The succinated proteome

Mass Spectrometry Reviews

Volumn 33, Issue 2, 2014, Pages 98-109

  Merkley, Eric D ^a   Metz, Thomas O ^a   Smith, Richard D ^a   Baynes, John W ^b   Frizzell, Norma ^b  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

chemical modification of proteins; cysteine; diabetes; fumarate; succination

Indexed keywords

CHEMICAL MODIFICATION OF PROTEINS; CYSTEINE; FUMARATES; INNER MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; POST-TRANSLATIONAL MODIFICATIONS; SUCCINATION;

AMINO ACIDS; CELL DEATH; CELL MEMBRANES; CHEMICAL MODIFICATION; DISEASES; ENZYME ACTIVITY; MAMMALS; MEDICAL PROBLEMS; MITOCHONDRIA; MOLECULAR BIOLOGY; NUTRITION;

PROTEINS;

CYSTEINE; DRUG DERIVATIVE; FUMARIC ACID; FUMARIC ACID DERIVATIVE; PROTEOME;

ANIMAL; CHEMICAL MODIFICATION OF PROTEINS; CHEMISTRY; CITRIC ACID CYCLE; DIABETES MELLITUS; HUMAN; METABOLISM; MITOCHONDRION; NEOPLASM; OXIDATIVE STRESS; REVIEW; SUCCINATION;

CHEMICAL MODIFICATION OF PROTEINS; CYSTEINE; DIABETES; FUMARATE; SUCCINATION;

ANIMALS; CITRIC ACID CYCLE; CYSTEINE; DIABETES MELLITUS; FUMARATES; HUMANS; MITOCHONDRIA; NEOPLASMS; OXIDATIVE STRESS; PROTEOME;

EID: 84893766747     PISSN: 02777037     EISSN: 10982787     Source Type: Journal    
DOI: 10.1002/mas.21382     Document Type: Review

References (67)

1. Adam J, Hatipoglu E, O'Flaherty L, Ternette N, Sahgal N, Lockstone H, Baban D, Nye E, Stamp GW, Wolhuter K, Stevens M, Fischer R, Carmeliet P, Maxwell PH, Pugh CW, Frizzell N, Soga T, Kessler BM, El-Bahrawy M, Ratcliffe PJ, Pollard PJ,. 2011. Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: Roles for fumarate in Keap1 succination and Nrf2 signaling. Cancer Cell 20: 524-537.
2. Alderson NL, Wang YP, Blatnik M, Frizzell N, Walla MD, Lyons TJ, Alt N, Carson JA, Nagai R, Thorpe SR, Baynes JW,. 2006. S-(2-succinyl)cysteine: A novel chemical modification of tissue proteins by a krebs cycle intermediate. Arch Biochem Biophys 450: 1-8. (Pubitemid 43782733)
3. Alt N, Carson JA, Alderson NL, Wang YP, Nagai R, Henle T, Thorpe SR, Baynes JW,. 2004. Chemical modification of muscle protein in diabetes. Arch Biochem Biophys 425: 200-206. (Pubitemid 38542812)
4. Ashrafian H, Czibik G, Bellahcene M, Aksentijevic D, Smith AC, Mitchell SJ, Dodd MS, Kirwan J, Byrne JJ, Ludwig C, Isackson H, Yavari A, Stottrup NB, Contractor H, Cahill TJ, Sahgal N, Ball DR, Birkler RID, Hargreaves L, Tennant DA, Land J, Lygate CA, Johannsen M, Kharbanda RK, Neubauer S, Redwood C, de Cabo R, Ahmet I, Talan M, Gunther UL, Robinson AJ, Viant MR, Pollard PJ, Tyler DJ, Watkins H,. 2012. Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway. Cell Metab 15: 361-371.
5. Bardella C, El-Bahrawy M, Frizzell N, Adam J, Ternette N, Hatipoglu E, Howarth K, O'Flaherty L, Roberts I, Turner G, Taylor J, Giaslakiotis K, Macaulay VM, Harris AL, Chandra A, Lehtonen HJ, Launonen V, Aaltonen LA, Pugh CW, Mihai R, Trudgian D, Kessler B, Baynes JW, Ratcliffe PJ, Tomlinson IP, Pollard PJ,. 2011. Aberrant succination of proteins in fumarate hydratase-deficient mice and hlrcc patients is a robust biomarker of mutation status. J Pathol 225: 4-11.
6. Bedhomme M, Adamo M, Marchand CH, Couturier J, Rouhier N, Lemaire SD, Zaffagnini M, Trost P,. 2012. Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J 445: 337-347.
7. Beltran L, Cutillas P,. 2012. Advances in phosphopeptide enrichment techniques for phosphoproteomics. Amino Acids 43: 1009-1024.
8. Blatnik M, Frizzell N, Thorpe SR, Baynes JW,. 2008. Inactivation of glyceraldehyde-3-phosphate dehydrogenase by fumarate in diabetes-Formation of S-(2-succinyl)cysteine, a novel chemical modification of protein and possible biomarker of mitochondrial stress. Diabetes 57: 41-49.
9. Blatnik M, Thorpe SR, Baynes JW,. 2008. Succination of proteins by fumarate. Ann N Y Acad Sci 1126: 272-275.
10. Brock JWC, Hinton DJS, Cotham WE, Metz TO, Thorpe SR, Baynes JW, Ames JM,. 2003. Proteomic analysis of the site specificity of glycation and carboxymethylation of ribonuclease. J Proteome Res 2: 506-513. (Pubitemid 37376845)
11. Brownlee M,. 2005. The pathobiology of diabetic complications-A unifying mechanism. Diabetes 54: 1615-1625. (Pubitemid 40770750)
12. Chang LC, Huang KC, Wu YW, Kao HL, Chen CL, Lai LP, Hwang JJ, Yang WS,. 2009. The clinical implications of blood adiponectin in cardiometabolic disorders. J Formos Med Assoc 108: 353-366.
13. Cross JV, Templeton DJ,. 2006. Regulation of signal transduction through protein cysteine oxidation. Antioxid Redox Signal 8: 1819-1827. (Pubitemid 44726354)
14. de Ferranti S, Mozaffarian D,. 2008. The perfect storm: Obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 54: 945-955. (Pubitemid 351793400)
15. Eng JK, McCormack AL, Yates JR,. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5: 976-989.
16. Frayn KN, Humphreys SM, Coppack SW,. 1995. Fuel selection in white adipose-tissue. Proc Nutr Soc 54: 177-189.
17. Frizzell N, Rajesh M, Jepson MJ, Nagai R, Carson JA, Thorpe SR, Baynes JW,. 2009. Succination of thiol groups in adipose tissue proteins in diabetes succination inhibits polymerization and secretion of adiponectin. J Biol Chem 284: 25772-25781.
18. Frizzell N, Lima M, Baynes JW,. 2011. Succination of proteins in diabetes. Free Radic Res 45: 101-109.
19. Frizzell N, Thomas SA, Carson JA, Baynes JW,. 2012. Mitochondrial stress causes increased succination of proteins in adipocytes in response to glucotoxicity. Biochem J J445: 247-254.
20. Ghoreschi K, Bruck J, Kellerer C, Deng CS, Peng HY, Rothfuss O, Hussain RZ, Gocke AR, Respa A, Glocova I, Valtcheva N, Alexander E, Feil S, Feil R, Schulze-Osthoff K, Rupec RA, Lovett-Racke AE, Dringen R, Racke MK, Rocken M,. 2011. Fumarates improve psoriasis and multiple sclerosis by inducing type II dendritic cells. J Exp Med 208: 2291-2303.
21. Giannessi D, Maltinti M, Del Ry S,. 2007. Adiponectin circulating levels: A new emerging biomarker of cardiovascular risk. Pharmacol Res 56: 459-467. (Pubitemid 350137773)
22. Goh SY, Cooper ME,. 2008. The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 93: 1143-1152. (Pubitemid 351519698)
23. Gundlach HG, Stein WH, Moore S,. 1959. The nature of the amino acid residues involved in the inactivation of ribonuclease by iodoacetate. J Biol Chem 234: 1754-1760.
24. Haynes WM, editor. 2012. CRC Handbook of Chemistry and Physics, 93rd edition. Cleveland, Ohio, USA: Chemical Rubber Company (online at: http://www.hbcpnetbase.com/).
25. Hu WT, Tedesco S, Faedda R, Petrone G, Cacciola SO, O'Keefe A, Sheehan D,. 2010. Covalent selection of the thiol proteome on activated thiol sepharose: A robust tool for redox proteomics. Talanta 80: 1569-1575.
26. Ishii T, Tatsuda E, Kumazawa S, Nakayama T, Uchida K,. 2003. Molecular basis of enzyme inactivation by an endogenous electrophile 4-hydroxy-2-nonenal: Identification of modification sites in glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 42: 3474-3480. (Pubitemid 36368641)
27. Kallen CH, Greevenbroek MJ, Stehouwer CA, Schalkwijk C,. 2009. Endoplasmic reticulum stress-induced apoptosis in the development of diabetes: Is there a role for adipose tissue and liver ? Apoptosis 14: 1424-1434.
28. Kanapin A, Batalov S, Davis MJ, Gough J, Grimmond S, Kawaji H, Magrane M, Matsuda H, Schonbach C, Teasdale RD, Yuan Z, Grp RG, Memebers GSL,. 2003. Mouse proteome analysis. Genome Res 13: 1335-1344. (Pubitemid 36827229)
29. Kettenhofen NJ, Wood MJ,. 2010. Formation, reactivity, and detection of protein sulfenic acids. Chem Res Toxicol 23: 1633-1646.
30. Kim S, Pevzner P,. 2012. MS-GF+: Universal and sensitive database search engine for mass spectrometry. 60th American Society for Mass Spectrometry Conference. Vancouver, Canada.
31. Kim S, Gupta N, Pevzner PA,. 2008. Spectral probabilities and generating functions of tandem mass spectra: A strike against decoy databases. J Proteome Res 7: 3354-3363.
32. Kim S, Mischerikow N, Bandeira N, Navarro JD, Wich L, Mohammed S, Heck AJR, Pevzner PA,. 2010. The generating function of CID, ETD, and CID/ETD pairs of tandem mass spectra: Applications to database search. Mol Cell Proteomics 9: 2840-2852.
33. Lai RK, Goldman P,. 1992. Organic-acid profiling in adipocyte differentiation of 3T3-F442A cells-Increased production of krebs cycle acid metabolites. Metab Clin Exp 41: 545-547.
34. Lin Y, Berg AH, Iyengar P, Lam TKT, Giacca A, Combs TP, Rajala MW, Du XL, Rollman B, Li WJ, Hawkins M, Barzilai N, Rhodes CJ, Fantus IG, Brownlee M, Scherer PE,. 2005. The hyperglycemia-induced inflammatory response in adipocytes-The role of reactive oxygen species. J Biol Chem 280: 4617-4626. (Pubitemid 40288630)
35. Linker RA, Lee D-H, Ryan S, van Dam AM, Conrad R, Bista P, Zeng W, Hronowsky X, Buko A, Chollate S, Ellrichmann G, Brück W, Dawson K, Goelz S, Wiese S, Scannevin RH, Lukashev M, Gold R,. 2011. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 134: 678-692.
36. Liu ML, Liu F,. 2010. Transcriptional and post-translational regulation of adiponectin. Biochem J 425: 41-52.
37. Liu M, Zhou LJ, Xu AM, Lam KSL, Wetzel MD, Xiang RH, Zhang JJ, Xin XB, Dong LQ, Liu F,. 2008. A disulfide-bond a oxidoreductase-like protein (DSBA-l) regulates adiponectin multimerization. Proc Natl Acad Sci USA 105: 18302-18307.
38. Livesay EA, Tang K, Taylor BK, Buschbach MA, Hopkins DF, LaMarche BL, Zhao R, Shen Y, Orton DJ, Moore RJ, Kelly RT, Udseth HR, Smith, RD,. 2007. Fully automated four-column capillary LC-MS system for maximizing throughput in proteomic analyses. Anal Chem 80 (1): 294-302. (Pubitemid 351448434)
39. Maller C, Schröder E, Eaton P,. 2011. Glyceraldehyde 3-phosphate dehydrogenase is unlikely to mediate hydrogen peroxide signaling: Studies with a novel anti-dimedone sulfenic acid antibody. Antixoxid Redox Signal 14: 49-60.
40. Mayampurath AM, Jaitly N, Purvine SO, Monroe ME, Auberry KJ, Adkins JN, Smith RD,. 2008. Deconmsn: A software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra. Bioinformatics 24: 1021-1023. (Pubitemid 351448041)
41. Merkley ED, Anderson BJ, Park J, Belchik SM, Shi L, Monroe ME, Smith RD, Lipton MS,. 2012. Detection and identification of heme c-modified peptides by histidine affinity chromatography, high-performance liquid chromatography-mass spectrometry, and database searching. J Proteome Res 11: 6147-6158.
42. Mitsuishi Y, Motohashi H, Yamamoto M,. 2012. The Keap1-Nrf2 system in cancers: Stress response and anabolic metabolism. Front Oncol 2: 200.
43. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, Yamamoto M, Motohashi H,. 2012. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22: 66-79.
44. Mohammed S, Heck AJR,. 2011. Strong cation exchange (SCX) based analytical methods for the targeted analysis of protein post-translational modifications. Curr Opin Biotechnol 22: 9-16.
45. Mostafa A, Randell E, Vasdev S, Gill V, Han Y, Gadag V, Raouf A, El Said H,. 2007. Plasma protein advanced glycation end products, carboxymethyl cysteine, and carboxyethyl cysteine, are elevated and related to nephropathy in patients with diabetes. Mol Cell Biochem 302: 35-42. (Pubitemid 47202318)
46. Mrowietz U, Altmeyer P, Bieber T, Röcken M, Schopf RE, Sterry W,. 2007. Treatment of psoriasis with fumaric acid esters (Fumaderm®). J Dtsch Dermatol Ges 5: 716-717. (Pubitemid 47099800)
47. Nagai R, Brock JW, Blatnik M, Baatz JE, Bethard J, Walla MD, Thorpe SR, Baynes JW, Frizzell N,. 2007. Succination of protein thiols during adipocyte maturation-A biomarker of mitochondrial stress. J Biol Chem 282: 34219-34228. (Pubitemid 350159439)
48. Nguyen T, Nioi P, Pickett CB,. 2009. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284: 13291-13295.
49. Ooi A, Wong JC, Petillo D, Roossien D, Perrier-Trudova V, Whitten D, Min BWH, Tan MH, Zhang ZF, Yang XMJ, Zhou M, Gardie B, Molinie V, Richard S, Tan PH, Teh BT, Furge KA,. 2011. An antioxidant response phenotype shared between hereditary and sporadic type 2 papillary renal cell carcinoma. Cancer Cell 20: 511-523.
50. Papadopoulou A, D'Souza M, Kappos L, Yaldizli O,. 2010. Dimethyl fumarate for multiple sclerosis. Expert Opin Invest Drugs 19: 1603-1612.
51. Pollard PJ, Brière JJ, Alam NA, Barwell J, Barclay E, Wortham NC, Hunt T, Mitchell M, Olpin S, Moat SJ, Hargreaves IP, Heales SJ, Chung YL, Griffiths JR, Dalgleish A, McGrath JA, Gleeson MJ, Hodgson SV, Poulsom R, Rustin P, Tomlinson IPM,. 2005. Accumulation of krebs cycle intermediates and over-expression of HIF1α in tumours which result from germline FH and SDH mutations. Hum Mol Genet 14: 2231-2239. (Pubitemid 41418022)
52. Pollard PJ, Spencer-Dene B, Shukla D, Howarth K, Nye E, El-Bahrawy M, Deheragoda M, Joannou M, McDonald S, Martin A, Igarashi P, Varsani-Brown S, Rosewell I, Poulsom R, Maxwell P, Stamp GW, Tomlinson IPM,. 2007. Targeted inactivation of FH1 causes proliferative renal cyst development and activation of the hypoxia pathway. Cancer Cell 11: 311-319. (Pubitemid 46518311)
53. Schmidt MM, Dringen R,. 2010. Fumaric acid diesters deprive cultured primary astrocytes rapidly of glutathione. Neurochem Int 57: 460-467.
54. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR,. 2000. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774. (Pubitemid 30212405)
55. Shah A, Mehta N, Reilly MP,. 2008. Adipose inflammation, insulin resistance, and cardiovascular disease. J Parenter Enteral Nutr 32: 638-644.
56. Ternette N, Yang M, Laroyia M, O'Flaherty L, Wolhuter K, Kato K, Fischer R, Kessler BM, Lappin T, Frizzell N, Soga T, Adam J, Pollard PJ,. 2013. Inhibition of mitochondrial aconitase by succination in fumarate hydratase deficiency. Cell Rep 28: 689-700.
57. Thomas SA, Storey KB, Baynes JW, Frizzell N,. 2012. Tissue distribution of S-(2-succino)cysteine (2SC), a biomarker of mitochondrial stress in obesity and diabetes. Obesity 20: 263-269.
58. Townsend DM,. 2007. S-glutathionylation: Indicator of cell stress and regulator of the unfolded protein response. Mol Interv 7: 313-324.
59. Van Gaal LF, Mertens IL, De Block CE,. 2006. Mechanisms linking obesity with cardiovascular disease. Nature 444: 875-880. (Pubitemid 46028447)
60. Washburn MP, Wolters D, Yates JR,. 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247. (Pubitemid 32220565)
61. Webster KA, Prentice H, Bishopric NH,. 2001. Oxidation of zinc finger transcription factors: Physiological consequences. Antioxid Redox Signal 3: 535-548. (Pubitemid 32785979)
62. Wood IS, de Heredia FP, Wang BH, Trayhurn P,. 2009. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc 68: 370-377.
63. Yang F, Shen YF, Camp DG, Smith RD,. 2012a. High-pH reversed-phase chromatography with fraction concatenation for 2D proteomic analysis. Expert Rev Proteomics 9: 129-134.
64. Yang M, Soga T, Pollard PJ, Adam J,. 2012b. The emerging role of fumarate as an oncometabolite. Front Oncol 2: 85.
65. Yin J, Gao Z, He Q, Zhou D, Guo Z, Ye J,. 2009. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab 296: E333-E342.
66. Zhang D,. 2010. The Nrf2-Keap1-ARE signaling pathway: The regulation and dual function of Nrf2 in cancer. Antioxid Redox Signaling 13: 1623-1626.
67. Zhang QB, Tang N, Brock JWC, Mottaz HM, Ames JM, Baynes JW, Smith RD, Metz TO,. 2007. Enrichment and analysis of nonenzymatically glycated peptides: Boronate affinity chromatography coupled with electron-transfer dissociation mass spectrometry. J Proteome Res 6: 2323-2330. (Pubitemid 46985120)