Myogenin regulates exercise capacity and skeletal muscle metabolism in the adult mouse

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Flynn, Jesse M ^a,b   Meadows, Eric ^a,b   Fiorotto, Marta ^c   Klein, William H ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; LACTIC ACID; MYOGENIN;

ADULT ANIMAL; AEROBIC METABOLISM; ALLELE; ANAEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD GLUCOSE MONITORING; CALORIMETRY; CONTROLLED STUDY; ENERGY BALANCE; ENERGY CONSUMPTION; EXERCISE; FEMALE; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GLYCOLYSIS; HISTOCHEMISTRY; LACTATE BLOOD LEVEL; MALE; MOUSE; MUSCLE METABOLISM; NONHUMAN; PROTEIN FUNCTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; TRANSGENE; TREADMILL EXERCISE; ANIMAL; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; MICE; MUSCLE, SKELETAL; MYOGENIN; PHYSICAL CONDITIONING, ANIMAL;

EID: 78149461195     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013535     Document Type: Article

References (55)

1. Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19-37.
2. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, et al. (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197-205.
3. Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371-423.
4. Schiaffino S, Sandri M, Murgia M (2007) Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology (Bethesda) 22: 69-278.
5. Le Grand F, Rudnicki MA (2007) Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19: 628-633.
6. Molkentin JD, Olson EN (1996) Defining the regulatory networks for muscle development. Curr Opin Genet Dev 6: 445-453.
7. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, et al. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364: 501-506.
8. Knapp JR, Davie JK, Myer A, Meadows E, Olson EN, et al. (2006) Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size. Development 133: 601-610.
9. Meadows E, Cho JH, Flynn JM, Klein WH (2008) Myogenin regulates a distinct genetic program in adult muscle stem cells. Dev Biol 322: 406-414.
10. Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798.
11. Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, et al. (1993) Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118:1137-1147.
12. Alapat DV, Chaudhry T, Ardakany-Taghavi R, Kohtz DS (2009) Fiber-types of sarcomeric proteins expressed in cultured myogenic cells are modulated by the dose of myogenin activity. Cell Signal 21: 128-135.
13. Hughes SM, Chi MM, Lowry OH, Gundersen K (1999) Myogenin induces a shift of enzyme activity from glycolytic to oxidative metabolism in muscles of transgenic mice. J Cell Biol 145: 633-642.
14. Brooks GA (2009) Cell-cell and intracellular lactate shuttles. J Physiol 587:5591-5600.
15. Gladden LB (2000) Muscle as a consumer of lactate. Med Sci Sports Exerc 32:764-771.
16. Robergs RA, Ghiasvand F, Parker D (2004) Biochemistry of exercise-induced metabolic acidosis. Am J Physiol Regul Integr Comp Physiol 287: R502-516.
17. Stringer W, Wasserman K, Casaburi R (1995) The VCO2/VO2 relationship during heavy, constant work rate exercise reflects the rate of lactic acid accumulation. Eur J Appl Physiol Occup Physiol 72: 25-31.
18. Nabben M, Hoeks J (2008) Mitochondrial uncoupling protein 3 and its role in cardiac- and skeletal muscle metabolism. Physiol Behav 94: 259-269.
19. Spangenburg EE, Brown DA, Johnson MS, Moore RL (2009) Alterations in peroxisome proliferator-activated receptor mRNA expression in skeletal muscle after acute and repeated bouts of exercise. Mol Cell Biochem 332: 225-231.
20. Fitts RH (2004) Mechanisms of Muscular Fatigue: Karger.
21. Hagberg H (1985) Intracellular pH during ischemia in skeletal muscle: relationship to membrane potential, extracellular pH, tissue lactic acid and ATP. Pflugers Arch 404: 342-347.
22. Sahlin K (1986) Metabolic Changes Limiting Muscle Performance. In: Saltin B, ed. Biochemistry of Exercise VI. ChampaignIL: Human Kinetics Publishers. Pp 323-343.
23. Sahlin K, Edstrom L, Sjoholm H, Hultman E (1981) Effects of lactic acid accumulation and ATP decrease on muscle tension and relaxation. Am J Physiol 240: C121-126.
24. Sahlin K, Harris RC, Nylind B, Hultman E (1976) Lactate content and pH in muscle obtained after dynamic exercise. Pflugers Arch 367: 143-149.
25. Sahlin K, Henriksson J (1984) Buffer capacity and lactate accumulation in skeletal muscle of trained and untrained men. Acta Physiol Scand 122: 331-339.
26. Sahlin K, Katz A, Henriksson J (1987) Redox state and lactate accumulation in human skeletal muscle during dynamic exercise. Biochem J 245: 551-556.
27. Sahlin K, Tonkonogi M, Soderlund K (1998) Energy supply and muscle fatigue in humans. Acta Physiol Scand 162: 261-266.
28. Noakes TD (1997) 1996 J.B. Wolffe Memorial Lecture. Challenging beliefs: ex Africa semper aliquid novi. Med Sci Sports Exerc 29: 571-590.
29. Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74: 49-94.
30. Hakimi P, Yang J, Casadesus G, Massillon D, Tolentino-Silva F, et al. (2007) Overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) in skeletal muscle repatterns energy metabolism in the mouse. J Biol Chem 282: 32844-32855.
31. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, et al. (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2: e294.
32. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
33. Frey N, Frank D, Lippl S, Kuhn C, Kogler H, et al. (2008) Calsarcin-2 deficiency increases exercise capacity in mice through calcineurin/NFAT activation. J Clin Invest 118: 3598-3608.
34. Gundersen K (1998) Determination of muscle contractile properties: the importance of the nerve. Acta Physiol Scand 162: 333-341.
35. Fischer KF, Lees JA, Newman JH (1986) Hypoglycemia in hospitalized patients. Causes and outcomes. N Engl J Med 315: 1245-1250.
36. Service FJ (1995) Hypoglycemic disorders. N Engl J Med 332: 1144-1152.
37. Baldwin KM, Cooke DA, Cheadle WG (1977) Time course adaptations in cardiac and skeletal muscle to different running programs. J Appl Physiol 42:267-272.
38. Baldwin KM, Klinkerfuss GH, Terjung RL, Mole PA, Holloszy JO (1972) Respiratory capacity of white, red, and intermediate muscle: adaptative response to exercise. Am J Physiol 222: 373-378.
39. Dudley GA, Abraham WM, Terjung RL (1982) Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. J Appl Physiol 53:844-850.
40. Holloszy JO, Oscai LB, Don IJ, Mole PA (1970) Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem Biophys Res Commun 40: 1368-1373.
41. Ishihara A, Inoue N, Katsuta S (1991) The relationship of voluntary running to fibre type composition, fibre area and capillary supply in rat soleus and plantaris muscles. Eur J Appl Physiol Occup Physiol 62: 211-215.
42. Rodnick KJ, Reaven GM, Haskell WL, Sims CR, Mondon CE (1989) Variations in running activity and enzymatic adaptations in voluntary running rats. J Appl Physiol 66: 1250-1257.
43. Sexton WL (1995) Vascular adaptations in rat hindlimb skeletal muscle after voluntary running-wheel exercise. J Appl Physiol 79: 287-296.
44. Robinson BH (2006) Lactic acidemia and mitochondrial disease. Mol Genet Metab 89: 3-13.
45. Carbone MA, Applegarth DA, Robinson BH (2002) Intron retention and frameshift mutations result in severe pyruvate carboxylase deficiency in two male siblings. Hum Mutat 20: 48-56.
46. Robinson BH, Oei J, Saudubray JM, Marsac C, Bartlett K, et al. (1987) The French and North American phenotypes of pyruvate carboxylase deficiency, correlation with biotin containing protein by 3H-biotin incorporation, 35S- streptavidin labeling, and Northern blotting with a cloned cDNA probe. Am J Hum Genet 40: 50-59.
47. Robinson BH, Oei J, Sherwood WG, Applegarth D, Wong L, et al. (1984) The molecular basis for the two different clinical presentations of classical pyruvate carboxylase deficiency. Am J Hum Genet 36: 283-294.
48. Yalcin A, Telang S, Clem B, Chesney J (2009) Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp Mol Pathol 86: 174-179.
49. Tang H, Macpherson P, Marvin M, Meadows E, Klein WH, et al. (2009) A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression. Mol Biol Cell 20: 1120-1131.
50. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
51. Guo W, Jiang L, Bhasin S, Khan SM, Swerdlow RH (2009) DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number deter-mination. Mitochondrion 9: 261-265.
52. Pette D, Tyler KR (1983) Response of succinate dehydrogenase activity in fibres of rabbit tibialis anterior muscle to chronic nerve stimulation. J Physiol 338: 1-9.
53. Katz S, Irizarry RA, Lin X, Tripputi M, Porter MW (2006) A summarization approach for Affymetrix GeneChip data using a reference training set from a large, biologically diverse database. BMC Bioinformatics 7: 464.
54. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210.
55. Abramoff M (2004) Image processing using ImageJ. Biophotonics International. pp 36-42.