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Crystal structure of rat heme oxygenase-1 in complex with heme.

Sugishima M, Omata Y, Kakuta Y, Sakamoto H, Noguchi M, Fukuyama K
FEBS Lett 471 61-6 (2000)
Cited: 72 times
EuropePMC logo PMID: 10760513

Abstract

Heme oxygenase catalyzes the oxidative cleavage of protoheme to biliverdin, the first step of heme metabolism utilizing O(2) and NADPH. We determined the crystal structures of rat heme oxygenase-1 (HO-1)-heme and selenomethionyl HO-1-heme complexes. Heme is sandwiched between two helices with the delta-meso edge of the heme being exposed to the surface. Gly143N forms a hydrogen bond to the distal ligand of heme, OH(-). The distance between Gly143N and the ligand is shorter than that in the human HO-1-heme complex. This difference may be related to a pH-dependent change of the distal ligand of heme. Flexibility of the distal helix may control the stability of the coordination of the distal ligand to heme iron. The possible role of Gly143 in the heme oxygenase reaction is discussed.

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  1. Structural and thermodynamic consequences of b heme binding for monomeric apoglobins and other apoproteins. Landfried DA, Vuletich DA, Pond MP, Lecomte JT. Gene 398 12-28 (2007)

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  2. Neuroprotective effects of melatonin and celecoxib against ethanol-induced neurodegeneration: a computational and pharmacological approach. Al Kury LT, Zeb A, Abidin ZU, Irshad N, Malik I, Alvi AM, Khalil AAK, Ahmad S, Faheem M, Khan AU, Shah FA, Li S. Drug Des Devel Ther 13 2715-2727 (2019)
  3. Electrostatic environment of hemes in proteins: pK(a)s of hydroxyl ligands. Song Y, Mao J, Gunner MR. Biochemistry 45 7949-7958 (2006)
  4. Flexible mapping of homology onto structure with homolmapper. Rockwell NC, Lagarias JC. BMC Bioinformatics 8 123 (2007)
  5. Mass spectrometric identification of lysine residues of heme oxygenase-1 that are involved in its interaction with NADPH-cytochrome P450 reductase. Higashimoto Y, Sugishima M, Sato H, Sakamoto H, Fukuyama K, Palmer G, Noguchi M. Biochem Biophys Res Commun 367 852-858 (2008)
  6. Carveol a Naturally-Derived Potent and Emerging Nrf2 Activator Protects Against Acetaminophen-Induced Hepatotoxicity. Rahman ZU, Al Kury LT, Alattar A, Tan Z, Alshaman R, Malik I, Badshah H, Uddin Z, Khan Khalil AA, Muhammad N, Khan S, Ali A, Shah FA, Li JB, Li S. Front Pharmacol 11 621538 (2020)
  7. Domain-Based Protein Docking with Extremely Large Conformational Changes. Christoffer C, Kihara D. J Mol Biol 434 167820 (2022)


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  1. Heme enzyme structure and function. Poulos TL. Chem Rev 114 3919-3962 (2014)
  2. Heme oxygenase and heme degradation. Kikuchi G, Yoshida T, Noguchi M. Biochem Biophys Res Commun 338 558-567 (2005)
  3. Heme degradation and vascular injury. Belcher JD, Beckman JD, Balla G, Balla J, Vercellotti G. Antioxid Redox Signal 12 233-248 (2010)
  4. Heme oxygenase: evolution, structure, and mechanism. Wilks A. Antioxid Redox Signal 4 603-614 (2002)
  5. Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. Shekhawat GS, Verma K. J Exp Bot 61 2255-2270 (2010)
  6. Structure and catalytic mechanism of heme oxygenase. Unno M, Matsui T, Ikeda-Saito M. Nat Prod Rep 24 553-570 (2007)
  7. Signaling function of heme oxygenase proteins. Dennery PA. Antioxid Redox Signal 20 1743-1753 (2014)
  8. Bacterial heme oxygenases. Frankenberg-Dinkel N. Antioxid Redox Signal 6 825-834 (2004)
  9. 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)
  10. Artificial metalloenzymes constructed from hierarchically-assembled proteins. Ueno T, Tabe H, Tanaka Y. Chem Asian J 8 1646-1660 (2013)
  11. 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)
  12. Crystal structure based design of functional metal/protein hybrids. Ueno T, Yokoi N, Abe S, Watanabe Y. J Inorg Biochem 101 1667-1675 (2007)
  13. The Nuclear Translocation of Heme Oxygenase-1 in Human Diseases. Yang Q, Wang W. Front Cell Dev Biol 10 890186 (2022)
  14. Recent Advances in the Understanding of the Reaction Chemistries of the Heme Catabolizing Enzymes HO and BVR Based on High Resolution Protein Structures. Sugishima M, Wada K, Fukuyama K. Curr Med Chem 27 3499-3518 (2020)

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  2. 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)
  3. Bacillus anthracis IsdG, a heme-degrading monooxygenase. Skaar EP, Gaspar AH, Schneewind O. J Bacteriol 188 1071-1080 (2006)
  4. Comparison of the heme-free and -bound crystal structures of human heme oxygenase-1. Lad L, Schuller DJ, Shimizu H, Friedman J, Li H, Ortiz de Montellano PR, Poulos TL. J Biol Chem 278 7834-7843 (2003)
  5. The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. Wegele R, Tasler R, Zeng Y, Rivera M, Frankenberg-Dinkel N. J Biol Chem 279 45791-45802 (2004)
  6. Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. Chim N, Iniguez A, Nguyen TQ, Goulding CW. J Mol Biol 395 595-608 (2010)
  7. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. Beckman JD, Chen C, Nguyen J, Thayanithy V, Subramanian S, Steer CJ, Vercellotti GM. J Biol Chem 286 3194-3202 (2011)
  8. Comparison of apo- and heme-bound crystal structures of a truncated human heme oxygenase-2. Bianchetti CM, Yi L, Ragsdale SW, Phillips GN. J Biol Chem 282 37624-37631 (2007)
  9. Crystal structure of heme oxygenase-1 from cyanobacterium Synechocystis sp. PCC 6803 in complex with heme. Sugishima M, Migita CT, Zhang X, Yoshida T, Fukuyama K. Eur J Biochem 271 4517-4525 (2004)
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  11. Oligomerization is crucial for the stability and function of heme oxygenase-1 in the endoplasmic reticulum. Hwang HW, Lee JR, Chou KY, Suen CS, Hwang MJ, Chen C, Shieh RC, Chau LY. J Biol Chem 284 22672-22679 (2009)
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  16. 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)
  17. Expression and characterization of cyanobacterium heme oxygenase, a key enzyme in the phycobilin synthesis. Properties of the heme complex of recombinant active enzyme. Migita CT, Zhang X, Yoshida T. Eur J Biochem 270 687-698 (2003)
  18. Solution NMR characterization of an unusual distal H-bond network in the active site of the cyanide-inhibited, human heme oxygenase complex of the symmetric substrate, 2,4-dimethyldeuterohemin. Li Y, Syvitski RT, Auclair K, Wilks A, Ortiz De Montellano PR, La Mar GN. J Biol Chem 277 33018-33031 (2002)
  19. Crystallographic and spectroscopic insights into heme degradation by Mycobacterium tuberculosis MhuD. Graves AB, Morse RP, Chao A, Iniguez A, Goulding CW, Liptak MD. Inorg Chem 53 5931-5940 (2014)
  20. MicroRNA-218 promotes high glucose-induced apoptosis in podocytes by targeting heme oxygenase-1. Yang H, Wang Q, Li S. Biochem Biophys Res Commun 471 582-588 (2016)
  21. The molecular basis of heme oxygenase deficiency in the pcd1 mutant of pea. Linley PJ, Landsberger M, Kohchi T, Cooper JB, Terry MJ. FEBS J 273 2594-2606 (2006)
  22. Alteration of the regiospecificity of human heme oxygenase-1 by unseating of the heme but not disruption of the distal hydrogen bonding network. Wang J, Evans JP, Ogura H, La Mar GN, Ortiz de Montellano PR. Biochemistry 45 61-73 (2006)
  23. Protein expressed by the ho2 gene of the cyanobacterium Synechocystis sp. PCC 6803 is a true heme oxygenase. Properties of the heme and enzyme complex. Zhang X, Migita CT, Sato M, Sasahara M, Yoshida T. FEBS J 272 1012-1022 (2005)
  24. Solution 1H NMR investigation of the active site molecular and electronic structures of substrate-bound, cyanide-inhibited HmuO, a bacterial heme oxygenase from Corynebacterium diphtheriae. Li Y, Syvitski RT, Chu GC, Ikeda-Saito M, Mar GN. J Biol Chem 278 6651-6663 (2003)
  25. Crystal structures of ferrous and ferrous-NO forms of verdoheme in a complex with human heme oxygenase-1: catalytic implications for heme cleavage. Lad L, Ortiz de Montellano PR, Poulos TL. J Inorg Biochem 98 1686-1695 (2004)
  26. Separation and identification of the regioisomers of verdoheme by reversed-phase ion-pair high-performance liquid chromatography, and characterization of their complexes with heme oxygenase. Sakamoto H, Omata Y, Adachi Y, Palmer G, Noguchi M. J Inorg Biochem 82 113-121 (2000)
  27. C-Terminal membrane spanning region of human heme oxygenase-1 mediates a time-dependent complex formation with cytochrome P450 reductase. Huber Iii WJ, Scruggs BA, Backes WL. Biochemistry 48 190-197 (2009)
  28. Expression of heme oxygenase-1 protects endothelial cells from irradiation-induced apoptosis. Ewing P, Wilke A, Eissner G, Holler E, Andreesen R, Gerbitz A. Endothelium 12 113-119 (2005)
  29. Spectroscopic characterization of a higher plant heme oxygenase isoform-1 from Glycine max (soybean)--coordination structure of the heme complex and catabolism of heme. Gohya T, Zhang X, Yoshida T, Migita CT. FEBS J 273 5384-5399 (2006)
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  31. The reactions of heme- and verdoheme-heme oxygenase-1 complexes with FMN-depleted NADPH-cytochrome P450 reductase. Electrons required for verdoheme oxidation can be transferred through a pathway not involving FMN. Higashimoto Y, Sato H, Sakamoto H, Takahashi K, Palmer G, Noguchi M. J Biol Chem 281 31659-31667 (2006)
  32. CO-trapping site in heme oxygenase revealed by photolysis of its co-bound heme complex: mechanism of escaping from product inhibition. Sugishima M, Sakamoto H, Noguchi M, Fukuyama K. J Mol Biol 341 7-13 (2004)
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  34. Crystal structures of the G139A, G139A-NO and G143H mutants of human heme oxygenase-1. A finely tuned hydrogen-bonding network controls oxygenase versus peroxidase activity. Lad L, Koshkin A, de Montellano PR, Poulos TL. J Biol Inorg Chem 10 138-146 (2005)
  35. Analysis of heme oxygenase isomers in rat. Xia ZW, Cui WJ, Zhang XH, Shen QX, Wang J, Li YZ, Chen SN, Yu SC. World J Gastroenterol 8 1123-1128 (2002)
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  49. Role of His63 in HutZ from Vibrio cholerae in the heme degradation reaction and heme binding. Uchida T, Dojun N, Sekine Y, Ishimori K. Dalton Trans 48 5408-5416 (2019)
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