Metabolic landscape of the healthy pancreas and pancreatic tumor microenvironment
Pancreatic cancer, one of the deadliest human malignancies, is characterized by a fibro-inflammatory tumor microenvironment and wide array of metabolic alterations. To comprehensively map metabolism in a cell type-specific manner, we harnessed a unique single-cell RNA-sequencing dataset of normal hu...
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creator | Bonilla, Monica E Radyk, Megan D Perricone, Matthew D Elhossiny, Ahmed M Harold, Alexis C Medina-Cabrera, Paola I Kadiyala, Padma Shi, Jiaqi Frankel, Timothy L Carpenter, Eileen S Green, Michael D Mitrea, Cristina Lyssiotis, Costas A Pasca di Magliano, Marina |
description | Pancreatic cancer, one of the deadliest human malignancies, is characterized by a fibro-inflammatory tumor microenvironment and wide array of metabolic alterations. To comprehensively map metabolism in a cell type-specific manner, we harnessed a unique single-cell RNA-sequencing dataset of normal human pancreata. This was compared with human pancreatic cancer samples using a computational pipeline optimized for this study. In the cancer cells we observed enhanced biosynthetic programs. We identified downregulation of mitochondrial programs in several immune populations, relative to their normal counterparts in healthy pancreas. Although granulocytes, B cells, and CD8+ T cells all downregulated oxidative phosphorylation, the mechanisms by which this occurred were cell type specific. In fact, the expression pattern of the electron transport chain complexes was sufficient to identify immune cell types without the use of lineage markers. We also observed changes in tumor-associated macrophage (TAM) lipid metabolism, with increased expression of enzymes mediating unsaturated fatty acid synthesis and upregulation in cholesterol export. Concurrently, cancer cells exhibited upregulation of lipid/cholesterol receptor import. We thus identified a potential crosstalk whereby TAMs provide cholesterol to cancer cells. We suggest that this may be a new mechanism boosting cancer cell growth and a therapeutic target in the future. |
doi_str_mv | 10.1172/jci.insight.180114 |
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To comprehensively map metabolism in a cell type-specific manner, we harnessed a unique single-cell RNA-sequencing dataset of normal human pancreata. This was compared with human pancreatic cancer samples using a computational pipeline optimized for this study. In the cancer cells we observed enhanced biosynthetic programs. We identified downregulation of mitochondrial programs in several immune populations, relative to their normal counterparts in healthy pancreas. Although granulocytes, B cells, and CD8+ T cells all downregulated oxidative phosphorylation, the mechanisms by which this occurred were cell type specific. In fact, the expression pattern of the electron transport chain complexes was sufficient to identify immune cell types without the use of lineage markers. We also observed changes in tumor-associated macrophage (TAM) lipid metabolism, with increased expression of enzymes mediating unsaturated fatty acid synthesis and upregulation in cholesterol export. Concurrently, cancer cells exhibited upregulation of lipid/cholesterol receptor import. We thus identified a potential crosstalk whereby TAMs provide cholesterol to cancer cells. We suggest that this may be a new mechanism boosting cancer cell growth and a therapeutic target in the future.</description><identifier>ISSN: 2379-3708</identifier><identifier>EISSN: 2379-3708</identifier><identifier>DOI: 10.1172/jci.insight.180114</identifier><identifier>PMID: 39315547</identifier><language>eng</language><publisher>United States: American Society for Clinical Investigation</publisher><subject>Cholesterol - metabolism ; Humans ; Lipid Metabolism ; Mitochondria - metabolism ; Oxidative Phosphorylation ; Pancreas - metabolism ; Pancreas - pathology ; Pancreatic Neoplasms - genetics ; Pancreatic Neoplasms - metabolism ; Pancreatic Neoplasms - pathology ; Single-Cell Analysis ; Tumor Microenvironment ; Tumor-Associated Macrophages - immunology ; Tumor-Associated Macrophages - metabolism</subject><ispartof>JCI insight, 2024-08, Vol.9 (18)</ispartof><rights>2024 Bonilla et al. 2024 Bonilla et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c284t-7bd494fa86c063913867c33963b84459aaf761531045e4d1ff5c1c42ad7408003</cites><orcidid>0000-0003-4951-7118 ; 0000-0001-9309-6141 ; 0000-0003-4893-1587 ; 0000-0001-5987-0404</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/PMC11457849/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11457849/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39315547$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bonilla, Monica E</creatorcontrib><creatorcontrib>Radyk, Megan D</creatorcontrib><creatorcontrib>Perricone, Matthew D</creatorcontrib><creatorcontrib>Elhossiny, Ahmed M</creatorcontrib><creatorcontrib>Harold, Alexis C</creatorcontrib><creatorcontrib>Medina-Cabrera, Paola I</creatorcontrib><creatorcontrib>Kadiyala, Padma</creatorcontrib><creatorcontrib>Shi, Jiaqi</creatorcontrib><creatorcontrib>Frankel, Timothy L</creatorcontrib><creatorcontrib>Carpenter, Eileen S</creatorcontrib><creatorcontrib>Green, Michael D</creatorcontrib><creatorcontrib>Mitrea, Cristina</creatorcontrib><creatorcontrib>Lyssiotis, Costas A</creatorcontrib><creatorcontrib>Pasca di Magliano, Marina</creatorcontrib><title>Metabolic landscape of the healthy pancreas and pancreatic tumor microenvironment</title><title>JCI insight</title><addtitle>JCI Insight</addtitle><description>Pancreatic cancer, one of the deadliest human malignancies, is characterized by a fibro-inflammatory tumor microenvironment and wide array of metabolic alterations. To comprehensively map metabolism in a cell type-specific manner, we harnessed a unique single-cell RNA-sequencing dataset of normal human pancreata. This was compared with human pancreatic cancer samples using a computational pipeline optimized for this study. In the cancer cells we observed enhanced biosynthetic programs. We identified downregulation of mitochondrial programs in several immune populations, relative to their normal counterparts in healthy pancreas. Although granulocytes, B cells, and CD8+ T cells all downregulated oxidative phosphorylation, the mechanisms by which this occurred were cell type specific. In fact, the expression pattern of the electron transport chain complexes was sufficient to identify immune cell types without the use of lineage markers. We also observed changes in tumor-associated macrophage (TAM) lipid metabolism, with increased expression of enzymes mediating unsaturated fatty acid synthesis and upregulation in cholesterol export. Concurrently, cancer cells exhibited upregulation of lipid/cholesterol receptor import. We thus identified a potential crosstalk whereby TAMs provide cholesterol to cancer cells. We suggest that this may be a new mechanism boosting cancer cell growth and a therapeutic target in the future.</description><subject>Cholesterol - metabolism</subject><subject>Humans</subject><subject>Lipid Metabolism</subject><subject>Mitochondria - metabolism</subject><subject>Oxidative Phosphorylation</subject><subject>Pancreas - metabolism</subject><subject>Pancreas - pathology</subject><subject>Pancreatic Neoplasms - genetics</subject><subject>Pancreatic Neoplasms - metabolism</subject><subject>Pancreatic Neoplasms - pathology</subject><subject>Single-Cell Analysis</subject><subject>Tumor Microenvironment</subject><subject>Tumor-Associated Macrophages - immunology</subject><subject>Tumor-Associated Macrophages - metabolism</subject><issn>2379-3708</issn><issn>2379-3708</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUVtPwyAYJUbjzNwf8MH00ZdOKFDokzGLt2TGmOgzoZSuLG2pQJfs34vZJfOJj3AufOcAcIPgHCGW3a-VmZvem1UT5ohDhMgZuMowK1LMID8_mSdg5v0aQogYySDll2CCC4woJewKfL7rIEvbGpW0sq-8koNObJ2ERieNlm1otskge-W09EkEHC4hEsLYWZd0Rjmr-41xtu90H67BRS1br2f7cwq-n5--Fq_p8uPlbfG4TFXGSUhZWZGC1JLnCua4QJjnTGFc5LjkhNBCyprliGIECdWkQnVNFVIkkxUjkEOIp-BhpzuMZacrFa2dbMXgTCfdVlhpxP-X3jRiZTciRkUZJ0VUuNsrOPszah9EZ7zSbQxC29GL6M1ZTjBlEZrtoHFX752ujz4Iir8-ROxD7PsQuz4i6fb0h0fKIX38C6DEim8</recordid><startdate>20240813</startdate><enddate>20240813</enddate><creator>Bonilla, Monica E</creator><creator>Radyk, Megan D</creator><creator>Perricone, Matthew D</creator><creator>Elhossiny, Ahmed M</creator><creator>Harold, Alexis C</creator><creator>Medina-Cabrera, Paola I</creator><creator>Kadiyala, Padma</creator><creator>Shi, Jiaqi</creator><creator>Frankel, Timothy L</creator><creator>Carpenter, Eileen S</creator><creator>Green, Michael D</creator><creator>Mitrea, Cristina</creator><creator>Lyssiotis, Costas A</creator><creator>Pasca di Magliano, Marina</creator><general>American Society for Clinical Investigation</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4951-7118</orcidid><orcidid>https://orcid.org/0000-0001-9309-6141</orcidid><orcidid>https://orcid.org/0000-0003-4893-1587</orcidid><orcidid>https://orcid.org/0000-0001-5987-0404</orcidid></search><sort><creationdate>20240813</creationdate><title>Metabolic landscape of the healthy pancreas and pancreatic tumor microenvironment</title><author>Bonilla, Monica E ; Radyk, Megan D ; Perricone, Matthew D ; Elhossiny, Ahmed M ; Harold, Alexis C ; Medina-Cabrera, Paola I ; Kadiyala, Padma ; Shi, Jiaqi ; Frankel, Timothy L ; Carpenter, Eileen S ; Green, Michael D ; Mitrea, Cristina ; Lyssiotis, Costas A ; Pasca di Magliano, Marina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c284t-7bd494fa86c063913867c33963b84459aaf761531045e4d1ff5c1c42ad7408003</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Cholesterol - metabolism</topic><topic>Humans</topic><topic>Lipid Metabolism</topic><topic>Mitochondria - metabolism</topic><topic>Oxidative Phosphorylation</topic><topic>Pancreas - metabolism</topic><topic>Pancreas - pathology</topic><topic>Pancreatic Neoplasms - genetics</topic><topic>Pancreatic Neoplasms - metabolism</topic><topic>Pancreatic Neoplasms - pathology</topic><topic>Single-Cell Analysis</topic><topic>Tumor Microenvironment</topic><topic>Tumor-Associated Macrophages - immunology</topic><topic>Tumor-Associated Macrophages - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bonilla, Monica E</creatorcontrib><creatorcontrib>Radyk, Megan D</creatorcontrib><creatorcontrib>Perricone, Matthew D</creatorcontrib><creatorcontrib>Elhossiny, Ahmed M</creatorcontrib><creatorcontrib>Harold, Alexis C</creatorcontrib><creatorcontrib>Medina-Cabrera, Paola I</creatorcontrib><creatorcontrib>Kadiyala, Padma</creatorcontrib><creatorcontrib>Shi, Jiaqi</creatorcontrib><creatorcontrib>Frankel, Timothy L</creatorcontrib><creatorcontrib>Carpenter, Eileen S</creatorcontrib><creatorcontrib>Green, Michael D</creatorcontrib><creatorcontrib>Mitrea, Cristina</creatorcontrib><creatorcontrib>Lyssiotis, Costas A</creatorcontrib><creatorcontrib>Pasca di Magliano, Marina</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>JCI insight</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bonilla, Monica E</au><au>Radyk, Megan D</au><au>Perricone, Matthew D</au><au>Elhossiny, Ahmed M</au><au>Harold, Alexis C</au><au>Medina-Cabrera, Paola I</au><au>Kadiyala, Padma</au><au>Shi, Jiaqi</au><au>Frankel, Timothy L</au><au>Carpenter, Eileen S</au><au>Green, Michael D</au><au>Mitrea, Cristina</au><au>Lyssiotis, Costas A</au><au>Pasca di Magliano, Marina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolic landscape of the healthy pancreas and pancreatic tumor microenvironment</atitle><jtitle>JCI insight</jtitle><addtitle>JCI Insight</addtitle><date>2024-08-13</date><risdate>2024</risdate><volume>9</volume><issue>18</issue><issn>2379-3708</issn><eissn>2379-3708</eissn><abstract>Pancreatic cancer, one of the deadliest human malignancies, is characterized by a fibro-inflammatory tumor microenvironment and wide array of metabolic alterations. To comprehensively map metabolism in a cell type-specific manner, we harnessed a unique single-cell RNA-sequencing dataset of normal human pancreata. This was compared with human pancreatic cancer samples using a computational pipeline optimized for this study. In the cancer cells we observed enhanced biosynthetic programs. We identified downregulation of mitochondrial programs in several immune populations, relative to their normal counterparts in healthy pancreas. Although granulocytes, B cells, and CD8+ T cells all downregulated oxidative phosphorylation, the mechanisms by which this occurred were cell type specific. In fact, the expression pattern of the electron transport chain complexes was sufficient to identify immune cell types without the use of lineage markers. We also observed changes in tumor-associated macrophage (TAM) lipid metabolism, with increased expression of enzymes mediating unsaturated fatty acid synthesis and upregulation in cholesterol export. 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subjects | Cholesterol - metabolism Humans Lipid Metabolism Mitochondria - metabolism Oxidative Phosphorylation Pancreas - metabolism Pancreas - pathology Pancreatic Neoplasms - genetics Pancreatic Neoplasms - metabolism Pancreatic Neoplasms - pathology Single-Cell Analysis Tumor Microenvironment Tumor-Associated Macrophages - immunology Tumor-Associated Macrophages - metabolism |
title | Metabolic landscape of the healthy pancreas and pancreatic tumor microenvironment |
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