Nat1 Deficiency Is Associated with Mitochondrial Dysfunction and Exercise Intolerance in Mice

Cell Reports

Volumn 17, Issue 2, 2016, Pages 527-540

  Chennamsetty, Indumathi ^a   Coronado, Michael ^b   Contrepois, Kévin ^a   Keller, Mark P ^c   Carcamo Orive, Ivan ^a   Sandin, John ^a   Fajardo, Giovanni ^b   Whittle, Andrew J ^b   Fathzadeh, Mohsen ^a   Snyder, Michael ^a   Reaven, Gerald ^a   Attie, Alan D ^c   Bernstein, Daniel ^b   Quertermous, Thomas ^a   Knowles, Joshua W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

adipose tissue; basal metabolic rate; fatty acids; insulin resistance; mitochondria; mitochondrial dysfunction; Nat1; NAT2; reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL DNA; NORADRENALIN TRANSPORTER; REACTIVE OXYGEN METABOLITE; ARYLAMINE ACETYLTRANSFERASE; ISOENZYME; N-ACETYLTRANSFERASE 1;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CELL RESPIRATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXERCISE; EXERCISE INTOLERANCE; GENE SILENCING; INSULIN RESISTANCE; METABOLITE; MITOCHONDRIAL FRAGMENTATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; MYOBLAST; NAT1 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; THERMOGENESIS; 3T3-L1 CELL LINE; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE; DEFICIENCY; GENETICS; INBORN ERROR OF METABOLISM; METABOLISM; PATHOLOGY;

3T3-L1 CELLS; ADENOSINE TRIPHOSPHATE; ADIPOCYTES; ANIMALS; ARYLAMINE N-ACETYLTRANSFERASE; INSULIN RESISTANCE; ISOENZYMES; MEMBRANE POTENTIAL, MITOCHONDRIAL; METABOLISM, INBORN ERRORS; MICE; MITOCHONDRIA; MYOCARDIUM; PHYSICAL CONDITIONING, ANIMAL; REACTIVE OXYGEN SPECIES;

EID: 85004191320     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.09.005     Document Type: Article

References (51)

1. Bogacka, I., Ukropcova, B., McNeil, M., Gimble, J.M., Smith, S.R., Structural and functional consequences of mitochondrial biogenesis in human adipocytes in vitro. J. Clin. Endocrinol. Metab. 90 (2005), 6650–6656.
2. Bogacka, I., Xie, H., Bray, G.A., Smith, S.R., Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 54 (2005), 1392–1399.
3. Cannon, B., Nedergaard, J., Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214 (2011), 242–253.
4. Chennamsetty, I., Claudel, T., Kostner, K.M., Baghdasaryan, A., Kratky, D., Levak-Frank, S., Frank, S., Gonzalez, F.J., Trauner, M., Kostner, G.M., Farnesoid X receptor represses hepatic human APOA gene expression. J. Clin. Invest. 121 (2011), 3724–3734.
5. 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., Ko, Y.G., Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49 (2006), 784–791.
6. Church, T.S., Cheng, Y.J., Earnest, C.P., Barlow, C.E., Gibbons, L.W., Priest, E.L., Blair, S.N., Exercise capacity and body composition as predictors of mortality among men with diabetes. Diabetes Care 27 (2004), 83–88.
7. Contrepois, K., Jiang, L., Snyder, M., Optimized analytical procedures for the untargeted metabolomic profiling of human urine and plasma by combining hydrophilic interaction (HILIC) and reverse-phase liquid chromatography (RPLC)-mass spectrometry. Mol. Cell. Proteomics 14 (2015), 1684–1695.
8. De Pauw, A., Tejerina, S., Raes, M., Keijer, J., Arnould, T., Mitochondrial (dys)function in adipocyte (de)differentiation and systemic metabolic alterations. Am. J. Pathol. 175 (2009), 927–939.
9. Desai, K.H., Sato, R., Schauble, E., Barsh, G.S., Kobilka, B.K., Bernstein, D., Cardiovascular indexes in the mouse at rest and with exercise: new tools to study models of cardiac disease. Am. J. Physiol. 272 (1997), H1053–H1061.
10. Disatnik, M.H., Ferreira, J.C.B., Campos, J.C., Gomes, K.S., Dourado, P.M.M., Qi, X., Mochly-Rosen, D., Acute inhibition of excessive mitochondrial fission after myocardial infarction prevents long-term cardiac dysfunction. J. Am. Heart Assoc., 2, 2013, e000461.
11. Dorn, G.W. 2nd, Mitochondrial dynamism and heart disease: changing shape and shaping change. EMBO Mol. Med. 7 (2015), 865–877.
12. Enerbäck, S., Jacobsson, A., Simpson, E.M., Guerra, C., Yamashita, H., Harper, M.-E., Kozak, L.P., Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387 (1997), 90–94.
13. Facchini, F.S., Hua, N., Abbasi, F., Reaven, G.M., Insulin resistance as a predictor of age-related diseases. J. Clin. Endocrinol. Metab. 86 (2001), 3574–3578.
14. Fang, Z.Y., Sharman, J., Prins, J.B., Marwick, T.H., Determinants of exercise capacity in patients with type 2 diabetes. Diabetes Care 28 (2005), 1643–1648.
15. Feldmann, H.M., Golozoubova, V., Cannon, B., Nedergaard, J., UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9 (2009), 203–209.
16. Ferrannini, E., Natali, A., Camastra, S., Nannipieri, M., Mari, A., Adam, K.-P., Milburn, M.V., Kastenmüller, G., Adamski, J., Tuomi, T., et al. Early metabolic markers of the development of dysglycemia and type 2 diabetes and their physiological significance. Diabetes 62 (2013), 1730–1737.
17. Floegel, A., Stefan, N., Yu, Z., Mühlenbruch, K., Drogan, D., Joost, H.-G., Fritsche, A., Häring, H.-U., Hrabě de Angelis, M., Peters, A., et al. Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes 62 (2013), 639–648.
18. Frayn, K.N., Adipose tissue and the insulin resistance syndrome. Proc. Nutr. Soc. 60 (2001), 375–380.
19. Gall, W.E., Beebe, K., Lawton, K.A., Adam, K.-P., Mitchell, M.W., Nakhle, P.J., Ryals, J.A., Milburn, M.V., Nannipieri, M., Camastra, S., et al., RISC Study Group. α-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS ONE, 5, 2010, e10883.
20. Giesbertz, P., Padberg, I., Rein, D., Ecker, J., Höfle, A.S., Spanier, B., Daniel, H., Metabolite profiling in plasma and tissues of ob/ob and db/db mice identifies novel markers of obesity and type 2 diabetes. Diabetologia 58 (2015), 2133–2143.
21. Handschin, C., Choi, C.S., Chin, S., Kim, S., Kawamori, D., Kurpad, A.J., Neubauer, N., Hu, J., Mootha, V.K., Kim, Y.-B., et al. Abnormal glucose homeostasis in skeletal muscle-specific PGC-1α knockout mice reveals skeletal muscle-pancreatic β cell crosstalk. J. Clin. Invest. 117 (2007), 3463–3474.
22. Johnson, A.M.F., Olefsky, J.M., The origins and drivers of insulin resistance. Cell 152 (2013), 673–684.
23. Kelley, D.E., He, J., Menshikova, E.V., Ritov, V.B., Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51 (2002), 2944–2950.
24. Kim, J.-Y., Hickner, R.C., Cortright, R.L., Dohm, G.L., Houmard, J.A., Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279 (2000), E1039–E1044.
25. Kim, J.-Y., van de Wall, E., Laplante, M., Azzara, A., Trujillo, M.E., Hofmann, S.M., Schraw, T., Durand, J.L., Li, H., Li, G., et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J. Clin. Invest. 117 (2007), 2621–2637.
26. Kim, H.-J., Kim, J.H., Noh, S., Hur, H.J., Sung, M.J., Hwang, J.-T., Park, J.H., Yang, H.J., Kim, M.-S., Kwon, D.Y., Yoon, S.H., Metabolomic analysis of livers and serum from high-fat diet induced obese mice. J. Proteome Res. 10 (2011), 722–731.
27. Kim, M.J., Yang, H.J., Kim, J.H., Ahn, C.-W., Lee, J.H., Kim, K.S., Kwon, D.Y., Obesity-related metabolomic analysis of human subjects in black soybean peptide intervention study by ultraperformance liquid chromatography and quadrupole-time-of-flight mass spectrometry. J. Obes., 2013, 2013, 874981.
28. Kleiner, S., Mepani, R.J., Laznik, D., Ye, L., Jurczak, M.J., Jornayvaz, F.R., Estall, J.L., Chatterjee Bhowmick, D., Shulman, G.I., Spiegelman, B.M., Development of insulin resistance in mice lacking PGC-1α in adipose tissues. Proc. Natl. Acad. Sci. USA 109 (2012), 9635–9640.
29. Knowles, J.W., Xie, W., Zhang, Z., Chennamsetty, I., Assimes, T.L., Paananen, J., Hansson, O., Pankow, J., Goodarzi, M.O., Carcamo-Orive, I., et al. RISC (Relationship between Insulin Sensitivity and Cardiovascular Disease) Consortium EUGENE2 (European Network on Functional Genomics of Type 2 Diabetes) Study GUARDIAN (Genetics UndeRlying DIAbetes in HispaNics) Consortium, SAPPHIRe (Stanford Asian and Pacific Program for Hypertension and Insulin Resistance) Study. Identification and validation of N-acetyltransferase 2 as an insulin sensitivity gene. J. Clin. Invest. 125 (2015), 1739–1751.
30. Lee, J., Ellis, J.M., Wolfgang, M.J., Adipose fatty acid oxidation is required for thermogenesis and potentiates oxidative stress-induced inflammation. Cell Rep. 10 (2015), 266–279.
31. Matthias, A., Ohlson, K.B.E., Fredriksson, J.M., Jacobsson, A., Nedergaard, J., Cannon, B., Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. J. Biol. Chem. 275 (2000), 25073–25081.
32. Morino, K., Petersen, K.F., Shulman, G.I., Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55:Suppl 2 (2006), S9–S15.
33. Newgard, C.B., An, J., Bain, J.R., Muehlbauer, M.J., Stevens, R.D., Lien, L.F., Haqq, A.M., Shah, S.H., Arlotto, M., Slentz, C.A., et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 9 (2009), 311–326.
34. Noland, R.C., Koves, T.R., Seiler, S.E., Lum, H., Lust, R.M., Ilkayeva, O., Stevens, R.D., Hegardt, F.G., Muoio, D.M., Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control. J. Biol. Chem. 284 (2009), 22840–22852.
35. Patti, M.-E., Corvera, S., The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr. Rev. 31 (2010), 364–395.
36. Petersen, K.F., Dufour, S., Befroy, D., Garcia, R., Shulman, G.I., Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350 (2004), 664–671.
37. Reaven, G.M., Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 37 (1988), 1595–1607.
38. Ricquier, D., Bouillaud, F., The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345 (2000), 161–179.
39. Roberts, L.D., Koulman, A., Griffin, J.L., Towards metabolic biomarkers of insulin resistance and type 2 diabetes: progress from the metabolome. Lancet Diabetes Endocrinol. 2 (2014), 65–75.
40. Schooneman, M.G., Vaz, F.M., Houten, S.M., Soeters, M.R., Acylcarnitines: reflecting or inflicting insulin resistance?. Diabetes 62 (2013), 1–8.
41. Schrauwen, P., Hesselink, M.K.C., Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53 (2004), 1412–1417.
42. Sivitz, W.I., Yorek, M.A., Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox Signal. 12 (2010), 537–577.
43. Tian, J., Keller, M.P., Oler, A.T., Rabaglia, M.E., Schueler, K.L., Stapleton, D.S., Broman, A.T., Zhao, W., Kendziorski, C., Yandell, B.S., et al. Identification of the bile acid transporter Slco1a6 as a candidate gene that broadly affects gene expression in mouse pancreatic islets. Genetics 201 (2015), 1253–1262.
44. Tu, Z., Keller, M.P., Zhang, C., Rabaglia, M.E., Greenawalt, D.M., Yang, X., Wang, I.M., Dai, H., Bruss, M.D., Lum, P.Y., et al. Integrative analysis of a cross-loci regulation network identifies App as a gene regulating insulin secretion from pancreatic islets. PLoS Genet., 8, 2012, e1003107.
45. Vianna, C.R., Huntgeburth, M., Coppari, R., Choi, C.S., Lin, J., Krauss, S., Barbatelli, G., Tzameli, I., Kim, Y.-B., Cinti, S., et al. Hypomorphic mutation of PGC-1β causes mitochondrial dysfunction and liver insulin resistance. Cell Metab. 4 (2006), 453–464.
46. Wang, Y., Rimm, E.B., Stampfer, M.J., Willett, W.C., Hu, F.B., Comparison of abdominal adiposity and overall obesity in predicting risk of type 2 diabetes among men. Am. J. Clin. Nutr. 81 (2005), 555–563.
47. Wang-Sattler, R., Yu, Z., Herder, C., Messias, A.C., Floegel, A., He, Y., Heim, K., Campillos, M., Holzapfel, C., Thorand, B., et al. Novel biomarkers for pre-diabetes identified by metabolomics. Mol. Syst. Biol., 8, 2012, 615.
48. Weyer, C., Foley, J.E., Bogardus, C., Tataranni, P.A., Pratley, R.E., Enlarged subcutaneous abdominal adipocyte size, but not obesity itself, predicts type II diabetes independent of insulin resistance. Diabetologia 43 (2000), 1498–1506.
49. Wolf, G., Brown adipose tissue: the molecular mechanism of its formation. Nutr. Rev. 67 (2009), 167–171.
50. Xia, J., Sinelnikov, I.V., Han, B., Wishart, D.S., MetaboAnalyst 3.0–making metabolomics more meaningful. Nucleic Acids Res. 43 (2015), W251–257.
51. Yip, J., Facchini, F.S., Reaven, G.M., Resistance to insulin-mediated glucose disposal as a predictor of cardiovascular disease. J. Clin. Endocrinol. Metab. 83 (1998), 2773–2776.