Skeletal muscle ATP kinetics are impaired in frail mice

Age

Volumn 36, Issue 1, 2014, Pages 21-30

  Akki, Ashwin ^a   Yang, Huanle ^a   Gupta, Ashish ^a   Chacko, Vadappuram P ^a   Yano, Toshiyuki ^a   Leppo, Michelle K ^a   Steenbergen, Charles ^a   Walston, Jeremy ^a   Weiss, Robert G ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

ATP; Creatine kinase; Frailty; Metabolism; Skeletal muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE KINASE; CREATINE PHOSPHATE; INTERLEUKIN 10; INTERLEUKIN 6; PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; FRAILTY; HINDLIMB; HYDROLYSIS; MALE; MOUSE; MUSCLE WEAKNESS; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; AGING; ANIMALS; CREATINE KINASE; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HYDROLYSIS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE WEAKNESS; MUSCLE, SKELETAL; PHENOTYPE; PHOSPHOCREATINE;

EID: 84899077849     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-013-9540-0     Document Type: Article

References (39)

1. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287-332
2. Balaban RS, Koretsky AP (2011) Interpretation of 31P NMR saturation transfer experiments: what you can't see might confuse you. Focus on "Standard magnetic resonance-based measurements of the Pi->ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles". Am J of Physiol Cell Physiol 301:C12-15
3. Barnes PR, Kemp GJ, Taylor DJ, Radda GK (1997) Skeletal muscle metabolism in myotonic dystrophy A 31P magnetic resonance spectroscopy study. Brain : A J of Neurol 120(Pt 10):1699-1711 (Pubitemid 27443047)
4. Bittl JA, DeLayre J, Ingwall JS (1987) Rate equation for creatine kinase predicts the in vivo reaction velocity: 31P NMR surface coil studies in brain, heart, and skeletal muscle of the living rat. Biochemistry 26:6083-6090
5. Cline GW, Vidal-Puig AJ, Dufour S, Cadman KS, Lowell BB, Shulman GI (2001) In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J Biol Chem 276:20240-20244
6. Conley KE, Amara CE, Bajpeyi S, Costford SR, Murray K, Jubrias SA, Arakaki L, Marcinek DJ, Smith SR (2013) Higher mitochondrial respiration and uncoupling with reduced electron transport chain content in vivo in muscle of sedentary versus active subjects. J Clin Endocrinol Metab 98:129-136
7. Das AM, Steuerwald U, Illsinger S (2010) Inborn errors of energy metabolism associated with myopathies. J Biomed Biotechnol 2010:340849
8. Dzeja PP, Terzic A (2003) Phosphotransfer networks and cellular energetics. J Exp Biol 206:2039-2047 (Pubitemid 36761807)
9. England K, Cotter TG (2005) Direct oxidative modifications of signalling proteins in mammalian cells and their effects on apoptosis. Redox Report : Comm in Free Radical Res 10:237-245 (Pubitemid 44111130)
10. Feng J, Xie H, Meany DL, Thompson LV, Arriaga EA, Griffin TJ (2008) Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria. The J of Gerontol Series A, Biol Sci and Med Sc 63:1137-1152 (Pubitemid 352772034)
11. From AH, Ugurbil K (2011) Standard magnetic resonance-based measurements of the Pi → ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles. Am J of Physiol Cell Physiol 301:C1-11
12. Gibbs C (1985) The cytoplasmic phosphorylation potential. Its possible role in the control of myocardial respiration and cardiac contractility. J Mol Cell Cardiol 17:727-731
13. Gupta A, Chacko VP, Schar M, Akki A, Weiss RG (2011) Impaired ATP kinetics in failing in vivo mouse heart. Circulation Cardiovascular Imaging 4:42-50
14. Gupta A, Akki A, Wang Y, Leppo M, Chacko VP, Foster D, Cicares V, Kirk J, Su J, Shi S, Lai S, Paolocci N, Steenbergen C, Gerstenblith G, Weiss RG (2012) Creatine kinase-mediated improvement of function in failing mouse hearts provides causal evidence the failing heart is energy-starved. J Clin Invest 122:291-302
15. Kanapuru B, Ershler WB (2009) Inflammation, coagulation, and the pathway to frailty. Am J Med 122:605-613
16. 31P magnetic resonance saturation transfer measurements of Pi/ATP exchange in insulin-resistant skeletal muscle. Am J Physiol Endocrinol Metab 294:E640-642, author reply E643-644
17. Kemp GJ, Brindle KM (2012) What do magnetic resonance-based measurements of Pi → ATP flux tell us about skeletal muscle metabolism? Diabetes 61:1927-1934
18. Ko F, Yu Q, Xue QL, Yao W, Brayton C, Yang H, Fedarko N, Walston J (2012) Inflammation and mortality in a frail mouse model. AGE (Dordr) 34:705-715
19. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274 (Pubitemid 23320290)
20. Marzetti E, Leeuwenburgh C (2006) Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol 41:1234-1238 (Pubitemid 44848392)
21. Nair KS (2005) Aging muscle. Am J Clin Nutr 81:953-963
22. Nuss JE, Amaning JK, Bailey CE, DeFord JH, Dimayuga VL, Rabek JP, Papaconstantinou J (2009) Oxidative modification and aggregation of creatine kinase from aged mouse skeletal muscle. Aging 1:557-572
23. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D (1998) Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17:1688-1699 (Pubitemid 28119122)
24. 2+ release in single skinned skeletal muscle fibres of the rat. J Physiol 512(Pt 1):97-108
25. Radda GK (1986) The use of NMR spectroscopy for the understanding of disease. Science 233:640-645
26. Ronner P, Friel E, Czerniawski K, Frankle S (1999) Luminometric assays of ATP, phosphocreatine, and creatine for estimation of free ADP and free AMP. Anal Biochem 275:208-216
27. Russ DW, Lanza IR (2011) The impact of old age on skeletal muscle energetics: supply and demand. Current Aging Sci 4:234-247
28. Saupe KW, Spindler M, Hopkins JC, ShenW, Ingwall JS (2000) Kinetic, thermodynamic, and developmental consequences of deleting creatine kinase isoenzymes from the heart. Reaction kinetics of the creatine kinase isoenzymes in the intact heart. J of Biol Chem 275:19742-19746 (Pubitemid 30441573)
29. Schrack JA, Simonsick EM, Ferrucci L (2010) The energetic pathway to mobility loss: an emerging new framework for longitudinal studies on aging. J Am Geriatr Soc 58(Suppl 2):S329-336
30. Schuh RA, Jackson KC, Khairallah RJ, Ward CW, Spangenburg EE (2012) Measuring mitochondrial respiration in intact single muscle fibers. Am J Physiol Regul Integr Comp Physiol 302:R712-719
31. Staunton L, O'Connell K, Ohlendieck K (2011) Proteomic profiling of mitochondrial enzymes during skeletal muscle aging. J of Aging Res 2011:908035
32. Steenbergen C, Deleeuw G, Rich T, Williamson JR (1977) Effects of acidosis and ischemia on contractility and intracellular pH of rat heart. Circ Res 41:849-858 (Pubitemid 8242791)
33. Ventura-Clapier R, Kaasik A, Veksler V (2004) Structural and functional adaptations of striated muscles to CK deficiency. Mol Cell Biochem 256-257:29-41 (Pubitemid 38181233)
34. Walston J, McBurnie MA, Newman A, Tracy RP, Kop WJ, Hirsch CH, Gottdiener J, Fried LP, Cardiovascular HS (2002) Frailty and activation of the inflammation and coagulation systems with and without clinical comorbidities: results from the Cardiovascular Health Study. Arch Intern Med 162:2333-2341 (Pubitemid 35332516)
35. Walston J, Hadley EC, Ferrucci L, Guralnik JM, Newman AB, Studenski SA, Ershler WB, Harris T, Fried LP (2006) Research agenda for frailty in older adults: toward a better understanding of physiology and etiology: summary from the American Geriatrics Society/National Institute on Aging Research Conference on Frailty in Older Adults. J Am Geriatr Soc 54:991-1001 (Pubitemid 43847040)
36. Walston J, Fedarko N, Yang H, Leng S, Beamer B, Espinoza S, Lipton A, Zheng H, Becker K (2008) The physical and biological characterization of a frail mouse model. J of Gerontol Series A, Biol Sci and Med Sci 63:391-398 (Pubitemid 351738421)
37. Weiss RG, Gerstenblith G, Bottomley PA (2005) ATP flux through creatine kinase in the normal, stressed, and failing human heart. Proc Natl Acad Sci U S A 102:808-813 (Pubitemid 40282747)
38. Wortmann RL (1991) Metabolic myopathies. Curr Opin Rheumatol 3:925-933
39. 31P NMR studies in Duchenne muscular dystrophy: age-related metabolic changes. Neurology 37:165-169