Protein-metabolite interactomics of carbohydrate metabolism reveal regulation of lactate dehydrogenase-Reference-Cited by-同舟云学术

Protein-metabolite interactomics of carbohydrate metabolism reveal regulation of lactate dehydrogenase

Published:2023-03-10 Issue:6636 Volume:379 Page:996-1003
ISSN:0036-8075
Container-title:Science
language:en
Short-container-title:Science

Author:

Hicks Kevin G.¹^ORCID,Cluntun Ahmad A.¹^ORCID,Schubert Heidi L.¹^ORCID,Hackett Sean R.²^ORCID,Berg Jordan A.¹^ORCID,Leonard Paul G.³⁴^ORCID,Ajalla Aleixo Mariana A.⁵^ORCID,Zhou Youjia⁶⁷^ORCID,Bott Alex J.¹^ORCID,Salvatore Sonia R.⁸^ORCID,Chang Fei⁸^ORCID,Blevins Aubrie¹^ORCID,Barta Paige¹^ORCID,Tilley Samantha¹^ORCID,Leifer Aaron¹^ORCID,Guzman Andrea¹,Arok Ajak¹,Fogarty Sarah¹⁹,Winter Jacob M.¹^ORCID,Ahn Hee-Chul¹⁰^ORCID,Allen Karen N.¹¹^ORCID,Block Samuel¹²,Cardoso Iara A.⁵^ORCID,Ding Jianping¹³^ORCID,Dreveny Ingrid¹⁴^ORCID,Gasper William C.¹⁵^ORCID,Ho Quinn¹⁵^ORCID,Matsuura Atsushi¹⁰,Palladino Michael J.¹⁶,Prajapati Sabin¹⁷¹⁸,Sun Pengkai¹³,Tittmann Kai¹⁷¹⁸^ORCID,Tolan Dean R.¹⁵^ORCID,Unterlass Judith¹⁹,VanDemark Andrew P.²⁰^ORCID,Vander Heiden Matthew G.¹²²¹^ORCID,Webb Bradley A.²²^ORCID,Yun Cai-Hong²³^ORCID,Zhao Pengkai²³^ORCID,Wang Bei⁶⁷^ORCID,Schopfer Francisco J.⁸²⁴²⁵²⁶^ORCID,Hill Christopher P.¹^ORCID,Nonato Maria Cristina⁵^ORCID,Muller Florian L.²⁷^ORCID,Cox James E.¹^ORCID,Rutter Jared¹⁹^ORCID

Affiliation:

1. Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA.

2. Calico Life Sciences LLC, South San Francisco, CA, USA.

3. Core for Biomolecular Structure and Function, University of Texas MD Anderson Cancer Center, Houston, TX, USA.

4. Institute for Applied Cancer Sciences, University of Texas MD Anderson Cancer Center, Houston, TX, USA.

5. Laboratório de Cristalografia de Proteinas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.

6. School of Computing, University of Utah, Salt Lake City, UT, USA.

7. Scientific Computing and Imaging Institute, University of Utah, Salt Lake City, UT, USA.

8. Department of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

9. Howard Hughes Medical Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.

10. Integrated Research Institute for Drug Development, College of Pharmacy, Dongguk University-Seoul, Goyang, The Republic of Korea.

11. Department of Chemistry, Boston University, Boston, MA, USA.

12. The Koch Institute for Integrative Cancer Research and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

13. 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.

14. Biodiscovery Institute, School of Pharmacy, University of Nottingham, Nottingham, UK.

15. Department of Biology, Boston University, Boston, MA, USA.

16. Department of Pharmacology and Chemical Biology, University of Pittsburgh, Pittsburgh, PA, USA.

17. Department of Molecular Enzymology, Göttingen Center of Molecular Biosciences, University of Göttingen, Göttingen, Germany.

18. Department of Structural Dynamics, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany.

19. Department of Oncology and Pathology, Karolinska Institute, Stockholm, Sweden.

20. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA.

21. Dana-Farber Cancer Institute, Boston, MA, USA.

22. Department of Biochemistry, West Virginia University, Morgantown, WV, USA.

23. Department of Biophysics, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China.

24. Pittsburgh Heart, Lung, and Blood Vascular Medicine Institute, Pittsburgh, PA, USA.

25. Pittsburgh Liver Research Center, Pittsburgh, PA, USA.

26. Center for Metabolism and Mitochondrial Medicine, Pittsburgh, PA, USA.

27. Department of Cancer Systems Imaging, University of Texas MD Anderson Cancer Center, Houston, TX, USA.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

Link

https://www.science.org/doi/pdf/10.1126/science.abm3452

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