Mitochondria and the Frozen Frog

The wood frog, <i>Rana sylvatica</i>, is the best-studied of a small group of amphibian species that survive whole body freezing during the winter months. These frogs endure the freezing of 65–70% of their total body water in extracellular ice masses. They have implemented multiple adapt...

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Main Authors: Janet M. Storey, Shaobo Wu, Kenneth B. Storey
Format: Article
Language:English
Published: MDPI AG 2021-04-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/10/4/543
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spelling doaj-78a62c9ec3fd4c3682c609957e6a27672021-04-01T23:03:11ZengMDPI AGAntioxidants2076-39212021-04-011054354310.3390/antiox10040543Mitochondria and the Frozen FrogJanet M. Storey0Shaobo Wu1Kenneth B. Storey2Department of Biology, Carleton University, Ottawa, ON K1S 5B6, CanadaInstitute of Blood Transfusion, Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC), Chengdu 610052, ChinaDepartment of Biology, Carleton University, Ottawa, ON K1S 5B6, CanadaThe wood frog, <i>Rana sylvatica</i>, is the best-studied of a small group of amphibian species that survive whole body freezing during the winter months. These frogs endure the freezing of 65–70% of their total body water in extracellular ice masses. They have implemented multiple adaptations that manage ice formation, deal with freeze-induced ischemia/reperfusion stress, limit cell volume reduction with the production of small molecule cryoprotectants (glucose, urea) and adjust a wide variety of metabolic pathways for prolonged life in a frozen state. All organs, tissues, cells and intracellular organelles are affected by freeze/thaw and its consequences. This article explores mitochondria in the frozen frog with a focus on both the consequences of freezing (e.g., anoxia/ischemia, cell volume reduction) and mitigating defenses (e.g., antioxidants, chaperone proteins, upregulation of mitochondria-encoded genes, enzyme regulation, etc.) in order to identify adaptive strategies that defend and adapt mitochondria in animals that can be frozen for six months or more every year. A particular focus is placed on freeze-responsive genes in wood frogs that are encoded on the mitochondrial genome including <i>ATP6/8</i>, <i>ND4</i> and <i>16S</i> RNA. These were strongly up-regulated during whole body freezing (24 h at −2.5 °C) in the liver and brain but showed opposing responses to two component stresses: strong upregulation in response to anoxia but no response to dehydration stress. This indicates that freeze-responsive upregulation of mitochondria-encoded genes is triggered by declining oxygen and likely has an adaptive function in supporting cellular energetics under indeterminate lengths of whole body freezing.https://www.mdpi.com/2076-3921/10/4/543<i>Rana sylvatica</i>antioxidant defensesfreezing survivalanoxiadehydrationmitochondrial genes
collection DOAJ
language English
format Article
sources DOAJ
author Janet M. Storey
Shaobo Wu
Kenneth B. Storey
spellingShingle Janet M. Storey
Shaobo Wu
Kenneth B. Storey
Mitochondria and the Frozen Frog
Antioxidants
<i>Rana sylvatica</i>
antioxidant defenses
freezing survival
anoxia
dehydration
mitochondrial genes
author_facet Janet M. Storey
Shaobo Wu
Kenneth B. Storey
author_sort Janet M. Storey
title Mitochondria and the Frozen Frog
title_short Mitochondria and the Frozen Frog
title_full Mitochondria and the Frozen Frog
title_fullStr Mitochondria and the Frozen Frog
title_full_unstemmed Mitochondria and the Frozen Frog
title_sort mitochondria and the frozen frog
publisher MDPI AG
series Antioxidants
issn 2076-3921
publishDate 2021-04-01
description The wood frog, <i>Rana sylvatica</i>, is the best-studied of a small group of amphibian species that survive whole body freezing during the winter months. These frogs endure the freezing of 65–70% of their total body water in extracellular ice masses. They have implemented multiple adaptations that manage ice formation, deal with freeze-induced ischemia/reperfusion stress, limit cell volume reduction with the production of small molecule cryoprotectants (glucose, urea) and adjust a wide variety of metabolic pathways for prolonged life in a frozen state. All organs, tissues, cells and intracellular organelles are affected by freeze/thaw and its consequences. This article explores mitochondria in the frozen frog with a focus on both the consequences of freezing (e.g., anoxia/ischemia, cell volume reduction) and mitigating defenses (e.g., antioxidants, chaperone proteins, upregulation of mitochondria-encoded genes, enzyme regulation, etc.) in order to identify adaptive strategies that defend and adapt mitochondria in animals that can be frozen for six months or more every year. A particular focus is placed on freeze-responsive genes in wood frogs that are encoded on the mitochondrial genome including <i>ATP6/8</i>, <i>ND4</i> and <i>16S</i> RNA. These were strongly up-regulated during whole body freezing (24 h at −2.5 °C) in the liver and brain but showed opposing responses to two component stresses: strong upregulation in response to anoxia but no response to dehydration stress. This indicates that freeze-responsive upregulation of mitochondria-encoded genes is triggered by declining oxygen and likely has an adaptive function in supporting cellular energetics under indeterminate lengths of whole body freezing.
topic <i>Rana sylvatica</i>
antioxidant defenses
freezing survival
anoxia
dehydration
mitochondrial genes
url https://www.mdpi.com/2076-3921/10/4/543
work_keys_str_mv AT janetmstorey mitochondriaandthefrozenfrog
AT shaobowu mitochondriaandthefrozenfrog
AT kennethbstorey mitochondriaandthefrozenfrog
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