Normalizing glutamine concentration causes mitochondrial uncoupling in an in vitro model of human skeletal muscle

Journal of Parenteral and Enteral Nutrition

Volumn 39, Issue 2, 2015, Pages 180-189

  Krajcova, Adela ^a   Ziak, Jakub ^a   Jiroutkova, Katerina ^a   Patkova, Jana ^a   Elkalaf, Moustafa ^a   Dzupa, Valer ^a   Trnka, Jan ^a   Duska, Frantisek ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

aerobic phosphorylation; bioenergetic failure; extracellular flux analysis; glutamine; human myoblasts

Indexed keywords

ADENOSINE TRIPHOSPHATE; CITRATE SYNTHASE; GLUTAMINE;

ANAEROBIC GLYCOLYSIS; ARTICLE; BIOENERGY; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MUSCLE BIOPSY; MYOBLAST; MYOTUBE; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SKELETAL MUSCLE; BIOPSY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRION; PHOSPHORYLATION;

BIOPSY; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT; ENERGY METABOLISM; GLUTAMINE; HUMANS; IN VITRO TECHNIQUES; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; OXYGEN CONSUMPTION; PHOSPHORYLATION;

EID: 84921940849     PISSN: 01486071     EISSN: 19412444     Source Type: Journal    
DOI: 10.1177/0148607113513801     Document Type: Article

References (48)

1. Canadian clinical practice guidelines. http://www.criticalcarenutrition.com/docs/cpgs2012/9.4a.pdf. Accessed August 25, 2013.
2. Andrews PJ, Avenell A, Noble DW, et al. Randomised trial of glutamine, selenium, or both, to supplement parenteral nutrition for critically ill patients. BMJ. 2011 ; 342: d1542
3. Heyland D, Muscedere J, Wischmeyer PE, et al. A randomized trial of glutamine and antioxidants in critically ill patients. N Engl J Med. 2013 ; 368: 1489-1497
4. Shi X, Garry DJ. Muscle stem cells in development, regeneration, and disease. Genes Dev. 2006 ; 20 (13). 1692-1708
5. Ukropcova B, McNeil M, Sereda O, et al. Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. J Clin Invest. 2005 ; 115 (7). 1934-1941
6. Zielke HR, Sumbilla CM, Zielke CL, et al Glutamine Metabolism in Mammalian Tissues. Berlin, Germany: Springer ; 1984 :
7. Marcora S, Lemmey A, Maddison P. Dietary treatment of rheumatoid cachexia with beta-hydroxy-beta-methylbutyrate, glutamine and arginine: a randomised controlled trial. Clin Nutr. 2005 ; 24 (3). 442-454
8. Tjäder I, Rooyackers O, Forsberg AM, et al. Effects on skeletal muscle of intravenous glutamine supplementation to ICU patients. Intensive Care Med. 2004 ; 30: 266-275
9. Bergström J, Fürst P, Norée LO, Vinnars E. Intracellular free amino acid concentration in human muscle tissue. J Appl Physiol. 1974 ; 36: 693-697
10. Reitzer LJ, Wice BM, Kennell D. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem. 1979 ; 254: 2669-2676
11. Hou Y-C, Chiu W-C, Yeh C-L, Yeh S-L. Glutamine modulates lipopolysaccharide-induced activation of NF-B via the Akt/mTOR pathway in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2012 ; 302: L174 - L183
12. Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y. Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol. 2007 ; 178: 93-105
13. Labitzke R, Friedl P. A serum-free medium formulation supporting growth of human umbilical cord vein endothelial cells in long-term cultivation. Cytotechnology. 2001 ; 35: 87-92
14. Aguer C, Gambarotta D, Mailloux RJ, et al. Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells. PLoS One. 2011 ; 6: e28536
15. Niklas J, Schräder E, Sandig V, Noll T, Heinzle E. Quantitative characterization of metabolism and metabolic shifts during growth of the new human cell line AGE1.HN using time resolved metabolic flux analysis. Bioprocess Biosyst Eng. 2011 ; 34: 533-545
16. EuroBioBank. Primary myoblast culture from fresh human muscle biopsy. INNCB-Marina Mora, August2004. http://www.eurobiobank.org/en/documents/sops.htm. Accessed August 28, 2013.
17. Thompson DB, Pratley R, Ossowski V. Remodeling lipid metabolism and improving insulin responsiveness in human primary myotubes. J Clin Invest. 1996 ; 98: 2346-2350
18. Freshney RI Culture of Animal Cells: A Manual of Basic Technique and Specialized Applications. New York, NY: Wiley-Blackwell ; 2010 :
19. Turowski GA, Rashid Z, Hong F, Madri JA, Basson MD. Glutamine modulates phenotype and stimulates proliferation in human colon cancer cell lines. Cancer Res. 1994 ; 54: 5974-5980
20. Cory AH, Owen TC, Barltrop JA, Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 1991 ; 3 (7). 207-212
21. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J. 2011 ; 435: 297-312
22. KuznetsovAV. Laboratory protocol: citrate synthase mitochondrial marker enzyme. http://www.oroboros.at/fileadmin/user-upload/Protocols/MiPNet08.14-CitrateSynthase.pdf. Accessed August 25, 2013.
23. Nicholls DG, Darley-Usmar VM, Wu M, Jensen PB, Rogers GW, Ferrick DA. Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp. 2010 ; (46). e2511
24. Smith JR. Glutamine metabolism and its physiological importance. JPEN J Parenter Enteral Nutr. 1990 ; 14: 40S - 44S
25. Buchman AL Modern Nutrition in Health and Disease. Shils ME Shike M Olson JA, ed. Philadelphia, PA: Lippincott Williams & Wilkins ; 563-570.
26. Parry-Billings M, Evans J, Calder PC, Newsholme EA. Does glutamine contribute to immunosuppression after major burns'. Lancet. 1990 ; 336: 523-525
27. Reeds PJ, Burrin DG. Glutamine and the bowel. J Nutr. 2001 ; 131: 2505S - 2508S
28. Ahmad S, White CW, Chang LY, Schneider BK, Allen CB. Glutamine protects mitochondrial structure and function in oxygen toxicity. Am J Physiol Lung Cell Mol Physiol. 2001 ; 280: L779 - L791
29. Duska F, Fric M, Pazout J, Waldauf P, Tma P, Pachl J. Frequent intravenous pulses of growth hormone together with alanylglutamine supplementation in prolonged critical illness after multiple trauma: effects on glucose control, plasma IGF-I and glutamine. Growth Horm IGF Res. 2008 ; 18 (1). 82-87
30. Pouw EM, Schols AM, Deutz NE, Wouters EF. Plasma and muscle amino acid levels in relation to resting energy expenditure and inflammation in stable chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998 ; 158 (3). 797-801
31. Planas M, Schwartz S, Arbos MA. Plasma glutamine levels in in septic patients. JPEN J Parenter Enteral Nutr. 1993 ; 17: 299-300
32. Jackson NC, Carroll PV, Russell-Jones DL, Sönksen PH, Treacher DF, Umpleby AM. The metabolic consequences of critical illness: acute effects on glutamine and protein metabolism. Am J Physiol. 1999 ; 276: E163 - E170
33. Nicklin P, Bergman P, Zhang B, et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell. 2009 ; 136: 521-534
34. Bodine SC, Stitt TN, Gonzalez M, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol. 2001 ; 3: 1014-1019
35. Nadanaciva S, Rana P, Beeson GC, et al. Assessment of drug-induced mitochondrial dysfunction via altered cellular respiration and acidification measured in a 96-well platform. J Bioenerg Biomembr. 2012 ; 44: 421-437
36. Mailloux RJ, Harper ME. Glucose regulates enzymatic sources of mitochondrial NADPH in skeletal muscle cells: a novel role for glucose-6-phosphate dehydrogenase. FASEB J. 2010 ; 24: 2495-2506
37. Zhang J, Nuebel E, Wisidagama DR, et al. Measuring energy metabolism in cultured cells, including human pluripotent stem cells and differentiated cells. Nat Protoc. 2012 ; 7: 1068-1085
38. Fleury C, Neverova M, Collins S, et al. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet. 1997 ; 15: 269-272
39. Hurtaud C, Gelly C, Chen Z, Lévi-Meyrueis C, Bouillaud F. Glutamine stimulates translation of uncoupling protein 2mRNA. Cell Mol Life Sci. 2007 ; 64: 1853-1860
40. Criscuolo F, Mozo J, Hurtaud C, Nübel T, Bouillaud F. UCP2, UCP3, avUCP, what do they do when proton transport is not stimulated' Possible relevance to pyruvate and glutamine metabolism. Biochim Biophys Acta. 2006 ; 1757: 1284-1291
41. Bakalar B, Duska F, Pachl J, et al. Parenterally administered dipeptide alanyl-glutamine prevents worsening of insulin sensitivity in multiple-trauma patients. Crit Care Med. 2006 ; 34 (2). 381-386
42. Déchelotte P, Hasselmann M, Cynober L, et al. L-alanyl-L-glutamine dipeptide-supplemented total parenteral nutrition reduces infectious complications and glucose intolerance in critically ill patients: the French controlled, randomized, double-blind, multicenter study. Crit Care Med. 2006 ; 34 (3). 598-604
43. Grau T, Bonet A, Miñambres E, et al. The effect of L-alanyl-L-glutamine dipeptide supplemented total parenteral nutrition on infectious morbidity and insulin sensitivity in critically ill patients. Crit Care Med. 2011 ; 39: 1263-1268
44. Duska F, Fric M, Waldauf P, et al. Frequent intravenous pulses of growth hormone together with glutamine supplementation in prolonged critical illness after multiple trauma: effects on nitrogen balance, insulin resistance, and substrate oxidation. Crit Care Med. 2008 ; 36 (6). 1707-1713
45. Iwashita S, Mikus C, Baier S, et al. Glutamine supplementation increases postprandial energy expenditure and fat oxidation in humans. JPEN J Parenter Enteral Nutr. 2006 ; 30: 76-80
46. Groening P, Huang Z, La Gamma EF, Levy RJ. Glutamine restores myocardial cytochrome c oxidase activity and improves cardiac function during experimental sepsis. JPEN J Parenter Enteral Nutr. 2011 ; 35: 249-254
47. Van den Berghe G. Low glutamine levels during critical illness - adaptive or maladaptive'. N Engl J Med. 2013 ; 368 (16). 1549-1550
48. Carré JE, Orban JC, Re L, et al. Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am J Respir Crit Care Med. 2010 ; 182 (6). 745-751