Hyperthermia induces injury to the intestinal mucosa in the mouse: Evidence for an oxidative stress mechanism

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 302, Issue 7, 2012, Pages

  Oliver, S R ^a   Phillips, N A ^a   Novosad, V L ^a   Bakos, M P ^a   Talbert, E E ^a   Clanton, T L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

BAPTA AM; Fluorescein isothiocyanate dextran; Heatstroke; Protein carbonyl; Small intestine

Indexed keywords

ACETYLCYSTEINE; LACTATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHELATION; CONTROLLED STUDY; CORE TEMPERATURE; DUODENUM; HEAT STROKE; HYPERTHERMIA; INTESTINE INJURY; INTESTINE MUCOSA PERMEABILITY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TIGHT JUNCTION;

ACETYLCYSTEINE; ANIMALS; BODY TEMPERATURE; CALCIUM; CHELATING AGENTS; DEXTRANS; FEVER; FLUORESCEIN-5-ISOTHIOCYANATE; INTESTINAL MUCOSA; L-LACTATE DEHYDROGENASE; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; TIGHT JUNCTIONS;

EID: 84859539776     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00595.2011     Document Type: Article

References (47)

1. Al-Sadi R, Ye D, Dokladny K, Ma TY. Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 180: 5653-5661, 2008.
2. Allen A, Flemstrom G, Garner A, Kivilaakso E. Gastroduodenal mucosal protection. Physiol Rev 73: 823-857, 1993.
3. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J. Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87: 545-564, 2007.
4. Bouchama A, Knochel JP. Heat stroke. N Engl J Med 346: 1978-1988, 2002.
5. Bouchama A, Ollivier V, Roberts G, Al Mohanna F, de Prost D, Eldali A, Saussereau E, El-Sayed R, Chollet-Martin S. Experimental heatstroke in baboon: analysis of the systemic inflammatory response. Shock 24: 332-335, 2005.
6. Brownlee IA, Knight J, Dettmar PW, Pearson JP. Action of reactive oxygen species on colonic mucus secretions. Free Radic Biol Med 43: 800-808, 2007.
7. Calderwood SK, Stevenson MA, Hahn GM. Effects of heat on cell calcium and inositol lipid metabolism. Radiat Res 113: 414-425, 1988.
8. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 101: 478-483, 1970.
9. Circu ML, Rodriguez C, Maloney R, Moyer MP, Aw TY. Contribution of mitochondrial GSH transport to matrix GSH status and colonic epithelial cell apoptosis. Free Radic Biol Med 44: 768-778, 2008.
10. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation- induced diarrhea in vivo. J Clin Invest 115: 2702-2715, 2005.
11. Dokladny K, Moseley PL, Ma TY. Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290: G204-G212, 2006.
12. Gathiram P, Gaffin SL, Brock-Utne JG, Wells MT. Time course of endotoxemia and cardiovascular changes in heat-stressed primates. Aviat Space Environ Med 58: 1071-1074, 1987.
13. Graber CD, Reinhold RB, Breman JG, Harley RA, Hennigar GR. Fatal heat stroke. Circulating endotoxin and gram-negative sepsis as complications. JAMA 216: 1195-1196, 1971.
14. Greenstock CL, Miller RW. The oxidation of Tiron by superoxide anion: kinetics of the reaction in aqueous solution and in chloroplasts. Biochim Biophys Acta 396: 11-16, 1975.
15. Grootjans J, Thuijls G, Derikx JP, van Dam RM, Dejong CH, Buurman WA. Rapid lamina propria retraction and zipper-like constriction of the epithelium preserves the epithelial lining in human small intestine exposed to ischaemia-reperfusion. J Pathol 224: 411-419, 2011.
16. Hall DM, Baumgardner KR, Oberley TD, Gisolfi CV. Splanchnic tissues undergo hypoxic stress during whole body hyperthermia. Am J Physiol Gastrointest Liver Physiol 276: G1195-G1203, 1999.
17. Hall DM, Buettner GR, Matthes RD, Gisolfi CV. Hyperthermia stimulates nitric oxide formation: electron paramagnetic resonance detection of. NO-heme in blood. J Appl Physiol 77: 548-553, 1994.
18. Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol 280: H509-H521, 2001.
19. Hammami MM, Bouchama A, Al-Sedairy S, Shail E, AlOhaly Y, Mohamed GE. Concentrations of soluble tumor necrosis factor and interleukin-6 receptors in heatstroke and heatstress. Crit Care Med 25: 1314-1319, 1997.
20. Hubbard RW, Bowers WD, Matthew WT, Curtis FC, Criss RE, Sheldon GM, Ratteree JW. Rat model of acute heatstroke mortality. J Appl Physiol 42: 809-816, 1977.
21. Kamel HM, Hume SP, Carr KE, Marigold JC, Michalowski A. Development of villous damage in mouse small intestine after local hyperthermia or irradiation. J Submicrosc Cytol Pathol 20: 185-193, 1988.
22. Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, Kregel KC. Hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J Appl Physiol 92: 1750-1761, 2002.
23. Leon L. The thermoregulatory consequences of heat stroke: are cytokines involved? J Therm Biol 31: 67-81, 2006.
24. Leon LR. Heat stroke and cytokines. Prog Brain Res 162: 481-524, 2007.
25. Leon LR, Blaha MD, DuBose DA. Time course of cytokine, corticosterone, and tissue injury responses in mice during heat strain recovery. J Appl Physiol 100: 1400-1409, 2006.
26. Leon LR, DuBose DA, Mason CW. Heat stress induces a biphasic thermoregulatory response in mice. Am J Physiol Regul Integr Comp Physiol 288: R197-R204, 2005.
27. Lim CL, Mackinnon LT. The roles of exercise-induced immune system disturbances in the pathology of heat stroke. Sports Med 36: 39-64, 2006.
28. Lucio M, Nunes C, Gaspar D, Ferreira H, Lima JLFC, Reis S. Antioxidant activity of vitamin E and Trolox: understanding of the factors that govern lipid peroxidation studies In vitro. Food Biophys 4: 312-320, 2009.
29. Malamud N, Haymaker W, Custer RP. Heat stroke; a clinico-pathologic study of 125 fatal cases. Mil Surg 99: 397-449, 1946.
30. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR, 2nd Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126, 2010.
31. 2+]: analysis at the single cell level by digitized imaging microscopy and cell survival. Cancer Res 51: 359-364, 1991.
32. Mirochnitchenko O, Palnitkar U, Philbert M, Inouye M. Thermosensitive phenotype of transgenic mice overproducing human glutathione peroxidases. Proc Natl Acad Sci USA 92: 8120-8124, 1995.
33. Moldéus P, Cotgreave IA. N-acetylcysteine. Methods Enzymol 234: 482-492, 1994.
34. Niu KC, Lin KC, Yang CY, Lin MT. Protective effects of alphatocopherol and mannitol in both circulatory shock and cerebral ischaemia injury in rat heatstroke. Clin Exp Pharmacol Physiol 30: 745-751, 2003.
35. Oliver SR, Wright VP, Parinandi N, Clanton TL. Thermal tolerance of contractile function in oxidative skeletal muscle: no protection by antioxidants and reduced tolerance with eicosanoid enyzme inhibition. Am J Physiol Regul Integr Comp Physiol 295: R1695-R1705, 2008.
36. Prosser C, Stelwagen K, Cummins R, Guerin P, Gill N, Milne C. Reduction in heat-induced gastrointestinal hyperpermeability in rats by bovine colostrum and goat milk powders. J Appl Physiol 96: 650-654, 2004.
37. Qin X, Sheth SU, Sharpe SM, Dong W, Lu Q, Xu D, Deitch EA. The mucus layer is critical in protecting against ischemia-reperfusion-mediated gut injury and in the restitution of gut barrier function. Shock 35: 275-281, 2011.
38. Schmid-Schonbein GW. 2008 Landis Award lecture. Inflammation and the autodigestion hypothesis. Microcirculation 16: 289-306, 2009.
39. Shapiro Y, Alkan M, Epstein Y, Newman F, Magazanik A. Increase in rat intestinal permeability to endotoxin during hyperthermia. Eur J Appl Physiol Occup Physiol 55: 410-412, 1986.
40. Singleton KD, Wischmeyer PE. Oral glutamine enhances heat shock protein expression and improves survival following hyperthermia. Shock 25: 295-299, 2006.
41. Skibba JL, Powers RH, Stadnicka A, Cullinane DW, Almagro UA, Kalbfleisch JH. Oxidative stress as a precursor to the irreversible hepatocellular injury caused by hyperthermia. Int J Hyperthermia 7: 749-761, 1991.
42. Stull JT, Blumenthal DK, Cooke R. Regulation of contraction by myosin phosphorylation. A comparison between smooth and skeletal muscles. Biochem Pharmacol 29: 2537-2543, 1980.
43. Suzuki T, Hara H. Difructose anhydride III and sodium caprate activate paracellular transport via different intracellular events in Caco-2 cells. Life Sci 79: 401-410, 2006.
44. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809, 2009.
45. Wright VP, Klawitter PF, Iscru DF, Merola AJ, Clanton TL. Superoxide scavengers augment contractile but not energetic responses to hypoxia in rat diaphragm. J Appl Physiol 98: 1753-1760, 2005.
46. Yang CF, Shen HM, Ong CN. Intracellular thiol depletion causes mitochondrial permeability transition in ebselen-induced apoptosis. Arch Biochem Biophys 380: 319-330, 2000.
47. Yang PC, He SH, Zheng PY. Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function. J Gastroenterol Hepatol 22: 1823-1831, 2007.