Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Aguer, Céline ^a   Gambarotta, Daniela ^a   Mailloux, Ryan J ^a   Moffat, Cynthia ^a   Dent, Robert ^b   McPherson, Ruth ^c   Harper, Mary Ellen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; CITRATE SYNTHASE; CYTOCHROME C OXIDASE; GALACTOSE; GLUCOSE; LACTIC ACID; ADENOSINE TRIPHOSPHATE; BIOLOGICAL MARKER;

ADULT; AEROBIC METABOLISM; ANAEROBIC GLYCOLYSIS; ARTICLE; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MITOCHONDRION; MYOBLAST; MYOTUBE; OBESITY; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; TISSUE DIFFERENTIATION; CELL CULTURE; CELL DIFFERENTIATION; CULTURE MEDIUM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MUSCLE CELL; OXIDATION REDUCTION REACTION; PATHOLOGY; PHOSPHORYLATION; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ADULT; AEROBIOSIS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA; DIABETES MELLITUS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; GALACTOSE; GLUCOSE; HUMANS; MALE; MITOCHONDRIA; MUSCLE CELLS; MUSCLE FIBERS, SKELETAL; OXIDATION-REDUCTION; PHOSPHORYLATION;

EID: 83455205885     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028536     Document Type: Article

References (45)

1. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, et al. (2003) Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52: 1319-1325.
2. Jackson S, Bagstaff SM, Lynn S, Yeaman SJ, Turnbull DM, et al. (2000) Decreased insulin responsiveness of glucose uptake in cultured human skeletal muscle cells from insulin-resistant nondiabetic relatives of type 2 diabetic families. Diabetes 49: 1169-1177.
3. Nikoulina SE, Ciaraldi TP, Carter L, Mudaliar S, Park KS, et al. (2001) Impaired muscle glycogen synthase in type 2 diabetes is associated with diminished phosphatidylinositol 3-kinase activation. J Clin Endocrinol Metab 86: 4307-4314.
4. Gaster M, Petersen I, Hojlund K, Poulsen P, Beck-Nielsen H, (2002) The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity. Diabetes 51: 921-927.
5. Gaster M, Rustan AC, Aas V, Beck-Nielsen H, (2004) Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes. Diabetes 53: 542-548.
6. Gaster M, Rustan AC, Beck-Nielsen H, (2005) Differential utilization of saturated palmitate and unsaturated oleate: evidence from cultured myotubes. Diabetes 54: 648-656.
7. Ortenblad N, Mogensen M, Petersen I, Hojlund K, Levin K, et al. (2005) Reduced insulin-mediated citrate synthase activity in cultured skeletal muscle cells from patients with type 2 diabetes: evidence for an intrinsic oxidative enzyme defect. Biochim Biophys Acta 1741: 206-214.
8. Aguer C, Mercier J, Man CY, Metz L, Bordenave S, et al. (2010) Intramyocellular lipid accumulation is associated with permanent relocation ex vivo and in vitro of fatty acid translocase (FAT)/CD36 in obese patients. Diabetologia 53: 1151-1163.
9. Kitzmann M, Lantier L, Hebrard S, Mercier J, Foretz M, et al. (2011) Abnormal metabolism flexibility in response to high palmitate concentrations in myotubes derived from obese type 2 diabetic patients. Biochim Biophys Acta 1812: 423-430.
10. Furling D, Marette A, Puymirat J, (1999) Insulin-like growth factor I circumvents defective insulin action in human myotonic dystrophy skeletal muscle cells. Endocrinology 140: 4244-4250.
11. Ukropcova B, McNeil M, Sereda O, de Jonge L, Xie H, et al. (2005) Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. J Clin Invest 115: 1934-1941.
12. Zuurveld JG, Oosterhof A, Veerkamp JH, van Moerkerk HT, (1985) Oxidative metabolism of cultured human skeletal muscle cells in comparison with biopsy material. Biochim Biophys Acta 844: 1-8.
13. Marroquin LD, Hynes J, Dykens JA, Jamieson JD, Will Y, (2007) Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol Sci 97: 539-547.
14. Shulga N, Wilson-Smith R, Pastorino JG, (2010) Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J Cell Sci 123: 894-902.
15. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, et al. (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 64: 985-993.
16. Ibsen KH, (1961) The Crabtree effect: a review. Cancer Res 21: 829-841.
17. Seshagiri PB, Bavister BD, (1991) Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the "crabtree effect". Mol Reprod Dev 30: 105-111.
18. Guppy M, Greiner E, Brand K, (1993) The role of the Crabtree effect and an endogenous fuel in the energy metabolism of resting and proliferating thymocytes. Eur J Biochem 212: 95-99.
19. Heidenreich RA, Mallee J, Rogers S, Segal S, (1993) Developmental and tissue-specific modulation of rat galactose-1-phosphate uridyltransferase steady state messenger RNA and specific activity levels. Pediatr Res 34: 416-419.
20. Robinson BH, Petrova-Benedict R, Buncic JR, Wallace DC, (1992) Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem Med Metab Biol 48: 122-126.
21. Reitzer LJ, Wice BM, Kennell D, (1979) Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem 254: 2669-2676.
22. Bustamante E, Pedersen PL, (1977) High aerobic glycolysis of rat hepatoma cells in culture: role of mitochondrial hexokinase. Proc Natl Acad Sci U S A 74: 3735-3739.
23. Rana P, Nadanaciva S, Will Y, (2011) Mitochondrial membrane potential measurement of H9c2 cells grown in high-glucose and galactose-containing media does not provide additional predictivity towards mitochondrial assessment. Toxicol In Vitro 25: 580-587.
24. Dykens JA, Jamieson J, Marroquin L, Nadanaciva S, Billis PA, et al. (2008) Biguanide-induced mitochondrial dysfunction yields increased lactate production and cytotoxicity of aerobically-poised HepG2 cells and human hepatocytes in vitro. Toxicol Appl Pharmacol 233: 203-210.
25. Kelley DE, He J, Menshikova EV, Ritov VB, (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950.
26. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, et al. (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56: 1592-1599.
27. Phielix E, Schrauwen-Hinderling VB, Mensink M, Lenaers E, Meex R, et al. (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes.
28. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI, (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671.
29. Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, et al. (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56: 1376-1381.
30. Minet AD, Gaster M, (2011) The dynamic equilibrium between ATP synthesis and ATP consumption is lower in isolated mitochondria from myotubes established from type 2 diabetic subjects compared to lean control. Biochem Biophys Res Commun 409: 591-595.
31. Minet AD, Gaster M, (2011) ATP synthesis is impaired in isolated mitochondria from myotubes established from type 2 diabetic subjects. Biochem Biophys Res Commun 402: 70-74.
32. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, et al. (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661-673.
33. Jager S, Handschin C, St-Pierre J, Spiegelman BM, (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 104: 12017-12022.
34. Koistinen HA, Galuska D, Chibalin AV, Yang J, Zierath JR, et al. (2003) 5-amino-imidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes. Diabetes 52: 1066-1072.
35. Foretz M, Ancellin N, Andreelli F, Saintillan Y, Grondin P, et al. (2005) Short-term overexpression of a constitutively active form of AMP-activated protein kinase in the liver leads to mild hypoglycemia and fatty liver. Diabetes 54: 1331-1339.
36. Foretz M, Carling D, Guichard C, Ferre P, Foufelle F, (1998) AMP-activated protein kinase inhibits the glucose-activated expression of fatty acid synthase gene in rat hepatocytes. J Biol Chem 273: 14767-14771.
37. Woods A, Azzout-Marniche D, Foretz M, Stein SC, Lemarchand P, et al. (2000) Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol Cell Biol 20: 6704-6711.
38. Kitzmann M, Bonnieu A, Duret C, Vernus B, Barro M, et al. (2006) Inhibition of Notch signaling induces myotube hypertrophy by recruiting a subpopulation of reserve cells. J Cell Physiol 208: 538-548.
39. Berridge MV, Tan AS, (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303: 474-482.
40. Costford SR, Crawford SA, Dent R, McPherson R, Harper ME, (2009) Increased susceptibility to oxidative damage in post-diabetic human myotubes. Diabetologia 52: 2405-2415.
41. Corpeleijn E, Hessvik NP, Bakke SS, Levin K, Blaak EE, et al. (2010) Oxidation of intramyocellular lipids is dependent on mitochondrial function and the availability of extracellular fatty acids. Am J Physiol Endocrinol Metab 299: E14-22.
42. Mailloux RJ, Harper ME, (2010) Glucose regulates enzymatic sources of mitochondrial NADPH in skeletal muscle cells; a novel role for glucose-6-phosphate dehydrogenase. FASEB J 24: 2495-2506.
43. Jacquemin V, Furling D, Bigot A, Butler-Browne GS, Mouly V, (2004) IGF-1 induces human myotube hypertrophy by increasing cell recruitment. Exp Cell Res 299: 148-158.
44. Petit JM, Maftah A, Ratinaud MH, Julien R, (1992) 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 209: 267-273.
45. Maftah A, Petit JM, Ratinaud MH, Julien R, (1989) 10-N nonyl-acridine orange: a fluorescent probe which stains mitochondria independently of their energetic state. Biochem Biophys Res Commun 164: 185-190.