Skeletal muscle microvascular and interstitial PO2 from rest to contractions
Key points Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance. The greatest resistance to oxygen transport into skeletal muscle...
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| Veröffentlicht in: | The Journal of physiology 2018-03, Vol.596 (5), p.869-883 |
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| creator | Hirai, Daniel M. Craig, Jesse C. Colburn, Trenton D. Eshima, Hiroaki Kano, Yutaka Sexton, William L. Musch, Timothy I. Poole, David C. |
| description | Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.
Oxygen pressure (PO2) gradients across the blood–myocyte interface are required for diffusive O2 transport, thereby supporting oxidative metabolism. The greatest resistance to O2 flux into skeletal muscle is considered to reside between the erythrocyte surface and adjacent sarcolemma, although this has not been measured during contractions. We tested the hypothesis that O2 gradients between skeletal muscle microvascular (PO2 mv ) and interstitial (PO2 is ) spaces would be present at rest and maintained or increased during contractions. PO2 mv and PO2 is were determined via phosphorescence quenching (Oxyphor probes G2 and G4, respectively) in the exposed rat spinotrapezius during the rest–contraction transient (1 Hz, 6 V; n = 8). PO2 mv was higher than PO2 is in all instances from rest (34.9 ± 6.0 versus 15.7 ± 6.4) to contractions (28.4 ± 5.3 versus 10.6 ± 5.2 mmHg, respectively) such that the mean PO2 gradient throughout the transient was 16.9 ± 6.6 mmHg (P 0.05). However, the speed of the PO2 is fall during contractions was slower than that of PO2 mv (time constant: 12.8 ± 4.7 versus 9.0 ± 5.1 s, respectively; P |
| doi_str_mv | 10.1113/JP275170 |
| format | Article |
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Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.
Oxygen pressure (PO2) gradients across the blood–myocyte interface are required for diffusive O2 transport, thereby supporting oxidative metabolism. The greatest resistance to O2 flux into skeletal muscle is considered to reside between the erythrocyte surface and adjacent sarcolemma, although this has not been measured during contractions. We tested the hypothesis that O2 gradients between skeletal muscle microvascular (PO2 mv ) and interstitial (PO2 is ) spaces would be present at rest and maintained or increased during contractions. PO2 mv and PO2 is were determined via phosphorescence quenching (Oxyphor probes G2 and G4, respectively) in the exposed rat spinotrapezius during the rest–contraction transient (1 Hz, 6 V; n = 8). PO2 mv was higher than PO2 is in all instances from rest (34.9 ± 6.0 versus 15.7 ± 6.4) to contractions (28.4 ± 5.3 versus 10.6 ± 5.2 mmHg, respectively) such that the mean PO2 gradient throughout the transient was 16.9 ± 6.6 mmHg (P < 0.05 for all). No differences in the amplitude of PO2 fall with contractions were observed between the microvasculature and interstitium (10.9 ± 2.3 versus 9.0 ± 3.5 mmHg, respectively; P > 0.05). However, the speed of the PO2 is fall during contractions was slower than that of PO2 mv (time constant: 12.8 ± 4.7 versus 9.0 ± 5.1 s, respectively; P < 0.05). Consistent with our hypothesis, a significant transmural gradient was sustained (but not increased) from rest to contractions. This supports that the blood–myocyte interface is the site of a substantial PO2 gradient driving O2 diffusion during metabolic transients. Based on Fick's law, elevated O2 flux with contractions must thus rely primarily on modulations in effective diffusing capacity (mainly erythrocyte haemodynamics and distribution) as the PO2 gradient is not increased.
Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.</description><identifier>ISSN: 0022-3751</identifier><identifier>EISSN: 1469-7793</identifier><identifier>DOI: 10.1113/JP275170</identifier><identifier>PMID: 29288568</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Contraction ; diffusion ; dynamics ; Hemodynamics ; Hypotheses ; kinetics ; Microvasculature ; Muscle ; Musculoskeletal system ; Oxidative metabolism ; oxygen gradients ; Phosphorescence ; Research Paper ; Sarcolemma ; Skeletal muscle</subject><ispartof>The Journal of physiology, 2018-03, Vol.596 (5), p.869-883</ispartof><rights>2017 The Authors. The Journal of Physiology © 2017 The Physiological Society</rights><rights>2017 The Authors. The Journal of Physiology © 2017 The Physiological Society.</rights><rights>Journal compilation © 2018 The Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0003-0913-9714 ; 0000-0003-1599-1751 ; 0000-0002-7861-637X ; 0000-0003-2441-3793</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830449/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830449/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29288568$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hirai, Daniel M.</creatorcontrib><creatorcontrib>Craig, Jesse C.</creatorcontrib><creatorcontrib>Colburn, Trenton D.</creatorcontrib><creatorcontrib>Eshima, Hiroaki</creatorcontrib><creatorcontrib>Kano, Yutaka</creatorcontrib><creatorcontrib>Sexton, William L.</creatorcontrib><creatorcontrib>Musch, Timothy I.</creatorcontrib><creatorcontrib>Poole, David C.</creatorcontrib><title>Skeletal muscle microvascular and interstitial PO2 from rest to contractions</title><title>The Journal of physiology</title><addtitle>J Physiol</addtitle><description>Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.
Oxygen pressure (PO2) gradients across the blood–myocyte interface are required for diffusive O2 transport, thereby supporting oxidative metabolism. The greatest resistance to O2 flux into skeletal muscle is considered to reside between the erythrocyte surface and adjacent sarcolemma, although this has not been measured during contractions. We tested the hypothesis that O2 gradients between skeletal muscle microvascular (PO2 mv ) and interstitial (PO2 is ) spaces would be present at rest and maintained or increased during contractions. PO2 mv and PO2 is were determined via phosphorescence quenching (Oxyphor probes G2 and G4, respectively) in the exposed rat spinotrapezius during the rest–contraction transient (1 Hz, 6 V; n = 8). PO2 mv was higher than PO2 is in all instances from rest (34.9 ± 6.0 versus 15.7 ± 6.4) to contractions (28.4 ± 5.3 versus 10.6 ± 5.2 mmHg, respectively) such that the mean PO2 gradient throughout the transient was 16.9 ± 6.6 mmHg (P < 0.05 for all). No differences in the amplitude of PO2 fall with contractions were observed between the microvasculature and interstitium (10.9 ± 2.3 versus 9.0 ± 3.5 mmHg, respectively; P > 0.05). However, the speed of the PO2 is fall during contractions was slower than that of PO2 mv (time constant: 12.8 ± 4.7 versus 9.0 ± 5.1 s, respectively; P < 0.05). Consistent with our hypothesis, a significant transmural gradient was sustained (but not increased) from rest to contractions. This supports that the blood–myocyte interface is the site of a substantial PO2 gradient driving O2 diffusion during metabolic transients. Based on Fick's law, elevated O2 flux with contractions must thus rely primarily on modulations in effective diffusing capacity (mainly erythrocyte haemodynamics and distribution) as the PO2 gradient is not increased.
Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.</description><subject>Contraction</subject><subject>diffusion</subject><subject>dynamics</subject><subject>Hemodynamics</subject><subject>Hypotheses</subject><subject>kinetics</subject><subject>Microvasculature</subject><subject>Muscle</subject><subject>Musculoskeletal system</subject><subject>Oxidative metabolism</subject><subject>oxygen gradients</subject><subject>Phosphorescence</subject><subject>Research Paper</subject><subject>Sarcolemma</subject><subject>Skeletal muscle</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNpdkVtLxDAQhYMoul7AXyAFX3ypJpOmSV4EWbyy4IL7HtKYajRt1qRV_Pdm8YL6NAzn43DmDEL7BB8TQujJzRw4IxyvoQmpallyLuk6mmAMUNKsbKHtlJ4wJhRLuYm2QIIQrBYTNLt7tt4O2hfdmIy3RedMDK86mdHrWOj-vnD9YGMa3OAyNb-Foo2hK6JNQzGEwoR-iNoMLvRpF2202ie79zV30OLifDG9Kme3l9fTs1m5hJpWJTOsobaRjWkkmJyD0xpazitDBLS4kVxTRokVhEFeeNNSDTWTVFouQNIddPppuxybzt4bu0rg1TK6Tsd3FbRTf5XePaqH8KqYoLiqVgZHXwYxvIz5ENW5ZKz3urdhTIpIAYIKiVlGD_-hT2GMfb5OAcYSV5gSyNTB70Q_Ub57zsDxJ_DmvH3_0QlWq_-p7_-pxc2cQG6CfgBlAovf</recordid><startdate>20180301</startdate><enddate>20180301</enddate><creator>Hirai, Daniel M.</creator><creator>Craig, Jesse C.</creator><creator>Colburn, Trenton D.</creator><creator>Eshima, Hiroaki</creator><creator>Kano, Yutaka</creator><creator>Sexton, William L.</creator><creator>Musch, Timothy I.</creator><creator>Poole, David C.</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>NPM</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0913-9714</orcidid><orcidid>https://orcid.org/0000-0003-1599-1751</orcidid><orcidid>https://orcid.org/0000-0002-7861-637X</orcidid><orcidid>https://orcid.org/0000-0003-2441-3793</orcidid></search><sort><creationdate>20180301</creationdate><title>Skeletal muscle microvascular and interstitial PO2 from rest to contractions</title><author>Hirai, Daniel M. ; Craig, Jesse C. ; Colburn, Trenton D. ; Eshima, Hiroaki ; Kano, Yutaka ; Sexton, William L. ; Musch, Timothy I. ; Poole, David C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p2634-5c5b3eb9bcb92c8567362f774c182f0b97a3531e8152b977bf3a265939e78293</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Contraction</topic><topic>diffusion</topic><topic>dynamics</topic><topic>Hemodynamics</topic><topic>Hypotheses</topic><topic>kinetics</topic><topic>Microvasculature</topic><topic>Muscle</topic><topic>Musculoskeletal system</topic><topic>Oxidative metabolism</topic><topic>oxygen gradients</topic><topic>Phosphorescence</topic><topic>Research Paper</topic><topic>Sarcolemma</topic><topic>Skeletal muscle</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hirai, Daniel M.</creatorcontrib><creatorcontrib>Craig, Jesse C.</creatorcontrib><creatorcontrib>Colburn, Trenton D.</creatorcontrib><creatorcontrib>Eshima, Hiroaki</creatorcontrib><creatorcontrib>Kano, Yutaka</creatorcontrib><creatorcontrib>Sexton, William L.</creatorcontrib><creatorcontrib>Musch, Timothy I.</creatorcontrib><creatorcontrib>Poole, David C.</creatorcontrib><collection>PubMed</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hirai, Daniel M.</au><au>Craig, Jesse C.</au><au>Colburn, Trenton D.</au><au>Eshima, Hiroaki</au><au>Kano, Yutaka</au><au>Sexton, William L.</au><au>Musch, Timothy I.</au><au>Poole, David C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Skeletal muscle microvascular and interstitial PO2 from rest to contractions</atitle><jtitle>The Journal of physiology</jtitle><addtitle>J Physiol</addtitle><date>2018-03-01</date><risdate>2018</risdate><volume>596</volume><issue>5</issue><spage>869</spage><epage>883</epage><pages>869-883</pages><issn>0022-3751</issn><eissn>1469-7793</eissn><abstract>Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.
Oxygen pressure (PO2) gradients across the blood–myocyte interface are required for diffusive O2 transport, thereby supporting oxidative metabolism. The greatest resistance to O2 flux into skeletal muscle is considered to reside between the erythrocyte surface and adjacent sarcolemma, although this has not been measured during contractions. We tested the hypothesis that O2 gradients between skeletal muscle microvascular (PO2 mv ) and interstitial (PO2 is ) spaces would be present at rest and maintained or increased during contractions. PO2 mv and PO2 is were determined via phosphorescence quenching (Oxyphor probes G2 and G4, respectively) in the exposed rat spinotrapezius during the rest–contraction transient (1 Hz, 6 V; n = 8). PO2 mv was higher than PO2 is in all instances from rest (34.9 ± 6.0 versus 15.7 ± 6.4) to contractions (28.4 ± 5.3 versus 10.6 ± 5.2 mmHg, respectively) such that the mean PO2 gradient throughout the transient was 16.9 ± 6.6 mmHg (P < 0.05 for all). No differences in the amplitude of PO2 fall with contractions were observed between the microvasculature and interstitium (10.9 ± 2.3 versus 9.0 ± 3.5 mmHg, respectively; P > 0.05). However, the speed of the PO2 is fall during contractions was slower than that of PO2 mv (time constant: 12.8 ± 4.7 versus 9.0 ± 5.1 s, respectively; P < 0.05). Consistent with our hypothesis, a significant transmural gradient was sustained (but not increased) from rest to contractions. This supports that the blood–myocyte interface is the site of a substantial PO2 gradient driving O2 diffusion during metabolic transients. Based on Fick's law, elevated O2 flux with contractions must thus rely primarily on modulations in effective diffusing capacity (mainly erythrocyte haemodynamics and distribution) as the PO2 gradient is not increased.
Key points
Oxygen pressure gradients across the microvascular walls are essential for oxygen diffusion from blood to tissue cells. At any given flux, the magnitude of these transmural gradients is proportional to the local resistance.
The greatest resistance to oxygen transport into skeletal muscle is considered to reside in the short distance between red blood cells and myocytes. Although crucial to oxygen transport, little is known about transmural pressure gradients within skeletal muscle during contractions.
We evaluated oxygen pressures within both the skeletal muscle microvascular and interstitial spaces to determine transmural gradients during the rest–contraction transient in anaesthetized rats.
The significant transmural gradient observed at rest was sustained during submaximal muscle contractions.
Our findings support that the blood–myocyte interface provides substantial resistance to oxygen diffusion at rest and during contractions and suggest that modulations in microvascular haemodynamics and red blood cell distribution constitute primary mechanisms driving increased transmural oxygen flux with contractions.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>29288568</pmid><doi>10.1113/JP275170</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-0913-9714</orcidid><orcidid>https://orcid.org/0000-0003-1599-1751</orcidid><orcidid>https://orcid.org/0000-0002-7861-637X</orcidid><orcidid>https://orcid.org/0000-0003-2441-3793</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Access via Wiley Online Library; EZB-FREE-00999 freely available EZB journals; Wiley Online Library (Open Access Collection); PubMed Central |
| subjects | Contraction diffusion dynamics Hemodynamics Hypotheses kinetics Microvasculature Muscle Musculoskeletal system Oxidative metabolism oxygen gradients Phosphorescence Research Paper Sarcolemma Skeletal muscle |
| title | Skeletal muscle microvascular and interstitial PO2 from rest to contractions |
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