Blood gases in hibernating and active ground squirrels: HbO2 affinity at 6 and 38 C

Musacchia, X. J.; Volkert, WA

doi:10.1152/ajplegacy.1971.221.1.128

Cited by 55 publications

(15 citation statements)

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“…Pa O 2 values of Ͻ80 mmHg have been reported in euthermic animals of other heterothermic species (5,15,29,40), although such low Pa O 2 levels have not been observed consistently (16,56). Low Pa O 2 , high Pa CO 2 , and low pH have been observed regularly in euthermic AGS in our laboratory over the past several years.…”

Section: Discussionmentioning

confidence: 49%

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Liu

Zhu²,

Rivera

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

119

133

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Although hypoxia tolerance in heterothermic mammals is well established, it is unclear whether the adaptive significance stems from hypoxia or other cellular challenge associated with euthermy, hibernation, or arousal. In the present study, blood gases, hemoglobin O 2 saturation (SO2), and indexes of cellular and physiological stress were measured during hibernation and euthermy and after arousal thermogenesis. Results show that arterial O 2 tension (PaO 2 ) and SO2 are severely diminished during arousal and that hypoxia-inducible factor (HIF)-1␣ accumulates in brain. Despite evidence of hypoxia, neither cellular nor oxidative stress, as indicated by inducible nitric oxide synthase (iNOS) levels and oxidative modification of biomolecules, was observed during late arousal from hibernation. Compared with rats, hibernating Arctic ground squirrels (Spermophilus parryii) are well oxygenated with no evidence of cellular stress, inflammatory response, neuronal pathology, or oxidative modification following the period of high metabolic demand necessary for arousal. In contrast, euthermic Arctic ground squirrels experience mild, chronic hypoxia with low SO 2 and accumulation of HIF-1␣ and iNOS and demonstrate the greatest degree of cellular stress in brain. These results suggest that Arctic ground squirrels experience and tolerate endogenous hypoxia during euthermy and arousal.torpor; ischemia; stroke; Spermophilus parryii; reperfusion; inflammation; oxidative stress HIBERNATION IS A UNIQUE PHYSIOLOGICAL STATE of prolonged periods of low body temperature, metabolism, blood flow, and other physiological processes that are disrupted by brief periodic arousal episodes when animals rewarm and reperfuse metabolically active tissues (7). During arousal thermogenesis, blood flow returns to brain and other organs in a reperfusionlike manner at a time of maximal oxygen demand (42, 58). Preservation of neuronal and other cellular morphology during low cerebral blood flow demonstrates that hibernating mammals tolerate pronounced fluctuations in blood flow (16,61). Physiological and cellular stress experienced during euthermy, hibernation, and arousal is less well characterized.Arterial oxygen tension (Pa O 2 ) and tissue lactate measurements show that hibernating ground squirrels are well oxygenated (16,20), sometimes exceeding values in the euthermic state (15). In contrast, oxygen supply may become limiting during arousal thermogenesis. Increases in brain tissue lactate levels during peak oxygen consumption during arousal from hibernation in bats suggest these animals experience oxygen deficiency during arousal and reperfusion (30). However, because tissue lactate was not reported for euthermic bats, it is unclear how brain tissue hypoxia experienced during arousal compares to the euthermic state. Moreover, Pa O 2 was not measured to address the relationship between blood and tissue oxygenation during euthermy, hibernation, and arousal. To characterize physiological challenges associated with arousal thermogenesis, we evaluated b...

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Section: Discussionmentioning

confidence: 49%

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Liu

Zhu²,

Rivera

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

119

133

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“…There may be an accumulation of carbon dioxide in body fluids during entrance into torpor at very low ambient temperatures, as was described for dormice (Kreienbühl et al, 1976;Elvert and Heldmaier, 2000b). Blood analyses have shown that when the temperature of the blood decreased, its pH increased and P CO ∑ decreased (Musacchia and Volkert, 1971;Kreienbühl et al, 1976;Rodeau and Malan, 1979;Malan, 1982). To maintain a constant P CO ∑ and pH, additional storage of large quantities of CO 2 are required (Malan, 1982).…”

Section: Preparation For Entrance Into Torpormentioning

confidence: 88%

Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis

Elvert¹,

Heldmaier

2005

Journal of Experimental Biology

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Dormice voluntarily enter torpor at ambient temperatures ranging between 0-28°C. This study describes heart rate, ventilation frequency, O 2 -consumption (defined as metabolic rate), CO 2 -production and body temperature during entrance into torpor. Their temporal relationship was analysed during the time course of metabolic depression at different ambient temperatures. Body temperature and heart rate were measured in unrestrained dormice with implanted transmitter. Ventilation frequency was monitored by total body plethysmography or infrared video monitoring. To compare entries into torpor at different T a these periods were distinguished into four different phases: the resting phase prior to torpor, the phase of pre-torpor adjustments, the reduction phase and the phase of steady state torpor. In the pre-torpor phase, dormice increased their ventilation, metabolic rate and heart rate, indicating that the torpid state is initiated by an enhanced metabolic activity for about an hour. This was followed by a rapid reduction of ventilation, metabolism and heart rate, which reached their minimum values long before body temperature completed its decline. The results of the present study show that the entrance into torpor is caused by an active respiratory, cardiac and metabolic depression.

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“…In addition to the hypoxic challenges associated with life underground and life at high altitude, many sciurid rodents face additional gas transport challenges associated with depressed ventilation and episodic breathing during winter hibernation (Milsom, 1992;Milsom and Jackson, 2011;Webb and Milsom, 1994). In hibernating ground squirrels, prolonged periods of apnea can result in wide fluctuations in arterial P O2 and plasma pH (Maginniss and Milsom, 1994;Malan et al, 1973;Musacchia and Volkert, 1971).…”

Section: Introductionmentioning

confidence: 99%

“…Other factors that modulate Hb-O 2 affinity are Cl -ions (Chiancone et al, 1972) and temperature (Antonini and Brunori, 1971), as well as protons and CO 2 , which also bind preferentially to deoxy-Hb and promote O 2 unloading in the tissue capillaries via the Bohr effect (Perutz, 1983;Weber and Fago, 2004). Increases in blood-O 2 affinity during winter hibernation have been documented in a number of mammals, and such changes are generally attributable to reductions in red cell DPG, increases in pH and/or decreased body temperature (Burlington and Whitten, 1971;Maginniss and Milsom, 1994;Musacchia and Volkert, 1971;Revsbech et al, 2013;Tempel and Musacchia, 1975 hibernation, experiments on purified Hbs are required to evaluate the independent and joint effects of DPG, pH and temperature on Hb-O 2 affinity under controlled conditions.…”

Section: Introductionmentioning

confidence: 99%

Hemoglobin function and allosteric regulation in semi-fossorial rodents (family Sciuridae) with different altitudinal ranges

Revsbech

Tufts

Projecto-Garcia

et al. 2013

Journal of Experimental Biology

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SUMMARYSemi-fossorial ground squirrels face challenges to respiratory gas transport associated with the chronic hypoxia and hypercapnia of underground burrows, and such challenges are compounded in species that are native to high altitude. During hibernation, such species must also contend with vicissitudes of blood gas concentrations and plasma pH caused by episodic breathing. Here, we report an analysis of hemoglobin (Hb) function in six species of marmotine ground squirrels with different altitudinal distributions. Regardless of their native altitude, all species have high Hb-O 2 affinities, mainly due to suppressed sensitivities to allosteric effectors [2,3-diphosphoglycerate (DPG) and chloride ions]. This suppressed anion sensitivity is surprising given that all canonical anion-binding sites are conserved. Two sciurid species, the golden-mantled and thirteen-lined ground squirrel, have Hb-O 2 affinities that are characterized by high pH sensitivity and low thermal sensitivity relative to the Hbs of humans and other mammals. The pronounced Bohr effect is surprising in light of highly unusual amino acid substitutions at the C-termini that are known to abolish the Bohr effect in human HbA. Taken together, the high O 2 affinity of sciurid Hbs suggests an enhanced capacity for pulmonary O 2 loading under hypoxic and hypercapnic conditions, while the large Bohr effect should help to ensure efficient O 2 unloading in tissue capillaries. In spite of the relatively low thermal sensitivities of the sciurid Hbs, our results indicate that the effect of hypothermia on Hb oxygenation is the main factor contributing to the increased blood-O 2 affinity in hibernating ground squirrels.

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Blood gases in hibernating and active ground squirrels: HbO2 affinity at 6 and 38 C

Cited by 55 publications

References 0 publications

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels

Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis

Hemoglobin function and allosteric regulation in semi-fossorial rodents (family Sciuridae) with different altitudinal ranges

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