Macrophages take up VLDL-sized emulsion particles through caveolae-mediated endocytosis and excrete part of the internalized triglycerides as fatty acids
Triglycerides are carried in the bloodstream as part of very low-density lipoproteins (VLDLs) and chylomicrons, which represent the triglyceride-rich lipoproteins. Triglyceride-rich lipoproteins and their remnants contribute to atherosclerosis, possibly by carrying remnant cholesterol and/or by exer...
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| Veröffentlicht in: | PLoS biology 2022-08, Vol.20 (8), p.e3001516-e3001516 |
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| creator | Deng, Lei Vrieling, Frank Stienstra, Rinke Hooiveld, Guido J Feitsma, Anouk L Kersten, Sander |
| description | Triglycerides are carried in the bloodstream as part of very low-density lipoproteins (VLDLs) and chylomicrons, which represent the triglyceride-rich lipoproteins. Triglyceride-rich lipoproteins and their remnants contribute to atherosclerosis, possibly by carrying remnant cholesterol and/or by exerting a proinflammatory effect on macrophages. Nevertheless, little is known about how macrophages process triglyceride-rich lipoproteins. Here, using VLDL-sized triglyceride-rich emulsion particles, we aimed to study the mechanism by which VLDL triglycerides are taken up, processed, and stored in macrophages. Our results show that macrophage uptake of VLDL-sized emulsion particles is dependent on lipoprotein lipase (LPL) and requires the lipoprotein-binding C-terminal domain but not the catalytic N-terminal domain of LPL. Subsequent internalization of VLDL-sized emulsion particles by macrophages is carried out by caveolae-mediated endocytosis, followed by triglyceride hydrolysis catalyzed by lysosomal acid lipase. It is shown that STARD3 is required for the transfer of lysosomal fatty acids to the ER for subsequent storage as triglycerides, while NPC1 likely is involved in promoting the extracellular efflux of fatty acids from lysosomes. Our data provide novel insights into how macrophages process VLDL triglycerides and suggest that macrophages have the remarkable capacity to excrete part of the internalized triglycerides as fatty acids. |
| doi_str_mv | 10.1371/journal.pbio.3001516 |
| format | Article |
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Triglyceride-rich lipoproteins and their remnants contribute to atherosclerosis, possibly by carrying remnant cholesterol and/or by exerting a proinflammatory effect on macrophages. Nevertheless, little is known about how macrophages process triglyceride-rich lipoproteins. Here, using VLDL-sized triglyceride-rich emulsion particles, we aimed to study the mechanism by which VLDL triglycerides are taken up, processed, and stored in macrophages. Our results show that macrophage uptake of VLDL-sized emulsion particles is dependent on lipoprotein lipase (LPL) and requires the lipoprotein-binding C-terminal domain but not the catalytic N-terminal domain of LPL. Subsequent internalization of VLDL-sized emulsion particles by macrophages is carried out by caveolae-mediated endocytosis, followed by triglyceride hydrolysis catalyzed by lysosomal acid lipase. It is shown that STARD3 is required for the transfer of lysosomal fatty acids to the ER for subsequent storage as triglycerides, while NPC1 likely is involved in promoting the extracellular efflux of fatty acids from lysosomes. Our data provide novel insights into how macrophages process VLDL triglycerides and suggest that macrophages have the remarkable capacity to excrete part of the internalized triglycerides as fatty acids.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3001516</identifier><identifier>PMID: 36026438</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Arteriosclerosis ; Atherosclerosis ; Biology and Life Sciences ; Caveolae ; Cholesterol ; Chylomicrons ; Domains ; Efflux ; Endocytosis ; Endoplasmic reticulum ; Fatty acids ; Flow cytometry ; Gene expression ; Heparan sulfate ; Inflammation ; Internalization ; Lipase ; Lipids ; Lipoprotein lipase ; Lipoproteins ; Lipoproteins (very low density) ; Low density lipoproteins ; Lysosomes ; Macrophages ; Medicine and Health Sciences ; Npc1 protein ; Pathogenesis ; Pathogens ; Physical Sciences ; Physiological aspects ; Proteins ; Research and Analysis Methods ; Steroidogenic acute regulatory protein ; Triglycerides</subject><ispartof>PLoS biology, 2022-08, Vol.20 (8), p.e3001516-e3001516</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Deng 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 Deng et al 2022 Deng et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c672t-be6e2fe7535ea29bc4510f1068e185335f779bb4a268f2e74ed65f7cf18d6b163</citedby><cites>FETCH-LOGICAL-c672t-be6e2fe7535ea29bc4510f1068e185335f779bb4a268f2e74ed65f7cf18d6b163</cites><orcidid>0000-0002-7786-9738</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/PMC9455861/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9455861/$$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></links><search><creatorcontrib>Deng, Lei</creatorcontrib><creatorcontrib>Vrieling, Frank</creatorcontrib><creatorcontrib>Stienstra, Rinke</creatorcontrib><creatorcontrib>Hooiveld, Guido J</creatorcontrib><creatorcontrib>Feitsma, Anouk L</creatorcontrib><creatorcontrib>Kersten, Sander</creatorcontrib><title>Macrophages take up VLDL-sized emulsion particles through caveolae-mediated endocytosis and excrete part of the internalized triglycerides as fatty acids</title><title>PLoS biology</title><description>Triglycerides are carried in the bloodstream as part of very low-density lipoproteins (VLDLs) and chylomicrons, which represent the triglyceride-rich lipoproteins. Triglyceride-rich lipoproteins and their remnants contribute to atherosclerosis, possibly by carrying remnant cholesterol and/or by exerting a proinflammatory effect on macrophages. Nevertheless, little is known about how macrophages process triglyceride-rich lipoproteins. Here, using VLDL-sized triglyceride-rich emulsion particles, we aimed to study the mechanism by which VLDL triglycerides are taken up, processed, and stored in macrophages. Our results show that macrophage uptake of VLDL-sized emulsion particles is dependent on lipoprotein lipase (LPL) and requires the lipoprotein-binding C-terminal domain but not the catalytic N-terminal domain of LPL. Subsequent internalization of VLDL-sized emulsion particles by macrophages is carried out by caveolae-mediated endocytosis, followed by triglyceride hydrolysis catalyzed by lysosomal acid lipase. It is shown that STARD3 is required for the transfer of lysosomal fatty acids to the ER for subsequent storage as triglycerides, while NPC1 likely is involved in promoting the extracellular efflux of fatty acids from lysosomes. Our data provide novel insights into how macrophages process VLDL triglycerides and suggest that macrophages have the remarkable capacity to excrete part of the internalized triglycerides as fatty acids.</description><subject>Arteriosclerosis</subject><subject>Atherosclerosis</subject><subject>Biology and Life Sciences</subject><subject>Caveolae</subject><subject>Cholesterol</subject><subject>Chylomicrons</subject><subject>Domains</subject><subject>Efflux</subject><subject>Endocytosis</subject><subject>Endoplasmic reticulum</subject><subject>Fatty acids</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Heparan sulfate</subject><subject>Inflammation</subject><subject>Internalization</subject><subject>Lipase</subject><subject>Lipids</subject><subject>Lipoprotein lipase</subject><subject>Lipoproteins</subject><subject>Lipoproteins (very low density)</subject><subject>Low density lipoproteins</subject><subject>Lysosomes</subject><subject>Macrophages</subject><subject>Medicine and Health Sciences</subject><subject>Npc1 protein</subject><subject>Pathogenesis</subject><subject>Pathogens</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Steroidogenic acute regulatory 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take up VLDL-sized emulsion particles through caveolae-mediated endocytosis and excrete part of the internalized triglycerides as fatty acids</title><author>Deng, Lei ; Vrieling, Frank ; Stienstra, Rinke ; Hooiveld, Guido J ; Feitsma, Anouk L ; Kersten, Sander</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c672t-be6e2fe7535ea29bc4510f1068e185335f779bb4a268f2e74ed65f7cf18d6b163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Arteriosclerosis</topic><topic>Atherosclerosis</topic><topic>Biology and Life Sciences</topic><topic>Caveolae</topic><topic>Cholesterol</topic><topic>Chylomicrons</topic><topic>Domains</topic><topic>Efflux</topic><topic>Endocytosis</topic><topic>Endoplasmic reticulum</topic><topic>Fatty acids</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Heparan sulfate</topic><topic>Inflammation</topic><topic>Internalization</topic><topic>Lipase</topic><topic>Lipids</topic><topic>Lipoprotein lipase</topic><topic>Lipoproteins</topic><topic>Lipoproteins (very low density)</topic><topic>Low density lipoproteins</topic><topic>Lysosomes</topic><topic>Macrophages</topic><topic>Medicine and Health Sciences</topic><topic>Npc1 protein</topic><topic>Pathogenesis</topic><topic>Pathogens</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Steroidogenic acute regulatory protein</topic><topic>Triglycerides</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Deng, Lei</creatorcontrib><creatorcontrib>Vrieling, Frank</creatorcontrib><creatorcontrib>Stienstra, Rinke</creatorcontrib><creatorcontrib>Hooiveld, Guido J</creatorcontrib><creatorcontrib>Feitsma, Anouk L</creatorcontrib><creatorcontrib>Kersten, 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Triglyceride-rich lipoproteins and their remnants contribute to atherosclerosis, possibly by carrying remnant cholesterol and/or by exerting a proinflammatory effect on macrophages. Nevertheless, little is known about how macrophages process triglyceride-rich lipoproteins. Here, using VLDL-sized triglyceride-rich emulsion particles, we aimed to study the mechanism by which VLDL triglycerides are taken up, processed, and stored in macrophages. Our results show that macrophage uptake of VLDL-sized emulsion particles is dependent on lipoprotein lipase (LPL) and requires the lipoprotein-binding C-terminal domain but not the catalytic N-terminal domain of LPL. Subsequent internalization of VLDL-sized emulsion particles by macrophages is carried out by caveolae-mediated endocytosis, followed by triglyceride hydrolysis catalyzed by lysosomal acid lipase. It is shown that STARD3 is required for the transfer of lysosomal fatty acids to the ER for subsequent storage as triglycerides, while NPC1 likely is involved in promoting the extracellular efflux of fatty acids from lysosomes. Our data provide novel insights into how macrophages process VLDL triglycerides and suggest that macrophages have the remarkable capacity to excrete part of the internalized triglycerides as fatty acids.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>36026438</pmid><doi>10.1371/journal.pbio.3001516</doi><orcidid>https://orcid.org/0000-0002-7786-9738</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arteriosclerosis Atherosclerosis Biology and Life Sciences Caveolae Cholesterol Chylomicrons Domains Efflux Endocytosis Endoplasmic reticulum Fatty acids Flow cytometry Gene expression Heparan sulfate Inflammation Internalization Lipase Lipids Lipoprotein lipase Lipoproteins Lipoproteins (very low density) Low density lipoproteins Lysosomes Macrophages Medicine and Health Sciences Npc1 protein Pathogenesis Pathogens Physical Sciences Physiological aspects Proteins Research and Analysis Methods Steroidogenic acute regulatory protein Triglycerides |
| title | Macrophages take up VLDL-sized emulsion particles through caveolae-mediated endocytosis and excrete part of the internalized triglycerides as fatty acids |
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