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To understand better the relationship between this distinct structural characteristic and the functional properties of IsdI, spectroscopic, electrochemical, and crystallographic results are reported that provide evidence that this heme ruffling is essential to the catalytic activity of the protein and eliminates the need for the water cluster in the distal heme pocket that is essential for the activity of classical heme oxygenases. The lack of heme orientational disorder in\n                    <jats:sup>1<\/jats:sup>\n                    H-NMR spectra of the protein argues that the catalytic formation of \u03b2- and \u03b4-biliverdin in nearly equal yield results from the ability of the protein to attack opposite sides of the heme ring rather than from binding of the heme substrate in two alternative orientations.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1101459108","type":"journal-article","created":{"date-parts":[[2011,7,26]],"date-time":"2011-07-26T00:02:29Z","timestamp":1311638549000},"page":"13071-13076","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":53,"title":["Electronic properties of the highly ruffled heme bound to the heme degrading enzyme IsdI"],"prefix":"10.1073","volume":"108","author":[{"given":"Shin-ichi J.","family":"Takayama","sequence":"first","affiliation":[{"name":"Department of Biochemistry and Molecular Biology,"},{"name":"University of British Columbia (UBC) Centre for Blood Research, and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georgia","family":"Ukpabi","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Life Sciences Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z3"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael E. 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J Am Chem Soc 132, 2811\u20132820 (2010).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/j.ica.2007.05.044","article-title":"Assignment of ferriheme resonances for high- and low-spin forms of nitrophorin 3 by 1H and 13C NMR spectroscopy and comparison to nitrophorin 2: Heme pocket structural similarities and differences","volume":"361","author":"Shokhireva TK","year":"2008","unstructured":"TK Shokhireva, RE Berry, H Zhang, NV Shokhirev, FA Walker, Assignment of ferriheme resonances for high- and low-spin forms of nitrophorin 3 by 1H and 13C NMR spectroscopy and comparison to nitrophorin 2: Heme pocket structural similarities and differences. Inorg Chim Acta 361, 925\u2013940 (2008).","journal-title":"Inorg Chim Acta"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"16267","DOI":"10.1021\/bi971677a","article-title":"Two enzymes with a common function but different heme ligands in the forms as isolated. Optical and magnetic properties of the heme groups in the oxidized forms of nitrite reductase, cytochrome cd1, from Pseudomonas stutzeri and Thiosphaera pantotropha","volume":"36","author":"Cheesman MR","year":"1997","unstructured":"MR Cheesman, et al., Two enzymes with a common function but different heme ligands in the forms as isolated. Optical and magnetic properties of the heme groups in the oxidized forms of nitrite reductase, cytochrome cd1, from Pseudomonas stutzeri and Thiosphaera pantotropha. Biochemistry 36, 16267\u201316276 (1997).","journal-title":"Biochemistry"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0010-8545(99)00029-6","article-title":"Magnetic spectroscopic (EPR, ESEEM, M\u00f6ssbauer MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins","volume":"185","author":"Walker FA","year":"1999","unstructured":"FA Walker, Magnetic spectroscopic (EPR, ESEEM, M\u00f6ssbauer MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins. Coord Chem Rev 185-186, 471\u2013534 (1999).","journal-title":"Coord Chem Rev"},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"12794","DOI":"10.1021\/ja106252b","article-title":"Modulating heme redox potential through protein-induced porphyrin distortion","volume":"132","author":"Olea C","year":"2010","unstructured":"C Olea, J Kuriyan, MA Marletta, Modulating heme redox potential through protein-induced porphyrin distortion. J Am Chem Soc 132, 12794\u201312795 (2010).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1039\/a827031z","article-title":"Nonplanar porphyrins and their significance in proteins","volume":"27","author":"Shelnutt JA","year":"1998","unstructured":"JA Shelnutt, et al., Nonplanar porphyrins and their significance in proteins. 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J Inorg Biochem 101, 1394\u20131399 (2007).","journal-title":"J Inorg Biochem"},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"3733","DOI":"10.1021\/bi982707s","article-title":"Replacement of the proximal histidine iron ligand by a cysteine or tyrosine converts heme oxygenase to an oxidase","volume":"38","author":"Liu Y","year":"1999","unstructured":"Y Liu, et al., Replacement of the proximal histidine iron ligand by a cysteine or tyrosine converts heme oxygenase to an oxidase. Biochemistry 38, 3733\u20133743 (1999).","journal-title":"Biochemistry"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"3979","DOI":"10.1021\/ja964007l","article-title":"Electrochemical generation and reactions of ferrylmyoglobins in water and microemulsions","volume":"119","author":"Onuoha AC","year":"1997","unstructured":"AC Onuoha, X Zu, JF Rusling, Electrochemical generation and reactions of ferrylmyoglobins in water and microemulsions. J Am Chem Soc 119, 3979\u20133986 (1997).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.jelechem.2004.07.011","article-title":"Direct electrochemistry and catalysis of heme-proteins entrapped in methyl cellulose films","volume":"574","author":"Li Y-M","year":"2004","unstructured":"Y-M Li, H-H Liu, D-W Pang, Direct electrochemistry and catalysis of heme-proteins entrapped in methyl cellulose films. J Electroanal Chem 574, 23\u201331 (2004).","journal-title":"J Electroanal Chem"},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1016\/S0021-9258(17)42212-5","article-title":"Heme\u2013heme oxygenase complex. Structure of the catalytic site and its implication for oxygen activation","volume":"269","author":"Takahashi S","year":"1994","unstructured":"S Takahashi, et al., Heme\u2013heme oxygenase complex. Structure of the catalytic site and its implication for oxygen activation. J Biol Chem 269, 1010\u20131014 (1994).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"6345","DOI":"10.1074\/jbc.270.11.6345","article-title":"Heme oxygenase-2","volume":"270","author":"Ishikawa K","year":"1995","unstructured":"K Ishikawa, et al., Heme oxygenase-2. J Biol Chem 270, 6345\u20136350 (1995).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"11842","DOI":"10.1021\/ja036147i","article-title":"The hydroxide complex of Pseudomonas aeruginosa heme oxygenase as a model of the low-spin iron(III) hydroperoxide intermediate in heme catabolism: 13C NMR spectroscopic studies suggest the active participation of the heme in macrocycle hydroxylation","volume":"125","author":"Caignan GA","year":"2003","unstructured":"GA Caignan, et al., The hydroxide complex of Pseudomonas aeruginosa heme oxygenase as a model of the low-spin iron(III) hydroperoxide intermediate in heme catabolism: 13C NMR spectroscopic studies suggest the active participation of the heme in macrocycle hydroxylation. J Am Chem Soc 125, 11842\u201311852 (2003).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","first-page":"24490","DOI":"10.1074\/jbc.274.35.24490","article-title":"The heme complex of HmuO a bacterial heme degradation enzyme from Corynebacterium diphtheriae","volume":"274","author":"Chu GC","year":"1999","unstructured":"GC Chu, T Tomita, FD S\u00f6nnichsen, T Yoshida, M Ikeda-Saito, The heme complex of HmuO a bacterial heme degradation enzyme from Corynebacterium diphtheriae. J Biol Chem 274, 24490\u201324496 (1999).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_43_2","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/0167-4838(93)90093-7","article-title":"Dynamics and thermodynamics of acid-alkaline transitions in metmyoglobins lacking the usual distal histidine residue","volume":"1203","author":"Yamamoto Y","year":"1993","unstructured":"Y Yamamoto, T Suzuki, H Hori, Dynamics and thermodynamics of acid-alkaline transitions in metmyoglobins lacking the usual distal histidine residue. 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J Am Chem Soc 128, 6657\u20136668 (2006).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"1780","DOI":"10.1021\/ol100434w","article-title":"Hybrid orbital deformation (HOD) effect and spectral red-shift property of nonplanar porphyrin","volume":"12","author":"Zhou Z","year":"2010","unstructured":"Z Zhou, C Cao, Q Liu, R Jiang, Hybrid orbital deformation (HOD) effect and spectral red-shift property of nonplanar porphyrin. Org Lett 12, 1780\u20131783 (2010).","journal-title":"Org Lett"},{"key":"e_1_3_4_46_2","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1021\/ja0280933","article-title":"Origin of the red shifts in the optical absorption bands of nonplanar tetraalkylporphyrins","volume":"125","author":"Haddad RE","year":"2003","unstructured":"RE Haddad, et al., Origin of the red shifts in the optical absorption bands of nonplanar tetraalkylporphyrins. J Am Chem Soc 125, 1253\u20131268 (2003).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_47_2","doi-asserted-by":"crossref","first-page":"8099","DOI":"10.1021\/ja0202659","article-title":"Do nonplanar distortions of porphyrins bring about strongly red-shifted electronic spectra? Controversy, consensus, new developments, and relevance to chelatases","volume":"124","author":"Ryeng H","year":"2002","unstructured":"H Ryeng, A Ghosh, Do nonplanar distortions of porphyrins bring about strongly red-shifted electronic spectra? Controversy, consensus, new developments, and relevance to chelatases. J Am Chem Soc 124, 8099\u20138103 (2002).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_48_2","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1016\/j.ccr.2006.03.001","article-title":"Electronic structures of highly deformed iron(III) porphyrin complexes","volume":"250","author":"Nakamura M","year":"2006","unstructured":"M Nakamura, Electronic structures of highly deformed iron(III) porphyrin complexes. Coord Chem Rev 250, 2271\u20132294 (2006).","journal-title":"Coord Chem Rev"},{"key":"e_1_3_4_49_2","doi-asserted-by":"crossref","first-page":"3519","DOI":"10.1021\/ic0515352","article-title":"NMR and EPR studies of chloroiron(III) tetraphenyl-chlorin and its complexes with imidazoles and pyridines of widely differing basicities","volume":"45","author":"Cai S","year":"2006","unstructured":"S Cai, TK Shokhireva, DL Lichtenberger, FA Walker, NMR and EPR studies of chloroiron(III) tetraphenyl-chlorin and its complexes with imidazoles and pyridines of widely differing basicities. Inorg Chem 45, 3519\u20133531 (2006).","journal-title":"Inorg Chem"},{"key":"e_1_3_4_50_2","doi-asserted-by":"crossref","first-page":"2848","DOI":"10.1021\/ic049089q","article-title":"Magnetic resonance spectroscopic investigations of the electronic ground and excited states in strongly nonplanar iron(III) dodecasubstituted porphyrins","volume":"44","author":"Yatsunyk LA","year":"2005","unstructured":"LA Yatsunyk, NV Shokhirev, FA Walker, Magnetic resonance spectroscopic investigations of the electronic ground and excited states in strongly nonplanar iron(III) dodecasubstituted porphyrins. Inorg Chem 44, 2848\u20132866 (2005).","journal-title":"Inorg Chem"},{"key":"e_1_3_4_51_2","doi-asserted-by":"crossref","first-page":"12109","DOI":"10.1021\/ja961971a","article-title":"\u03c0-Acid ligands in iron(III) porphyrinates. Characterization of low-spin bis(tert-butylisocyanide)(porphyrinato)iron(III) complexes having ((d\n                  xz,d\n                  yz)4(d\n                  xy)1 ground states","volume":"118","author":"Walker FA","year":"1996","unstructured":"FA Walker, et al., \u03c0-Acid ligands in iron(III) porphyrinates. Characterization of low-spin bis(tert-butylisocyanide)(porphyrinato)iron(III) complexes having ((dxz,dyz)4(dxy)1 ground states. J Am Chem Soc 118, 12109\u201312118 (1996).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_52_2","doi-asserted-by":"crossref","first-page":"7066","DOI":"10.1021\/ja00044a017","article-title":"Models of the cytochromes b. Low-spin bis-ligated (porphinato)iron(III) complexes with unusual molecular structures and NMR, EPR, and M\u00f6ssbauer spectra","volume":"114","author":"Safo MK","year":"1992","unstructured":"MK Safo, et al., Models of the cytochromes b. Low-spin bis-ligated (porphinato)iron(III) complexes with unusual molecular structures and NMR, EPR, and M\u00f6ssbauer spectra. J Am Chem Soc 114, 7066\u20137075 (1992).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_53_2","doi-asserted-by":"crossref","first-page":"7373","DOI":"10.1021\/ja960344i","article-title":"Low-temperature MCD studies of low-spin ferric complexes of tetramesitylporphyrinate: Evidence for the novel (d\n                  xz,d\n                  yz)4(d\n                  xy)1 ground state which models the spectroscopic properties of heme d","volume":"118","author":"Cheesman MR","year":"1996","unstructured":"MR Cheesman, FA Walker, Low-temperature MCD studies of low-spin ferric complexes of tetramesitylporphyrinate: Evidence for the novel (dxz,dyz)4(dxy)1 ground state which models the spectroscopic properties of heme d. J Am Chem Soc 118, 7373\u20137380 (1996).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_54_2","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.jinorgbio.2004.09.016","article-title":"Heme oxygenase, steering dioxygen activation toward heme hydroxylation","volume":"99","author":"Rivera M","year":"2005","unstructured":"M Rivera, Y Zeng, Heme oxygenase, steering dioxygen activation toward heme hydroxylation. J Inorg Biochem 99, 337\u2013354 (2005).","journal-title":"J Inorg Biochem"},{"key":"e_1_3_4_55_2","doi-asserted-by":"crossref","first-page":"6077","DOI":"10.1021\/ja017334o","article-title":"Models of the low-spin iron(III) hydroperoxide intermediate of heme oxygenase: Magnetic resonance evidence for thermodynamic stabilization of the dxy electronic state at ambient temperatures","volume":"124","author":"Rivera M","year":"2002","unstructured":"M Rivera, et al., Models of the low-spin iron(III) hydroperoxide intermediate of heme oxygenase: Magnetic resonance evidence for thermodynamic stabilization of the dxy electronic state at ambient temperatures. J Am Chem Soc 124, 6077\u20136089 (2002).","journal-title":"J Am Chem Soc"},{"key":"e_1_3_4_56_2","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s007750050115","article-title":"Control of metalloprotein redox potentials: What does site-directed mutagenesis of hemoproteins tell us?","volume":"2","author":"Mauk AG","year":"1997","unstructured":"AG Mauk, GR Moore, Control of metalloprotein redox potentials: What does site-directed mutagenesis of hemoproteins tell us? J Biol Inorg Chem 2, 119\u2013125 (1997).","journal-title":"J Biol Inorg Chem"},{"key":"e_1_3_4_57_2","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/S0014-5793(00)01353-3","article-title":"Crystal structure of rat heme oxygenase-1 in complex with heme","volume":"471","author":"Sugishima M","year":"2000","unstructured":"M Sugishima, et al., Crystal structure of rat heme oxygenase-1 in complex with heme. FEBS Lett 471, 61\u201366 (2000).","journal-title":"FEBS Lett"},{"key":"e_1_3_4_58_2","article-title":"Recent changes to the MOSFLM package for processing film and image plate data","author":"Leslie AGW","year":"1992","unstructured":"AGW Leslie, Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography No. 26, 1992).","journal-title":"Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography No. 26"},{"key":"e_1_3_4_59_2","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1107\/S0907444994003112","article-title":"The CCP4 suite: Programs for protein crystallography","volume":"50","year":"1994","unstructured":", The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760\u2013763 (1994).","journal-title":"Acta Crystallogr D Biol Crystallogr"},{"key":"e_1_3_4_60_2","doi-asserted-by":"crossref","first-page":"1022","DOI":"10.1107\/S0021889897006766","article-title":"MOLREP: An automated program for molecular replacement","volume":"30","author":"Vagin A","year":"1997","unstructured":"A Vagin, A Teplyakov, MOLREP: An automated program for molecular replacement. J Appl Crystallogr 30, 1022\u20131025 (1997).","journal-title":"J Appl Crystallogr"},{"key":"e_1_3_4_61_2","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1107\/S0907444996012255","article-title":"Refinement of macromolecular structures by the maximum-likelihood method","volume":"53","author":"Murshudov GN","year":"1997","unstructured":"GN Murshudov, AA Vagin, EJ Dodson, Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240\u2013255 (1997).","journal-title":"Acta Crystallogr D Biol Crystallogr"},{"key":"e_1_3_4_62_2","doi-asserted-by":"crossref","first-page":"2126","DOI":"10.1107\/S0907444904019158","article-title":"Coot: Model-building tools for molecular graphics","volume":"60","author":"Emsley P","year":"2004","unstructured":"P Emsley, K Cowtan, Coot: Model-building tools for molecular graphics. 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