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Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin
Heme oxygenase (HO) converts heme to carbon monoxide, biliverdin, and free iron, products that are essential in cellular redox signaling and iron recycling. In higher plants, HO is also involved in the biosynthesis of photoreceptor pigment precursors. Despite many common enzymatic reactions, the ami...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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American Society for Biochemistry and Molecular Biology
2020
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7948506/ https://www.ncbi.nlm.nih.gov/pubmed/33839679 http://dx.doi.org/10.1074/jbc.RA120.016271 |
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author | Tohda, Rei Tanaka, Hideaki Mutoh, Risa Zhang, Xuhong Lee, Young-Ho Konuma, Tsuyoshi Ikegami, Takahisa Migita, Catharina T. Kurisu, Genji |
author_facet | Tohda, Rei Tanaka, Hideaki Mutoh, Risa Zhang, Xuhong Lee, Young-Ho Konuma, Tsuyoshi Ikegami, Takahisa Migita, Catharina T. Kurisu, Genji |
author_sort | Tohda, Rei |
collection | PubMed |
description | Heme oxygenase (HO) converts heme to carbon monoxide, biliverdin, and free iron, products that are essential in cellular redox signaling and iron recycling. In higher plants, HO is also involved in the biosynthesis of photoreceptor pigment precursors. Despite many common enzymatic reactions, the amino acid sequence identity between plant-type and other HOs is exceptionally low (∼19.5%), and amino acids that are catalytically important in mammalian HO are not conserved in plant-type HOs. Structural characterization of plant-type HO is limited to spectroscopic characterization by electron spin resonance, and it remains unclear how the structure of plant-type HO differs from that of other HOs. Here, we have solved the crystal structure of Glycine max (soybean) HO-1 (GmHO-1) at a resolution of 1.06 Å and carried out the isothermal titration calorimetry measurements and NMR spectroscopic studies of its interaction with ferredoxin, the plant-specific electron donor. The high-resolution X-ray structure of GmHO-1 reveals several novel structural components: an additional irregularly structured region, a new water tunnel from the active site to the surface, and a hydrogen-bonding network unique to plant-type HOs. Structurally important features in other HOs, such as His ligation to the bound heme, are conserved in GmHO-1. Based on combined data from X-ray crystallography, isothermal titration calorimetry, and NMR measurements, we propose the evolutionary fine-tuning of plant-type HOs for ferredoxin dependency in order to allow adaptation to dynamic pH changes on the stroma side of the thylakoid membrane in chloroplast without losing enzymatic activity under conditions of fluctuating light. |
format | Online Article Text |
id | pubmed-7948506 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | American Society for Biochemistry and Molecular Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-79485062021-03-19 Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin Tohda, Rei Tanaka, Hideaki Mutoh, Risa Zhang, Xuhong Lee, Young-Ho Konuma, Tsuyoshi Ikegami, Takahisa Migita, Catharina T. Kurisu, Genji J Biol Chem Research Article Heme oxygenase (HO) converts heme to carbon monoxide, biliverdin, and free iron, products that are essential in cellular redox signaling and iron recycling. In higher plants, HO is also involved in the biosynthesis of photoreceptor pigment precursors. Despite many common enzymatic reactions, the amino acid sequence identity between plant-type and other HOs is exceptionally low (∼19.5%), and amino acids that are catalytically important in mammalian HO are not conserved in plant-type HOs. Structural characterization of plant-type HO is limited to spectroscopic characterization by electron spin resonance, and it remains unclear how the structure of plant-type HO differs from that of other HOs. Here, we have solved the crystal structure of Glycine max (soybean) HO-1 (GmHO-1) at a resolution of 1.06 Å and carried out the isothermal titration calorimetry measurements and NMR spectroscopic studies of its interaction with ferredoxin, the plant-specific electron donor. The high-resolution X-ray structure of GmHO-1 reveals several novel structural components: an additional irregularly structured region, a new water tunnel from the active site to the surface, and a hydrogen-bonding network unique to plant-type HOs. Structurally important features in other HOs, such as His ligation to the bound heme, are conserved in GmHO-1. Based on combined data from X-ray crystallography, isothermal titration calorimetry, and NMR measurements, we propose the evolutionary fine-tuning of plant-type HOs for ferredoxin dependency in order to allow adaptation to dynamic pH changes on the stroma side of the thylakoid membrane in chloroplast without losing enzymatic activity under conditions of fluctuating light. American Society for Biochemistry and Molecular Biology 2020-12-24 /pmc/articles/PMC7948506/ /pubmed/33839679 http://dx.doi.org/10.1074/jbc.RA120.016271 Text en © 2020 THE AUTHORS https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Research Article Tohda, Rei Tanaka, Hideaki Mutoh, Risa Zhang, Xuhong Lee, Young-Ho Konuma, Tsuyoshi Ikegami, Takahisa Migita, Catharina T. Kurisu, Genji Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title | Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title_full | Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title_fullStr | Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title_full_unstemmed | Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title_short | Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
title_sort | crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7948506/ https://www.ncbi.nlm.nih.gov/pubmed/33839679 http://dx.doi.org/10.1074/jbc.RA120.016271 |
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