Effects of hypoxia on vertebrate blood vessels

Abstract

Hypoxia contracts mammalian respiratory vessels and increases vascular resistance in respiratory tissues of many vertebrates. In systemic vessels these responses vary, hypoxia relaxes mammalian vessels and contracts systemic arteries from cyclostomes. It has been proposed that hypoxic vasoconstriction in cyclostome systemic arteries is the antecedent to mammalian hypoxic pulmonary vasoconstriction, however, phylogenetic characterization of hypoxic responses is lacking. In this study, we characterized the hypoxic response of isolated systemic and respiratory vessels from a variety of vertebrates using standard myography. Pre-gill/respiratory (ventral aorta, afferent branchial artery, pulmonary artery) and post-gill/systemic (dorsal and thoracic aortas, efferent branchial artery) from lamprey (Petromyzon marinus), sandbar shark (Carcharhinus plumbeus), yellowfin tuna (Thunnus albacares), American bullfrog (Rana catesbeiana), American alligator (Alligator mississippiensis), Pekin duck (Anas platyrhynchos domesticus), chicken (Gallus domesticus) and rat (Rattus norvegicus) were exposed to hypoxia at rest or during pre-stimulation (elevated extracellular potassium, epinephrine or norepinephrine). Hypoxia produced a relaxation or transient contraction followed by relaxation in all pre-gill vessels, except for contraction in lamprey, and vasoconstriction or tri-phasic constriction-dilation-constriction in all pulmonary vessels. Hypoxia contracted systemic vessels from all animals except shark and rat and in pre-contracted rat aortas it produced a transient contraction followed by relaxation. These results show that while the classic "systemic hypoxic vasodilation and pulmonary hypoxic vasoconstriction" may occur in the microcirculation, the hypoxic response of the vertebrate macrocirculation is quite variable. These findings also suggest that hypoxic vasoconstriction is a phylogenetically ancient response.

Oxygen dependency of hydrogen sulfide-mediated vasoconstriction in cyclostome aortas

“…Collectively, these findings suggest that H 2 S contraction and HVC have a common, or at least similar, excitation pathway in hagfish vessels. This is consistent with other studies Dombkowski et al, 2004;Dombkowski et al, 2005;Olson et al, 2006;Russell et al, 2007) that have shown that the vascular response to hypoxia is identical to that of H 2 S irrespective of whether this response is contraction, relaxation, multi-phasic, or, as in the case of hagfish ventral aorta and afferent branchial arteries, no response at all. We have also observed identical hypoxic and H 2 S responses in trout approximately doubled the force of the original N 2 contraction, whereas raising cysteine to 10·mmol·l -1 relaxed the vessels back to the original N 2 level (* significant increase from N 2 ; † significant decrease from 1·mmol·l -1 cysteine; N=7).…”

“…Our model of the role of H 2 S metabolism in oxygen sensing and/or signal transduction appears to accommodate both hypoxic vasoconstriction (HVC) and hypoxic vasodilation (HVD) in vertebrate smooth muscle (Olson et al, 2007). This model is based on the balance between H 2 S production by vascular tissue and its inactivation through oxidation, and it provides a simple and rapid mechanism that couples the concentration of a vasoactive molecule directly to P O 2.…”

“…Although HVC and HVD may be modulated by endothelial-derived and/or circulating substances (Félétou et al, 1995;Jacobs and Zeldin, 2001;Kerkhof et al, 2001;Liu et al, 2001;Aaronson et al, 2002;Deussen et al, 2006), the basic responses are intrinsic to the vascular smooth muscle cell (Madden et al, 1992). In non-mammalian vertebrates, HVC has been observed in both systemic and respiratory conductance vessels Russell et al, 2001;Smith et al, 2001;Russell et al, 2007) and HVC appears to be an intrinsic response of vascular smooth muscle cells in the cyclostome dorsal aorta as well . HVD has only recently been systematically examined in non-mammalian vertebrates (Russell et al, 2007) and while it is common in systemic vessels it is not necessarily the predominant response.…”

“…In non-mammalian vertebrates, HVC has been observed in both systemic and respiratory conductance vessels Russell et al, 2001;Smith et al, 2001;Russell et al, 2007) and HVC appears to be an intrinsic response of vascular smooth muscle cells in the cyclostome dorsal aorta as well . HVD has only recently been systematically examined in non-mammalian vertebrates (Russell et al, 2007) and while it is common in systemic vessels it is not necessarily the predominant response.…”

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

“…Fish are able to compensate for decreasing environmental O 2 by increasing gill ventilation (Graham, 1997), increasing gill perfusion (Russell et al, 2008;Smith et al, 2001), increasing gill surface area (Sollid et al, 2005;Sollid and Nilsson, 2006), altering cardiac output (Speers-Roesch et al, 2010), increasing the blood Hb concentration or Hb-O 2 binding affinity (Wells, 2009) hypoxia-sensitive species (Mandic et al, 2009b). Higher levels of ATP coupled with high intrinsic Hb-O 2 binding affinity in hypoxiatolerant sculpins result in a significant capacity to endure not only severe hypoxia, but also large fluctuations in O 2 .…”