Abstract
Heatstroke is considered an important condition that may contribute to endothelial cell damage. The aim of this study was to assess temporal profiles of the cytokine (IL-6 and IL-8) and mRNA production when endothelial cells undergo higher temperature stimuli. In the first group, human umbilical vascular endothelial cells (HUVECs) were cultured at 4 different temperatures (37, 38, 39 or 40°C) for 1, 3 and 5 h. In the second group, HUVECs were cultured at 37°C for 4 h or 23 h, after stimulation by heating for one hour at the same culture temperatures used in the first group (37°C to 40°C). After culturing, IL-6 and IL-8 mRNA and protein levels were measured. It has been found the cytokine mRNA levels being significantly higher (p < 0.001) in all cells incubated at higher temperaturesthan those in the control (cultivation at 37°C). At the same time, the production of IL-6 and 8 at a higher temperature (39, 40°C) was significantly lower (p < 0.001) than at 37°C (control), and the decrease was temperature dependent. However, IL-6 and IL-8 levelswere significantly greater in the cells at 23 h after transient hyperthermic (40°C, 1 h) stimulation than in control ones (p < 0.001). After a transient hyperthermia, the production of the cytokinesin HUVECs is initially inhibited and then augmented. The results indicated that tissue injury might continue to develop after a hyperthermic event. There might be a potent risk for underestimation of cytokine induced tissue injury in the acute phase of a heatstroke.
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Kinoshita K., Chatzipanteli K., Vitarbo E., Truettner J.S., Alonso O.F., Dietrich W.D. 2002. Interleukin-1beta messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: Importance of injury severity and brain temperature. Neurosurgery. 51, 195–203.
Vitarbo E.A., Chatzipanteli K., Kinoshita K., Truettner J.S., Alonso O.F., Dietrich W.D. 2004. Tumor necrosis factor alpha expression and protein levels after fluid percussion injury in rats: The effect of injury severity and brain temperature. Neurosurgery. 55, 416–425.
Noda A., Kinoshita K., Sakurai A., Matsumoto T., Mugishima H., Tanjoh K. 2008. Hyperglycemia and lipopolysaccharide decrease depression effect of interleukin 8 production by hypothermia: An experimental study with endothelial cells. Intensive Care Med. 34, 109–115.
Russwurm S., Stonans I., Schwerter K., Stonane E., Meissner W., Reinhart K. 2002. Direct influence of mild hypothermia on cytokine expression and release in cultures of human peripheral blood mononuclear cells. J. Interferon Cytokine Res. 22, 215–221.
Fairchild K.D., Viscardi R.M., Hester L., Singh I.S., Hasday J.D. 2000. Effects of hypothermia and hyperthermia on cytokine production by cultured human mononuclear phagocytes from adults and newborns. J. Interferon Cytokine Res. 20, 1049–1055.
Ensor, J.E., Crawford E.K., Hasday J.D. 1995. Warming macrophages to febrile range destabilizes tumor necrosis factor-mRNA without inducing heat shock. Am. J. Physiol. Cell Physiol. 269, C1140–C1146.
Ensor J.E., Wiener S.M., McCrea K.A., Viscardi R.M., Crawford E.K., Hasday J.D. 1994. Differential effects of hyperthermia on macrophage interleukin-6 and tumor necrosis factor-expression. Am. J. Physiol. Cell Physiol. 266, C967–C974.
Jiang Q., Cross A.S., Singh I.S., Chem T.T., Viscardi R.M., Hasday J.D. 2000. Febrile core temperatureis essential for optimal host defense in bacterial peritonitis. Infect. Immun. 68, 1265–1270.
Bouchama A., Hammani M.M., Haq A., Jackson J., al-Sedairy S. 1996. Evidence for endothelial cell activation/injury in heatstroke. Crit. Care Med. 24, 1173–1178.
Hammami M.M., Bouchama A., Al-Sedairy S., Shail E., Al-Ohaly Y., Mohamed G.E. 1997. Concentrations of soluble tumor necrosis factor and interleukin-6 receptors in heatstroke and heat stress. Crit. Care Med. 25, 1314–1319.
Hubbard R.W., Bowers W.D., Matthew W.T., Curtis F.C., Criss R.E., Sheldon G.M., Ratteree J.W. 1977. Rat model of acute heatstroke mortality. J. Appl. Physiol. 42, 809–816.
Lu K.C., Wang J.Y., Lin S.H., Chu P., Lin Y.F. 2004. Role of circulating cytokines and chemokines in exertional heatstroke. Crit. Care Med. 32, 399–403.
Bouchama A., Al-Sedairy S., Siddiqui S., Shail E., Rezeig M. 1993. Elevated pyrogenic cytokines in heatstroke. Chest. 104, 1498–502.
Bouchama A., Knochel J.P. 2002. Heat stroke. N. Engl. J. Med. 346, 1978–1988.
Bouchama A., Parhar R.S., el-Yazigi A., Sheth K., al-Sedairy S. 1991. Endotoxemia and release of tumor necrosis factor and interleukin 1 in acute heatstroke. J. Appl. Physiol. 70, 2640–2644.
Meng Q., He C., Shuaib A., Wang C.X. 2012. Hyperthermia worsens ischaemic brain injury through destruction of microvessels in an embolic model in rats. Int. J. Hyperthermia. 28, 24–32.
Shah N.G., Tulapurkar M.E., Damarla M., Singh I.S., Goldblum S.E., Shapiro P., Hasday J.D. 2012. Febrilerange hyperthermia augments reversible TNF-α-induced hyperpermeability in human microvascular lung endothelial cells. Int. J. Hyperthermia. 28, 627–635.
Mantovani A., Dejana E. 1989. Cytokines as communication signals between leukocytes and endothelial cells. Immunol.Today. 10, 370–375.
Baggiolini M., Dewald B., Moser B. 1994. Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv. Immunol. 55, 97–179.
Singh I.S., Viscardi R.M., Kalvakolanu I., Calderwood S., Hasday J.D. 2000. Inhibition of tumor necrosis factoralpha transcription in macrophages exposed to febrile range temperature. A possible role for heat shock factor-1 as a negative transcriptional regulator. J. Biol. Chem. 275, 9841–9848.
Bouchama A., Roberts G., Al Mohanna F., El-Sayed R., Lach B., Chollet-Martin S., Ollivier V., Al Baradei R., Loualich A., Nakeeb S., Eldali A., de Prost D. 2005. Inflammatory, hemostatic and clinical changes in a baboon experimental model for heatstroke. J. Appl. Physiol. 98, 697–705.
Gathiram P., Wells M.T., Brock-Utne J.G., Gaffin S.L. 1987. Antilipopolysaccharide improves survival in primates subjected to heatstroke. Circ Shock. 23, 57–164.
Gathiram P., Wells M.T, Raidoo D., Brock-Utne J.G., Gaffin S.L. 1988. Portal and systemic plasma lipopolysaccharide concentrations in heat-stressed primates. Circ Shock. 25, 223–230.
Hall D.M., Buettner G.R., Oberley L.W., Xu L, Matthes R.D., Gisolfi C.V. 2001. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am. J. Physiol. Heart Circ. Physiol. 280, H509–H521.
Lambert G.P., Gisolfi C.V., Berg D.J., Moseley P.L., Oberley L.W., Kregel K.C. 2002. Selected contribution: Hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J. Appl. Physiol. 92, 1750–1761.
Nakabe N., Kokura S., Shimozawa M., Katada K., Sakamoto N., Ishikawa T., Handa O., Takagi T., Naito Y., Yoshida N., Yoshikawa T. 2007. Hyperthermia attenuates TNF-alpha-induced up regulation of endothelial cell adhesion molecules in human arterial endothelial cells. Int. J. Hyperthermia. 23, 217–224.
Wong H.R., Ryan M.A., Menendez I.Y., Wispé J.R. 1999. Heat shock activates the I-kappa-B-alpha promoter and increases I-kappa-B-alpha mRNA expression. Cell Stress Chaperones. 4, 1–7.
Eshel G.M, Safar P., Stezoski W. 2001.The role of the gut in the pathogenesis of death due to hyperthermia. Am. J. Forensic. Med. Pathol. 22, 100–104.
Fukumura D., Miura S., Kurose I., Higuchi H., Suzuki H., Ebinuma H., Han J.Y., Watanabe N., Wakabayashi G., Kitajima M., Ishii H. 1996. IL-1 is an important mediator for microcirculatory changes in endotoxininduced intestinal mucosal damage. Dig. Dis. Sci. 41, 2482–2492.
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Published in Russian in Molekulyarnaya Biologiya, 2014, Vol. 48, No. 3, pp. 429–435.
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Kinoshita, K., Sakurai, A., Yamaguchi, J. et al. Delayed augmentation effect of cytokine production after hyperthermia stimuli. Mol Biol 48, 371–376 (2014). https://doi.org/10.1134/S0026893314030108
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DOI: https://doi.org/10.1134/S0026893314030108