Epigallocatechin-3-gallate improves plantaris muscle recovery after disuse in aged rats

Experimental Gerontology

Volumn 50, Issue 1, 2014, Pages 82-94

  Alway, Stephen E ^a   Bennett, Brian T ^a   Wilson, Joseph C ^a   Edens, Neile K ^b   Pereira, Suzette L ^b  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ABBOTT LABORATORIES   (United States)

Author keywords

Apoptosis; Catechin; Muscle atrophy; Muscle fiber area; Muscle function; Sarcopenia

Indexed keywords

EPIGALLOCATECHIN GALLATE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; PROTEIN BAX; TEAVIGO; UNCLASSIFIED DRUG; WATER;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FISCHER/BROWN NORWAY RAT; IMMOBILIZATION; INBRED RAT STRAIN; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE MASS; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; RAT; SENESCENCE; SOLEUS MUSCLE; STEM CELL;

APOPTOSIS; CATECHIN; MUSCLE ATROPHY; MUSCLE FIBER AREA; MUSCLE FUNCTION; SARCOPENIA;

AGING; ANIMALS; APOPTOSIS; BODY WEIGHT; CATECHIN; DRUG EVALUATION, PRECLINICAL; GLYCOGEN SYNTHASE KINASE 3; HINDLIMB SUSPENSION; ISOMETRIC CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUSCULAR ATROPHY; ORGAN SIZE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, INBRED BN; RATS, INBRED F344; SIGNAL TRANSDUCTION; STEM CELLS; WEIGHT-BEARING;

EID: 84890628188     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.11.011     Document Type: Article

References (68)

1. Adams G.R. Satellite cell proliferation and skeletal muscle hypertrophy. Appl. Physiol. Nutr. Metab. 2006, 31:782-790.
2. Alway S.E. Force and contractile characteristics after stretch overload in quail anterior latissimus dorsi muscle. J. Appl. Physiol. 1994, 77:135-141.
3. Alway S.E. Attenuation of Ca(2+)-activated ATPase and shortening velocity in hypertrophied fast twitch skeletal muscle from aged Japanese quail. Exp. Gerontol. 2002, 37:665-678.
4. Alway S.E., Siu P.M. Nuclear apoptosis contributes to sarcopenia. Exerc. Sport Sci. Rev. 2008, 36:51-57.
5. Alway S.E., Lowe D.A., Chen K.D. The effects of age and hindlimb suspension on the levels of expression of the myogenic regulatory factors MyoD and myogenin in rat fast and slow skeletal muscles. Exp. Physiol. 2001, 86:509-517.
6. Alway S.E., Martyn J.K., Ouyang J., Chaudhrai A., Murlasits Z.S. Id2 expression during apoptosis and satellite cell activation in unloaded and loaded quail skeletal muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 284:R540-R549.
7. Andrianjafiniony T., Dupre-Aucouturier S., Letexier D., Couchoux H., Desplanches D. Oxidative stress, apoptosis, and proteolysis in skeletal muscle repair after unloading. Am. J. Physiol. Cell Physiol. 2010, 299:C307-C315.
8. Bellinger A.M., Mongillo M., Marks A.R. Stressed out: the skeletal muscle ryanodine receptor as a target of stress. J. Clin. Invest. 2008, 118:445-453.
9. Bruusgaard J.C., Egner I.M., Larsen T.K., Dupre-Aucouturier S., Desplanches D., Gundersen K. No change in myonuclear number during muscle unloading and reloading. J. Appl. Physiol. 2012, 113:290-296. (1985.).
10. Chen K.D., Alway S.E. A physiological level of clenbuterol does not prevent atrophy or loss of force in skeletal muscle of old rats. J. Appl. Physiol. 2000, 89:606-612.
11. Clifford M.N., van der Hooft J.J., Crozier A. Human studies on the absorption, distribution, metabolism, and excretion of tea polyphenols. Am. J. Clin. Nutr. 2013, 98:1619S-1630S. (1985.).
12. Cutlip R.G., Stauber W.T., Willison R.H., McIntosh T.A., Means K.H. Dynamometer for rat plantar flexor muscles in vivo. Med. Biol. Eng. Comput. 1997, 35:540-543.
13. Degens H. The role of systemic inflammation in age-related muscle weakness and wasting. Scand. J. Med. Sci. Sports 2010, 20:28-38.
14. Deschenes M.R., Britt A.A., Chandler W.C. A comparison of the effects of unloading in young adult and aged skeletal muscle. Med. Sci. Sports Exerc. 2001, 33:1477-1483.
15. El H.M., Jean E., Turki A., Hugon G., Vernus B., Bonnieu A., Passerieux E., Hamade A., Mercier J., Laoudj-Chenivesse D., Carnac G. Glutathione peroxidase 3, a new retinoid target gene, is crucial for human skeletal muscle precursor cell survival. J. Cell Sci. 2012, 125:6147-6156.
16. Fulle S., Di D.S., Puglielli C., Pietrangelo T., Beccafico S., Bellomo R., Protasi F., Fano G. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp. Gerontol. 2005, 40:189-197.
17. Gallegly J.C., Turesky N.A., Strotman B.A., Gurley C.M., Peterson C.A., Dupont-Versteegden E.E. Satellite cell regulation of muscle mass is altered at old age. J. Appl. Physiol. 2004, 97:1082-1090.
18. Gharaibeh B., Chun-Lansinger Y., Hagen T., Ingham S.J., Wright V., Fu F., Huard J. Biological approaches to improve skeletal muscle healing after injury and disease. Birth Defects Res. C Embryo. Today 2012, 96:82-94.
19. Haddad F., Adams G.R. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J. Appl. Physiol. 2006, 100:1188-1203.
20. Hao Y., Jackson J.R., Wang Y., Edens N., Pereira S.L., Alway S.E. Beta-hydroxy-beta-methylbutyrate reduces myonuclear apoptosis during recovery from hind limb suspension-induced muscle fiber atrophy in aged rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:R701-R715.
21. Haramizu S., Ota N., Hase T., Murase T. Catechins attenuate eccentric exercise-induced inflammation and loss of force production in muscle in senescence-accelerated mice. J. Appl. Physiol. 2011, 111:1654-1663.
22. Hikida R.S. Aging changes in satellite cells and their functions. Curr. Aging Sci. 2011, 4:279-297.
23. Jackson J.R., Ryan M.J., Hao Y., Alway S.E. Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R1572-R1581.
24. Jackson J.R., Ryan M.J., Alway S.E. Long-term supplementation with resveratrol alleviates oxidative stress but does not attenuate sarcopenia in aged mice. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:751-764.
25. Kawano F., Takeno Y., Nakai N., Higo Y., Terada M., Ohira T., Nonaka I., Ohira Y. Essential role of satellite cells in the growth of rat soleus muscle fibers. Am. J. Physiol. Cell Physiol. 2008, 295:C458-C467.
26. Kim A., Chiu A., Barone M.K., Avino D., Wang F., Coleman C.I., Phung O.J. Green tea catechins decrease total and low-density lipoprotein cholesterol: a systematic review and meta-analysis. J. Am. Diet. Assoc. 2011, 111:1720-1729.
27. Kinnard R.S., Mylabathula D.B., Uddemarri S., Rice K.M., Wright G.L., Blough E.R. Regulation of p70S6k, GSK-3beta, and calcineurin in rat striated muscle during aging. Biogerontology 2005, 6:173-184.
28. Kortebein P., Symons T.B., Ferrando A., Paddon-Jones D., Ronsen O., Protas E., Conger S., Lombeida J., Wolfe R., Evans W.J. Functional impact of 10days of bed rest in healthy older adults. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:1076-1081.
29. Lawler J.M., Song W., Demaree S.R. Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic. Biol. Med. 2003, 35:9-16.
30. Lawler J.M., Kwak H.B., Kim J.H., Lee Y., Hord J.M., Martinez D.A. biphasic stress response in the soleus during reloading following hindlimb unloading. Med. Sci. Sports Exerc. 2012, 44:600-609.
31. Marzetti E., Hwang J.C., Lees H.A., Wohlgemuth S.E., Dupont-Versteegden E.E., Carter C.S., Bernabei R., Leeuwenburgh C. Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy. Biochim. Biophys. Acta 2010, 1800:235-244.
32. Miyazaki M., Hitomi Y., Kizaki T., Ohno H., Katsumura T., Haga S., Takemasa T. Calcineurin-mediated slow-type fiber expression and growth in reloading condition. Med. Sci. Sports Exerc. 2006, 38:1065-1072.
33. Mozdziak P.E., Pulvermacher P.M., Schultz E. Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading. J. Appl. Physiol. 2001, 91:183-190.
34. Murlasits Z., Cutlip R.G., Geronilla K.B., Rao K.M., Wonderlin W.F., Alway S.E. Resistance training increases heat shock protein levels in skeletal muscle of young and old rats. Exp. Gerontol. 2006, 41:398-406.
35. Myburgh K.H., Kruger M.J., Smith C. Accelerated skeletal muscle recovery after in vivo polyphenol administration. J. Nutr. Biochem. 2012, 23:1072-1079.
36. Oishi Y., Ogata T., Yamamoto K.I., Terada M., Ohira T., Ohira Y., Taniguchi K., Roy R.R. Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiol. (Oxf.) 2008, 192:381-395.
37. O'Leary M.F., Vainshtein A., Carter H.N., Zhang Y., Hood D.A. Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals. Am. J. Physiol. Cell Physiol. 2012, 303:C447-C454.
38. O'Leary M.F., Vainshtein A., Iqbal S., Ostojic O., Hood D.A. Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle. Am. J. Physiol. Cell Physiol. 2013, 304:C422-C430.
39. Ota N., Soga S., Haramizu S., Yokoi Y., Hase T., Murase T. Tea catechins prevent contractile dysfunction in unloaded murine soleus muscle: a pilot study. Nutrition 2011, 27:955-959.
40. Pae M., Wu D. Immunomodulating effects of epigallocatechin-3-gallate from green tea: mechanisms and applications. Food Funct. 2013, 4:1287-1303.
41. Pae M., Ren Z., Meydani M., Shang F., Smith D., Meydani S.N., Wu D. Dietary supplementation with high dose of epigallocatechin-3-gallate promotes inflammatory response in mice. J. Nutr. Biochem. 2012, 23:526-531.
42. Pellegrino M.A., Desaphy J.F., Brocca L., Pierno S., Camerino D.C., Bottinelli R. Redox homeostasis, oxidative stress and disuse muscle atrophy. J. Physiol. 2011, 589:2147-2160.
43. Peterson J.M., Bryner R., Alway S.E. Satellite cell proliferation is reduced in muscles of obese Zucker rats, but restored with loading. Am. J. Physiol. Cell Physiol. 2008, 295:C521-C528.
44. Pistilli E.E., Siu P.M., Alway S.E. Molecular regulation of apoptosis in fast plantaris muscles of aged rats. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:245-255.
45. Pistilli E.E., Siu P.M., Alway S.E. Interleukin-15 responses to aging and unloading-induced skeletal muscle atrophy. Am. J. Physiol. Cell Physiol. 2007, 292:C1298-C1304.
46. Quadrilatero J., Alway S.E., Dupont-Versteegden E.E. Skeletal muscle apoptotic response to physical activity: potential mechanisms for protection. Appl. Physiol. Nutr. Metab. 2011, 36:608-617.
47. Ryan M.J., Dudash H.J., Docherty M., Geronilla K.B., Baker B.A., Cutlip R.G., Alway S.E. Aging-dependent regulation of antioxidant enzymes and redox status in chronically loaded rat dorsiflexor muscles. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:1015-1026.
48. Shefer G., Rauner G., Stuelsatz P., Benayahu D., Yablonka-Reuveni Z. Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice. FEBS J. 2013, 280:4063-4073.
49. Siu P.M., Alway S.E. Deficiency of the Bax gene attenuates denervation-induced apoptosis. Apoptosis 2006, 11:967-981.
50. Siu P.M., Pistilli E.E., Alway S.E. Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1015-R1026.
51. Siu P.M., Pistilli E.E., Butler D.C., Alway S.E. Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am. J. Physiol. Cell Physiol. 2005, 288:C338-C349.
52. Siu P.M., Pistilli E.E., Murlasits Z., Alway S.E. Hindlimb unloading increases muscle content of cytosolic but not nuclear Id2 and p53 proteins in young adult and aged rats. J. Appl. Physiol. 2006, 100:907-916.
53. Siu P.M., Pistilli E.E., Alway S.E. Age-dependent increase in oxidative stress in gastrocnemius muscle with unloading. J. Appl. Physiol. 2008, 105:1695-1705.
54. 2-mediated oxidative stress in differentiated C2C12 myotubes. Life Sci. 2009, 84:468-481.
55. Sugiura T., Abe N., Nagano M., Goto K., Sakuma K., Naito H., Yoshioka T., Powers S.K. Changes in PKB/Akt and calcineurin signaling during recovery in atrophied soleus muscle induced by unloading. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R1273-R1278.
56. Teng B.T., Tam E.W., Benzie I.F., Siu P.M. Protective effect of caspase inhibition on compression-induced muscle damage. J. Physiol. 2011, 589:3349-3369.
57. Urish K.L., Vella J.B., Okada M., Deasy B.M., Tobita K., Keller B.B., Cao B., Piganelli J.D., Huard J. Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol. Biol. Cell 2009, 20:509-520.
58. van der Meer S.F., Jaspers R.T., Jones D.A., Degens H. The time course of myonuclear accretion during hypertrophy in young adult and older rat plantaris muscle. Ann. Anat. 2011, 193:56-63.
59. van der Meer S.F., Jaspers R.T., Jones D.A., Degens H. Time-course of changes in the myonuclear domain during denervation in young-adult and old rat gastrocnemius muscle. Muscle Nerve 2011, 43:212-222.
60. van der Velden J.L., Langen R.C., Kelders M.C., Willems J., Wouters E.F., Janssen-Heininger Y.M., Schols A.M. Myogenic differentiation during regrowth of atrophied skeletal muscle is associated with inactivation of GSK-3beta. Am. J. Physiol. Cell Physiol. 2007, 292:C1636-C1644.
61. Verhees K.J., Schols A.M., Kelders M.C., Op den Kamp C.M., van der Velden J.L., Langen R.C. Glycogen synthase kinase-3beta is required for the induction of skeletal muscle atrophy. Am. J. Physiol. Cell Physiol. 2011, 301:C995-C1007.
62. Verhees K.J., Pansters N.A., Schols A.M., Langen R.C. Regulation of skeletal muscle plasticity by glycogen synthase kinase-3beta: a potential target for the treatment of muscle wasting. Curr. Pharm. Des. 2013, 19:3276-3298.
63. Wilson G.J., Wilson J.M., Manninen A.H. Effects of beta-hydroxy-beta-methylbutyrate (HMB) on exercise performance and body composition across varying levels of age, sex, and training experience: a review. Nutr. Metab. (Lond.) 2008, 5:1-17.
64. Wohlgemuth S.E., Seo A.Y., Marzetti E., Lees H.A., Leeuwenburgh C. Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp. Gerontol. 2010, 45:138-148.
65. Wu M., Falasca M., Blough E.R. Akt/protein kinase B in skeletal muscle physiology and pathology. J. Cell. Physiol. 2011, 226:29-36.
66. Wust R.C., Degens H. Factors contributing to muscle wasting and dysfunction in COPD patients. Int. J. Chron. Obstruct. Pulmon. Dis. 2007, 2:289-300.
67. Zarzhevsky N., Carmeli E., Fuchs D., Coleman R., Stein H., Reznick A.Z. Recovery of muscles of old rats after hindlimb immobilisation by external fixation is impaired compared with those of young rats. Exp. Gerontol. 2001, 36:125-140.
68. Zhu S., Nagashima M., Khan M.A., Yasuhara S., Kaneki M., Martyn J.A. Lack of caspase-3 attenuates immobilization-induced muscle atrophy and loss of tension generation along with mitigation of apoptosis and inflammation. Muscle Nerve 2013, 47:711-721.