Mitochondrial physiology varies with parity and body mass in the laboratory mouse (Mus musculus)
The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal’s ability to support self-maintenance and longevity. In th...
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container_title | Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology |
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creator | Park, Noel R. Taylor, Halie A. Andreasen, Victoria A. Williams, Ashley S. Niitepõld, Kristjan Yap, Kang Nian Kavazis, Andreas N. Hood, Wendy R. |
description | The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal’s ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female’s body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction. |
doi_str_mv | 10.1007/s00360-020-01285-2 |
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For example, the energetic costs of reproduction may reduce an animal’s ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female’s body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction.</description><identifier>ISSN: 0174-1578</identifier><identifier>EISSN: 1432-136X</identifier><identifier>DOI: 10.1007/s00360-020-01285-2</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Animal Physiology ; Biochemistry ; Biomedical and Life Sciences ; Biomedicine ; Body mass ; Damage ; Dependent variables ; Displays ; Females ; Human Physiology ; Laboratories ; Laboratory animals ; Life history ; Life Sciences ; Liver ; Mitochondria ; Original Paper ; Oxidation ; Oxidative stress ; Parity ; Performance enhancement ; Physiology ; Reactive oxygen species ; Reproduction ; Zoology</subject><ispartof>Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology, 2020-07, Vol.190 (4), p.465-477</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2020</rights><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2020.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c352t-e361f78604db6f9a9aebfc712c029aee22777c4b05078e76d2c1b653bb2385e73</citedby><cites>FETCH-LOGICAL-c352t-e361f78604db6f9a9aebfc712c029aee22777c4b05078e76d2c1b653bb2385e73</cites><orcidid>0000-0002-1392-6684 ; 0000-0003-3180-1372 ; 0000-0002-7069-9326 ; 0000-0001-8805-1520 ; 0000-0002-2979-6984 ; 0000-0002-8398-3908 ; 0000-0003-3615-2674</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00360-020-01285-2$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00360-020-01285-2$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids></links><search><creatorcontrib>Park, Noel R.</creatorcontrib><creatorcontrib>Taylor, Halie A.</creatorcontrib><creatorcontrib>Andreasen, Victoria A.</creatorcontrib><creatorcontrib>Williams, Ashley S.</creatorcontrib><creatorcontrib>Niitepõld, Kristjan</creatorcontrib><creatorcontrib>Yap, Kang Nian</creatorcontrib><creatorcontrib>Kavazis, Andreas N.</creatorcontrib><creatorcontrib>Hood, Wendy R.</creatorcontrib><title>Mitochondrial physiology varies with parity and body mass in the laboratory mouse (Mus musculus)</title><title>Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology</title><addtitle>J Comp Physiol B</addtitle><description>The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal’s ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female’s body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction.</description><subject>Animal Physiology</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Body mass</subject><subject>Damage</subject><subject>Dependent variables</subject><subject>Displays</subject><subject>Females</subject><subject>Human Physiology</subject><subject>Laboratories</subject><subject>Laboratory animals</subject><subject>Life history</subject><subject>Life Sciences</subject><subject>Liver</subject><subject>Mitochondria</subject><subject>Original Paper</subject><subject>Oxidation</subject><subject>Oxidative stress</subject><subject>Parity</subject><subject>Performance enhancement</subject><subject>Physiology</subject><subject>Reactive oxygen species</subject><subject>Reproduction</subject><subject>Zoology</subject><issn>0174-1578</issn><issn>1432-136X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNp9kE9LxDAQxYMouK5-AU8BL-uhOknapnuUxX-wixcFbzFN090ubVMzrdJvb9YVBA8ehhmG33s8HiHnDK4YgLxGAJFCBDwM41kS8QMyYbHgERPp6yGZAJNxxBKZHZMTxC0AxCyLJ-RtVfXObFxb-ErXtNuMWLnarUf6oX1lkX5W_YZ24e5HqtuC5q4YaaMRadXSfmNprXPnde98eLsBLZ2tBqTNgGaoB7w8JUelrtGe_ewpebm7fV48RMun-8fFzTIyIuF9ZEXKSpmlEBd5Ws71XNu8NJJxAzzclnMppYlzSEBmVqYFNyxPE5HnXGSJlWJKZnvfzrv3wWKvmgqNrWvd2hBL8ZiBhGQuIKAXf9CtG3wb0u2oEEEkMg0U31PGO0RvS9X5qtF-VAzUrnS1L12F0tV36YoHkdiLMMDt2vpf639UXxSQhNo</recordid><startdate>20200701</startdate><enddate>20200701</enddate><creator>Park, Noel R.</creator><creator>Taylor, Halie A.</creator><creator>Andreasen, Victoria A.</creator><creator>Williams, Ashley S.</creator><creator>Niitepõld, Kristjan</creator><creator>Yap, Kang Nian</creator><creator>Kavazis, Andreas N.</creator><creator>Hood, Wendy R.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QR</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1392-6684</orcidid><orcidid>https://orcid.org/0000-0003-3180-1372</orcidid><orcidid>https://orcid.org/0000-0002-7069-9326</orcidid><orcidid>https://orcid.org/0000-0001-8805-1520</orcidid><orcidid>https://orcid.org/0000-0002-2979-6984</orcidid><orcidid>https://orcid.org/0000-0002-8398-3908</orcidid><orcidid>https://orcid.org/0000-0003-3615-2674</orcidid></search><sort><creationdate>20200701</creationdate><title>Mitochondrial physiology varies with parity and body mass in the laboratory mouse (Mus musculus)</title><author>Park, Noel R. ; 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B, Biochemical, systemic, and environmental physiology</jtitle><stitle>J Comp Physiol B</stitle><date>2020-07-01</date><risdate>2020</risdate><volume>190</volume><issue>4</issue><spage>465</spage><epage>477</epage><pages>465-477</pages><issn>0174-1578</issn><eissn>1432-136X</eissn><abstract>The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal’s ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female’s body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. 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subjects | Animal Physiology Biochemistry Biomedical and Life Sciences Biomedicine Body mass Damage Dependent variables Displays Females Human Physiology Laboratories Laboratory animals Life history Life Sciences Liver Mitochondria Original Paper Oxidation Oxidative stress Parity Performance enhancement Physiology Reactive oxygen species Reproduction Zoology |
title | Mitochondrial physiology varies with parity and body mass in the laboratory mouse (Mus musculus) |
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