  6. Imposing function down a (cupin)-barrel: secondary structure and metal stereochemistry in the αKG-dependent oxygenases. Hangasky JA, Taabazuing CY, Valliere MA, Knapp MJ. Metallomics 5 287-301 (2013)
  7. Structural definitions of Jumonji family demethylase selectivity. Pilka ES, James T, Lisztwan JH. Drug Discov Today 20 743-749 (2015)
  8. Adventures in Defining Roles of Oxygenases in the Regulation of Protein Biosynthesis. Walport LJ, Schofield CJ. Chem Rec 18 1760-1781 (2018)

Articles citing this publication (21)

  1. Quantitative high-throughput screening identifies 8-hydroxyquinolines as cell-active histone demethylase inhibitors. King ON, Li XS, Sakurai M, Kawamura A, Rose NR, Ng SS, Quinn AM, Rai G, Mott BT, Beswick P, Klose RJ, Oppermann U, Jadhav A, Heightman TD, Maloney DJ, Schofield CJ, Simeonov A. PLoS One 5 e15535 (2010)
  2. Structure of human RNA N⁶-methyladenine demethylase ALKBH5 provides insights into its mechanisms of nucleic acid recognition and demethylation. Aik W, Scotti JS, Choi H, Gong L, Demetriades M, Schofield CJ, McDonough MA. Nucleic Acids Res 42 4741-4754 (2014)
  3. Selective inhibitors of the JMJD2 histone demethylases: combined nondenaturing mass spectrometric screening and crystallographic approaches. Rose NR, Woon EC, Kingham GL, King ON, Mecinović J, Clifton IJ, Ng SS, Talib-Hardy J, Oppermann U, McDonough MA, Schofield CJ. J Med Chem 53 1810-1818 (2010)
  4. JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes. Cliffe LJ, Kieft R, Southern T, Birkeland SR, Marshall M, Sweeney K, Sabatini R. Nucleic Acids Res 37 1452-1462 (2009)
  5. Analysis of Jmjd6 cellular localization and testing for its involvement in histone demethylation. Hahn P, Wegener I, Burrells A, Böse J, Wolf A, Erck C, Butler D, Schofield CJ, Böttger A, Lengeling A. PLoS One 5 e13769 (2010)
  6. Studies on the catalytic domains of multiple JmjC oxygenases using peptide substrates. Williams ST, Walport LJ, Hopkinson RJ, Madden SK, Chowdhury R, Schofield CJ, Kawamura A. Epigenetics 9 1596-1603 (2014)
  7. Asparagine and aspartate hydroxylation of the cytoskeletal ankyrin family is catalyzed by factor-inhibiting hypoxia-inducible factor. Yang M, Ge W, Chowdhury R, Claridge TD, Kramer HB, Schmierer B, McDonough MA, Gong L, Kessler BM, Ratcliffe PJ, Coleman ML, Schofield CJ. J Biol Chem 286 7648-7660 (2011)
  8. Development of homogeneous luminescence assays for histone demethylase catalysis and binding. Kawamura A, Tumber A, Rose NR, King ON, Daniel M, Oppermann U, Heightman TD, Schofield C. Anal Biochem 404 86-93 (2010)
  9. First-principles study of non-heme Fe(II) halogenase SyrB2 reactivity. Kulik HJ, Blasiak LC, Marzari N, Drennan CL. J Am Chem Soc 131 14426-14433 (2009)
  10. Investigating the contribution of the active site environment to the slow reaction of hypoxia-inducible factor prolyl hydroxylase domain 2 with oxygen. Tarhonskaya H, Chowdhury R, Leung IK, Loik ND, McCullagh JS, Claridge TD, Schofield CJ, Flashman E. Biochem J 463 363-372 (2014)
  11. Aspartate/asparagine-β-hydroxylase crystal structures reveal an unexpected epidermal growth factor-like domain substrate disulfide pattern. Pfeffer I, Brewitz L, Krojer T, Jensen SA, Kochan GT, Kershaw NJ, Hewitson KS, McNeill LA, Kramer H, Münzel M, Hopkinson RJ, Oppermann U, Handford PA, McDonough MA, Schofield CJ. Nat Commun 10 4910 (2019)
  12. Biochemical and structural investigations clarify the substrate selectivity of the 2-oxoglutarate oxygenase JMJD6. Islam MS, McDonough MA, Chowdhury R, Gault J, Khan A, Pires E, Schofield CJ. J Biol Chem 294 11637-11652 (2019)
  13. Biochemical characterization of L-DOPA 2,3-dioxygenase, a single-domain type I extradiol dioxygenase from lincomycin biosynthesis. Colabroy KL, Hackett WT, Markham AJ, Rosenberg J, Cohen DE, Jacobson A. Arch Biochem Biophys 479 131-138 (2008)
  14. Distribution and prediction of catalytic domains in 2-oxoglutarate dependent dioxygenases. Kundu S. BMC Res Notes 5 410 (2012)
  15. O2 Activation by Nonheme FeII α-Ketoglutarate-Dependent Enzyme Variants: Elucidating the Role of the Facial Triad Carboxylate in FIH. Iyer SR, Chaplin VD, Knapp MJ, Solomon EI. J Am Chem Soc 140 11777-11783 (2018)
  16. Reaction pathway engineering converts a radical hydroxylase into a halogenase. Neugebauer ME, Kissman EN, Marchand JA, Pelton JG, Sambold NA, Millar DC, Chang MCY. Nat Chem Biol 18 171-179 (2022)
  17. Prevention of apoptosis by the interaction between FIH1 and Bax. Yan B, Kong M, Chen YH. Mol Cell Biochem 348 1-9 (2011)
  18. Human Oxygenase Variants Employing a Single Protein FeII Ligand Are Catalytically Active. Brasnett A, Pfeffer I, Brewitz L, Chowdhury R, Nakashima Y, Tumber A, McDonough MA, Schofield CJ. Angew Chem Int Ed Engl 60 14657-14663 (2021)
  19. Chloride Supports O2 Activation in the D201G Facial Triad Variant of Factor-Inhibiting Hypoxia Inducible Factor, an α-Ketoglutarate Dependent Oxygenase. Chaplin VD, Hangasky JA, Huang HT, Duan R, Maroney MJ, Knapp MJ. Inorg Chem 57 12588-12595 (2018)
  20. Assembly of a mononuclear ferrous site using a bulky aldehyde-imidazole ligand. Li J, Molenda MA, Biros SM, Staples RJ, Chavez FA. Inorganica Chim Acta 464 152-156 (2017)
  21. Hydroxylation of the NOTCH1 intracellular domain regulates Notch signaling dynamics. Ferrante F, Giaimo BD, Friedrich T, Sugino T, Mertens D, Kugler S, Gahr BM, Just S, Pan L, Bartkuhn M, Potente M, Oswald F, Borggrefe T. Cell Death Dis 13 600 (2022)


Related citations provided by authors (2)

  1. Structure of Factor-Inhibiting Hypoxia-Inducible Factor (Hif) Reveals Mechanism of Oxidative Modification of Hif-1 Alpha. Elkins JM, Hewitson KS, Mcneill LA, Seibel JF, Schlemminger I, Pugh CW, Ratcliffe PJ, Schofield CJ J. Biol. Chem. 278 1802- (2003)
  2. Selective Inhibition of Factor Inhibiting Hypoxia Inducible Factor. Mcdonough MA, Mcneill LA, Tilliet M, Papamicael CA, Chen QY, Banerji B, Hewitson KS, Schofield CJ J. Am. Chem. Soc. 127 7680- (2005)

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