ArticleScience (New York, N.Y.)2023
Protein-metabolite interactomics of carbohydrate metabolism reveal regulation of lactate dehydrogenase.
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Article in Science (New York, N.Y.), 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 87 papers.
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87citing papers in PubMed
25.7field-weighted citation impact, top 1% of its field
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87 citing papers in PubMed, 140 citations in OpenAlex.
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- Model-based inference of enzyme inhibitions from perturbation-induced metabolic dynamics.bioRxiv : the preprint server for biology · 2026Article
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- Advances and opportunities for computational interrogation of plant proteins.The Plant journal : for cell and molecular biology · 2026Review
- Association of serum lactate dehydrogenase levels with the severity of microvascular invasion in hepatocellular carcinoma: a retrospective cross-sectional study.Journal of gastrointestinal oncology · 2026Article
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- Often forgotten but essential: long-chain acyl-CoAs in metabolic control.Nature metabolism · 2026Article
- Inhibition of FicD-mediated AMPylation and deAMPylation by isoprenoid diphosphates.Proceedings of the National Academy of Sciences of the United States of America · 2026Article
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- Global loss of metabolic responsiveness and elevated enzyme in leptin deficient obese mice during starvation.NPJ systems biology and applications · 2026Article
27 more citing papers are in PubMed but not listed here.
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Authors and funding
46 authors at 15 institutions in 7 countries.
Kevin G HicksDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0001-5067-7608
Ahmad A CluntunDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0001-7612-8375
Heidi L SchubertDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0003-1762-8390
Sean R HackettCalico Life Sciences LLC, South San Francisco, CA, USA.ORCID 0000-0002-9553-4341
Jordan A BergDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-5096-0558
Paul G LeonardCore for Biomolecular Structure and Function, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0003-2661-5532
Mariana A Ajalla AleixoLaboratório de Cristalografia de Proteinas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.ORCID 0000-0002-3172-1156
Youjia ZhouSchool of Computing, University of Utah, Salt Lake City, UT, USA.ORCID 0000-0002-4501-8496
Alex J BottDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0003-2273-8922
Sonia R SalvatoreDepartment of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.ORCID 0000-0002-9942-3905
Fei ChangDepartment of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.ORCID 0000-0002-3724-2455
Aubrie BlevinsDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-4546-7267
Paige BartaDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0001-6848-0758
Samantha TilleyDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-7701-4430
Aaron LeiferDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-1005-7604
Andrea GuzmanDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.
Ajak ArokDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.
Sarah FogartyDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.
Jacob M WinterDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0001-7152-183X
Hee-Chul Ahn *Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University-Seoul, Goyang, The Republic of Korea.ORCID 0000-0001-6793-085X
Karen N Allen *Department of Chemistry, Boston University, Boston, MA, USA.ORCID 0000-0001-7296-0551
Samuel Block *The Koch Institute for Integrative Cancer Research and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
Iara A Cardoso *Laboratório de Cristalografia de Proteinas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.ORCID 0000-0002-0288-4706
Jianping Ding *State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, University of Chinese Academy of Sciences, Shanghai, China.ORCID 0000-0001-7029-7346
Ingrid Dreveny *Biodiscovery Institute, School of Pharmacy, University of Nottingham, Nottingham, UK.ORCID 0000-0003-2256-642X
William C Gasper *Department of Biology, Boston University, Boston, MA, USA.ORCID 0000-0003-4847-9957
Quinn Ho *Department of Biology, Boston University, Boston, MA, USA.ORCID 0000-0001-8847-5518
Atsushi Matsuura *Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University-Seoul, Goyang, The Republic of Korea.
Michael J Palladino *Department of Pharmacology and Chemical Biology, University of Pittsburgh, Pittsburgh, PA, USA.
Sabin Prajapati *Department of Molecular Enzymology, Göttingen Center of Molecular Biosciences, University of Göttingen, Göttingen, Germany.
Pengkai Sun *State Key Laboratory of Molecular Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, University of Chinese Academy of Sciences, Shanghai, China.
Kai Tittmann *Department of Molecular Enzymology, Göttingen Center of Molecular Biosciences, University of Göttingen, Göttingen, Germany.ORCID 0000-0001-7891-7108
Dean R Tolan *Department of Biology, Boston University, Boston, MA, USA.ORCID 0000-0002-0598-7241
Judith Unterlass *Department of Oncology and Pathology, Karolinska Institute, Stockholm, Sweden.
Andrew P VanDemark *Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA.ORCID 0000-0003-3424-4831
Matthew G Vander Heiden *The Koch Institute for Integrative Cancer Research and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.ORCID 0000-0002-6702-4192
Bradley A Webb *Department of Biochemistry, West Virginia University, Morgantown, WV, USA.ORCID 0000-0002-5299-2852
Cai-Hong Yun *Department of Biophysics, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China.ORCID 0000-0002-5880-8307
Pengkai Zhao *Department of Biophysics, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China.ORCID 0000-0002-6257-0573
Bei WangSchool of Computing, University of Utah, Salt Lake City, UT, USA.ORCID 0000-0002-9240-0700
Francisco J SchopferDepartment of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.ORCID 0000-0001-9526-695X
Christopher P HillDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0001-6796-7740
Maria Cristina NonatoLaboratório de Cristalografia de Proteinas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.ORCID 0000-0002-4916-1505
Florian L MullerDepartment of Cancer Systems Imaging, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0001-7568-2948
James E CoxDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-5977-2350
Jared RutterDepartment of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID 0000-0002-2710-9765
University of Utah · USUniversity of Pittsburgh · USBoston University · USUniversidade de Ribeirão Preto · BRCenter for Excellence in Molecular Cell Science · CNDongguk University · KRHoward Hughes Medical Institute · USMax Planck Institute for Biophysical Chemistry · DEPeking University · CNThe University of Texas MD Anderson Cancer Center · USDana-Farber Cancer Institute · USKarolinska Institutet · SEMassachusetts Institute of Technology · USUniversity of Nottingham · GBWest Virginia University · US
Funding
PRE-DOCTORAL TRAINING IN THE BIOLOGICAL SCIENCEST32GM007287 · NIGMS · MASSACHUSETTS INSTITUTE OF TECHNOLOGY · PI BELL, STEPHEN P., KEATING, AMY E · 1985 to 2019
$40.8MTRAINING IN CARDIOVASCULAR RESEARCHT32HL007576 · NHLBI · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI Stavros George Drakos, Robin M Shaw · 1985 to 2026
$10.6MProteomics CoreU54DK110858 · NIDDK · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI Anna E Beaudin, JAMES Eric COX · 2016 to 2026
$8.6MRESEARCH TRAINING IN HEMATOLOGYT32DK007115 · NIDDK · UNIVERSITY OF UTAH · PI LEIBOLD, ELIZABETH ANN, PRCHAL, JOSEF T · 1986 to 2020
$8.4MUnderstanding the role of metabolism in cancerR35CA242379 · NCI · MASSACHUSETTS INSTITUTE OF TECHNOLOGY · PI VANDER HEIDEN, MATTHEW G. · 2019 to 2025
$5.8MInterdisciplinary Training Program in MetabolismT32DK091317 · NIDDK · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI SCOTT A SUMMERS · 2011 to 2026
$4.8MFormation and metabolism of nitrated fatty acidsR01GM125944 · NIGMS · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI SCHOPFER, FRANCISCO JOSE · 2018 to 2025
$3.4MMitochondrial Biochemistry: From Mechanisms to DiseaseR35GM131854 · NIGMS · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI Jared P Rutter · 2019 to 2026
$3.3MAnalysis of cancer cell metabolism in diverse environmental conditionsR01CA201276 · NCI · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI VANDER HEIDEN, MATTHEW G., VITKUP, DENNIS · 2016 to 2020
$3.0MDeveloping the first TPI Df therapeuticsR01HD105311 · NICHD · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI PALLADINO, MICHAEL JOHN, VOGT, ANDREAS · 2021 to 2025
$2.7MTargeting fructokinase, endogenous fructose production and purine degradation for the prevention and treatment of hereditary fructose intoleranceR01DK108859 · NIDDK · UNIVERSITY OF COLORADO DENVER · PI Miguel Angel Lanaspa Garcia · 2016 to 2026
$2.4MPredominant protective role in hepatic steatosis and obesity by fish oil-derived furansR01DK112854 · NIDDK · UNIVERSITY OF PITTSBURGH AT PITTSBURGH · PI SCHOPFER, FRANCISCO JOSE · 2018 to 2021
$1.6MNCI NIH HHS F30 CA243440NCI NIH HHS F99 CA253744NCI NIH HHS K00 CA212445NCI NIH HHS R01 CA201276NCI NIH HHS R35 CA242379NHLBI NIH HHS T32 HL007576NICHD NIH HHS R01 HD105311NIDDK NIH HHS R01 DK108859NIDDK NIH HHS R01 DK112854NIDDK NIH HHS T32 DK007115NIDDK NIH HHS T32 DK091317NIDDK NIH HHS U54 DK110858NIGMS NIH HHS R01 GM103369NIGMS NIH HHS R01 GM125944NIGMS NIH HHS R35 GM131854NIGMS NIH HHS T32 GM007287NIH HHS S10 OD016232NIH HHS S10 OD018210NIH HHS S10 OD021505
Abstract
Metabolic networks are interconnected and influence diverse cellular processes. The protein-metabolite interactions that mediate these networks are frequently low affinity and challenging to systematically discover. We developed mass spectrometry integrated with equilibrium dialysis for the discovery of allostery systematically (MIDAS) to identify such interactions. Analysis of 33 enzymes from human carbohydrate metabolism identified 830 protein-metabolite interactions, including known regulators, substrates, and products as well as previously unreported interactions. We functionally validated a subset of interactions, including the isoform-specific inhibition of lactate dehydrogenase by long-chain acyl-coenzyme A. Cell treatment with fatty acids caused a loss of pyruvate-lactate interconversion dependent on lactate dehydrogenase isoform expression. These protein-metabolite interactions may contribute to the dynamic, tissue-specific metabolic flexibility that enables growth and survival in an ever-changing nutrient environment.
Indexed as
Carbohydrate MetabolismL-Lactate DehydrogenaseMetabolomeAllosteric RegulationFatty AcidsHumansMass SpectrometryOrgan SpecificityFatty AcidsL-Lactate Dehydrogenase
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