Chronic hindlimb suspension unloading markedly decreases turnover rates of skeletal and cardiac muscle proteins and adipose tissue triglycerides

Journal of Applied Physiology

Volumn 119, Issue 1, 2015, Pages 16-26

  Bederman, Ilya R ^a   Lai, Nicola ^a,b   Shuster, Jeffrey ^a   Henderson, Leigh ^a   Ewart, Steven ^a   Cabrera, Marco E ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Case Western Reserve University   (United States)

Author keywords

Deuterated water; Energy expenditure; Hindlimb suspension unloading; Mass spectrometry; Protein turnover; Triglyceride turnover

Indexed keywords

MUSCLE PROTEIN; TRIACYLGLYCEROL;

ADIPOSE TISSUE; ANIMAL; BODY WATER; BODY WEIGHT; CARDIAC MUSCLE; EATING; ENERGY METABOLISM; GROWTH; IMMOBILIZATION; KINETICS; MALE; METABOLISM; MUSCLE ATROPHY; PATHOLOGY; PHYSIOLOGY; RAT; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ADIPOSE TISSUE; ANIMALS; BODY WATER; BODY WEIGHT; EATING; ENERGY METABOLISM; GROWTH; HINDLIMB SUSPENSION; KINETICS; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOCARDIUM; RATS; RATS, SPRAGUE-DAWLEY; TRIGLYCERIDES;

EID: 84937196468     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00004.2014     Document Type: Article

References (54)

1. Babij P, Booth FW. Alpha-actin and cytochrome c mRNAs in atrophied adult rat skeletal muscle. Am J Physiol Cell Physiol 254: C651-C656, 1988.
2. Bajotto G, Shimomura Y. Determinants of disuse-induced skeletal muscle atrophy: exercise and nutrition countermeasures to prevent protein loss. J Nutr Sci Vitaminol (Tokyo) 52: 233-247, 2006.
3. Bederman IR, Chandramouli V, Sandlers Y, Henderson L, Cabrera ME. Time course of hepatic gluconeogenesis during hindlimb suspension unloading. Exp Physiol 98: 278-289, 2013.
4. 2 production and the tissue-specific dynamics of lipid and protein in vivo. Am J Physiol Endocrinol Metab 290: E1048-E1056, 2006.
5. Belloto E, Diraison F, Basset A, Allain G, Abdallah P, Beylot M. Determination of protein replacement rates by deuterated water: validation of underlying assumptions. Am J Physiol Endocrinol Metab 292: E1340-E1347, 2007.
6. Blanc S, Geloen A, Pachiaudi C, Gharib C, Normand S. Validation of the doubly labeled water method in rats during isolation and simulated weightlessness. Am J Physiol Regul Integr Comp Physiol 279: R1964-R1979, 2000.
7. Booth FW, Shanely RA. The biochemical basis of the health effects of exercise: an integrative view. Proc Nutr Soc 63: 199-203, 2004.
8. Brunengraber DZ, McCabe BJ, Katanik J, Previs SF. Gas chromatography-mass spectrometry assay of the (18)O enrichment of water as trimethyl phosphate. Anal Biochem 306: 278-282, 2002.
9. Cobelli C, Foster D, Toffolo GM. Tracer Kinetics in Biomedical Research: From Data to Model. New York: Plenum, 2000.
10. Cogo PE, Toffolo GM, Gucciardi A, Benetazzo A, Cobelli C, Carnielli VP. Surfactant disaturated phosphatidylcholine kinetics in infants with bronchopulmonary dysplasia measured with stable isotopes and a two-compartment model. J Appl Physiol (1985) 99: 323-329, 2005.
11. Cogo PE, Toffolo GM, Ori C, Vianello A, Chierici M, Gucciardi A, Cobelli C, Baritussio A, Carnielli VP. Surfactant disaturated-phosphatidylcholine kinetics in acute respiratory distress syndrome by stable isotopes and a two compartment model. Respir Res 8: 13, 2007.
12. Deavers DR, Musacchia XJ, Meininger GA. Model for antiorthostatic hypokinesia: head-down tilt effects on water and salt excretion. J Appl Physiol 49: 576-582, 1980.
13. Dorfman TA, Levine BD, Tillery T, Peshock RM, Hastings JL, Schneider SM, Macias BR, Biolo G, Hargens AR. Cardiac atrophy in women following bed rest. J Appl Physiol (1985) 103: 8-16, 2007.
14. 2O to study the influence of feeding on protein synthesis: effect of isotope equilibration in vivo vs. in cell culture. Am J Physiol Endocrinol Metab 288: E1277-E1283, 2005.
15. Flakoll PJ, Zheng M, Vaughan S, Borel MJ. Determination of stable isotopic enrichment and concentration of glycerol in plasma via gas chromatography-mass spectrometry for the estimation of lipolysis in vivo. J Chromatogr B Biomed Sci Appl 744: 47-54, 2000.
16. Goldspink DF, Morton AJ, Loughna P, Goldspink G. The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat. Pflügers Arch 407: 333-340, 1986.
17. Hilder TL, Baer LA, Fuller PM, Fuller CA, Grindeland RE, Wade CE, Graves LM. Insulin-independent pathways mediating glucose uptake in hindlimb-suspended skeletal muscle. J Appl Physiol 99: 2181-2188, 2005.
18. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287: C834-C843, 2004.
19. Jaspers SR, Henriksen EJ, Satarug S, Tischler ME. Effects of stretching and disuse on amino acids in muscles of rat hind limbs. Metabolism 38: 303-310, 1989.
20. Kasumov T, Willard B, Li L, Li M, Conger H, Buffa JA, Previs S, McCullough A, Hazen SL, Smith JD. 2H2O-based high-density lipoprotein turnover method for the assessment of dynamic high-density lipoprotein function in mice. Arterioscler Thromb Vasc Biol 33: 1994-2003, 2013.
21. 2O: advantage of isotope fractionation during gas chromatography. Am J Physiol Endocrinol Metab 284: E1043-E1048, 2003.
22. Lane HW, Gretebeck RJ, Schoeller DA, Davis-Street J, Socki RA, Gibson EK. Comparison of ground-based and space flight energy expenditure and water turnover in middle-aged healthy male US astronauts. Am J Clin Nutr 65: 4-12, 1997.
23. Lane HW, Gretebeck RJ, Smith SM. Nutrition, endocrinology, and body composition during space flight. Nutr Res 18: 1923-1934, 1998.
24. Leach CS, Leonard JI, Rambaut PC. Dynamics of weight loss during prolonged spaceflight. Physiologist 22: S61-S62, 1979.
25. Leonard JI, Leach CS, Rambaut PC. Quantitation of tissue loss during prolonged space flight. Am J Clin Nutr 38: 667-679, 1983.
26. 2O metabolic labeling. Mol Cell Proteomics 11: M111, 2012.
27. Loughna P, Goldspink G, Goldspink DF. Effect of inactivity and passive stretch on protein turnover in phasic and postural rat muscles. J Appl Physiol (1985) 61: 173-179, 1986.
28. Morey-Holton E, Globus RK, Kaplansky A, Durnova G. The hindlimb unloading rat model: literature overview, technique update and comparison with space flight data. Adv Space Biol Med 10: 7-40, 2005.
29. Morey-Holton ER, Globus RK. Hindlimb unloading of growing rats: a model for predicting skeletal changes during space flight. Bone 22: 83S-88S, 1998.
30. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92: 1367-1377, 2002.
31. Musacchia XJ, Deavers D, Meininger GA, Davis TP. A model for hypokinesia: effects on muscle atrophy in the rat. J Appl Physiol 48: 479-486, 1980.
32. Park E, Schultz E. A simple hindlimb suspension apparatus. Aviat Space Environ Med 64: 401-404, 1993.
33. Passonneau J, Lowry O. Enzymatic Analysis. A Practical Guide. Totowa, NJ: Humana, 1993.
34. Perhonen MA, Franco F, Lane LD, Buckey JC, Blomqvist CG, Zerwekh JE, Peshock RM, Weatherall PT, Levine BD. Cardiac atrophy after bed rest and spaceflight. J Appl Physiol (1985) 91: 645-653, 2001.
35. Pfleiderer G, Grein W, Wieland T. Specific determination of L-alanine and L-glutamine by means of glutamic-pyruvic transaminase. Ann Acad Sci Fenn A 60: 381-388, 1955.
36. 2O: application to patients with end-stage renal disease. Am J Physiol Endocrinol Metab 286: E665-E672, 2004.
37. Ray CA, Vasques M, Miller TA, Wilkerson MK, Delp MD. Effect of short-term microgravity and long-term hindlimb unloading on rat cardiac mass and function. J Appl Physiol 91: 1207-1213, 2001.
38. Speakman JR. Doubly Labeled Water. Theory and Practice. London: Chapman and Hall, 1997.
39. Speakman JR. The history and theory of the doubly labeled water technique. Am J Clin Nutr 68: 932S-938S, 1998.
40. Speakman JR, Racey PA. Measurement of CO2 production by the doubly labeled water technique. J Appl Physiol 61: 1200-1202, 1986.
41. Steffen JM, Musacchia XJ. Disuse atrophy, plasma corticosterone, and muscle glucocorticoid receptor levels. Aviat Space Environ Med 58: 996-1000, 1987.
42. Stein TP, Leskiw MJ, Schluter MD, Hoyt RW, Lane HW, Gretebeck RE, LeBlanc AD. Energy expenditure and balance during spaceflight on the space shuttle. Am J Physiol Regul Integr Comp Physiol 276: R1739-R1748, 1999.
43. Stein TP, Wade CE. Protein turnover in atrophying muscle: from nutritional intervention to microarray expression analysis. Curr Opin Clin Nutr Metab Care 6: 95-102, 2003.
44. Stein TP, Wade CE. Metabolic consequences of muscle disuse atrophy. J Nutr 135: 1824S-1828S, 2005.
45. Tada O, Yokogoshi H. Effect of different dietary protein composition on skeletal muscle atrophy by suspension hypokinesia/hypodynamia in rats. J Nutr Sci Vitaminol (Tokyo) 48: 115-119, 2002.
46. Taillandier D, Bigard X, Desplanches D, Attaix D, Guezennec CY, Arnal M. Role of protein intake on protein synthesis and fiber distribution in the unweighted soleus muscle. J Appl Physiol 75: 1226-1232, 1993.
47. Taillandier D, Guezennec CY, Patureau-Mirand P, Bigard X, Arnal M, Attaix D. A high protein diet does not improve protein synthesis in the nonweight-bearing rat tibialis anterior muscle. J Nutr 126: 266-272, 1996.
48. Thomason DB, Biggs RB, Booth FW. Protein metabolism and betamyosin heavy-chain mRNA in unweighted soleus muscle. Am J Physiol Regul Integr Comp Physiol 257: R300-R305, 1989.
49. Thomason DB, Booth FW. Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68: 1-12, 1990.
50. Thomason DB, Herrick RE, Surdyka D, Baldwin KM. Time course of soleus muscle myosin expression during hindlimb suspension and recovery. J Appl Physiol 63: 130-137, 1987.
51. Tischler ME, Jaspers SR, Henriksen EJ, Jacob S. Responses of skeletal muscle to unloading-a review. Physiologist 28: S13-S16, 1985.
52. Wang D, Liem DA, Lau E, Ng DC, Bleakley BJ, Cadeiras M, Deng MC, Lam MP, Ping P. Characterization of human plasma proteome dynamics using deuterium oxide. Proteomics Clin Appl 8: 610-619, 2014.
53. 2 max of nontrained and trained rats. J Appl Physiol 74: 1941-1947, 1993.
54. Zderic TW, Hamilton MT. Physical inactivity amplifies the sensitivity of skeletal muscle to the lipid-induced downregulation of lipoprotein lipase activity. J Appl Physiol 100: 249-257, 2006.