Mitochondrial stress causes increased succination of proteins in adipocytes in response to glucotoxicity

Biochemical Journal

Volumn 445, Issue 2, 2012, Pages 247-254

  Frizzell, Norma ^a   Thomas, Sonia A ^b   Carson, James A ^b   Baynes, John W ^a  

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

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Adipocyte; Cysteine; Fumarate; Mitochondrial hyperpolarization; Pseudohypoxia; Succination

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; FUMARIC ACID; GLUCOSE; METFORMIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CELL STRESS; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOTOXICITY; GLUCOTOXICITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN MODIFICATION;

3T3 CELLS; ADIPOCYTES; ANIMALS; ANOXIA; BLOTTING, WESTERN; CELL SURVIVAL; CITRIC ACID CYCLE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUMARATES; GLUCOSE; MALATES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; OXIDATIVE PHOSPHORYLATION COUPLING FACTORS; OXIDATIVE STRESS; SUCCINIC ACID; SWEETENING AGENTS;

MUS;

EID: 84863192640     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112142     Document Type: Article

References (61)

1. Alderson, N. L., Wang, Y., Blatnik, M., Frizzell, N., Walla, M. D., Lyons, T. J., Alt, N., Carson, J. A., Nagai, R., Thorpe, S. R. and Baynes, J. W. (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)
2. Nagai, R., Brock, J. W., Blatnik, M., Baatz, J. E., Bethard, J., Walla, M. D., Thorpe, S. R., Baynes, J. W. and Frizzell, N. (2007) Succination of protein thiols during adipocyte maturation: a biomarker of mitochondrial stress. J. Biol. Chem. 282, 34219-34228 (Pubitemid 350159439)
3. Frizzell, N., Rajesh, M., Jepson, M. J., Nagai, R., Carson, J. A., Thorpe, S. R. and Baynes, J. W. (2009) Succination of thiol groups in adipose tissue proteins in diabetes: succination inhibits polymerization and secretion of adiponectin. J. Biol. Chem. 284, 25772-257781
4. Blatnik, M., Frizzell, N., Thorpe, S. R. and Baynes, J. W. (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
5. Fruebis, J., Tsao, T. S., Javorschi, S., Ebbets-Reed, D., Erickson, M. R., Yen, F. T., Bihain, B. E. and Lodish, H. F. (2001) Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl. Acad. Sci. U.S.A. 98, 2005-2010 (Pubitemid 32165613)
6. Hamilton, M. P., Gore, M. O., Ayers, C. R., Xinyu, W., McGuire, DK. and Scherer, P.E. (2011) Adiponectin and cardiovascular risk profile in patients with type 2 diabetes mellitus: parameters associated with adiponectin complex distribution. Diabetes Vasc. Dis. Res. 8, 190-194
7. Pajvani, U.B, Hawkins, M., Combs, T. P., Rajala, M. W., Doebber, T., Berger, J. P., Wagner, J. A., Wu, M., Knopps, A., Xiang, A. H. et al. (2004) Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem. 279, 12152-12162 (Pubitemid 38445780)
8. Bardella, C., El-Bahrawy, M., Frizzell, N., Adam, J., Ternette, N., Hatipoglu, E., Howarth, K., O'Flaherty, L., Roberts, I., Turner, G. et al. (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
9. Adam, J., Hatipoglu, E., O'Flaherty, L., Ternette, N., Sahgal, N., Lockstone, H., Baban, D., Nye, E., Stamp, G., Carmeliet, P. et al. (2011) Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: role of Nrf2 signaling and fumarate mediated succination of KEAP1. Cancer Cell 20, 524-537
10. Thomas, S. A., Storey, K. B., Baynes, J. W. and Frizzell, N. (2012) Tissue distribution of S-(2-succino)cysteine (2SC), a biomarker of mitochondrial stress in obesity and diabetes. Obesity 20, 263-269
11. Gao, C. L., Zhu, C., Zhao, Y. P., Chen, X. H., Ji, C. B., Zhang, C. M., Zhu, J. G., Xia, Z. K., Tong, M. L. and Guo, X. R. (2010) Mitochondrial dysfunction is induced by high levels of glucose and free fatty acids in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 320, 25-33
12. Bournat, J. C. and Brown, C. W. (2010) Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol., Diabetes Obes. 17, 446-452
13. Frizzell, N. and Baynes, J. W. (2009) Modification of cysteine residues in protein by endogenous oxidants and electrophiles. In Endogenous Toxins: Diet, Genetics, Disease and Treatment (O'Brien, P. J. and Bruce, W. R., eds), pp. 43-58, Wiley VCH, Weinheim
14. Frizzell, N., Lima, M. and Baynes, J. W. (2011) Succination of proteins in diabetes. Free Radical Res. 45, 101-109
15. Choo, H. J., Kim, J. H., Kwon, O. B., Lee, C. S., Mun, J. Y., Han, S. S., Yoon, Y. S., Yoon, G., Choi, K. M. and Ko, Y. G. (2006) Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49, 784-791 (Pubitemid 43361881)
16. Gregor, M. F. and Hotamisligil, G. S. (2007) Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J. Lipid Res. 48, 1905-1914 (Pubitemid 47360610)
17. Alkhouri, N., Gornicka, A., Berk. M, P., Thapaliya, S., Dixon, L. J., Kashyap, S., Schauer, P. R. and Feldstein, A. E. (2010) Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J. Biol. Chem. 285, 3428-3438
18. Sinha, R., Dufour, S., Petersen, K. F., LeBon, V., Enoksson, S., Ma, Y. Z., Savoye, M., Rothman, D. L., Shulman, G. I. and Caprio, S. (2002) Assessment of skeletal muscle triglyceride content by 1H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 51, 1022-1027 (Pubitemid 34438345)
19. Petersen, K. F., Dufour, S., Befroy, D., Lehrke, M., Hendler, R. E. and Shulman, G. I. (2005) Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 54, 603-608 (Pubitemid 40322060)
20. Garvey, W. T., Olefsky, J. M., Matthaei, S. and Marshall, S. (1987) Glucose and insulin co-regulate the glucose transport system in primary cultured adipocytes. A new mechanism of insulin resistance. J. Biol. Chem. 262, 189-197 (Pubitemid 17000002)
21. Robinson, K. A. and Buse, M. G. (2008) Mechanisms of high-glucose/ insulin-mediated desensitization of acute insulin-stimulated glucose transport and Akt activation. Am. J. Physiol. Endocrinol. Metab. 294, E870-E881
22. Virtue, S. and Vidal-Puig, A. (2010) Adipose tissue expandability, lipotoxicity and the metabolic syndrome - an allostatic perspective. Biochim. Biophys. Acta 1801, 338-349
23. 2emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J. Clin. Invest. 119, 573-581
24. Samuel, V. T., Petersen, K. F. and Shulman, G. I. (2010) Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277
25. Poitout, V. and Robertson, R. P. (2008) Glucolipotoxicity: fuel excess and β-cell dysfunction. Endocr. Rev. 29, 351-366 (Pubitemid 351679704)
26. Wang, T., Zang, Y., Ling, W., Corkey, B. E. and Guo, W. (2003) Metabolic partitioning of endogenous fatty acid in adipocytes. Obes. Res. 11, 880-887 (Pubitemid 41137526)
27. Frayn, K. N., Langin, D. and Karpe, F. (2008) Fatty acid-induced mitochondrial uncoupling in adipocytes is not a promising target for treatment of insulin resistance unless adipocyte oxidative capacity is increased. Diabetologia 51, 394-397
28. Lowry, O. H., Rosenbrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
29. Folch, J., Lees, M. and Stanley, G.H.S. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509
30. Hatch, M. D. (1978) Simple spectrophotometric assay for fumarate hydratase in crude tissue extracts. Anal. Biochem. 85, 271-275
31. El-Mir, M. Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M. and Leverve, X. (2000) Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 275, 223-228 (Pubitemid 30038975)
32. +, free radicals, and vascular dysfunction in early diabetes mellitus. Diabetologia 40, S115-S117
33. Williamson, J. R., Chang, K., Frangos, M., Hasan, K. S., Ido, Y., Kawamura, T., Nyengaard, J. R., van den Enden, M., Kilo, C. and Tilton, R. G. (1993) Hyperglycemic pseudohypoxia and diabetic complications. Diabetes 42, 801-813 (Pubitemid 23151571)
34. Passarella, S., Atlante, A., Valenti, D. and de Bari, L. (2003) The role of mitochondrial transport in energy metabolism. Mitochondrion 2, 319-343 (Pubitemid 36537724)
35. Norman, C., Howell, K. A., Millar, A. H., Whelan, J. M. and Day, D. A. (2004) Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 134, 492-501 (Pubitemid 38178720)
36. Goldfine, A. B., Fonseca, V., Jablonski, K. A., Pyle, L., Staten, M. A. and Shoelson, S. E. (2010) TINSAL-T2D (Targeting Inflammation Using Salsalate in Type 2 Diabetes) Study Team. The effects of salsalate on glycemic control in patients with type 2 diabetes: a randomized trial. Ann. Intern. Med. 152, 346-357
37. Si, Y., Shi, H. and Lee, K. (2009) Metabolic flux analysis of mitochondrial uncoupling in 3T3-L1 adipocytes. PLoS ONE 4, e7000
38. Detaille, D., Guigas, B., Leverve, X., Wiernsperger, N. and Devos, P. (2002) Obligatory role of membrane events in the regulatory effect of metformin on the respiratory chain function. Biochem. Pharmacol. 63, 1259-1272 (Pubitemid 34311995)
39. Owen, M. R., Doran, E. and Halestrap, A. P. (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 348, 607-614 (Pubitemid 30410251)
40. Scheen, A. J. (1996) Clinical pharmacokinetics of metformin. Clin. Pharmacokinet. 30, 359-371
41. Wang, D. S., Kusuhara, H., Kato, Y., Jonker, J. W., Schinkel, A. H. and Sugiyama, Y. (2003) Involvement of organic cation transporter 1 in the lactic acidosis caused by metformin. Mol. Pharmacol. 63, 844-848 (Pubitemid 36368991)
42. Mullen, A. R., Wheaton, W. W., Jin, E. S., Chen, P. H., Sullivan, L. B., Cheng, T., Yang, Y., Linehan, W. M., Chandel, N. S. and DeBerardinis, R. J. (2011) Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 20, 385-388
43. Grisouard, J., Timper, K., Radimerski, T. M., Frey, D. M., Peterli, R., Kola, B., Korbonits, M., Herrmann, P., Krähenbühl, S., Zulewski, H. et al. (2010) Mechanisms of metformin action on glucose transport and metabolism in human adipocytes. Biochem. Pharmacol. 80, 1736-1745
44. Dichtwald, S., Weinbroum, A. A., Sorkine, P., Ekstein, M. P. and Dahan, E. (2012) Metformin-associated lactic acidosis following acute kidney injury. Efficacious treatment with continuous renal replacement therapy. Diabetes Med. 29, 245-250
45. Arroyo, D., Melero, R., Panizo, N., Goicoechea, M., Rodríguez- Benítez, P., Vinuesa, S. G., Verde, E., Tejedor, A. and Luño, J. (2011) Metformin-associated acute kidney injury and lactic acidosis. Int. J. Nephrol. 2011, 749653
46. van Berlo-van de Laar, I. R., Vermeij, C. G. and Doorenbos, C. J. (2011) Metformin associated lactic acidosis: incidence and clinical correlation with metformin serum concentration measurements. J. Clin. Pharm. Ther. 36, 376-382
47. Protti, A., Russo, R., Tagliabue, P., Vecchio, S., Singer, M., Rudiger, A., Foti, G., Rossi, A., Mistraletti, G. and Gattinoni, L. (2010) Oxygen consumption is depressed in patients with lactic acidosis due to biguanide intoxication. Crit. Care 14, R22
48. Wen, Y. K. (2009) Impact of acute kidney injury on metformin-associated lactic acidosis. Int. Urol. Nephrol. 41, 967-972
49. Suchard, J. R. and Grotsky, T. A. (2008) Fatal metformin overdose presenting with progressive hyperglycemia. West. J. Emerg. Med. 9, 160-164
50. Hong, Y. C., O'Boyle, C. P., Chen, I. C., Hsiao, C. T. and Kuan, J. T. (2008) Metformin-associated lactic acidosis in a pregnant patient. Gynecol. Obstet. Invest. 66, 138-141
51. Lacher, M., Hermanns-Clausen, M., Haeffner, K., Brandis, M. and Pohl, M. (2005) Severe metformin intoxication with lactic acidosis in an adolescent. Eur. J. Pediatr. 164, 362-365 (Pubitemid 40869009)
52. Yin, J., Gao, Z., He, Q., Zhou, D., Guo, Z. and 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
53. Hosogai, N., Fukuhara, A., Oshima, K., Miyata, Y., Tanaka, S., Segawa, K., Furukawa, S., Tochino, Y., Komuro, R., Matsuda, M. and Shimomura, I. (2007) Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56, 901-911 (Pubitemid 46525054)
54. Wood, I. S, de Heredia, F. P., Wang, B. and Trayhurn, P. (2009) Cellular hypoxia and adipose tissue dysfunction in obesity. Proc. Nutr. Soc. 68, 370-377
55. Halberg, N., Khan, T., Trujillo, M. E., Wernstedt-Asterholm, I., Attie, A. D., Sherwani, S., Wang, Z. V., Landskroner-Eiger, S., Dineen, S., Magalang, U. J. et al. (2009) Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 29, 4467-4483
56. Gagnon, A. and Sorisky, A. (1998) The effect of glucose concentration on insulin-induced 3T3-L1 adipose cell differentiation. Obes. Res. 6, 157-163 (Pubitemid 128679657)
57. Curtis, J. M., Grimsrud, P. A., Wright, W. S., Xu, X., Foncea, R. E., Graham, D. W., Brestoff, J. R., Wiczer, B. M., Ilkayeva, O., Cianflone, K. et al. (2010) Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes 59, 1132-1142
58. Yeop Han, C., Kargi, A. Y., Omer, M., Chan, C. K., Wabitsch, M., O'Brien, K. D., Wight, T. N. and Chait, A. (2010) Differential effect of saturated and unsaturated free fatty acids on the generation of monocyte adhesion and chemotactic factors by adipocytes: dissociation of adipocyte hypertrophy from inflammation. Diabetes 59, 386-396
59. Wu, X., Zhu, L., Zilbering, A., Mahadev, K., Motoshima, H., Yao, J. and Goldstein, B. J. (2005) Hyperglycemia potentiates H2O2 production in adipocytes and enhances insulin signal transduction: potential role for oxidative inhibition of thiol-sensitive protein-tyrosine phosphatases. Antioxid. Redox Signaling 7, 526-537 (Pubitemid 40563193)
60. Wang, T., Si, Y., Shirihai, O. S., Si, H., Schultz, V., Corkey, R. F., Hu, L., Deeney, J. T., Guo, W. and Corkey, B. E. (2010) Respiration in adipocytes is inhibited by reactive oxygen species. Obesity 18, 1493-1502
61. Lin, Y., Berg, A. H., Iyengar, P., Lam, T. K., Giacca, A., Combs, T. P., Rajala, M. W., Du, X., Rollman, B., Li, W. et al. (2005) The hyperglycemia-induced inflammatory response in adipocytes: the role of reactive oxygen species. J. Biol. Chem. 280, 4617-4626 (Pubitemid 40288630)