The worsening of tibialis anterior muscle atrophy during recovery post-immobilization correlates with enhanced connective tissue area, proteolysis, and apoptosis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 11, 2012, Pages

  Slimani, Lamia ^a,b   Micol, Didier ^c   Amat, Julien ^a,b   Delcros, Geoffrey ^a,b   Meunier, Bruno ^c   Taillandier, Daniel ^a,b   Polge, Cécile ^a,b   Béchet, Daniel ^a,b   Dardevet, Dominique ^a,b   Picard, Brigitte ^c   Attaix, Didier ^a,b   Listrat, Anne ^c   Combaret, Lydie ^a,b  

^a CEMAGREF   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c UMR1213 HERBIVORES   (France)

Author keywords

Caspase 9; Extracellular matrix remodeling; Matrix metalloproteases; Reloading; Ubiquitin proteasome proteolysis

Indexed keywords

APOPTOSOME; COLLAGEN TYPE 1; COLLAGEN TYPE 12; COLLAGEN TYPE 18; COLLAGEN TYPE 4; MESSENGER RNA; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN IIB; PEPTIDASE; PROTEASOME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAST APPLICATION; CAST REMOVAL; CATABOLISM; CONNECTIVE TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; HINDLIMB; IMMOBILIZATION; MALE; MUSCLE ATROPHY; MUSCLE RIGIDITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIBIALIS ANTERIOR MUSCLE;

ANIMALS; APOPTOSIS; COLLAGEN; CONNECTIVE TISSUE CELLS; IMMOBILIZATION; MALE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSIN HEAVY CHAINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; RNA, MESSENGER; TIME FACTORS; UBIQUITIN;

EID: 84870535998     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00379.2012     Document Type: Article

References (51)

1. Alway S, Martyn J, Ouyang J, Chaudhrai A, Murlasits Z. Id2 expression during apoptosis and satellite cell activation in unloaded and loaded quail skeletal muscles. Am J Physiol Regul Integr Comp Physiol 284: R540-R549, 2003.
2. 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 299: C307-C315, 2010.
3. Aszódi A, Legate KR, Nakchbandi I, Fässler R. What mouse mutants teach us about extracellular matrix function. Annu Rev Cell Dev Biol 22: 591-621, 2006.
4. Attaix D, Ventadour S, Codran A, Béchet D, Taillandier D, Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 41: 173-186, 2005.
5. Baldwin KM, Haddad F. Skeletal muscle plasticity: cellular and molecular responses to altered physical activity paradigms. Am J Phys Med Rehabil 81, 11 Suppl: S40-S51, 2002.
6. Berthon P, Duguez S, Favier F, Amirouche A, Feasson L, Vico L, Denis C, Freyssenet D. Regulation of ubiquitin-proteasome system, caspase enzyme activities, and extracellular proteinases in rat soleus muscle in response to unloading. Pflugers Arch 454: 625-633, 2007.
7. Bodine S, Latres E, Baumhueter S, Lai V, Nunez L, Clarke B, Poueymirou W, Panaro F, Na E, Dharmarajan K, Pan Z, Valenzuela D, DeChiara T, Stitt T, Yancopoulos G, Glass D. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
8. Booth F. Effect of limb immobilization on skeletal muscle. J Appl Physiol 52: 1113-1118, 1982.
9. Bornstein P, Sage E. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 14: 608-616, 2002.
10. Bruusgaard JC, Gundersen K. In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J Clin Invest 118: 1450-1457, 2008.
11. Cain K, Brown D, Langlais C, Cohen G. Caspase activation involves the formation of the aposome, a large (similar to 700 kDa) caspase-activating complex. J Biol Chem 274: 22686-22692, 1999.
12. Chargé SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84: 209-238, 2004.
13. Clarke B, Drujan D, Willis M, Murphy L, Corpina R, Burova E, Rakhilin S, Stitt T, Patterson C, Latres E, Glass D. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6: 376-385, 2007.
14. Cohen S, Brault J, Gygi S, Glass D, Valenzuela D, Gartner C, Latres E, Goldberg A. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185: 1083-1095, 2009.
15. Cornachione A, Cação-Benedini LO, Martinez EZ, Neder L, Cláudia Mattiello-Sverzut A. Effects of eccentric and concentric training on capillarization and myosin heavy chain contents in rat skeletal muscles after hindlimb suspension. Acta Histochem 113: 277-282, 2011.
16. Cornachione A, Cação-Benedini LO, Shimano MM, Volpon JB, Martinez EZ, Mattiello-Sverzut AC. Morphological comparison of different protocols of skeletal muscle remobilization in rats after hindlimb suspension. Scand J Med Sci Sports 18: 453-461, 2008.
17. Evans WJ. Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr 91: 1123S-1127S, 2010.
18. Fang C, Sun X, Li B, Fischer D, Pritts T, Penner G, Hasselgren P. Burn injuries in rats upregulate the gene expression of the ubiquitinconjugating enzyme E2(14k) in skeletal muscle. J Burn Care Rehabil 21: 528-534, 2000.
19. Flint F, Pickering K. Demonstration of collagen in meat-products by an improved picro-sirius red polarization method. Analyst 109: 1505-1506, 1984.
20. Fujita N, Fujimoto T, Tasaki H, Arakawa T, Matsubara T, Miki A. Influence of muscle length on muscle atrophy in the mouse tibialis anterior and soleus muscles. Biomed Res 30: 39-45, 2009.
21. Goldspink D. The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J Physiol 264: 267-282, 1977.
22. Guillot C, Steinberg J, Delliaux S, Kipson N, Jammes Y, Badier M. Physiological, histological and biochemical properties of rat skeletal muscles in response to hindlimb suspension. J Electromyogr Kinesiol 18: 276-283, 2008.
23. Gustafsson T, Osterlund T, Flanagan JN, von Waldén F, Trappe TA, Linnehan RM, Tesch PA. Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 109: 721-727, 2010.
24. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551, 2001.
25. Heng A, Ventadour S, Jarzaguet M, Pouch-Pelissier M, Guezennec C, Bigard X, Attaix D, Taillandier D. Coordinate expression of the 19S regulatory complex and evidence for ubiquitin-dependent telethonin degradation in the unloaded soleus muscle. Int J Biochem Cell Biol 40: 2544-2552, 2008.
26. Hughes SM, Blau HM. Migration of myoblasts across basal lamina during skeletal-muscle development. Nature 345: 350-353, 1990.
27. Järvinen TA, Józsa L, Kannus P, Järvinen TL, Järvinen M. Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles. An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil 23: 245-254, 2002.
28. Jones SW, Hill RJ, Krasney PA, O'Conner B, Peirce N, Greenhaff PL. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18: 1025-1027, 2004.
29. Józsa L, Kannus P, Thöring J, Reffy A, Järvinen M, Kvist M. The effect of tenotomy and immobilisation on intramuscular connective tissue. A morphometric and microscopic study in rat calf muscles. J Bone Joint Surg Br 72: 293-297, 1990.
30. Kalhovde JM, Jerkovic R, Sefland I, Cordonnier C, Calabria E, Schiaffino S, Lømo T. "Fast" and "slow" muscle fibres in hindlimb muscles of adult rats regenerate from intrinsically different satellite cells. J Physiol 562: 847-857, 2005.
31. Lang SM, Kazi AA, Hong-Brown L, Lang CH. Delayed recovery of skeletal muscle mass following hindlimb immobilization in mTOR heterozygous mice. PLoS One 7: e38910, 2012.
32. Lapier TK, Burton HW, Almon R, Cerny F. Alterations in intramuscular connective tissue after limb casting affect contraction-induced muscle injury. J Appl Physiol 78: 1065-1069, 1995.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 25: 402-408, 2001.
34. Magne H, Savary-Auzeloux I, Migné C, Peyron MA, Combaret L, Rémond D, Dardevet D. Contrarily to whey and high protein diets, dietary free leucine supplementation cannot reverse the lack of recovery of muscle mass after prolonged immobilization during ageing. J Physiol 590: 2035-2049, 2012.
35. Magne H, Savary-Auzeloux I, Vazeille E, Claustre A, Attaix D, Anne L, Sante-Lhoutellier V, Gatellier P, Dardevet D, Combaret L. Lack of muscle recovery after immobilization in old rats does not result from a defect in normalization of the ubiquitin-proteasome and the caspasedependent apoptotic pathways. J Physiol 589: 511-524, 2011.
36. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. Autophagy is required to maintain muscle mass. Cell Metab 10: 507-515, 2009.
37. Mattiello-Sverzut AC, Carvalho LC, Cornachione A, Nagashima M, Neder L, Shimano AC. Morphological effects of electrical stimulation and intermittent muscle stretch after immobilization in soleus muscle. Histol Histopathol 21: 957-964, 2006.
38. Mizunoya W, Wakamatsu J, Tatsumi R, Ikeuchi Y. Protocol for high-resolution separation of rodent myosin heavy chain isoforms in a mini-gel electrophoresis system. Anal Biochem 377: 111-113, 2008.
39. Ogata T, Machida S, Oishi Y, Higuchi M, Muraoka I. Differential cell death regulation between adult-unloaded and aged rat soleus muscle. Mech Ageing Dev 130: 328-336, 2009.
40. Polge C, Heng AE, Jarzaguet M, Ventadour S, Claustre A, Combaret L, Béchet D, Matondo M, Uttenweiler-Joseph S, Monsarrat B, Attaix D, Taillandier D. Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J 25: 3790-3802, 2011.
41. Reich KA, Chen YW, Thompson PD, Hoffman EP, Clarkson PM. Forty-eight hours of unloading and 24 h of reloading lead to changes in global gene expression patterns related to ubiquitination and oxidative stress in humans. J Appl Physiol 109: 1404-1415, 2010.
42. Rodriguez M, Schaper J. Apoptosis: measurement and technical issues. J Mol Cell Cardiol 38: 15-20, 2005.
43. Sandri M, Minetti C, Pedemonte M, Carraro U. Apoptotic myonuclei in human Duchenne muscular dystrophy. Lab Invest 78: 1005-1016, 1998.
44. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. Global quantification of mammalian gene expression control. Nature 473: 337-342, 2011.
45. 2+-activated and ATP-ubiquitindependent proteinases in the unweighted rat soleus muscle. Biochem J 316: 65-72, 1996.
46. Vazeille E, Codran A, Claustre A, Averous J, Listrat A, Béchet D, Taillandier D, Dardevet D, Attaix D, Combaret L. The ubiquitinproteasome and the mitochondria-associated apoptotic pathways are sequentially downregulated during recovery after immobilization-induced muscle atrophy. Am J Physiol Endocrinol Metab 295: E1181-E1190, 2008.
47. Vazeille E, Slimani L, Claustre A, Magne H, Labas R, Béchet D, Taillandier D, Dardevet D, Astruc T, Attaix D, Combaret L. Curcumin treatment prevents increased proteasome and apoptosome activities in rat skeletal muscle during reloading and improves subsequent recovery. J Nutr Biochem 23: 245-251, 2012.
48. Vescovo G, Zennaro R, Sandri M, Carraro U, Leprotti C, Ceconi C, Ambrosio GB, Dalla Libera L. Apoptosis of skeletal muscle myofibers and interstitial cells in experimental heart failure. J Mol Cell Cardiol 30: 2449-2459, 1998.
49. Willems ME, Miller GR, Stauber FD, Stauber WT. Effects of repeated lengthening contractions on skeletal muscle adaptations in female rats. J Physiol Sci 60: 143-150, 2010.
50. Zhong H, Roy R, Woo J, Kim J, Edgerton V. Differential modulation of myosin heavy chain phenotype in an inactive extensor and flexor muscle of adult rats. J Anat 210: 19-31, 2007.
51. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, Heintz N, Yue Z. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 11: 468-476, 2009.