A Class of Reactive Acyl-CoA Species Reveals the Non-enzymatic Origins of Protein Acylation

Cell Metabolism

Volumn 25, Issue 4, 2017, Pages 823-837.e8

  Wagner, Gregory R ^a,b   Bhatt, Dhaval P ^a   O'Connell, Thomas M ^a   Thompson, J Will ^b   Dubois, Laura G ^b   Backos, Donald S ^c   Yang, Hao ^d,e   Mitchell, Grant A ^d   Ilkayeva, Olga R ^a   Stevens, Robert D ^a   Grimsrud, Paul A ^a   Hirschey, Matthew D ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e NORTHWEST A F UNIVERSITY   (China)

Author keywords

acyl CoA; chemical biology; non enzymatic; post translational modifications; protein acylation; sirtuins

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COENZYME A; ACYL COENZYME A; COENZYME A; HYDROXYMETHYLGLUTARYL COENZYME A LYASE; LYSINE; MALATE DEHYDROGENASE; PROTEOME; SUCCINYL COENZYME A; 3-HYDROXY-3-METHYLGLUTARYL-COENZYME A; ACID ANHYDRIDE; GLUTARYL-COENZYME A; PROTEIN; SUCCINYL-COENZYME A;

ACYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL METABOLISM; CITRIC ACID CYCLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME METABOLISM; HUMAN; IN VIVO STUDY; LIVER TISSUE; METABOLIC REGULATION; METABOLITE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; BIOCATALYSIS; METABOLISM; METABOLOME; MITOCHONDRION; PROTEIN PROCESSING;

ACYL COENZYME A; ACYLATION; ANHYDRIDES; BIOCATALYSIS; CITRIC ACID CYCLE; LYSINE; METABOLOME; MITOCHONDRIA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; PROTEOMICS;

EID: 85017028168     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2017.03.006     Document Type: Article

References (48)

1. Anderson, K.A., Green, M.F., Huynh, F.K., Wagner, G.R., Hirschey, M.D., SnapShot: mammalian sirtuins. Cell, 159, 2014 956–956.
2. Anderson, K.A., Huynh, F.K., Fisher-Wellman, K., Stuart, J.D., Peterson, B.S., Douros, J.D., Wagner, G.R., Thompson, J.W., Madsen, A.S., Green, M.F., et al. SIRT4 is a lysine deacylase that controls leucine metabolism and insulin secretion. Cell Metab 25 (2017), 838–855 this issue.
3. Bender, M.L., Mechanisms of catalysis of nucleophilic reactions of carboxylic acid derivatives. Chem. Rev. 60 (1960), 53–113.
4. Brooks, B.R., Brooks, C.L. 3rd, Mackerell, A.D. Jr., Nilsson, L., Petrella, R.J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., et al. CHARMM: the biomolecular simulation program. J. Comput. Chem. 30 (2009), 1545–1614.
5. Buckel, W., Acetic anhydride: an intermediate analogue in the acyl-exchange reaction of citramalate lyase. Eur. J. Biochem. 64 (1976), 263–267.
6. Calvo, S.E., Clauser, K.R., Mootha, V.K., MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins. Nucleic Acids Res. 44:D1 (2016), D1251–D1257.
7. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M.L., Rehman, M., Walther, T.C., Olsen, J.V., Mann, M., Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325 (2009), 834–840.
8. Du, J., Zhou, Y., Su, X., Yu, J.J., Khan, S., Jiang, H., Kim, J., Woo, J., Kim, J.H., Choi, B.H., et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 334 (2011), 806–809.
9. Feig, M., Onufriev, A., Lee, M.S., Im, W., Case, D.A., Brooks, C.L. 3rd, Performance comparison of generalized born and Poisson methods in the calculation of electrostatic solvation energies for protein structures. J. Comput. Chem. 25 (2004), 265–284.
10. Feldman, J.L., Baeza, J., Denu, J.M., Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins. J. Biol. Chem. 288 (2013), 31350–31356.
11. Gauthier, N., Wu, J.W., Wang, S.P., Allard, P., Mamer, O.A., Sweetman, L., Moser, A.B., Kratz, L., Alvarez, F., Robitaille, Y., et al. A liver-specific defect of Acyl-CoA degradation produces hyperammonemia, hypoglycemia and a distinct hepatic Acyl-CoA pattern. PLoS ONE, 8, 2013, e60581.
12. Gibson, G.E., Blass, J.P., Beal, M.F., Bunik, V., The alpha-ketoglutarate-dehydrogenase complex: a mediator between mitochondria and oxidative stress in neurodegeneration. Mol. Neurobiol. 31 (2005), 43–63.
13. Grimsrud, P.A., Carson, J.J., Hebert, A.S., Hubler, S.L., Niemi, N.M., Bailey, D.J., Jochem, A., Stapleton, D.S., Keller, M.P., Westphall, M.S., et al. A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis. Cell Metab. 16 (2012), 672–683.
14. Hebert, A.S., Dittenhafer-Reed, K.E., Yu, W., Bailey, D.J., Selen, E.S., Boersma, M.D., Carson, J.J., Tonelli, M., Balloon, A.J., Higbee, A.J., et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol. Cell 49 (2013), 186–199.
15. Hirschey, M.D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D.B., Grueter, C.A., Harris, C., Biddinger, S., Ilkayeva, O.R., et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464 (2010), 121–125.
16. Hornbeck, P.V., Zhang, B., Murray, B., Kornhauser, J.M., Latham, V., Skrzypek, E., PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 43 (2015), D512–D520.
17. Jiang, H., Khan, S., Wang, Y., Charron, G., He, B., Sebastian, C., Du, J., Kim, R., Ge, E., Mostoslavsky, R., et al. SIRT6 regulates TNF-α secretion through hydrolysis of long-chain fatty acyl lysine. Nature 496 (2013), 110–113.
18. Karamanlidis, G., Lee, C.F., Garcia-Menendez, L., Kolwicz, S.C. Jr., Suthammarak, W., Gong, G., Sedensky, M.M., Morgan, P.G., Wang, W., Tian, R., Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 18 (2013), 239–250.
19. Koves, T.R., Li, P., An, J., Akimoto, T., Slentz, D., Ilkayeva, O., Dohm, G.L., Yan, Z., Newgard, C.B., Muoio, D.M., Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J. Biol. Chem. 280 (2005), 33588–33598.
20. Kraus, W.E., Muoio, D.M., Stevens, R., Craig, D., Bain, J.R., Grass, E., Haynes, C., Kwee, L., Qin, X., Slentz, D.H., et al. Metabolomic quantitative trait loci (mQTL) mapping implicates the ubiquitin proteasome system in cardiovascular disease pathogenesis. PLoS Genet., 11, 2015, e1005553.
21. Laurieri, N., Dairou, J., Egleton, J.E., Stanley, L.A., Russell, A.J., Dupret, J.M., Sim, E., Rodrigues-Lima, F., From arylamine N-acetyltransferase to folate-dependent acetyl CoA hydrolase: impact of folic acid on the activity of (HUMAN)NAT1 and its homologue (MOUSE)NAT2. PLoS ONE, 9, 2014, e96370.
22. López-Otín, C., Blasco, M.A., Partridge, L., Serrano, M., Kroemer, G., The hallmarks of aging. Cell 153 (2013), 1194–1217.
23. Madsen, A.S., Andersen, C., Daoud, M., Anderson, K.A., Laursen, J.S., Chakladar, S., Huynh, F.K., Colaço, A.R., Backos, D.S., Fristrup, P., et al. Investigating the sensitivity of NAD+-dependent sirtuin deacylation activities to NADH. J. Biol. Chem. 291 (2016), 7128–7141.
24. McDonnell, E., Peterson, B.S., Bomze, H.M., Hirschey, M.D., SIRT3 regulates progression and development of diseases of aging. Trends Endocrinol. Metab. 26 (2015), 486–492.
25. Mitchell, G.A., Wang, S.P., Ashmarina, L., Robert, M.F., Bouchard, G., Laurin, N., Kassovska-Bratinova, S., Boukaftane, Y., Inborn errors of ketogenesis. Biochem. Soc. Trans. 26 (1998), 136–140.
26. Moellering, R.E., Cravatt, B.F., Functional lysine modification by an intrinsically reactive primary glycolytic metabolite. Science 341 (2013), 549–553.
27. Nakagawa, T., Lomb, D.J., Haigis, M.C., Guarente, L., SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 137 (2009), 560–570.
28. Paik, W.K., Pearson, D., Lee, H.W., Kim, S., Nonenzymatic acetylation of histones with acetyl-CoA. Biochim. Biophys. Acta 213 (1970), 513–522.
29. Park, J., Chen, Y., Tishkoff, D.X., Peng, C., Tan, M., Dai, L., Xie, Z., Zhang, Y., Zwaans, B.M., Skinner, M.E., et al. SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol. Cell 50 (2013), 919–930.
30. Peng, C., Lu, Z., Xie, Z., Cheng, Z., Chen, Y., Tan, M., Luo, H., Zhang, Y., He, W., Yang, K., et al. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell. Proteomics, 10, 2011, 10.1074/mcp.M111.012658.
31. Rardin, M.J., He, W., Nishida, Y., Newman, J.C., Carrico, C., Danielson, S.R., Guo, A., Gut, P., Sahu, A.K., Li, B., et al. SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. Cell Metab. 18 (2013), 920–933.
32. Roe, C.R., Millington, D.S., Maltby, D.A., Identification of 3-methylglutarylcarnitine. A new diagnostic metabolite of 3-hydroxy-3-methylglutaryl-coenzyme A lyase deficiency. J. Clin. Invest. 77 (1986), 1391–1394.
33. Sena, L.A., Chandel, N.S., Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48 (2012), 158–167.
34. Simic, Z., Weiwad, M., Schierhorn, A., Steegborn, C., Schutkowski, M., The ɛ-amino group of protein lysine residues is highly susceptible to nonenzymatic acylation by several physiological acyl-CoA thioesters. ChemBioChem 16 (2015), 2337–2347.
35. Simon, E.J., Shemin, D., The preparation of s-succinyl coenzyme-a. J. Am. Chem. Soc., 75, 1953, 2520.
36. Tan, M., Peng, C., Anderson, K.A., Chhoy, P., Xie, Z., Dai, L., Park, J., Chen, Y., Huang, H., Zhang, Y., et al. Lysine glutarylation is a protein posttranslational modification regulated by SIRT5. Cell Metab. 19 (2014), 605–617.
37. Tanner, K.G., Trievel, R.C., Kuo, M.H., Howard, R.M., Berger, S.L., Allis, C.D., Marmorstein, R., Denu, J.M., Catalytic mechanism and function of invariant glutamic acid 173 from the histone acetyltransferase GCN5 transcriptional coactivator. J. Biol. Chem. 274 (1999), 18157–18160.
38. Wagner, G.R., Hirschey, M.D., Nonenzymatic protein acylation as a carbon stress regulated by sirtuin deacylases. Mol. Cell 54 (2014), 5–16.
39. Wagner, G.R., Payne, R.M., Widespread and enzyme-independent Nε-acetylation and Nε-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J. Biol. Chem. 288 (2013), 29036–29045.
40. Wagner, G.R., Pride, P.M., Babbey, C.M., Payne, R.M., Friedreich's ataxia reveals a mechanism for coordinate regulation of oxidative metabolism via feedback inhibition of the SIRT3 deacetylase. Hum. Mol. Genet. 21 (2012), 2688–2697.
41. Weinert, B.T., Iesmantavicius, V., Wagner, S.A., Schölz, C., Gummesson, B., Beli, P., Nyström, T., Choudhary, C., Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol. Cell 51 (2013), 265–272.
42. Weinert, B.T., Iesmantavicius, V., Moustafa, T., Schölz, C., Wagner, S.A., Magnes, C., Zechner, R., Choudhary, C., Acetylation dynamics and stoichiometry in Saccharomyces cerevisiae. Mol. Syst. Biol., 10, 2014, 716.
43. Weinert, B.T., Moustafa, T., Iesmantavicius, V., Zechner, R., Choudhary, C., Analysis of acetylation stoichiometry suggests that SIRT3 repairs nonenzymatic acetylation lesions. EMBO J. 34 (2015), 2620–2632.
44. Willems, P.H., Rossignol, R., Dieteren, C.E., Murphy, M.P., Koopman, W.J., Redox homeostasis and mitochondrial dynamics. Cell Metab. 22 (2015), 207–218.
45. Xie, Z., Dai, J., Dai, L., Tan, M., Cheng, Z., Wu, Y., Boeke, J.D., Zhao, Y., Lysine succinylation and lysine malonylation in histones. Mol. Cell. Proteomics 11 (2012), 100–107.
46. Yu, W., Dittenhafer-Reed, K.E., Denu, J.M., SIRT3 protein deacetylates isocitrate dehydrogenase 2 (IDH2) and regulates mitochondrial redox status. J. Biol. Chem. 287 (2012), 14078–14086.
47. Zhang, Z., Tan, M., Xie, Z., Dai, L., Chen, Y., Zhao, Y., Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 7 (2011), 58–63.
48. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 327 (2010), 1000–1004.