Mechanisms for the control of local tissue blood flow during thermal interventions: influence of temperature-dependent ATP release from human blood and endothelial cells

TY - JOUR

T1 - Mechanisms for the control of local tissue blood flow during thermal interventions

T2 - influence of temperature-dependent ATP release from human blood and endothelial cells

AU - Kalsi, Kameljit K

AU - Chiesa, Scott T

AU - Trangmar, Steven J

AU - Ali, Leena

AU - Lotlikar, Makrand D

AU - González-Alonso, José

N1 - © 2016, The Authors. This is the final published version of the article (version of record) uploaded in accordance with the publisher’s self- archiving policy. It first appeared online at http://dx.doi.org/10.1113/EP08591.

PY - 2017/2/1

Y1 - 2017/2/1

N2 - Local tissue perfusion changes with alterations in temperature during heating and cooling, but the thermosensitivity of the vascular ATP signalling mechanisms for control of blood flow during thermal interventions remains unknown. Here we tested the hypotheses that the release of the vasodilator mediator ATP from human erythrocytes, but not from endothelial cells or other blood constituents, is sensitive to both increases and reductions in temperature and that increasing intravascular ATP availability with ATP infusion would potentiate thermal hyperaemia in limb tissues. We first measured blood temperature (Tb ), brachial artery blood flow (BABF) and plasma [ATP] during passive arm heating and cooling in healthy males and found they increased by 3.0 ± 1.2°C, 105 ± 25 ml min(-1) °C(-1) and 2-fold (all P < 0.05) with heating, but decreased or remained unchanged with cooling. In additional males, intrabrachial artery ATP infusion increased skin and deep tissue perfusion to levels equal or above thermal hyperaemia. In isolated erythrocyte samples exposed to different temperatures, ATP release increased 1.9-fold from 33°C to 39°C (P < 0.05) and declined by ∼50% at 20°C (P < 0.05), but no changes were observed in cultured human endothelial cells, plasma or serum samples. In conclusion, increases in plasma [ATP] and skin and deep tissue perfusion with limb heating are associated with elevations in ATP release from erythrocytes, but not from endothelial cells or other blood constituents. Erythrocyte ATP release is also sensitive to temperature reductions, suggesting erythrocytes may function as thermal sensors and ATP signalling generators for tissue perfusion control during thermal interventions. This article is protected by copyright. All rights reserved.

AB - Local tissue perfusion changes with alterations in temperature during heating and cooling, but the thermosensitivity of the vascular ATP signalling mechanisms for control of blood flow during thermal interventions remains unknown. Here we tested the hypotheses that the release of the vasodilator mediator ATP from human erythrocytes, but not from endothelial cells or other blood constituents, is sensitive to both increases and reductions in temperature and that increasing intravascular ATP availability with ATP infusion would potentiate thermal hyperaemia in limb tissues. We first measured blood temperature (Tb ), brachial artery blood flow (BABF) and plasma [ATP] during passive arm heating and cooling in healthy males and found they increased by 3.0 ± 1.2°C, 105 ± 25 ml min(-1) °C(-1) and 2-fold (all P < 0.05) with heating, but decreased or remained unchanged with cooling. In additional males, intrabrachial artery ATP infusion increased skin and deep tissue perfusion to levels equal or above thermal hyperaemia. In isolated erythrocyte samples exposed to different temperatures, ATP release increased 1.9-fold from 33°C to 39°C (P < 0.05) and declined by ∼50% at 20°C (P < 0.05), but no changes were observed in cultured human endothelial cells, plasma or serum samples. In conclusion, increases in plasma [ATP] and skin and deep tissue perfusion with limb heating are associated with elevations in ATP release from erythrocytes, but not from endothelial cells or other blood constituents. Erythrocyte ATP release is also sensitive to temperature reductions, suggesting erythrocytes may function as thermal sensors and ATP signalling generators for tissue perfusion control during thermal interventions. This article is protected by copyright. All rights reserved.

U2 - 10.1113/EP085910

DO - 10.1113/EP085910

M3 - Article

C2 - 27859767

SN - 1469-445X

JO - EXPERIMENTAL PHYSIOLOGY

JF - EXPERIMENTAL PHYSIOLOGY

ER -