Abstract
Nitric oxide (NO) is a signalling molecule involved in several physiological processes, in both prokaryotes and eukaryotes, and nitrite is being recognised as an NO source particularly relevant to cell signalling and survival under challenging conditions. The “non-respiratory” nitrite reduction to NO is carried out by “non-dedicated” nitrite reductases, making use of metalloproteins present in cells to carry out other functions, such as several molybdoenzymes (a new class of nitric oxide-forming nitrite reductases). This minireview will highlight the physiological relevance of molybdenum-dependent nitrite-derived NO formation in mammalian, plant and bacterial signalling (and other) pathways. The mammalian xanthine oxidase/xanthine dehydrogenase, aldehyde oxidase, mitochondrial amidoxime-reducing component, plant nitrate reductase and bacterial aldehyde oxidoreductase and nitrate reductases will be considered. The nitrite reductase activity of each molybdoenzyme will be described and the review will be oriented to discuss the feasibility of the reactions from a (bio)chemical point of view. In addition, the molecular mechanism proposed for the molybdenum-dependent nitrite reduction will be discussed in detail.
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Notes
See the contributions of both Hu and Ribbe and Bjornsson, Neese, Schrock, Einsle and DeBeer in this JBIC issue.
See Hille et al.’s contribution in this J Biol Inorg Chem issue.
See Kappler and Enemark’s contribution in this J Biol Inorg Chem issue.
See Ott et al.’s contribution in this J Biol Inorg Chem issue.
Mammalian XO and XD are two forms of the same protein (same gene product). Mammalian XO enzymes are synthesised as an NAD+-dependent dehydrogenase form, the XD, and are believed to exist mostly as XD under normal physiological conditions [3, 27–32]. However, the XD form can be readily converted into a strict oxidase form, the XO. The only "functional" distinction between XD and XO lies in the electron acceptor used by each form: while XD transfers the electrons preferentially to NAD+, XO fails to react with NAD+ and uses exclusively dioxygen. During the XD into XO conversion process (through oxidation of cysteine residues or limited proteolysis), the protein conformation at the FAD centre is modified and this conformational alteration is responsible for the differentiated oxidising substrate specificity displayed by XO and XD [30, 230–237, 239, 242] (note that both dioxygen and NAD+ react at the FAD centre). On the other hand, the protein structure at the Fe/S and molybdenum centres is not changed during the conversion and, in accordance, the two enzyme forms, XO and XD, are virtually identical with respect to the binding and catalysis of substrates at the molybdenum centre [3, 27–30]. This is also the case of the nitrite reduction reaction that, as will be described, occurs at the molybdenum centre. For these reasons, XO and XD can be considered as one unique enzyme for the discussion of the overall structural organisation and molybdenum reactivity (reaction mechanism).
Enzyme forms whose FAD centre was chemically removed.
Enzyme form whose molybdenum sulpho group was chemically removed.
Although in XD/XO/AO, the electrons consumption by dioxygen is made via the FAD centre.
Because the enzyme does not catalyse the sulphite oxidation by molecular oxygen, a more appropriate name (Enzyme Nomenclature Commitee, IUBMB) would be sulphite oxidoreductase (SOR).
See Kappler and Enemark’s contribution in this JBIC issue.
Caused by the inability to synthesise the pyranopterin cofactor or certain point mutations.
Because SO is not regenerated during the nitrite reduction reaction (SO catalyses a single turnover reaction), the values above indicated as k cat and K m are better described as k electron transfer and K d values [333].
NaR is highly regulated by complex transcriptional, translational and posttranslational mechanisms. The posttranslational regulation involves the phosphorylation of a serine residue in the linker region between the molybdenum and haem domains [413, 414]. The phosphorylation is catalysed by protein kinases, including AMP-activated [415] and calcium-dependent kinases [416]. This phosphorylation creates a recognition site that recruits a specific regulatory protein (one member of the 14-3-3 family), whose binding effectively inhibits the enzyme [417–419]. Thus, mutation of the key serine residue to an aspartate results in a plant that has the NaR always active [420–422]. In vivo, the NaR inactivation occurs rapidly in darkness or when carbon dioxide is removed. This posttranslational regulation is essential to lower the NaR activity at night, when photosynthetically generated reducing equivalents are not available to reduce nitrite to ammonia. In this way, the nocturnal nitrite levels would not increase to dangerous concentrations [423].
Nitrite is promptly transported to the leaves’ chloroplasts or roots’ plastids, where it is rapidly reduced by SNIR, so that it does not accumulate.
The inhibition of the photosynthetic electron flow causes nitrite accumulation, because its transport to the chloroplasts depends on the pH gradient across the chloroplast envelope (buildup by the photosynthetic activity). In addition, its reduction to ammonium is hindered in the absence of photosynthetically reduced ferredoxin [470, 471].
The conversion of XD into an XO form is not common to all plants: while the enzyme from Arabidopsis thaliana does not have the two corresponding cysteine residues [479] involved in the conversion mechanism of the mammalian enzyme, the pea leaf peroxisomal enzyme was described to exist mainly (70 %) as an XO form [480–482].
It should be noted that the eukaryotic assimilatory cytoplasmatic NaR (discussed above), belonging to the SO family, is distinct from any type of prokaryotic NaR.
If nitrite was to bind to the oxidised molybdenum of XO, then its preliminary incubation in the enzyme reaction mixture, before the addition of xanthine or aldehyde, would modify the K m value of the reducing substrate relatively to add nitrite after the reducing substrate addition, which was not observed (parallel to competitive inhibition).
In spite of the nitrite-binding mode in CuNiR being a "bidentate nitrito" mode, it is tempting not to follow all the similarities between the molybdenum- and copper-containing enzymes.
Abbreviations
- AO:
-
Aldehyde oxidase
- AOR:
-
Aldehyde oxidoreductases
- CuNiR:
-
Copper-containing nitrite reductase (one of the enzymes responsible for the respiratory nitrite reduction to NO)
- DMSOR:
-
Dimethylsulphoxide reductase
- DPI:
-
Diphenyleneiodonium chloride
- EPR:
-
Electron paramagnetic resonance spectroscopy
- Fe/S:
-
Iron–sulphur centre
- mARC:
-
Mammalian mitochondrial amidoxime-reducing component
- MOSC:
-
From molybdenum cofactor sulphurase C-terminal domain (proteins involved in pyranopterin cofactor biosynthesis)
- NaR:
-
Nitrate reductase (all types of nitrate reductase enzymes)
- NiR:
-
Nitrite reductases (“dedicated” and “non-dedicated” enzymes)
- NO:
-
Nitric oxide radical
- NOS:
-
NO synthases
- ROS:
-
Reactive oxygen species
- SO:
-
Sulphite oxidase
- SOD:
-
Superoxide dismutase
- XD:
-
Xanthine dehydrogenase
- XO:
-
Xanthine oxidase
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Acknowledgments
This work was supported by projects PTDC/QUI-BIQ/100366/2008 and PEst-C/EQB/LA0006/2013 (Fundação para a Ciência e Tecnologia/MCTES, Portugal).
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Maia, L.B., Moura, J.J.G. Nitrite reduction by molybdoenzymes: a new class of nitric oxide-forming nitrite reductases. J Biol Inorg Chem 20, 403–433 (2015). https://doi.org/10.1007/s00775-014-1234-2
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DOI: https://doi.org/10.1007/s00775-014-1234-2