Abstract
Many anurans have excellent dehydration tolerance that allows endurance of the loss of up to 50-60% of total body water. One of the effects of severe dehydration is circulatory impairment due the reduced volume and increased viscosity of blood, which leads to organ hypoxia. The rehydration situation, therefore, involves a reoxygenation of tissues that may include elements of oxidative stress that resemble the injury in post-ischemic reperfusion of mammalian organs. The role of endogenous defenses against oxygen radicals in the tolerance of severe dehydration by leopard frogs, Rana pipiens, was investigated by monitoring the activities of antioxidant enzymes and glutathione levels (reduced GSH and oxidized GSSG) in leg muscle and liver of control, 50%-dehydrated, and fully rehydrated frogs. The maximal activities of muscle catalase and liver glutathione peroxidase, measured per mg soluble protein, increased significantly by 52 and 74%, respectively, after dehydration whereas muscle superoxide dismutase and glutathione reductase activities responded oppositely, decreasing by 32 and 35%, respectively. Enzyme activities returned to control levels after full rehydration. Hepatic GSH and GSSG increased early in the rehydration process (30% recovery of total body water), but returned to control levels after full recovery. A similar trend was observed for liver GSSG. The elevation of antioxidant defenses against peroxides during dehydration could provide protection against post-hypoxic oxyradical stress during rehydration. Indeed, analysis of one product of lipid peroxidation, thiobarbituric acid reactive substances, in frog tissues gave no indication of oxidative stress during the dehydration/rehydration cycle.
Similar content being viewed by others
References
Dole JW: The role of substrate moisture and dew in the water economy of leopard frogs, Rana pipiens. Copeia 1967: 141–149, 1967
Lee AK: Water economy of the burrowing frog, Heleioporus eyrei (Gray). Copeia 1968: 741–745, 1968
Pinder AW, Storey KB, Ultsch GR: Estivation and hibernation. In: M.E. Feder and W.W. Burggren (eds). Environmental Physiology of the Amphibians. University of Chicago Press, Chicago, 1992, pp 250–274
Hillman S: Physiological correlates of differential dehydration tolerance in anuran amphibians. Copeia 1980: 125–129, 1980
Jorgensen CB: 200 years of amphibian water economy: From Robert Townson to the present. Biol Rev Camp Philos Soc 72: 153–237, 1997
Thorson T, Svihla A: Correlation of the habitat of amphibians with their ability to survive the loss of body water. Ecology 24: 374–381, 1943
Thorson T: The relationship of water economy to terrestrialism in amphibians. Ecology 36: 100–116, 1955
Churchill TA, Storey KB: Dehydration tolerance in wood frogs: A new perspective on development of amphibian freeze tolerance. Am J Physiol 265: R1324–R1332, 1993
Hillman S: The roles of oxygen delivery and electrolyte levels in the dehydrational death of Xenopus laevis. J Comp Physiol 128: 169‐175, 1978
Hillman S: Dehydrational effects on brain and cerebrospinal fluid electrolytes in two amphibians. Physiol Zool 61: 254–259, 1988
Gatten RE Jr: Activity of anuran amphibians: tolerance to dehydration. Physiol Zool 60: 576–585, 1987
Hillman S: Dehydrational effects on cardiovascular and metabolic capacity in two amphibians. Physiol Zool 60: 608–613, 1987
Churchill TA, Storey KB: Effects of dehydration on organ metabolism in the frog Pseudacris crucifer: Hyperglycemic responses to dehydration mimic freezing‐induced cryoprotectant production. J Comp Physiol B 164: 492–498, 1994
Churchill TA, Storey KB: Metabolic effects of dehydration on an aquatic frog, Rana pipiens. J exp Biol 198: 147–154, 1995
Green CJ: Renal transplantation and ischemia‐reperfusion injury. In: D. Blake and P.G. Winyard (eds). Immunopharmacology of Free Radical Species. Academic Press, New York, 1995, pp 85–96
Henry TD, Archer SL, Nelson D, Weir EK, From AHL: Postischemic oxygen radical production varies with duration of ischemia. Am J Physiol 264: H1478–H1484, 1993
Singh I, Gulati S, Orak JK, Singh AK: Expression of antioxidant enzymes in rat kidney during ischemia‐reperfusion injury. Mol Cell Biochem 125: 97–104, 1993
Halliwell B, Gutteridge JMC: Role of free radicals and catalytic metal ions in human disease: An overview. Meth Enzymol 186: 1–85, 1990
Hermes‐Lima M, Storey KB: Oxidative inactivation of GST from a freezing tolerant reptile. Mol Cell Biochem 124: 149–158, 1993
Hermes‐Lima M, Storey KB: Relationship between anoxia exposure and antioxidant status of the frog Rana pipiens. Am J Physiol 271: R918–R925, 1996
Hermes‐Lima M, Storey KB: Role of antioxidants in the tolerance of freezing and anoxia by garter snakes. Am J Physiol 265: R646–R652, 1993
Willmore WG, Storey KB: Antioxidant systems and anoxia tolerance in a freshwater turtle Trachemys scripta elegans. Mol Cell Biochem 170: 177–185, 1997
Willmore WG, Storey KB: Glutathione systems and anoxia tolerance in turtles. Am J Physiol 273: R219–R225, 1997
Storey KB: Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29: 1715–1733, 1996
Joanisse DR, Storey KB: Oxidative damage and antioxidants in Rana sylvatica, the freeze tolerant wood frog. Am J Physiol 271: R545–R553, 1996
Costanzo JP, Lee RE Jr, DeVries AL, Wang T, Layne JR JR: Survival mechanisms of vertebrate ectotherms at subfreezing temperatures: Applications in cryomedicine. FASEB J 9: 351–358, 1995
Storey KB: Metabolic adaptations supporting anoxia tolerance in reptiles: Recent advances. Comp Biochem Physiol B 113: 23–35, 1996
Christiansen J, Penney D: Anaerobic glycolysis and lactic acid accumulation in cold submerged Rana pipiens. J Comp Physiol 87: 237–245, 1973
Rose FL, Drotman RB: Anaerobiosis in a frog, Rana pipiens. J Exp Zool 166: 427–431, 1967
Hermes‐Lima M, Storey KB: Antioxidant defenses and metabolic depression in a pulmonate snail. Am J Physiol 268: R1386–R1393, 1995
Griffith OW: Determination of glutathione and glutathione disulfide using glutathione reductase and 2‐vinylpyridine. Anal Biochem 106: 207–212, 1980
Singal SS, Saxema M, Ahmad H, Awasthi S, Haque AK, Awasthi YC: Glutathione S‐transferase of human lung: Characterization and evaluation of the protective role of the ????????‐class isozymes against lipid peroxidation. Arch Biochem Biophys 299: 232–241, 1992
Dhaunsi GS, Singh I, Hanevold CD: Peroxisomal participation in the cellular response to the oxidative stress of endotoxin. Mol Cell Biochem 126: 25–35, 1993
Perez‐Campo R, Lopez‐Torres M, Rosa C, Cadenas S, Barja de Quiroga G: A comparative study of free radicals in vertebrates I. Antioxidant enzymes. Comp Physiol 105 B: 749–755, 1993
Buzadzic B, Spasic MB, Saicic ZS, Radojicic R, Petrovic VM: Seasonal dependence of the activity of antioxidant defense enzymes in the ground squirrel (Citellus citellus): The effect of cold. Comp Biochem Physiol 101 B: 547–551, 1992
Grundy JE, Storey KB: Antioxidant defenses and lipid peroxidative damage in estivating toads, Scaphiopus couchii. J Comp Physiol B. (in press) 1998
Jaeschke H, Mitchell JR: Mitochondria and xanthine oxidase both generate reactive oxygen species in isolated perfused rat liver after hypoxic injury. Biochem Biophys Res Commun 160: 140–147, 1989
Turrens JF, Freeman BA, Levitt JG, Crapo JD: The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys 217: 401–410, 1982
Jamieson D, Chance B, Cadenas E, Boveris A: The relation of free radical production to hyperoxia. Ann Rev Physiol 48: 703–719, 1986
Hermes‐Lima M, Wang EM, Schuman HM, Storey KB, Ponka P: Oxidative degradation of deoxyribose catalyzed by Fe(III)‐EDTA complex. Kinetic aspects and potential usefulness for sub‐micromolar iron measurements. Mol Cell Biochem 137: 65–73, 1994
Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO: Requirement for superoxide in excitotoxic cell death. Neuron 16: 345–355, 1996
Mosialou E, Piemonte F, Andersson C, Vos RME, van Bladeren OJ, Morgenstern R: Microsomal glutathione transferase: Lipid‐derived substrates and lipid dependence. Arch Biochem Biophys 320: 210–216, 1995
Barja de Quiroga G: Brown fat thermogenesis and exercise: Two examples of physiological oxidative stress. Free Rad Biol Med 13: 325–340, 1992
Ku HH, Brunk UT, Sohal RS: Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Rad Biol Med 15: 621–627, 1993
Shlafer M, Mer CL, Adkins S: Mitochondrial hydrogen peroxide generation and activities of glutathione peroxide and superoxide dismutase following global ischemia. J Mol Cell Cardiol 19: 1195–1206, 1987
Barja G, Cadenas S, Pérez‐Campo R, López‐Torres M: Low mitochondrial free‐radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radical Res 21: 317–327, 1994
Hermes‐Lima M, Storey JM, Storey KB: Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp Biochem Physiol B (in press) 1998
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hermes-Lima, M., Storey, K.B. Role of antioxidant defenses in the tolerance of severe dehydration by anurans. The case of the leopard frog Rana pipiens. Mol Cell Biochem 189, 79–89 (1998). https://doi.org/10.1023/A:1006868208476
Issue Date:
DOI: https://doi.org/10.1023/A:1006868208476