Ordered Motions in the Nitric-Oxide Dioxygenase Mechanism of Flavohemoglobin and Assorted Globins with Tightly Coupled Reductases

Gardner, Paul R.

doi:10.1007/5584_2022_751

Paul R. Gardner²

Part of the book series: Advances in Experimental Medicine and Biology ((PROTRE,volume 1414))

223 Accesses
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Abstract

Nitric-oxide dioxygenases (NODs) activate and combine O₂ with NO to form nitrate. A variety of oxygen-binding hemoglobins with associated partner reductases or electron donors function as enzymatic NODs. Kinetic and structural investigations of the archetypal two-domain microbial flavohemoglobin-NOD have illuminated an allosteric mechanism that employs selective tunnels for O₂ and NO, gates for NO and nitrate, transient O₂ association with ferric heme, and an O₂ and NO-triggered, ferric heme spin crossover-driven, motion-controlled, and dipole-regulated electron-transfer switch. The proposed mechanism facilitates radical-radical coupling of ferric-superoxide with NO to form nitrate while preventing suicidal ferrous-NO formation. Diverse globins display the structural and functional motifs necessary for a similar allosteric NOD mechanism. In silico docking simulations reveal monomeric erythrocyte hemoglobin alpha-chain and beta-chain intrinsically matched and tightly coupled with NADH-cytochrome b₅ oxidoreductase and NADPH-cytochrome P450 oxidoreductase, respectively, forming membrane-bound flavohemoglobin-like mammalian NODs. The neuroprotective neuroglobin manifests a potential NOD role in a close-fitting ternary complex with membrane-bound NADH-cytochrome b₅ oxidoreductase and cytochrome b₅. Cytoglobin interfaces weakly with cytochrome b₅ for O₂ and NO-regulated electron-transfer and coupled NOD activity. The mechanistic model also provides insight into the evolution of O₂ binding cooperativity in hemoglobin and a basis for the discovery of allosteric NOD inhibitors.

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Abbreviations

B5:: Cytochrome b₅
B5OR:: NADH-cytochrome b₅ reductase
Cygb:: Cytoglobin
CYPOR:: NADPH-cytochrome P450 oxidoreductase
ET:: Electron transfer
flavoHb:: Flavohemoglobin
Hb:: Hemoglobin
Leghb:: Leghemoglobin
LT:: Long tunnel
Mb:: Myoglobin
MD:: Molecular dynamics
Ngb:: Neuroglobin
NOD:: Nitric-oxide dioxygenase
ST:: Short tunnel
VHb:: Vitreoscilla Hb

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Acknowledgments

This work was initiated at the Cincinnati Children’s Hospital Medical Center with support from an American Heart Association Scientist Development Grant (9730193 N), a National Institutes of Health Grant (GM65090), and the Cincinnati Children’s Hospital Research Foundation Trustees Grant. I am especially grateful to my collaborators, many of whom are listed as coauthors in the cited literature. To the many of those whose work contributed to this review but whom I have not acknowledged with citation, I apologize. For the incisive peer review comments, I am most grateful. I thank John Olson, and other members of the globin community, for helping me to initially recognize the NO inhibition paradox and potential complexities of the NOD mechanism and for sending me forth better prepared to resolve it. I acknowledge stimulating discussion and insight concerning the O-atom rearrangement mechanism generously given by the late Henry Taube. I thank David Beratan for steering me to relevant ET literature early on. Finally, I would also like to take this opportunity to thank Jane and Dave Richardson for their enthusiastic and inspiring lessons in protein structure, design, and graphic analysis during my graduate studies.

Conflicts of Interest

The author has financial interest in the development of therapeutic effectors of NODs.

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Miami Valley Biotech, Lansing, NY, USA
Paul R. Gardner

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Paul R. Gardner
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Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX, USA
M. Zouhair Atassi

1 Supplementary Electronic Material (S)

Table 1S

NOD Features within Microbial Single Domain Globins (DOCX 106 kb)

Table 2S

NOD Features within Worm Hbs (DOCX 106 kb)

Table 3S

NOD Features within Group 1 Truncated Hbs (DOCX 106 kb)

Table 4S

NOD Features within FlavoHb-like Mammalian Globins (DOCX 106 kb)

Table 5S

NOD Features within Mb-like Globins (DOCX 106 kb)

Table 6S

NOD Features within Assorted Phytoglobins (DOCX 106 kb)

Table 7S

Group 2 Truncated Hbs and the Mini-Hb (DOCX 106 kb)

Table 8S

Hb and Reductase Domain Contacts in the FlavoHb-NODs (DOCX 106 kb)

Table 9S

Hb α-Chain and B5OR Subunit Contacts in the Alpha-NOD (DOCX 106 kb)

Table 10S

Hb β-Chain and CYPOR Subunit Contacts in the Beta-NOD (DOCX 106 kb)

Table 11S

Cygb and B5 Contacts in the Cygb-NOD (DOCX 106 kb)

Table 12S

Ngb, B5, and B5OR Contacts in the Docked Ternary Complex (DOCX 106 kb)

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Gardner, P.R. (2022). Ordered Motions in the Nitric-Oxide Dioxygenase Mechanism of Flavohemoglobin and Assorted Globins with Tightly Coupled Reductases. In: Atassi, M.Z. (eds) Protein Reviews. Advances in Experimental Medicine and Biology(), vol 1414. Springer, Cham. https://doi.org/10.1007/5584_2022_751

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DOI: https://doi.org/10.1007/5584_2022_751
Published: 16 December 2022
Publisher Name: Springer, Cham
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Online ISBN: 978-3-031-28670-4
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