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The evolution of nitric oxide signalling in vertebrate blood vessels

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Abstract

Nitric oxide is one of the most important signalling molecules involved in the regulation of physiological function. It first came to prominence when it was discovered that the vascular endothelium of mammals synthesises and releases nitric oxide (NO) to mediate a potent vasodilation. Subsequently, it was shown that NO is synthesised in the endothelium by a specific isoform of nitric oxide synthase (NOS) called NOS3. Following this discovery, it was assumed that an endothelial NO/NOS3 system would be present in all vertebrate blood vessels. This review will discuss the latest genomic, anatomical and physiological evidence which demonstrates that an endothelial NO/NOS3 signalling is not ubiquitous in non-mammalian vertebrates, and that there have been key evolutionary steps that have led to the endothelial NO signalling system being a regulatory system found only in reptiles, birds and mammals. Furthermore, the emerging role of nitrite as an endocrine source of NO for vascular regulation is discussed.

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Abbreviations

ACh:

Acetylcholine

cGMP:

Guanosine 3′:5′-cyclic monophosphate

EDH:

Endothelium-derived hyperpolarisation

EDRF:

Endothelium-derived relaxing factor

ETC:

Electron transport chain

GC:

Guanylyl cyclase

GTP:

Guanosine triphosphate

Hb:

Haemoglobin

IHC:

Immunohistochemistry

IR:

Immunoreactivity

NADPH:

Nicotinamide adenine dinucleotide phosphate

l-NAME:

N 5-[imino(nitroamino)methyl]-l-ornithine methyl ester monohydrochloride

NO:

Nitric oxide

NOS:

Nitric oxide synthase

ODQ:

1H-[1,2,4]oxadiazolo[4,3-a]quinoxaline-1-one

PDZ:

Post synaptic density protein (PSD95)/drosophila disc large tumour suppressor protein/zona occludens-1 protein domain

ROS:

Reactive oxygen species

SIN-1:

3-Morpholinosyndnomine

SNP:

Sodium nitroprusside

WGD:

Whole genome duplication

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Donald, J.A., Forgan, L.G. & Cameron, M.S. The evolution of nitric oxide signalling in vertebrate blood vessels. J Comp Physiol B 185, 153–171 (2015). https://doi.org/10.1007/s00360-014-0877-1

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