Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats

Naked mole rats (Heterocephalus glaber) are among the most hypoxia-tolerant mammals, but their physiological responses to acute and chronic sustained hypoxia (CSH), and the molecular underpinnings of these responses, are poorly understood. In the present study we evaluated the acute hypoxic ventilat...

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Main Authors: Yvonne A. Dzal, Allison Seow, Lisa G. Borecky, Danielle Chung, Sharn K. G. Gill, William K. Milsom, Matthew E. Pamenter
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2019.00106/full
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author Yvonne A. Dzal
Yvonne A. Dzal
Allison Seow
Lisa G. Borecky
Danielle Chung
Sharn K. G. Gill
William K. Milsom
Matthew E. Pamenter
Matthew E. Pamenter
Matthew E. Pamenter
author_facet Yvonne A. Dzal
Yvonne A. Dzal
Allison Seow
Lisa G. Borecky
Danielle Chung
Sharn K. G. Gill
William K. Milsom
Matthew E. Pamenter
Matthew E. Pamenter
Matthew E. Pamenter
author_sort Yvonne A. Dzal
collection DOAJ
description Naked mole rats (Heterocephalus glaber) are among the most hypoxia-tolerant mammals, but their physiological responses to acute and chronic sustained hypoxia (CSH), and the molecular underpinnings of these responses, are poorly understood. In the present study we evaluated the acute hypoxic ventilatory response and the occurrence of ventilatory acclimatization to hypoxia following CSH exposure (8–10 days in 8% O2) of naked mole rats. We also investigated the role of excitatory glutamatergic signaling in the control of ventilation and metabolism in these conditions. Animals acclimated to normoxia (control) or CSH and then exposed to acute hypoxia (7% O2 for 1 h) exhibited elevated tidal volume (VT), but decreased breathing frequency (fR). As a result, total ventilation (V.E) remained unchanged. Conversely, VT was lower in CSH animals relative to controls, suggesting that there is ventilatory plasticity following acclimatization to chronic hypoxia. Both control and CSH-acclimated naked mole rats exhibited similar 60–65% decreases in O2 consumption rate during acute hypoxia, and as a result their air convection requirement (ACR) increased ∼2.4 to 3-fold. Glutamatergic receptor inhibition decreased fR, V.E, and the rate of O2 consumption in normoxia but did not alter these ventilatory or metabolic responses to acute hypoxia in either the control or CSH groups. Taken together, these findings indicate that ventilatory acclimatization to hypoxia is atypical in naked mole rats, and glutamatergic signaling is not involved in their hypoxic ventilatory or metabolic responses to acute or chronic hypoxia.
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spelling doaj.art-d28f2e1d16624f79b5567ce22f9cdb612022-12-22T00:40:42ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-02-011010.3389/fphys.2019.00106429089Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole RatsYvonne A. Dzal0Yvonne A. Dzal1Allison Seow2Lisa G. Borecky3Danielle Chung4Sharn K. G. Gill5William K. Milsom6Matthew E. Pamenter7Matthew E. Pamenter8Matthew E. Pamenter9Department of Zoology, University of British Columbia, Vancouver, BC, CanadaDepartment of Biology, Centre for Forest Interdisciplinary Research, University of Winnipeg, Winnipeg, MB, CanadaDepartment of Zoology, University of British Columbia, Vancouver, BC, CanadaDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaDepartment of Zoology, University of British Columbia, Vancouver, BC, CanadaDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaDepartment of Zoology, University of British Columbia, Vancouver, BC, CanadaDepartment of Zoology, University of British Columbia, Vancouver, BC, CanadaDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaUniversity of Ottawa Brain and Mind Research Institute, Ottawa, ON, CanadaNaked mole rats (Heterocephalus glaber) are among the most hypoxia-tolerant mammals, but their physiological responses to acute and chronic sustained hypoxia (CSH), and the molecular underpinnings of these responses, are poorly understood. In the present study we evaluated the acute hypoxic ventilatory response and the occurrence of ventilatory acclimatization to hypoxia following CSH exposure (8–10 days in 8% O2) of naked mole rats. We also investigated the role of excitatory glutamatergic signaling in the control of ventilation and metabolism in these conditions. Animals acclimated to normoxia (control) or CSH and then exposed to acute hypoxia (7% O2 for 1 h) exhibited elevated tidal volume (VT), but decreased breathing frequency (fR). As a result, total ventilation (V.E) remained unchanged. Conversely, VT was lower in CSH animals relative to controls, suggesting that there is ventilatory plasticity following acclimatization to chronic hypoxia. Both control and CSH-acclimated naked mole rats exhibited similar 60–65% decreases in O2 consumption rate during acute hypoxia, and as a result their air convection requirement (ACR) increased ∼2.4 to 3-fold. Glutamatergic receptor inhibition decreased fR, V.E, and the rate of O2 consumption in normoxia but did not alter these ventilatory or metabolic responses to acute hypoxia in either the control or CSH groups. Taken together, these findings indicate that ventilatory acclimatization to hypoxia is atypical in naked mole rats, and glutamatergic signaling is not involved in their hypoxic ventilatory or metabolic responses to acute or chronic hypoxia.https://www.frontiersin.org/article/10.3389/fphys.2019.00106/fullventilatory acclimatization to hypoxiaAMPA receptorNMDA receptorhypoxic ventilatory responsehypoxic metabolic response
spellingShingle Yvonne A. Dzal
Yvonne A. Dzal
Allison Seow
Lisa G. Borecky
Danielle Chung
Sharn K. G. Gill
William K. Milsom
Matthew E. Pamenter
Matthew E. Pamenter
Matthew E. Pamenter
Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
Frontiers in Physiology
ventilatory acclimatization to hypoxia
AMPA receptor
NMDA receptor
hypoxic ventilatory response
hypoxic metabolic response
title Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
title_full Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
title_fullStr Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
title_full_unstemmed Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
title_short Glutamatergic Receptors Modulate Normoxic but Not Hypoxic Ventilation and Metabolism in Naked Mole Rats
title_sort glutamatergic receptors modulate normoxic but not hypoxic ventilation and metabolism in naked mole rats
topic ventilatory acclimatization to hypoxia
AMPA receptor
NMDA receptor
hypoxic ventilatory response
hypoxic metabolic response
url https://www.frontiersin.org/article/10.3389/fphys.2019.00106/full
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