Heart Function under Hypothermia Study on Mechanism of Ca Ion Regulation in Hearts of Mammalian Hibernators

Noriaki KONDO

doi:10.11276/jsvc1984.28.71

Heart Function under Hypothermia

Study on Mechanism of Ca Ion Regulation in Hearts of Mammalian Hibernators

Noriaki KONDO

Author information

Keywords: Ca²⁺ regulation, cold tolerance, heart, mammalian hibernation, sarcoplasmic reticulum

JOURNAL FREE ACCESS

1995 Volume 28 Issue 2 Pages 71-76

DOI https://doi.org/10.11276/jsvc1984.28.71

Details

Published: 1995 Received: - Available on J-STAGE: September 17, 2009 Accepted: - Advance online publication: - Revised: -
Correction information
Date of correction: September 17, 2009 Reason for correction: - Correction: CITATION Details: Wrong : 2) Horwitz E. R., Kimura J. and J. C. Ellory (1994) : Temperature/sensitivity of the Na-Ca exchange in cardiac cells from the guinea-pig and the asiatic chipmunk. J. therm. Biol. 19, 349-356.
3) Liu B., Wohlfart B. and B. W. Johansson (1990) : Effects of low temperature on contraction in papillary muscles from rabbit, rat, and hedgehog. Cryobiol. 27, 539-546.
4) Kondo N. and S. Shibata (1993) : The effect of creatine on the developed tension and metabolic kinetics of isolated rabbit atria after prolonged cold storage. Gen. PharmacoL 14, 597-602.
5) Hochachka P. W. (1986) : Defense strategies against hypoxia and hypothermia. Science, 231 : 234-241.
6) Senturia J. B. Stewart S. and M. Menaker (1970): Rate-temperature relationship in the isolated hearts of ground squirrels. Comp. Biochem. Physiol. 33, 43-50.
7) Johasson B. W. (1963) : The effect of aconitine, adrenaline and procaine, and changes in the ionic concentration in the production of ventricular fibrillation in a hibernator (hedgehog) and a nonhibernator (guinea-pig) at different temperatures. Cardiologia 43, 158-169.
8) Duker G. D., Olsson S.-O., Hecht N. H., Senturia J. and B. W. Johansson (1983) : Ventricular fibrillation in hibernators and nonhibernators. Cryobiol. 20, 407-420.
9) Jacobs H. K. and F. E. South (1976) : Effects of temperature on cardiac transmembrane potentials in hibernation. Am. J. Physiol. 230, 403-409.
10) Kimzey S. L. and J. S. Willis (1971) : Temperature adaptation of active sodium-potassium transport and of passive permeability in erythrocytes of ground squirrels. J. Gen. Physiol. 58. 634-649.
11) Charnok J. S., Dryden W. F. and R. J. Marshall (1983) : Seasonal variations in drug response and staircase phenomena in atrial muscle from a hibernating rodent (Spermophilus richardsonii). Br. J. Pharmacol. 78, 151-158.
12) Kondo N. and S. Shibata (1984) : Calcium source for excitation-contraction coupling in myocardium of nonhibernating and hibernating chipmunks. Science 225, 641-643.
13) Kondo N. (1986) : Excitation-contraction coupling in myocardium of nonhibernating and hibernating chipmunks myocardium: Effects of isoprenaline, a high calcium medium and ryanodine, Circ. Res. 59, 221-228.
14) Kondo N. (1986) : Excitation-contraction coupling in hibernating chipmunks myocardium. Exper ientia 42, 1220-1222.
15) Herve J. C., Yamaoka K., Twist W., Powell T., Ellory J. C. and L. C. H. Wang (1992) : Temperature dependence of electrophysiolgical properties of guinea pig and ground squirrel myocytes. Am. J. Physiol. 263, R177-R184.
17) Kondo N. (1986) : Comparison between effects of caffeine and ryanodine on electromechanical coupling in myocardium of hibernating chipmunks : role of internal Ca stores. Br. J. Pharmacol. 94, 1287-1291.
18) Belke D. D., Milner R. E. and L. C. H. Wang (1991) : Seasonal variations in the rate and capacity of cardiac SR calcium accumulation in a hibernating species. Cryobiol. 28, 354-363.
19) Liu B., Arlock P., Wohkfart B. and B. W. Johansson (1991) : Temperature effects on the Na and Ca currents in rat and hedghog ventricular muscle. Cryobiol. 27, 539-546.
20) Milner R. E., Michalak M. and L. C. H. Wang (1991) : Altered properties of calsequestrin and the ryanodine receptor in the cardiac sarcoplasmic reticulum of hibernating mammals. Biochim. Biophys. Acta. 1063, 120-128.
21) Kondo N. and J. Kondo : Identification of novel types of protein specific for mammalian hibernation with circannual rhythm. In : Circadian Clocks from Cell to Human. Hiroshige T. and K. Honma eds., pp. 89-96, Hokkaido University Press, Sapporo, 1992.
22) Kondo N. and J. Kondo (1992) : Identification of novel blood proteins specific for mammalian hiberna-tion. J. Biol. Chem. 267, 473-478.
23) Srere H. K., Wang L. C. H. and S. L. Martin (1992) : Central role for differential gene expression in mammalian hibernation. Proc. Natl. Acad. Sci. USA 89, 7119-7123.
24) Takamatsu N., Ohba K. I., Kondo J., Kondo N. and N. Shiba (1993) : Hibernation-associated gene regulation of plasma proteins with a collagen-like domain in mammalian hibernators. Mol. Cell. Biol. 13, 1516-1521.

Right : 2) Horwitz E. R., Kimura J. and J. C. Ellory (1994) : Temperature/sensitivity of the Na-Ca exchange in cardiac cells from the guinea-pig and the asiatic chipmunk. J. therm. Biol. 19, 349-356.
3) Liu B., Wohlfart B. and B. W. Johansson (1990) : Effects of low temperature on contraction in papillary muscles from rabbit, rat, and hedgehog. Cryobiol. 27, 539-546.
4) Kondo N. and S. Shibata (1993) : The effect of creatine on the developed tension and metabolic kinetics of isolated rabbit atria after prolonged cold storage. Gen. Pharmacol., 14, 597-602.
5) Hochachka P. W. (1986) : Defense strategies against hypoxia and hypothermia. Science, 231 : 234-241.
6) Senturia J. B. Stewart S. and M. Menaker (1970): Rate-temperature relationship in the isolated hearts of ground squirrels. Comp. Biochem. Physiol. 33, 43-50.
7) Johasson B. W. (1963) : The effect of aconitine, adrenaline and procaine, and changes in the ionic concentration in the production of ventricular fibrillation in a hibernator (hedgehog) and a nonhibernator (guinea-pig) at different temperatures. Cardiologia 43, 158-169.
8) Duker G. D., Olsson S.-O., Hecht N. H., Senturia J. and B. W. Johansson (1983) : Ventricular fibrillation in hibernators and nonhibernators. Cryobiol. 20, 407-420.
9) Jacobs H. K. and F. E. South (1976) : Effects of temperature on cardiac transmembrane potentials in hibernation. Am. J. Physiol. 230, 403-409.
10) Kimzey S. L. and J. S. Willis (1971) : Temperature adaptation of active sodium-potassium transport and of passive permeability in erythrocytes of ground squirrels. J. Gen. Physiol. 58. 634-649.
11) Charnok J. S., Dryden W. F. and R. J. Marshall (1983) : Seasonal variations in drug response and staircase phenomena in atrial muscle from a hibernating rodent (Spermophilus richardsonii). Br. J. Pharmacol. 78, 151-158.
12) Kondo N. and S. Shibata (1984) : Calcium source for excitation-contraction coupling in myocardium of nonhibernating and hibernating chipmunks. Science 225, 641-643.
13) Kondo N. (1986) : Excitation-contraction coupling in myocardium of nonhibernating and hibernating chipmunks myocardium: Effects of isoprenaline, a high calcium medium and ryanodine, Circ. Res. 59, 221-228.
14) Kondo N. (1986) : Excitation-contraction coupling in hibernating chipmunks myocardium. Experientia 42, 1220-1222.
15) Herve J. C., Yamaoka K., Twist W., Powell T., Ellory J. C. and L. C. H. Wang (1992) : Temperature dependence of electrophysiolgical properties of guinea pig and ground squirrel myocytes. Am. J. Physiol. 263, R177-R184.
17) Kondo N. (1986) : Comparison between effects of caffeine and ryanodine on electromechanical coupling in myocardium of hibernating chipmunks : role of internal Ca stores. Br. J. Pharmacol. 94, 1287-1291.
18) Belke D. D., Milner R. E. and L. C. H. Wang (1991) : Seasonal variations in the rate and capacity of cardiac SR calcium accumulation in a hibernating species. Cryobiol. 28, 354-363.
19) Liu B., Arlock P., Wohkfart B. and B. W. Johansson (1991) : Temperature effects on the Na and Ca currents in rat and hedghog ventricular muscle. Cryobiol. 27, 539-546.
20) Milner R. E., Michalak M. and L. C. H. Wang (1991) : Altered properties of calsequestrin and the ryanodine receptor in the cardiac sarcoplasmic reticulum of hibernating mammals. Biochim. Biophys. Acta. 1063, 120-128.
21) Kondo N. and J. Kondo : Identification of novel types of protein specific for mammalian hibernation with circannual rhythm. In : Circadian Clocks from Cell to Human. Hiroshige T. and K. Honma eds., pp. 89-96, Hokkaido University Press, Sapporo, 1992.
22) Kondo N. and J. Kondo (1992) : Identification of novel blood proteins specific for mammalian hibernation. J. Biol. Chem. 267, 473-478.
23) Srere H. K., Wang L. C. H. and S. L. Martin (1992) : Central role for differential gene expression in mammalian hibernation. Proc. Natl. Acad. Sci. USA 89, 7119-7123.
24) Takamatsu N., Ohba K. I., Kondo J., Kondo N. and N. Shiba (1993) : Hibernation-associated gene regulation of plasma proteins with a collagen-like domain in mammalian hibernators. Mol. Cell. Biol. 13, 1516-1521.

Abstract

Most mammals are not capable of surviving at low body temperature for extended periods. Although some degree of hypothermia provides an advantage in medical treatment, such as organ plantation and open heart surgery, through depression of the energy consumption and prevention of accumulation of harmful metabolites, the lowering of body temperature causes serious cold-damage to cells, probably by overloading Ca²⁺, resulting from a perturbation of membrane ion regulation. Mammalian hibernators undergo extreme hypothermia (near 0°C) during hibernation without any damage to their bodies, indicating the existence of an effective strategy for the protection of cells and tissues against cold. Recent studies on excitation-contraction coupling of cardiac muscles of hibernators found dramatic changes in Ca²⁺ regulatory systems, Ca channels and sarcoplasmic reticulum (SR), during hibernation. The contraction usually depends on Ca²⁺ influx through Ca channels, whereas during hibernation, Ca²⁺ for contraction is derived mainly from intracellular Ca stores, SR. Further electrophysiological and biochemical studies in hibernating animals revealed that these are attributed to both the marked enhancement of the Ca²⁺ uptake ability of SR and much less activation of Ca channels. These changes greatly contribute to the reduction of cytoplasmic Ca²⁺ after contraction. Thus, during hibernation, hearts are kept functioning normally at low body temperature through avoiding Ca²⁺ overload. The present mechanism of adaptation to cold provides a useful model for studying a strategy for overcoming cold injury.

Corresponding author

Correction information

Register with J-STAGE for free!