Abstract
Naked mole-rats are highly social and strictly subterranean rodents that live in large communal colonies in sealed and chronically oxygen-depleted burrows. Brain slices from naked mole-rats show extreme tolerance to hypoxia compared to slices from other mammals, as indicated by maintenance of synaptic transmission under more hypoxic conditions and three fold longer latency to anoxic depolarization. A key factor in determining whether or not the cellular response to hypoxia is reversible or leads to cell death may be the elevation of intracellular calcium concentration. In the present study, we used fluorescent imaging techniques to measure relative intracellular calcium changes in CA1 pyramidal cells of hippocampal slices during hypoxia. We found that calcium accumulation during hypoxia was significantly and substantially attenuated in slices from naked mole-rats compared to slices from laboratory mice. This was the case for both neonatal (postnatal day 6) and older (postnatal day 20) age groups. Furthermore, while both species demonstrated more calcium accumulation at older ages, the older naked mole-rats showed a smaller calcium accumulation response than even the younger mice. A blunted intracellular calcium response to hypoxia may contribute to the extreme hypoxia tolerance of naked mole-rat neurons. The results are discussed in terms of a general hypothesis that a very prolonged or arrested developmental process may allow adult naked mole-rat brain to retain the hypoxia tolerance normally only seen in neonatal mammals.
Highlights
Naked mole-rats (Heterocephalus glaber) initially received a great deal of attention when scientists discovered that they had a eusocial lifestyle similar to that of bees and termites [1]
Hippocampal Cornu Ammonis area 1 (CA1) pyramidal cells of both naked mole-rats and mice responded to hypoxia with a decrease in fura-2 fluorescence, corresponding to an increase in intracellular calcium
The responses to hypoxia for these naked mole-rats were not significantly different from the P20 group. These results suggest that the difference in hypoxia tolerance between mice and naked mole-rats at P20 is not due to a difference in rate of maturation
Summary
Naked mole-rats (Heterocephalus glaber) initially received a great deal of attention when scientists discovered that they had a eusocial lifestyle similar to that of bees and termites [1]. Naked mole-rats are the only known poikilothermic mammals [9], and they live an extraordinarily long life (,30 years) [10]. They lack a sense of inflammatory pain and pain from chemical irritants including capsaicin and acid [11,12], and they show a profound resistance to cancer [13,14]. Naked mole-rats are mouse-size rodents that naturally live in large colonies of up to 290 individuals in sealed subterranean burrows in northern East Africa [16]. Oxygen depletion (and carbon dioxide accumulation) is even more pronounced for naked mole-rats since large groups of conspecifics huddle together in nests 1.5–2.5 m underground, competing for the same poorly ventilated air [16,19]
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