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Metabolite Exchange between Mammalian Organs Quantified in Pigs

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Jang, Cholsoon, Hui, Sheng, Zeng, Xianfeng, Cowan, Alexis J., Wang, Lin, Chen, Li, Morscher, Raphael J., Reyes, Jorge, Frezza, Christian, Hwang, Ho Young, Imai, Akito, Saito, Yoshiaki, Okamoto, Keitaro, Vaspoli, Christine, Kasprenski, Loewe, Zsido, Gerald A., Gorman, Joseph H., Gorman, Robert C., Rabinowitz, Joshua D.·2019·Cell Metabolism

DOI 10.1016/j.cmet.2019.06.002PMC PMC6726553

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Abstract

Mammalian organs continually exchange metabolites via circulation, but systems-level analysis of this shuttling process is lacking. Here, we compared, in fasted pigs, metabolite concentrations in arterial blood versus draining venous blood from 11 organs. Greater than 90% of metabolites showed arterial-venous differences across at least one organ. Surprisingly, the liver and kidneys released not only glucose but also amino acids, both of which were consumed primarily by the intestine and pancreas. The liver and kidneys exhibited additional unexpected activities: liver preferentially burned unsaturated over more atherogenic saturated fatty acids, whereas the kidneys were unique in burning circulating citrate and net oxidizing lactate to pyruvate, thereby contributing to circulating redox homeostasis. Furthermore, we observed more than 700 other cases of tissue-specific metabolite production or consumption, such as release of nucleotides by the spleen and TCA intermediates by pancreas. These data constitute a high-value resource, providing a quantitative atlas of inter-organ metabolite exchange.

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Authors: Jang, C., Hui, S., Zeng, X., Cowan, A. J., Wang, L., Chen, L., Morscher, R. J., Reyes, J., Frezza, C., Hwang, H. Y., Imai, A., Saito, Y., Okamoto, K., Vaspoli, C., Kasprenski, L., Zsido, G. A., Gorman, J. H., Gorman, R. C., & Rabinowitz, J. D.
Affiliations: Princeton University (US)
University of Cambridge (GB)
University of Pennsylvania (US)
Corresponding author: Rabinowitz, Joshua D.
ORCID: Jang, Cholsoon
Hui, Sheng
Zeng, Xianfeng
Cowan, Alexis J.
Wang, Lin
Chen, Li
Morscher, Raphael J.
Reyes, Jorge
Frezza, Christian
Hwang, Ho Young
Imai, Akito
Saito, Yoshiaki
Okamoto, Keitaro
Rabinowitz, Joshua D.
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2019-09
Volume: 30
Issue: 3
Pages: 594-606.e3
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2019.06.002
PMC: PMC6726553
OpenAlex: W2954321663
Cited by: 256
References: 54
Citations by year: 2026: 26 · 2025: 31 · 2024: 40 · 2023: 56 · 2022: 35 · 2021: 42 · 2020: 21 · 2019: 5
FWCI: 8.47
Type: journal article
Language: en
Update notices: erratum (2022-09-06)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 368 d)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
Funders: American Diabetes Association (1-17-PDF-076, 1DP1DK113643)
NIH (K99DK117066)
Diabetes Research Center (P30 DK019525)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
Keywords: arteriovenous differences, organ metabolism, liver, kidney, glucose metabolism, amino acid metabolism, fatty acid oxidation, citrate metabolism, lactate oxidation, redox homeostasis, nucleotide release, fasting state, porcine model
MeSH terms: Amino Acids, Animals, Arteries, Blood Glucose, Fasting, Fatty Acids, Intestinal Mucosa, Kidney, Liver, Male, Mice, Inbred C57BL, Pancreas, Spleen, Swine, Veins, Pyruvic Acid, Citric Acid, Lactic Acid, Mice

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Metabolite Exchange between Mammalian Organs Quantified in Pigs

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