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Roles of distal Asp in heme oxygenase from Corynebacterium diphtheriae, HmuO: A water-driven oxygen activation mechanism.

Matsui T, Furukawa M, Unno M, Tomita T, Ikeda-Saito M
J Biol Chem 280 2981-9 (2005)
Related entries: 1wnv, 1wnx

Cited: 31 times
EuropePMC logo PMID: 15528205

Abstract

Heme oxygenases found in mammals, plants, and bacteria catalyze degradation of heme using the same mechanism. Roles of distal Asp (Asp-136) residue in HmuO, a heme oxygenase of Corynebacterium diphtheriae, have been investigated by site-directed mutagenesis, enzyme kinetics, resonance Raman spectroscopy, and x-ray crystallography. Replacements of the Asp-136 by Ala and Phe resulted in reduced heme degradation activity due to the formation of ferryl heme, showing that the distal Asp is critical in HmuO heme oxygenase activity. D136N HmuO catalyzed heme degradation at a similar efficiency to wild type and D136E HmuO, implying that the carboxylate moiety is not required for the heme catabolism by HmuO. Resonance Raman results suggest that the inactive ferryl heme formation in the HmuO mutants is induced by disruption of the interaction between a reactive Fe-OOH species and an adjacent distal pocket water molecule. Crystal structural analysis of the HmuO mutants confirms partial disappearance of this nearby water in D136A HmuO. Our results provide the first experimental evidence for the catalytic importance of the nearby water molecule that can be universally critical in heme oxygenase catalysis and propose that the distal Asp helps in positioning the key water molecule at a position suitable for efficient activation of the Fe-OOH species.

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Reviews citing this publication (6)

  1. Heme oxygenase and heme degradation. Kikuchi G, Yoshida T, Noguchi M. Biochem Biophys Res Commun 338 558-567 (2005)
  2. Structure and catalytic mechanism of heme oxygenase. Unno M, Matsui T, Ikeda-Saito M. Nat Prod Rep 24 553-570 (2007)
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  4. Biosynthetic inorganic chemistry. Lu Y. Angew Chem Int Ed Engl 45 5588-5601 (2006)
  5. Synthetic Fe/Cu Complexes: Toward Understanding Heme-Copper Oxidase Structure and Function. Adam SM, Wijeratne GB, Rogler PJ, Diaz DE, Quist DA, Liu JJ, Karlin KD. Chem Rev 118 10840-11022 (2018)
  6. Crystallographic studies of heme oxygenase complexed with an unstable reaction intermediate, verdoheme. Unno M, Matsui T, Ikeda-Saito M. J Inorg Biochem 113 102-109 (2012)

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  1. The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Reniere ML, Ukpabi GN, Harry SR, Stec DF, Krull R, Wright DW, Bachmann BO, Murphy ME, Skaar EP. Mol Microbiol 75 1529-1538 (2010)
  2. Convergent evolution of enzyme active sites is not a rare phenomenon. Gherardini PF, Wass MN, Helmer-Citterich M, Sternberg MJ. J Mol Biol 372 817-845 (2007)
  3. Resonance Raman spectroscopy of oxoiron(IV) porphyrin pi-cation radical and oxoiron(IV) hemes in peroxidase intermediates. Terner J, Palaniappan V, Gold A, Weiss R, Fitzgerald MM, Sullivan AM, Hosten CM. J Inorg Biochem 100 480-501 (2006)
  4. Distinct reaction pathways followed upon reduction of oxy-heme oxygenase and oxy-myoglobin as characterized by Mössbauer spectroscopy. Garcia-Serres R, Davydov RM, Matsui T, Ikeda-Saito M, Hoffman BM, Huynh BH. J Am Chem Soc 129 1402-1412 (2007)
  5. Heme utilization by pathogenic bacteria: not all pathways lead to biliverdin. Wilks A, Ikeda-Saito M. Acc Chem Res 47 2291-2298 (2014)
  6. O(2)- and H(2)O(2)-dependent verdoheme degradation by heme oxygenase: reaction mechanisms and potential physiological roles of the dual pathway degradation. Matsui T, Nakajima A, Fujii H, Matera KM, Migita CT, Yoshida T, Ikeda-Saito M. J Biol Chem 280 36833-36840 (2005)
  7. Electronic properties of the highly ruffled heme bound to the heme degrading enzyme IsdI. Takayama SJ, Ukpabi G, Murphy ME, Mauk AG. Proc Natl Acad Sci U S A 108 13071-13076 (2011)
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  9. Unique coupling of mono- and dioxygenase chemistries in a single active site promotes heme degradation. Matsui T, Nambu S, Goulding CW, Takahashi S, Fujii H, Ikeda-Saito M. Proc Natl Acad Sci U S A 113 3779-3784 (2016)
  10. Non-enzymatic conversion of chlorophyll-a into chlorophyll-d in vitro: a model oxidation pathway for chlorophyll-d biosynthesis. Fukusumi T, Matsuda K, Mizoguchi T, Miyatake T, Ito S, Ikeda T, Tamiaki H, Oba T. FEBS Lett 586 2338-2341 (2012)
  11. Spectroscopic insights into axial ligation and active-site H-bonding in substrate-bound human heme oxygenase-2. Gardner JD, Yi L, Ragsdale SW, Brunold TC. J Biol Inorg Chem 15 1117-1127 (2010)
  12. The orbital ground state of the azide-substrate complex of human heme oxygenase is an indicator of distal H-bonding: implications for the enzyme mechanism. Ogura H, Evans JP, Peng D, Satterlee JD, Ortiz de Montellano PR, La Mar GN. Biochemistry 48 3127-3137 (2009)
  13. Tyrosine oxidation in heme oxygenase: examination of long-range proton-coupled electron transfer. Smirnov VV, Roth JP. J Biol Inorg Chem 19 1137-1148 (2014)
  14. 1H NMR study of the effect of variable ligand on heme oxygenase electronic and molecular structure. Ma LH, Liu Y, Zhang X, Yoshida T, La Mar GN. J Inorg Biochem 103 10-19 (2009)
  15. A Metagenomic Analysis of Bacterial Microbiota in the Digestive Tract of Triatomines. Carels N, Gumiel M, da Mota FF, de Carvalho Moreira CJ, Azambuja P. Bioinform Biol Insights 11 1177932217733422 (2017)
  16. Coupling of the distal hydrogen bond network to the exogenous ligand in substrate-bound, resting state human heme oxygenase. Peng D, Ogura H, Zhu W, Ma LH, Evans JP, Ortiz de Montellano PR, La Mar GN. Biochemistry 48 11231-11242 (2009)
  17. Reaction intermediates in the heme degradation reaction by HutZ from Vibrio cholerae. Uchida T, Sekine Y, Dojun N, Lewis-Ballester A, Ishigami I, Matsui T, Yeh SR, Ishimori K. Dalton Trans 46 8104-8109 (2017)
  18. Hydrogen sulfide bypasses the rate-limiting oxygen activation of heme oxygenase. Matsui T, Sugiyama R, Sakanashi K, Tamura Y, Iida M, Nambu Y, Higuchi T, Suematsu M, Ikeda-Saito M. J Biol Chem 293 16931-16939 (2018)
  19. Solution 1H NMR characterization of substrate-free C. diphtheriae heme oxygenase: pertinence for determining magnetic axes in paramagnetic substrate complexes. Du Z, Unno M, Matsui T, Ikeda-Saito M, La Mar GN. J Inorg Biochem 104 1063-1070 (2010)
  20. A novel mechanism of heme degradation to biliverdin studied by QM/MM and QM calculations. Alavi FS, Gheidi M, Zahedi M, Safari N, Ryde U. Dalton Trans 47 8283-8291 (2018)
  21. Biomimic O2 activation hydroxylates a meso-carbon of the porphyrin ring regioselectively under mild conditions. Yamanishi K, Yairi T, Suzuki K, Kondo M. Chem Commun (Camb) 49 9296-9298 (2013)
  22. The Asp99-Arg188 salt bridge of the Pseudomonas aeruginosa HemO is critical in allowing conformational flexibility during catalysis. Heinzl GA, Huang W, Robinson E, Xue F, Moëne-Loccoz P, Wilks A. J Biol Inorg Chem 23 1057-1070 (2018)
  23. An unexpected reactivity of the P460 cofactor in hydroxylamine oxidoreductase. Dietl A, Maalcke W, Barends TR. Acta Crystallogr D Biol Crystallogr 71 1708-1713 (2015)
  24. Function Coupling Mechanism of PhuS and HemO in Heme Degradation. Lee MJY, Wang Y, Jiang Y, Li X, Ma J, Tan H, Turner-Wood K, Rahman MN, Chen G, Jia Z. Sci Rep 7 11273 (2017)


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