Intra-cardiac transfer of fatty acids from capillary to cardiomyocyte
Blood-borne fatty acids (Fa) are important substrates for energy conversion in the mammalian heart. After release from plasma albumin, Fa traverse the endothelium and the interstitial compartment to cross the sarcolemma prior to oxidation in the cardiomyocytal mitochondria. The aims of the present s...
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| description | Blood-borne fatty acids (Fa) are important substrates for energy conversion in the mammalian heart. After release from plasma albumin, Fa traverse the endothelium and the interstitial compartment to cross the sarcolemma prior to oxidation in the cardiomyocytal mitochondria. The aims of the present study were to elucidate the site with lowest Fa permeability (i.e., highest Fa resistance) in the overall Fa trajectory from capillary to cardiomyocyte and the relative contribution of unbound Fa (detach pathway, characterized by the dissociation time constant τAlbFa) and albumin-bound Fa (contact pathway, characterized by the membrane reaction rate parameter dAlb) in delivering Fa to the cellular membranes. In this study, an extensive set of 34 multiple indicator dilution experiments with radiolabeled albumin and palmitate on isolated rabbit hearts was analysed by means of a previously developed mathematical model of Fa transfer dynamics. In these experiments, the ratio of the concentration of palmitate to albumin was set at 0.91. The analysis shows that total cardiac Fa permeability, Ptot, is indeed related to the albumin concentration in the extracellular compartment as predicted by the mathematical model. The analysis also reveals that the lowest permeability may reside in the boundary zones containing albumin in the microvascular and interstitial compartment. However, the permeability of the endothelial cytoplasm, Pec, may influence overall Fa permeability, Ptot, as well. The model analysis predicts that the most likely value of τAlbFa ranges from about 200 to 400 ms. In case τAlbFa is fast, i.e., about 200 ms, the extracellular contact pathway appears to be of minor importance in delivering Fa to the cell membrane. If Fa dissociation from albumin is slower, e.g. τAlbFa equals 400 ms, the contribution of the contact pathway may vary from minimal (dAlb≤5 nm) to substantial (dAlb about 100 nm). In the latter case, the permeability of the endothelial cytoplasm varies from infinite (no hindrance) to low (substantial hindrance) to keep the overall Fa flux at a fixed level. Definitive estimation of the impact of endothelial permeability on Ptot and the precise contribution of the contact pathway to overall transfer of Fa in boundary zones containing albumin requires adequate physicochemical experimentation to delineate the true value of, among others, τAlbFa, under physiologically relevant circumstances. Our analysis also implies that concentration differences of |
| doi_str_mv | 10.1371/journal.pone.0261288 |
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After release from plasma albumin, Fa traverse the endothelium and the interstitial compartment to cross the sarcolemma prior to oxidation in the cardiomyocytal mitochondria. The aims of the present study were to elucidate the site with lowest Fa permeability (i.e., highest Fa resistance) in the overall Fa trajectory from capillary to cardiomyocyte and the relative contribution of unbound Fa (detach pathway, characterized by the dissociation time constant τAlbFa) and albumin-bound Fa (contact pathway, characterized by the membrane reaction rate parameter dAlb) in delivering Fa to the cellular membranes. In this study, an extensive set of 34 multiple indicator dilution experiments with radiolabeled albumin and palmitate on isolated rabbit hearts was analysed by means of a previously developed mathematical model of Fa transfer dynamics. In these experiments, the ratio of the concentration of palmitate to albumin was set at 0.91. The analysis shows that total cardiac Fa permeability, Ptot, is indeed related to the albumin concentration in the extracellular compartment as predicted by the mathematical model. The analysis also reveals that the lowest permeability may reside in the boundary zones containing albumin in the microvascular and interstitial compartment. However, the permeability of the endothelial cytoplasm, Pec, may influence overall Fa permeability, Ptot, as well. The model analysis predicts that the most likely value of τAlbFa ranges from about 200 to 400 ms. In case τAlbFa is fast, i.e., about 200 ms, the extracellular contact pathway appears to be of minor importance in delivering Fa to the cell membrane. If Fa dissociation from albumin is slower, e.g. τAlbFa equals 400 ms, the contribution of the contact pathway may vary from minimal (dAlb≤5 nm) to substantial (dAlb about 100 nm). In the latter case, the permeability of the endothelial cytoplasm varies from infinite (no hindrance) to low (substantial hindrance) to keep the overall Fa flux at a fixed level. Definitive estimation of the impact of endothelial permeability on Ptot and the precise contribution of the contact pathway to overall transfer of Fa in boundary zones containing albumin requires adequate physicochemical experimentation to delineate the true value of, among others, τAlbFa, under physiologically relevant circumstances. Our analysis also implies that concentration differences of unbound Fa are the driving force of intra-cardiac Fa transfer; an active, energy requiring transport mechanism is not necessarily involved. Membrane-associated proteins may facilitate Fa transfer in the boundary zones containing albumin by modulating the membrane reaction rate parameter, dAlb, and, hence, the contribution of the contact pathway to intra-cardiac Fa transfer.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0261288</identifier><identifier>PMID: 35089937</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Albumin ; Albumins ; Animals ; Aqueous solutions ; Bioengineering ; Biological Transport ; Biology and Life Sciences ; Capillaries - metabolism ; Cardiomyocytes ; Cardiopulmonary system ; Cardiovascular system ; Cell membranes ; Cytoplasm ; Dilution ; Dissociation ; Endothelium ; Energy conversion ; Experimentation ; Experiments ; Fatty acids ; Fatty Acids - metabolism ; Health aspects ; Heart ; Heart rate ; Laboratory animals ; Mathematical models ; Medical research ; Medicine and Health Sciences ; Medicine, Experimental ; Membranes ; Metabolism ; Microvasculature ; Mitochondria ; Models, Theoretical ; Myocytes, Cardiac - metabolism ; Ostomy ; Oxidation ; Palmitates - metabolism ; Palmitic acid ; Parameters ; Permeability ; Physiological aspects ; Physiology ; Protein Binding ; Proteins ; Rabbits ; Research and Analysis Methods ; Sarcolemma ; Serum Albumin - metabolism ; Substrates ; Time constant</subject><ispartof>PloS one, 2022-01, Vol.17 (1), p.e0261288-e0261288</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 van der Vusse et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 van der Vusse et al 2022 van der Vusse et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-b55f179cebf08cd8bb2d5cbb14781cc79b3417c390400020b282908d962fc6883</citedby><cites>FETCH-LOGICAL-c692t-b55f179cebf08cd8bb2d5cbb14781cc79b3417c390400020b282908d962fc6883</cites><orcidid>0000-0001-9655-9869</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/PMC8797212/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8797212/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35089937$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van der Vusse, Ger J</creatorcontrib><creatorcontrib>Arts, Theo</creatorcontrib><creatorcontrib>Bassingthwaighte, James B</creatorcontrib><creatorcontrib>Reneman, Robert S</creatorcontrib><title>Intra-cardiac transfer of fatty acids from capillary to cardiomyocyte</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Blood-borne fatty acids (Fa) are important substrates for energy conversion in the mammalian heart. After release from plasma albumin, Fa traverse the endothelium and the interstitial compartment to cross the sarcolemma prior to oxidation in the cardiomyocytal mitochondria. The aims of the present study were to elucidate the site with lowest Fa permeability (i.e., highest Fa resistance) in the overall Fa trajectory from capillary to cardiomyocyte and the relative contribution of unbound Fa (detach pathway, characterized by the dissociation time constant τAlbFa) and albumin-bound Fa (contact pathway, characterized by the membrane reaction rate parameter dAlb) in delivering Fa to the cellular membranes. In this study, an extensive set of 34 multiple indicator dilution experiments with radiolabeled albumin and palmitate on isolated rabbit hearts was analysed by means of a previously developed mathematical model of Fa transfer dynamics. In these experiments, the ratio of the concentration of palmitate to albumin was set at 0.91. The analysis shows that total cardiac Fa permeability, Ptot, is indeed related to the albumin concentration in the extracellular compartment as predicted by the mathematical model. The analysis also reveals that the lowest permeability may reside in the boundary zones containing albumin in the microvascular and interstitial compartment. However, the permeability of the endothelial cytoplasm, Pec, may influence overall Fa permeability, Ptot, as well. The model analysis predicts that the most likely value of τAlbFa ranges from about 200 to 400 ms. In case τAlbFa is fast, i.e., about 200 ms, the extracellular contact pathway appears to be of minor importance in delivering Fa to the cell membrane. If Fa dissociation from albumin is slower, e.g. τAlbFa equals 400 ms, the contribution of the contact pathway may vary from minimal (dAlb≤5 nm) to substantial (dAlb about 100 nm). In the latter case, the permeability of the endothelial cytoplasm varies from infinite (no hindrance) to low (substantial hindrance) to keep the overall Fa flux at a fixed level. Definitive estimation of the impact of endothelial permeability on Ptot and the precise contribution of the contact pathway to overall transfer of Fa in boundary zones containing albumin requires adequate physicochemical experimentation to delineate the true value of, among others, τAlbFa, under physiologically relevant circumstances. Our analysis also implies that concentration differences of unbound Fa are the driving force of intra-cardiac Fa transfer; an active, energy requiring transport mechanism is not necessarily involved. Membrane-associated proteins may facilitate Fa transfer in the boundary zones containing albumin by modulating the membrane reaction rate parameter, dAlb, and, hence, the contribution of the contact pathway to intra-cardiac Fa transfer.</description><subject>Albumin</subject><subject>Albumins</subject><subject>Animals</subject><subject>Aqueous solutions</subject><subject>Bioengineering</subject><subject>Biological Transport</subject><subject>Biology and Life Sciences</subject><subject>Capillaries - metabolism</subject><subject>Cardiomyocytes</subject><subject>Cardiopulmonary system</subject><subject>Cardiovascular system</subject><subject>Cell membranes</subject><subject>Cytoplasm</subject><subject>Dilution</subject><subject>Dissociation</subject><subject>Endothelium</subject><subject>Energy conversion</subject><subject>Experimentation</subject><subject>Experiments</subject><subject>Fatty acids</subject><subject>Fatty Acids - metabolism</subject><subject>Health aspects</subject><subject>Heart</subject><subject>Heart rate</subject><subject>Laboratory animals</subject><subject>Mathematical models</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Medicine, Experimental</subject><subject>Membranes</subject><subject>Metabolism</subject><subject>Microvasculature</subject><subject>Mitochondria</subject><subject>Models, Theoretical</subject><subject>Myocytes, Cardiac - metabolism</subject><subject>Ostomy</subject><subject>Oxidation</subject><subject>Palmitates - metabolism</subject><subject>Palmitic acid</subject><subject>Parameters</subject><subject>Permeability</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Rabbits</subject><subject>Research and Analysis Methods</subject><subject>Sarcolemma</subject><subject>Serum Albumin - metabolism</subject><subject>Substrates</subject><subject>Time constant</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkltr2zAcxc1YWbtu32BshsFYH5LpYtnSy6CUbgsUCru9Cl0TBdvKJHks335y45Z49GH4wUL-naO_jk9RvIJgCXEDP2z9EHrRLne-N0uAaogofVKcQYbRokYAPz1anxbPY9wCQDCt62fFKSaAMoabs-J61acgFkoE7YQq87qP1oTS29KKlPalUE7H0gbflUrsXNuKsC-TL-8Uvtt7tU_mRXFiRRvNy-l9Xvz4dP396svi5vbz6uryZqFqhtJCEmJhw5SRFlClqZRIEyUlrBoKlWqYxBVsFGagAgAgIBFFDFDNamRVTSk-L94cfHetj3xKIHJUI0xYdmGZWB0I7cWW74Lr8rzcC8fvNnxYcxGSU63hmAhMkSS1rlClSSUsELTSSGhJKCY2e32cThtkZ7QyY1TtzHT-pXcbvva_OW1YgyDKBu8ng-B_DSYm3rmoTM6wN344zE1pQ-k499t_0MdvN1FrkS_geuvzuWo05Zd1TgoB1lSZWj5C5UebzqlcF-vy_kxwMRNkJpk_aS2GGPnq29f_Z29_ztl3R-zGiDZtom-H5Hwf52B1AFXwMQZjH0KGgI9tv0-Dj23nU9uz7PXxD3oQ3dcb_wUGE_kD</recordid><startdate>20220128</startdate><enddate>20220128</enddate><creator>van der Vusse, Ger J</creator><creator>Arts, Theo</creator><creator>Bassingthwaighte, James B</creator><creator>Reneman, Robert S</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9655-9869</orcidid></search><sort><creationdate>20220128</creationdate><title>Intra-cardiac transfer of fatty acids from capillary to cardiomyocyte</title><author>van der Vusse, Ger J ; Arts, Theo ; Bassingthwaighte, James B ; Reneman, Robert S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-b55f179cebf08cd8bb2d5cbb14781cc79b3417c390400020b282908d962fc6883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Albumin</topic><topic>Albumins</topic><topic>Animals</topic><topic>Aqueous solutions</topic><topic>Bioengineering</topic><topic>Biological Transport</topic><topic>Biology and Life Sciences</topic><topic>Capillaries - 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After release from plasma albumin, Fa traverse the endothelium and the interstitial compartment to cross the sarcolemma prior to oxidation in the cardiomyocytal mitochondria. The aims of the present study were to elucidate the site with lowest Fa permeability (i.e., highest Fa resistance) in the overall Fa trajectory from capillary to cardiomyocyte and the relative contribution of unbound Fa (detach pathway, characterized by the dissociation time constant τAlbFa) and albumin-bound Fa (contact pathway, characterized by the membrane reaction rate parameter dAlb) in delivering Fa to the cellular membranes. In this study, an extensive set of 34 multiple indicator dilution experiments with radiolabeled albumin and palmitate on isolated rabbit hearts was analysed by means of a previously developed mathematical model of Fa transfer dynamics. In these experiments, the ratio of the concentration of palmitate to albumin was set at 0.91. The analysis shows that total cardiac Fa permeability, Ptot, is indeed related to the albumin concentration in the extracellular compartment as predicted by the mathematical model. The analysis also reveals that the lowest permeability may reside in the boundary zones containing albumin in the microvascular and interstitial compartment. However, the permeability of the endothelial cytoplasm, Pec, may influence overall Fa permeability, Ptot, as well. The model analysis predicts that the most likely value of τAlbFa ranges from about 200 to 400 ms. In case τAlbFa is fast, i.e., about 200 ms, the extracellular contact pathway appears to be of minor importance in delivering Fa to the cell membrane. If Fa dissociation from albumin is slower, e.g. τAlbFa equals 400 ms, the contribution of the contact pathway may vary from minimal (dAlb≤5 nm) to substantial (dAlb about 100 nm). In the latter case, the permeability of the endothelial cytoplasm varies from infinite (no hindrance) to low (substantial hindrance) to keep the overall Fa flux at a fixed level. Definitive estimation of the impact of endothelial permeability on Ptot and the precise contribution of the contact pathway to overall transfer of Fa in boundary zones containing albumin requires adequate physicochemical experimentation to delineate the true value of, among others, τAlbFa, under physiologically relevant circumstances. Our analysis also implies that concentration differences of unbound Fa are the driving force of intra-cardiac Fa transfer; an active, energy requiring transport mechanism is not necessarily involved. Membrane-associated proteins may facilitate Fa transfer in the boundary zones containing albumin by modulating the membrane reaction rate parameter, dAlb, and, hence, the contribution of the contact pathway to intra-cardiac Fa transfer.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>35089937</pmid><doi>10.1371/journal.pone.0261288</doi><tpages>e0261288</tpages><orcidid>https://orcid.org/0000-0001-9655-9869</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_2623591479 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Albumin Albumins Animals Aqueous solutions Bioengineering Biological Transport Biology and Life Sciences Capillaries - metabolism Cardiomyocytes Cardiopulmonary system Cardiovascular system Cell membranes Cytoplasm Dilution Dissociation Endothelium Energy conversion Experimentation Experiments Fatty acids Fatty Acids - metabolism Health aspects Heart Heart rate Laboratory animals Mathematical models Medical research Medicine and Health Sciences Medicine, Experimental Membranes Metabolism Microvasculature Mitochondria Models, Theoretical Myocytes, Cardiac - metabolism Ostomy Oxidation Palmitates - metabolism Palmitic acid Parameters Permeability Physiological aspects Physiology Protein Binding Proteins Rabbits Research and Analysis Methods Sarcolemma Serum Albumin - metabolism Substrates Time constant |
| title | Intra-cardiac transfer of fatty acids from capillary to cardiomyocyte |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T23%3A08%3A05IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Intra-cardiac%20transfer%20of%20fatty%20acids%20from%20capillary%20to%20cardiomyocyte&rft.jtitle=PloS%20one&rft.au=van%20der%20Vusse,%20Ger%20J&rft.date=2022-01-28&rft.volume=17&rft.issue=1&rft.spage=e0261288&rft.epage=e0261288&rft.pages=e0261288-e0261288&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0261288&rft_dat=%3Cgale_plos_%3EA690820974%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2623591479&rft_id=info:pmid/35089937&rft_galeid=A690820974&rft_doaj_id=oai_doaj_org_article_35a382b56d424d54af0a84d2adb5835f&rfr_iscdi=true |