Abnormal neonatal sodium handling in skin precedes hypertension in the SAME rat
We discovered high Na + and water content in the skin of newborn Sprague–Dawley rats, which reduced ~ 2.5-fold by 7 days of age, indicating rapid changes in extracellular volume (ECV). Equivalent changes in ECV post birth were also observed in C57Bl/6 J mice, with a fourfold reduction over 7 days, t...
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| Veröffentlicht in: | Pflügers Archiv 2021-06, Vol.473 (6), p.897-910 |
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| creator | Mullins, Linda Ivy, Jessica Ward, Mairi Tenstad, Olav Wiig, Helge Kitada, Kento Manning, Jon Rakova, Natalia Muller, Dominik Mullins, John |
| description | We discovered high Na
+
and water content in the skin of newborn Sprague–Dawley rats, which reduced ~ 2.5-fold by 7 days of age, indicating rapid changes in extracellular volume (ECV). Equivalent changes in ECV post birth were also observed in C57Bl/6 J mice, with a fourfold reduction over 7 days, to approximately adult levels. This established the generality of increased ECV at birth. We investigated early sodium and water handling in neonates from a second rat strain, Fischer, and an Hsd11b2-knockout rat modelling the syndrome of apparent mineralocorticoid excess (SAME). Despite Hsd11b2
−/−
animals exhibiting lower skin Na
+
and water levels than controls at birth, they retained ~ 30% higher Na
+
content in their pelts at the expense of K
+
thereafter. Hsd11b2
−/−
neonates exhibited incipient hypokalaemia from 15 days of age and became increasingly polydipsic and polyuric from weaning. As with adults, they excreted a high proportion of ingested Na
+
through the kidney, (56.15 ± 8.21% versus control 34.15 ± 8.23%; n = 4; P |
| doi_str_mv | 10.1007/s00424-021-02582-7 |
| format | Article |
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+
and water content in the skin of newborn Sprague–Dawley rats, which reduced ~ 2.5-fold by 7 days of age, indicating rapid changes in extracellular volume (ECV). Equivalent changes in ECV post birth were also observed in C57Bl/6 J mice, with a fourfold reduction over 7 days, to approximately adult levels. This established the generality of increased ECV at birth. We investigated early sodium and water handling in neonates from a second rat strain, Fischer, and an Hsd11b2-knockout rat modelling the syndrome of apparent mineralocorticoid excess (SAME). Despite Hsd11b2
−/−
animals exhibiting lower skin Na
+
and water levels than controls at birth, they retained ~ 30% higher Na
+
content in their pelts at the expense of K
+
thereafter. Hsd11b2
−/−
neonates exhibited incipient hypokalaemia from 15 days of age and became increasingly polydipsic and polyuric from weaning. As with adults, they excreted a high proportion of ingested Na
+
through the kidney, (56.15 ± 8.21% versus control 34.15 ± 8.23%; n = 4; P < 0.0001), suggesting that changes in nephron electrolyte transporters identified in adults, by RNA-seq analysis, occur by 4 weeks of age. Our data reveal that Na
+
imbalance in the Hsd11b2
−/−
neonate leads to excess Na
+
storage in skin and incipient hypokalaemia, which, together with increased, glucocorticoid-induced Na
+
uptake in the kidney, then contribute to progressive, volume contracted, salt-sensitive hypertension. Skin Na
+
plays an important role in the development of SAME but, equally, may play a key physiological role at birth, supporting post-natal growth, as an innate barrier to infection or as a rudimentary kidney.</description><identifier>ISSN: 0031-6768</identifier><identifier>EISSN: 1432-2013</identifier><identifier>DOI: 10.1007/s00424-021-02582-7</identifier><identifier>PMID: 34028587</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>11-beta-Hydroxysteroid Dehydrogenase Type 2 - genetics ; 11-beta-Hydroxysteroid Dehydrogenase Type 2 - metabolism ; Age ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Birth ; Blood Pressure ; Cell Biology ; Glucocorticoids ; Human Physiology ; Hypertension ; Kidney - metabolism ; Kidneys ; Male ; Mice ; Mice, Inbred C57BL ; Mineralocorticoid Excess Syndrome, Apparent - genetics ; Mineralocorticoid Excess Syndrome, Apparent - metabolism ; Mineralocorticoid Excess Syndrome, Apparent - physiopathology ; Molecular and Genomic Physiology ; Molecular Medicine ; Neonates ; Neurosciences ; Rats ; Rats, Inbred F344 ; Rats, Sprague-Dawley ; Receptors ; Skin ; Skin - metabolism ; Sodium - metabolism ; Water content ; Water levels ; Weaning</subject><ispartof>Pflügers Archiv, 2021-06, Vol.473 (6), p.897-910</ispartof><rights>The Author(s) 2021</rights><rights>The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-c8274cd56373bc6f89124579163ec05f16b6463af02d69411a7f872745b5c88d3</citedby><cites>FETCH-LOGICAL-c474t-c8274cd56373bc6f89124579163ec05f16b6463af02d69411a7f872745b5c88d3</cites><orcidid>0000-0002-6743-8707</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/s00424-021-02582-7$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00424-021-02582-7$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34028587$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mullins, Linda</creatorcontrib><creatorcontrib>Ivy, Jessica</creatorcontrib><creatorcontrib>Ward, Mairi</creatorcontrib><creatorcontrib>Tenstad, Olav</creatorcontrib><creatorcontrib>Wiig, Helge</creatorcontrib><creatorcontrib>Kitada, Kento</creatorcontrib><creatorcontrib>Manning, Jon</creatorcontrib><creatorcontrib>Rakova, Natalia</creatorcontrib><creatorcontrib>Muller, Dominik</creatorcontrib><creatorcontrib>Mullins, John</creatorcontrib><title>Abnormal neonatal sodium handling in skin precedes hypertension in the SAME rat</title><title>Pflügers Archiv</title><addtitle>Pflugers Arch - Eur J Physiol</addtitle><addtitle>Pflugers Arch</addtitle><description>We discovered high Na
+
and water content in the skin of newborn Sprague–Dawley rats, which reduced ~ 2.5-fold by 7 days of age, indicating rapid changes in extracellular volume (ECV). Equivalent changes in ECV post birth were also observed in C57Bl/6 J mice, with a fourfold reduction over 7 days, to approximately adult levels. This established the generality of increased ECV at birth. We investigated early sodium and water handling in neonates from a second rat strain, Fischer, and an Hsd11b2-knockout rat modelling the syndrome of apparent mineralocorticoid excess (SAME). Despite Hsd11b2
−/−
animals exhibiting lower skin Na
+
and water levels than controls at birth, they retained ~ 30% higher Na
+
content in their pelts at the expense of K
+
thereafter. Hsd11b2
−/−
neonates exhibited incipient hypokalaemia from 15 days of age and became increasingly polydipsic and polyuric from weaning. As with adults, they excreted a high proportion of ingested Na
+
through the kidney, (56.15 ± 8.21% versus control 34.15 ± 8.23%; n = 4; P < 0.0001), suggesting that changes in nephron electrolyte transporters identified in adults, by RNA-seq analysis, occur by 4 weeks of age. Our data reveal that Na
+
imbalance in the Hsd11b2
−/−
neonate leads to excess Na
+
storage in skin and incipient hypokalaemia, which, together with increased, glucocorticoid-induced Na
+
uptake in the kidney, then contribute to progressive, volume contracted, salt-sensitive hypertension. Skin Na
+
plays an important role in the development of SAME but, equally, may play a key physiological role at birth, supporting post-natal growth, as an innate barrier to infection or as a rudimentary kidney.</description><subject>11-beta-Hydroxysteroid Dehydrogenase Type 2 - genetics</subject><subject>11-beta-Hydroxysteroid Dehydrogenase Type 2 - metabolism</subject><subject>Age</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Birth</subject><subject>Blood Pressure</subject><subject>Cell Biology</subject><subject>Glucocorticoids</subject><subject>Human Physiology</subject><subject>Hypertension</subject><subject>Kidney - metabolism</subject><subject>Kidneys</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mineralocorticoid Excess Syndrome, Apparent - genetics</subject><subject>Mineralocorticoid Excess Syndrome, Apparent - metabolism</subject><subject>Mineralocorticoid Excess Syndrome, Apparent - physiopathology</subject><subject>Molecular and Genomic Physiology</subject><subject>Molecular Medicine</subject><subject>Neonates</subject><subject>Neurosciences</subject><subject>Rats</subject><subject>Rats, Inbred F344</subject><subject>Rats, Sprague-Dawley</subject><subject>Receptors</subject><subject>Skin</subject><subject>Skin - metabolism</subject><subject>Sodium - metabolism</subject><subject>Water content</subject><subject>Water levels</subject><subject>Weaning</subject><issn>0031-6768</issn><issn>1432-2013</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kUtP3DAUhS1UBMPjD3SBInXTTcr129kgjRCFSiAWwNpyHGcmNLEHO0Hi39fD8CgsWPghne-e6-uD0HcMvzCAPE4AjLASCM6LK1LKLTTDjJKSAKbf0AyA4lJIoXbRXkr3AECYIjtolzIgiis5Q9fz2oc4mL7wLngz5ksKTTcNxdL4pu_8ouh8kf7mbRWddY1LxfJp5eLofOqCX6vj0hU386uzIprxAG23pk_u8OXcR3e_z25PL8rL6_M_p_PL0jLJxtIqIpltuKCS1la0qsKEcVlhQZ0F3mJRCyaoaYE0omIYG9kqmWt4za1SDd1HJxvf1VQPrrHOj9H0ehW7wcQnHUynPyq-W-pFeNQKZ2NCs8HPF4MYHiaXRj10ybq-N_kjpqQJp5hTJqHK6I9P6H2Yos_jrSlaKSkYZIpsKBtDStG1b4_BoNd56U1eOueln_PSMhcd_T_GW8lrQBmgGyBlyS9cfO_9he0_hKGfjQ</recordid><startdate>20210601</startdate><enddate>20210601</enddate><creator>Mullins, Linda</creator><creator>Ivy, Jessica</creator><creator>Ward, Mairi</creator><creator>Tenstad, Olav</creator><creator>Wiig, Helge</creator><creator>Kitada, Kento</creator><creator>Manning, Jon</creator><creator>Rakova, Natalia</creator><creator>Muller, Dominik</creator><creator>Mullins, John</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7TK</scope><scope>7TS</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6743-8707</orcidid></search><sort><creationdate>20210601</creationdate><title>Abnormal neonatal sodium handling in skin precedes hypertension in the SAME rat</title><author>Mullins, Linda ; Ivy, Jessica ; Ward, Mairi ; Tenstad, Olav ; Wiig, Helge ; Kitada, Kento ; Manning, Jon ; Rakova, Natalia ; Muller, Dominik ; Mullins, John</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-c8274cd56373bc6f89124579163ec05f16b6463af02d69411a7f872745b5c88d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>11-beta-Hydroxysteroid Dehydrogenase Type 2 - genetics</topic><topic>11-beta-Hydroxysteroid Dehydrogenase Type 2 - metabolism</topic><topic>Age</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Birth</topic><topic>Blood Pressure</topic><topic>Cell Biology</topic><topic>Glucocorticoids</topic><topic>Human Physiology</topic><topic>Hypertension</topic><topic>Kidney - metabolism</topic><topic>Kidneys</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mineralocorticoid Excess Syndrome, Apparent - genetics</topic><topic>Mineralocorticoid Excess Syndrome, Apparent - metabolism</topic><topic>Mineralocorticoid Excess Syndrome, Apparent - physiopathology</topic><topic>Molecular and Genomic Physiology</topic><topic>Molecular Medicine</topic><topic>Neonates</topic><topic>Neurosciences</topic><topic>Rats</topic><topic>Rats, Inbred F344</topic><topic>Rats, Sprague-Dawley</topic><topic>Receptors</topic><topic>Skin</topic><topic>Skin - metabolism</topic><topic>Sodium - metabolism</topic><topic>Water content</topic><topic>Water levels</topic><topic>Weaning</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mullins, Linda</creatorcontrib><creatorcontrib>Ivy, Jessica</creatorcontrib><creatorcontrib>Ward, Mairi</creatorcontrib><creatorcontrib>Tenstad, Olav</creatorcontrib><creatorcontrib>Wiig, Helge</creatorcontrib><creatorcontrib>Kitada, Kento</creatorcontrib><creatorcontrib>Manning, Jon</creatorcontrib><creatorcontrib>Rakova, Natalia</creatorcontrib><creatorcontrib>Muller, Dominik</creatorcontrib><creatorcontrib>Mullins, John</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Pflügers Archiv</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mullins, Linda</au><au>Ivy, Jessica</au><au>Ward, Mairi</au><au>Tenstad, Olav</au><au>Wiig, Helge</au><au>Kitada, Kento</au><au>Manning, Jon</au><au>Rakova, Natalia</au><au>Muller, Dominik</au><au>Mullins, John</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Abnormal neonatal sodium handling in skin precedes hypertension in the SAME rat</atitle><jtitle>Pflügers Archiv</jtitle><stitle>Pflugers Arch - Eur J Physiol</stitle><addtitle>Pflugers Arch</addtitle><date>2021-06-01</date><risdate>2021</risdate><volume>473</volume><issue>6</issue><spage>897</spage><epage>910</epage><pages>897-910</pages><issn>0031-6768</issn><eissn>1432-2013</eissn><abstract>We discovered high Na
+
and water content in the skin of newborn Sprague–Dawley rats, which reduced ~ 2.5-fold by 7 days of age, indicating rapid changes in extracellular volume (ECV). Equivalent changes in ECV post birth were also observed in C57Bl/6 J mice, with a fourfold reduction over 7 days, to approximately adult levels. This established the generality of increased ECV at birth. We investigated early sodium and water handling in neonates from a second rat strain, Fischer, and an Hsd11b2-knockout rat modelling the syndrome of apparent mineralocorticoid excess (SAME). Despite Hsd11b2
−/−
animals exhibiting lower skin Na
+
and water levels than controls at birth, they retained ~ 30% higher Na
+
content in their pelts at the expense of K
+
thereafter. Hsd11b2
−/−
neonates exhibited incipient hypokalaemia from 15 days of age and became increasingly polydipsic and polyuric from weaning. As with adults, they excreted a high proportion of ingested Na
+
through the kidney, (56.15 ± 8.21% versus control 34.15 ± 8.23%; n = 4; P < 0.0001), suggesting that changes in nephron electrolyte transporters identified in adults, by RNA-seq analysis, occur by 4 weeks of age. Our data reveal that Na
+
imbalance in the Hsd11b2
−/−
neonate leads to excess Na
+
storage in skin and incipient hypokalaemia, which, together with increased, glucocorticoid-induced Na
+
uptake in the kidney, then contribute to progressive, volume contracted, salt-sensitive hypertension. Skin Na
+
plays an important role in the development of SAME but, equally, may play a key physiological role at birth, supporting post-natal growth, as an innate barrier to infection or as a rudimentary kidney.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>34028587</pmid><doi>10.1007/s00424-021-02582-7</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-6743-8707</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Pflügers Archiv, 2021-06, Vol.473 (6), p.897-910 |
| issn | 0031-6768 1432-2013 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8164623 |
| source | MEDLINE; SpringerLink Journals - AutoHoldings |
| subjects | 11-beta-Hydroxysteroid Dehydrogenase Type 2 - genetics 11-beta-Hydroxysteroid Dehydrogenase Type 2 - metabolism Age Animals Biomedical and Life Sciences Biomedicine Birth Blood Pressure Cell Biology Glucocorticoids Human Physiology Hypertension Kidney - metabolism Kidneys Male Mice Mice, Inbred C57BL Mineralocorticoid Excess Syndrome, Apparent - genetics Mineralocorticoid Excess Syndrome, Apparent - metabolism Mineralocorticoid Excess Syndrome, Apparent - physiopathology Molecular and Genomic Physiology Molecular Medicine Neonates Neurosciences Rats Rats, Inbred F344 Rats, Sprague-Dawley Receptors Skin Skin - metabolism Sodium - metabolism Water content Water levels Weaning |
| title | Abnormal neonatal sodium handling in skin precedes hypertension in the SAME rat |
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