Sirtuin 4 is a lipoamidase regulating pyruvate dehydrogenase complex activity

Cell

Volumn 159, Issue 7, 2014, Pages 1615-1625

  Mathias, Rommel A ^a,b   Greco, Todd M ^a   Oberstein, Adam ^a   Budayeva, Hanna G ^a   Chakrabarti, Rumela ^a   Rowland, Elizabeth A ^a   Kang, Yibin ^a   Shenk, Thomas ^a   Cristea, Ileana M ^a  

^a PRINCETON UNIVERSITY   (United States)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; CITRIC ACID; DIHYDROLIPOAMIDE ACETYLTRANSFERASE; GLUTAMINE; LYSINE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVIC ACID; SIRTUIN 4; AMIDASE; LIPOAMIDASE; LIPOAMIDE; MITOCHONDRIAL PROTEIN; SIRT4 PROTEIN, HUMAN; SIRT4 PROTEIN, MOUSE; SIRTUIN; THIOCTIC ACID;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CATALYSIS; CELL SPECIFICITY; CITRIC ACID CYCLE; CONTROLLED STUDY; DEACETYLATION; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEMALE; FIBROBLAST; GENE SWITCHING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; RAT; STABLE EXPRESSION; WESTERN BLOTTING; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; GENE SILENCING; GENETICS; LIVER; METABOLISM; MITOCHONDRION;

AMIDOHYDROLASES; ANIMALS; GENE KNOCKDOWN TECHNIQUES; GLUTAMINE; HUMANS; LIVER; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PYRUVATE DEHYDROGENASE COMPLEX; RATS; SIRTUINS; THIOCTIC ACID;

EID: 84919933749     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.11.046     Document Type: Article

References (51)

1. N. Ahuja, B. Schwer, S. Carobbio, D. Waltregny, B.J. North, V. Castronovo, P. Maechler, and E. Verdin Regulation of insulin secretion by SIRT4, a mitochondrial ADP-ribosyltransferase J. Biol. Chem. 282 2007 33583 33592
2. C.A. Brautigam, R.M. Wynn, J.L. Chuang, M. Machius, D.R. Tomchick, and D.T. Chuang Structural insight into interactions between dihydrolipoamide dehydrogenase (E3) and E3 binding protein of human pyruvate dehydrogenase complex Structure 14 2006 611 621
3. H. Choi, B. Larsen, Z.Y. Lin, A. Breitkreutz, D. Mellacheruvu, D. Fermin, Z.S. Qin, M. Tyers, A.C. Gingras, and A.I. Nesvizhskii SAINT: probabilistic scoring of affinity purification-mass spectrometry data Nat. Methods 8 2011 70 73
4. I.M. Cristea, R. Williams, B.T. Chait, and M.P. Rout Fluorescent proteins as proteomic probes Mol. Cell. Proteomics 4 2005 1933 1941
5. A. Csibi, S.M. Fendt, C. Li, G. Poulogiannis, A.Y. Choo, D.J. Chapski, S.M. Jeong, J.M. Dempsey, A. Parkhitko, and T. Morrison The mTORC1 pathway stimulates glutamine metabolism and cell proliferation by repressing SIRT4 Cell 153 2013 840 854
6. J. Du, Y. Zhou, X. Su, J.J. Yu, S. Khan, H. Jiang, J. Kim, J. Woo, J.H. Kim, and B.H. Choi Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase Science 334 2011 806 809
7. J. Fan, C. Shan, H.B. Kang, S. Elf, J. Xie, M. Tucker, T.L. Gu, M. Aguiar, S. Lonning, and H. Chen Tyr phosphorylation of PDP1 toggles recruitment between ACAT1 and SIRT3 to regulate the pyruvate dehydrogenase complex Mol. Cell 53 2014 534 548
8. J.L. Feldman, J. Baeza, and J.M. Denu Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins J. Biol. Chem. 288 2013 31350 31356
9. R.A. Frye Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity Biochem. Biophys. Res. Commun. 260 1999 273 279
10. L. Guarente Sir2 links chromatin silencing, metabolism, and aging Genes Dev. 14 2000 1021 1026
11. M.C. Haigis, R. Mostoslavsky, K.M. Haigis, K. Fahie, D.C. Christodoulou, A.J. Murphy, D.M. Valenzuela, G.D. Yancopoulos, M. Karow, and G. Blander SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells Cell 126 2006 941 954
12. R.A. Harris, M.M. Bowker-Kinley, P. Wu, J. Jeng, and K.M. Popov Dihydrolipoamide dehydrogenase-binding protein of the human pyruvate dehydrogenase complex. DNA-derived amino acid sequence, expression, and reconstitution of the pyruvate dehydrogenase complex J. Biol. Chem. 272 1997 19746 19751
13. D. Häussinger, W. Gerok, and H. Sies Inhibition of pyruvate dehydrogenase during the metabolism of glutamine and proline in hemoglobin-free perfused rat liver Eur. J. Biochem. 126 1982 69 76
14. S. Imai, C.M. Armstrong, M. Kaeberlein, and L. Guarente Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase Nature 403 2000 795 800
15. Y. Ishihama, J. Rappsilber, and M. Mann Modular stop and go extraction tips with stacked disks for parallel and multidimensional Peptide fractionation in proteomics J. Proteome Res. 5 2006 988 994
16. S.M. Jeong, C. Xiao, L.W. Finley, T. Lahusen, A.L. Souza, K. Pierce, Y.H. Li, X. Wang, G. Laurent, and N.J. German SIRT4 has tumor-suppressive activity and regulates the cellular metabolic response to DNA damage by inhibiting mitochondrial glutamine metabolism Cancer Cell 23 2013 450 463
17. H. Jiang, S. Khan, Y. Wang, G. Charron, B. He, C. Sebastian, J. Du, R. Kim, E. Ge, and R. Mostoslavsky SIRT6 regulates TNF-α secretion through hydrolysis of long-chain fatty acyl lysine Nature 496 2013 110 113
18. E. Jing, B.T. O'Neill, M.J. Rardin, A. Kleinridders, O.R. Ilkeyeva, S. Ussar, J.R. Bain, K.Y. Lee, E.M. Verdin, and C.B. Newgard Sirt3 regulates metabolic flexibility of skeletal muscle through reversible enzymatic deacetylation Diabetes 62 2013 3404 3417
19. P. Joshi, T.M. Greco, A.J. Guise, Y. Luo, F. Yu, A.I. Nesvizhskii, and I.M. Cristea The functional interactome landscape of the human histone deacetylase family Mol. Syst. Biol. 9 2013 672 10.1038/msb.2013.1026
20. G. Laurent, V.C. de Boer, L.W. Finley, M. Sweeney, H. Lu, T.T. Schug, Y. Cen, S.M. Jeong, X. Li, A.A. Sauve, and M.C. Haigis SIRT4 represses peroxisome proliferator-activated receptor α activity to suppress hepatic fat oxidation Mol. Cell. Biol. 33 2013 4552 4561
21. G. Laurent, N.J. German, A.K. Saha, V.C. de Boer, M. Davies, T.R. Koves, N. Dephoure, F. Fischer, G. Boanca, and B. Vaitheesvaran SIRT4 coordinates the balance between lipid synthesis and catabolism by repressing malonyl CoA decarboxylase Mol. Cell 50 2013 686 698
22. H. Lin, X. Su, and B. He Protein lysine acylation and cysteine succination by intermediates of energy metabolism ACS Chem. Biol. 7 2012 947 960
23. T.C. Linn, F.H. Pettit, and L.J. Reed Alpha-keto acid dehydrogenase complexes. X. Regulation of the activity of the pyruvate dehydrogenase complex from beef kidney mitochondria by phosphorylation and dephosphorylation Proc. Natl. Acad. Sci. USA 62 1969 234 241
24. D.B. Lombard, F.W. Alt, H.L. Cheng, J. Bunkenborg, R.S. Streeper, R. Mostoslavsky, J. Kim, G. Yancopoulos, D. Valenzuela, and A. Murphy Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation Mol. Cell. Biol. 27 2007 8807 8814
25. E. Michishita, J.Y. Park, J.M. Burneskis, J.C. Barrett, and I. Horikawa Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins Mol. Biol. Cell 16 2005 4623 4635
26. N. Nasrin, X. Wu, E. Fortier, Y. Feng, O.C. Bare', S. Chen, X. Ren, Z. Wu, R.S. Streeper, and L. Bordone SIRT4 regulates fatty acid oxidation and mitochondrial gene expression in liver and muscle cells J. Biol. Chem. 285 2010 31995 32002
27. C.B. Newgard, and J.D. McGarry Metabolic coupling factors in pancreatic beta-cell signal transduction Annu. Rev. Biochem. 64 1995 689 719
28. J.C. Newman, W. He, and E. Verdin Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease J. Biol. Chem. 287 2012 42436 42443
29. L. Nilsson, and B. Kågedal Co-purification of human serum lipoamidase and biotinidase: evidence that the two enzyme activities are due to the same enzyme protein Biochem. J. 291 1993 545 551
30. L. Nilsson, and E. Ronge Lipoamidase and biotinidase deficiency: evidence that lipoamidase and biotinidase are the same enzyme in human serum Eur. J. Clin. Chem. Clin. Biochem. 30 1992 119 126
31. J. Oizumi, and K. Hayakawa Liberation of lipoate by human serum lipoamidase from bovine heart pyruvate dehydrogenase Biochem. Biophys. Res. Commun. 162 1989 658 663
32. C. Peng, Z. Lu, Z. Xie, Z. Cheng, Y. Chen, M. Tan, H. Luo, Y. Zhang, W. He, and K. Yang The first identification of lysine malonylation substrates and its regulatory enzyme Mol. Cell. Proteomics 10 2011 012658 10.1074/mcp.M1111.012658
33. R.N. Perham Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein Biochemistry 30 1991 8501 8512
34. G.A. Radke, K. Ono, S. Ravindran, and T.E. Roche Critical role of a lipoyl cofactor of the dihydrolipoyl acetyltransferase in the binding and enhanced function of the pyruvate dehydrogenase kinase Biochem. Biophys. Res. Commun. 190 1993 982 991
35. M. Rahmatullah, G.A. Radke, P.C. Andrews, and T.E. Roche Changes in the core of the mammalian-pyruvate dehydrogenase complex upon selective removal of the lipoyl domain from the transacetylase component but not from the protein X component J. Biol. Chem. 265 1990 14512 14517
36. M.J. Rardin, S.E. Wiley, R.K. Naviaux, A.N. Murphy, and J.E. Dixon Monitoring phosphorylation of the pyruvate dehydrogenase complex Anal. Biochem. 389 2009 157 164
37. M.J. Rardin, W. He, Y. Nishida, J.C. Newman, C. Carrico, S.R. Danielson, A. Guo, P. Gut, A.K. Sahu, and B. Li SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks Cell Metab. 18 2013 920 933
38. D. Rauh, F. Fischer, M. Gertz, M. Lakshminarasimhan, T. Bergbrede, F. Aladini, C. Kambach, C.F. Becker, J. Zerweck, M. Schutkowski, and C. Steegborn An acetylome peptide microarray reveals specificities and deacetylation substrates for all human sirtuin isoforms Nat Commun 4 2013 2327 10.1038/ncomms3327
39. H.W. Rhee, P. Zou, N.D. Udeshi, J.D. Martell, V.K. Mootha, S.A. Carr, and A.Y. Ting Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging Science 339 2013 1328 1331
40. T.E. Roche, S.L. Powers-Greenwood, W.F. Shi, W.B. Zhang, S.Z. Ren, E.D. Roche, D.J. Cox, and C.M. Sorensen Sizing of bovine heart and kidney pyruvate dehydrogenase complex and dihydrolipoyl transacetylase core by quasielastic light scattering Biochemistry 32 1993 5629 5637
41. A. Schuetz, J.R. Min, T. Antoshenko, C.L. Wang, A. Allali-Hassani, A.P. Dong, P. Loppnau, M. Vedadi, A. Bochkarev, R. Sternglanz, and A.N. Plotnikov Structural basis of inhibition of the human NAD+-dependent deacetylase SIRT5 by suramin Structure 15 2007 377 389
42. S.D. Sherrod, M.V. Myers, M. Li, J.S. Myers, K.L. Carpenter, B. Maclean, M.J. Maccoss, D.C. Liebler, and A.J. Ham Label-free quantitation of protein modifications by pseudo selected reaction monitoring with internal reference peptides J. Proteome Res. 11 2012 3467 3479
43. B.C. Smith, and J.M. Denu Sir2 protein deacetylases: evidence for chemical intermediates and functions of a conserved histidine Biochemistry 45 2006 272 282
44. M. Tan, C. Peng, K.A. Anderson, P. Chhoy, Z. Xie, L. Dai, J. Park, Y. Chen, H. Huang, and Y. Zhang Lysine glutarylation is a protein posttranslational modification regulated by SIRT5 Cell Metab. 19 2014 605 617
45. Y.C. Tsai, T.M. Greco, A. Boonmee, Y. Miteva, and I.M. Cristea Functional proteomics establishes the interaction of SIRT7 with chromatin remodeling complexes and expands its role in regulation of RNA polymerase I transcription Mol. Cell. Proteomics 11 2012 60 76
46. E. Verdin, M.D. Hirschey, L.W. Finley, and M.C. Haigis Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling Trends Biochem. Sci. 35 2010 669 675
47. J.A. Vizcaíno, E.W. Deutsch, R. Wang, A. Csordas, F. Reisinger, D. Ríos, J.A. Dianes, Z. Sun, T. Farrah, and N. Bandeira ProteomeXchange provides globally coordinated proteomics data submission and dissemination Nat. Biotechnol. 32 2014 223 226
48. O. Wieland, and B. Jagow-Westermann ATP-dependent inactivation of heart muscle pyruvate dehydrogenase and reactivation by Mg(++) FEBS Lett. 3 1969 271 274
49. M. Wirth, S. Karaca, D. Wenzel, L. Ho, D. Tishkoff, D.B. Lombard, E. Verdin, H. Urlaub, M. Jedrusik-Bode, and W. Fischle Mitochondrial SIRT4-type proteins in Caenorhabditis elegans and mammals interact with pyruvate carboxylase and other acetylated biotin-dependent carboxylases Mitochondrion 13 2013 705 720
50. Z.H. Zhou, D.B. McCarthy, C.M. O'Connor, L.J. Reed, and J.K. Stoops The remarkable structural and functional organization of the eukaryotic pyruvate dehydrogenase complexes Proc. Natl. Acad. Sci. USA 98 2001 14802 14807
51. Y. Zhu, Y. Yan, D.R. Principe, X. Zou, A. Vassilopoulos, and D. Gius SIRT3 and SIRT4 are mitochondrial tumor suppressor proteins that connect mitochondrial metabolism and carcinogenesis Cancer Metab 2 2014 15