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Components of energy expenditure in themdx mouse model of Duchenne muscular dystrophy

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Abstract

Previous observations showing that basal heat production rates and glucose metabolism were reduced inmdx mouse skeletal muscles incubated in vitro led us to study the components of total energy expenditure by open-circuit indirect calorimetry in the intact, free-movingmdx mouse. Our purpose was to verify if themdx mouse exhibited whole-body alterations in energy metabolism. The results revealed that total and basal energy expenditure, as well as spontaneous activity, energetic cost of activity, and, therefore, energy expended in relation to activity were not significantly different in C57B1 / 10 (control) and in dystrophic (mdx) mice. In contrast, the thermic effect of food was 32% larger inmdx than in control mice and was accompanied by significant differences in postprandial glucose and lipid oxidation. The present in vivo study could not show a direct demonstration that impaired glucose metabolism by skeletal muscles participated in this phenomenon. However, since postprandial glucose metabolism by skeletal muscles contributes a significant part of the thermic effect of food, the present data are in line with previous studies in vitro that show thatmdx mouse skeletal muscles probably suffer an impaired control of their energy metabolism.

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References

  1. Anderson JE, Bressler BH, Ovalle WK (1988) Functional regeneration of the hindlimb skeletal muscle of themdx mouse. J Muscle Res Cell Motif 9:499–515

    Google Scholar 

  2. Arahata K, Ishiura S, Ishiguro T, Tsukahara T, Suhara Y, Eguchi C, Ishihara T, Nonaka I, Ozawa E, Sugita H (1988) Immunostaining of skeletal and cardiac muscle surface membrane with antibody against Duchenne muscular dystrophy peptide. Nature 333:861–863

    Google Scholar 

  3. Ashworth A (1969) Metabolic rate during recovery from protein-calorie malnutrition: the need for a new concept of specific dynamic action. Nature 223:407–409

    Google Scholar 

  4. Bulfield G, Siller WG, Wight PAL, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse, Proc Natl Acad Sci USA 81:1189–1192

    Google Scholar 

  5. Carnwath JW, Shotton DM (1987) Muscular dystrophy in themdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J Neurol Sci 80:39–54

    Google Scholar 

  6. Chinet A, Clausen T, Girardier L (1977) Microcalorimetric determination of energy expenditure due to active sodiumpotassium transport in the soleus muscle and brown adipose tissue of the rat. J Physiol (Lond) 265:43–61

    Google Scholar 

  7. Chinet A, Decrouy A, Even PC (1992) Ca2+-dependent heat production under basal and near basal conditions in the mouse soleus muscle. J Physiol (Lond) 455:663–678

    Google Scholar 

  8. Chinet AE, Even PC, Decrouy A (1994) Dystrophin-dependent efficiency of metabolic pathways in mouse skeletal muscles. Experientia 50:602–605

    Google Scholar 

  9. Dangain J, Vrbova G (1984) Muscle development inmdx mutant mice. Muscle Nerve 7:700–704

    Google Scholar 

  10. Dauncey MJ, Brown D (1987) Role of activity-induced thermogenesis in twenty-four hour energy expenditure of lean and genetically obese (Ob/Ob) mice. Q J Exp Physiol 72:549–559

    Google Scholar 

  11. Decrouy A, Even PC, Chinet A (1993) Decreased rates of Ca2+-dependent heat production in slow- and fast-twitch muscles from the dystrophic (mdx) mouse. Experientia 49:843–849

    Google Scholar 

  12. DeFronzo RA, Jacot E, Jéquier E, Maeder E, Wahren J, Felber J-P (1981) The effect of insulin on the disposal of intravenous glucose: result from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30:1000–1007

    Google Scholar 

  13. Dunn JF, Frostick S, Brown G, Radda GK (1991) Energy status of cells lacking dystrophin: an in vivo/in vitro study ofmdx mouse skeletal muscle. Biochim Biophys Acta 1096:115–120

    Google Scholar 

  14. Dunn JF, Tracey I, Radda GK (1993) Exercice metabolism in Duchenne muscular dystrophy: a biochemical and31P-nuclear magnetic resonance study of mdx mice. Proc R Soc Lond [Biol] 251:201–206

    Google Scholar 

  15. Dupont-Versteegden EE, Baldwin RA, McCarter RJ, Vonlanthen MG (1994) Does muscular dystrophy affect metabolic rate. J Neurol Sci 121:203–207

    Google Scholar 

  16. Elia M (1992) Organ and tissue contribution to metabolic rate. In: Kinney JM, Tucker HN (eds) Energy metabolism: tissue determinant and cellular corollaries. Raven, New York, pp 61–80

    Google Scholar 

  17. Even PC, Nicolaidis S (1993) Adaptative changes in energy expenditure during mild and severe feed restriction in the rat. Br J Nutr 70:421–431

    Google Scholar 

  18. Even PC, Perrier E, Aucouturier J-L, Nicolaidis S (1991) Utilization of the method of Kalman filtering for the on-line computation of background metabolism in the free-moving free-feeding rat. Physiol Behav 49:177–187

    Google Scholar 

  19. Even PC, Mokhtarian A, Pelé A (1994) Practical aspects of indirect calorimetry in the laboratory animals. Neurosci Biobehav Rev 18:435–447

    Google Scholar 

  20. Even PC, Decrouy A, Chinet A (1994) Defective regulation of energy metabolism in mdx-mouse skeletal muscles. Biochem J 304:649–654

    Google Scholar 

  21. Garlick PJ (1986) Protein synthesis and energy expenditure in relation to feeding. Int J Vitam Nutr Res 56:197–200

    Google Scholar 

  22. Haymond MW, Strobel KE, DeVivo DC (1978) Muscle wasting and carbohydrate homeostasis in Duchenne muscular dystrophy Neurology 28:1224–1231

    Google Scholar 

  23. Henriksson J (1990) The possible role of skeletal muscle in the adaptation to periods of energy deficiency. Eur J Clin Nutr 44 [Suppl 1]: 55–64

    Google Scholar 

  24. Hoover-Plow J, Nelson B (1985) Oxygen consumption in mice (I strain) after feeding. J Nutr 115:303–310

    Google Scholar 

  25. Ianasescu V, Luca N, Vuia O (1976) Respiratory control and oxidative phosphorylation in dystrophic muscle. Acta Neurol Scand 43:564–572

    Google Scholar 

  26. Kemp GJ, Taylor DJ, Dunn JF, Frostickand SP, Radda GK (1993) Cellular energetic of dystrophic muscle. J Neurol Sci 116:201–206

    Google Scholar 

  27. Kleiber M (1947) Body-size and metabolic rate. Physiol Rev 27:511–541

    Google Scholar 

  28. Krieger I (1978) Relation of specific dynamic action of food (SDA) to growth in rats. Am J Clin Nutr 31:764–768

    Google Scholar 

  29. Lilling G, Beitner R (1991) Altered allosteric properties of cytoskeleton-bound phosphofructokinase in muscle frommdx mice with X chromosome-linked muscular dystrophy (mdx). Biochem Med Metabol Biol 45:319–325

    Google Scholar 

  30. MacLennan PA, McArdle A, Edwards RT (1991) Acute effects of phorbol esters on the protein-synthetic rate and carbohydrate metabolism of normal andmdx mouse muscles. Biochem J 275:477–483

    Google Scholar 

  31. Morrison SD (1967) The constancy of the energy expended by rats on spontaneous activity, and the distribution of activity between feeding and non feeding. J Physiol (Lond) 197: 305–323

    Google Scholar 

  32. Muntoni F, Mateddu A, Marchei F, Clerk A, Serra G (1993) Muscular weakness in themdx mouse. J Neurol Sci 120:71–77

    Google Scholar 

  33. Nishio H, Wada H, Matsuo T, Horikawa H, Takahashi K, Nakajima T, Matsuo M, Nakamura H (1990) Glucose, free fatty acid and ketone metabolism in Duchenne muscular dystrophy. Brain Dev 12:390–402

    Google Scholar 

  34. Olson E, Vignos PJ, Woodlock J, Perry T (1968) Oxidative phosphorylation of skeletal muscle in human muscular dystrophy. J Lab Clin Med 71:220–231

    Google Scholar 

  35. Takagi A, Shimada Y, Mozai T (1970) Studies on plasma free fatty acid and ketone bodies in young patients with muscular atrophy. Neurology 20:904–908

    Google Scholar 

  36. Tanabe Y, Esaki K, Nomura T (1986) Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta Neuropathol (Berl) 69:91–95

    Google Scholar 

  37. Torres LFB, Duchen LW (1987) The mutantmdx: inherited myopathy in the mouse. Brain 110:269–299

    Google Scholar 

  38. Turner PR, Westwood T, Regen CM, Steinhardt RA (1988) Increased protein degradation results from elevated free calcium levels found in muscle frommdx mice. Nature 333:735–738

    Google Scholar 

  39. Vignos PJ, Lefkowitz M (1959) A biochemical study of certain skeletal muscle constituents in human progressive muscular dystrophy. J Clin Invest 38:873–881

    Google Scholar 

  40. Younkin DP, Berman P, Sladky J, Chee C, Bank W, Chance B (1987) TI 31P NMR studies in Duchenne muscular dystrophy:age-related metabolic changes. Neurology 37:165–169

    Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Neurobiologie des Régulations, CNRS URA 1860, College de France, 11 Pl. Marcelin-Berthelot, F-75231, Paris Cedex 05, France

    A. Mokhtarian & P. C. Even

  2. Département de Physiologie, Centre Médical Universitaire, Faculté de Médecine, 1 rue Michel-Servet, CH-1211, Geneve 4, Switzerland

    A. Decrouy & A. Chinet

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  1. A. Mokhtarian
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  2. A. Decrouy
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  3. A. Chinet
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  4. P. C. Even
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Mokhtarian, A., Decrouy, A., Chinet, A. et al. Components of energy expenditure in themdx mouse model of Duchenne muscular dystrophy. Pflugers Arch. 431, 527–532 (1996). https://doi.org/10.1007/BF02191899

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  • DOI: https://doi.org/10.1007/BF02191899

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