Costamere remodeling with muscle loading and unloading in healthy young men

Journal of Anatomy

Volumn 223, Issue 5, 2013, Pages 525-536

  Li, Ruowei ^a   Narici, Marco V ^a,b   Erskine, Robert M ^a,c   Seynnes, Olivier R ^a,d   Rittweger, Jörn ^a,e   Pišot, Rado ^f   Šimunič, Boštjan ^f   Flück, Martin ^a,g  

^a MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^d NORWEGIAN SCHOOL OF SPORT SCIENCES   (Norway)

^e German Aerospace   (Germany)

^f UNIVERSITY OF PRIMORSKA   (Slovenia)

^g UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Atrophy; Focal adhesion kinase; Human; Hypertrophy; Load; Muscle; Myofibril; Vinculin

Indexed keywords

BETA1 INTEGRIN; FOCAL ADHESION KINASE; GAMMA VINCULIN; METAVINCULIN; MYOSIN HEAVY CHAIN; UNCLASSIFIED DRUG; VINCULIN;

ADULT; ARTICLE; BED REST; CLINICAL ARTICLE; CONTROLLED STUDY; COSTAMERE; HUMAN; HUMAN TISSUE; MALE; MUSCLE CELL; MUSCLE MASS; MUSCLE THICKNESS; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; RESISTANCE TRAINING; SARCOLEMMA; VASTUS LATERALIS MUSCLE;

ATROPHY; FOCAL ADHESION KINASE; HUMAN; HYPERTROPHY; LOAD; MUSCLE; MYOFIBRIL; VINCULIN;

ADULT; ANALYSIS OF VARIANCE; COSTAMERES; CYTOSKELETAL PROTEINS; EXERCISE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MALE; MUSCLE FIBERS, SKELETAL; QUADRICEPS MUSCLE; REST; YOUNG ADULT;

EID: 84885424359     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12101     Document Type: Article

References (62)

1. Adams GR, Caiozzo VJ, Baldwin KM (2003) Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol 95, 2185-2201.
2. Aikawa R, Nagai T, Kudoh S, et al. (2002) Integrins play a critical role in mechanical stress-induced p38 MAPK activation. Hypertension 39, 233-238.
3. Anastasi G, Cutroneo G, Santoro G, et al. (2008) Costameric proteins in human skeletal muscle during muscular inactivity. J Anat 213, 284-295.
4. Baar K, Esser K (1999) Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol 276, C120-C127.
5. Barton ER (2006) Impact of sarcoglycan complex on mechanical signal transduction in murine skeletal muscle. Am J Physiol Cell Physiol 290, C411-C419.
6. Baum O, Planitzer G, Richter H, et al. (2000) Irregular costameres represent nitric oxide synthase-1-positive sarcolemma invaginations enriched in contracted skeletal muscle fibres. Histochem J 32, 743-751.
7. Bloomfield SA (1997) Changes in musculoskeletal structure and function with prolonged bed rest. Med Sci Sports Exerc 29, 197-206.
8. de Boer MD, Maganaris CN, Seynnes OR, et al. (2007a) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583, 1079-1091.
9. de Boer MD, Selby A, Atherton P, et al. (2007b) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585, 241-251.
10. Borina E, Pellegrino MA, D'Antona G, et al. (2010) Myosin and actin content of human skeletal muscle fibers following 35 days bed rest. Scand J Med Sci Sports 20, 65-73.
11. Bozyczko D, Decker C, Muschler J, et al. (1989) Integrin on developing and adult skeletal muscle. Exp Cell Res 183, 72-91.
12. Carter A, Flueck M (2012) A polymerase chain reaction-based methodology to detect gene doping. Eur J Appl Physiol 112, 1527-1536.
13. Chopard A, Pons F, Marini JF (2002) Vinculin and meta-vinculin in fast and slow rat skeletal muscle before and after hindlimb suspension. Pflugers Arch 444, 627-633.
14. Chopard A, Arrighi N, Carnino A, et al. (2005) Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long-term bedrest with or without exercise. Faseb J 19, 1722-1724.
15. Chopard A, Hillock S, Jasmin BJ (2009) Molecular events and signalling pathways involved in skeletal muscle disuse-induced atrophy and the impact of countermeasures. J Cell Mol Med 13, 3032-3050.
16. Coffey VG, Zhong Z, Shield A, et al. (2006) Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. Faseb J 20, 190-192.
17. Dumbauld DW, Shin H, Gallant ND, et al. (2010) Contractility modulates cell adhesion strengthening through focal adhesion kinase and assembly of vinculin-containing focal adhesions. J Cell Physiol 223, 746-756.
18. Durieux AC, D'Antona G, Desplanches D, et al. (2009) Focal adhesion kinase is a load-dependent governor of the slow contractile and oxidative muscle phenotype. J Physiol 587, 3703-3717.
19. Erskine RM, Jones DA, Maganaris CN, et al. (2009) In vivo specific tension of the human quadriceps femoris muscle. Eur J Appl Physiol 106, 827-838.
20. Ervasti JM (2003) Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278, 13591-13594.
21. Evans M, Morine K, Kulkarni C, et al. (2008) Expression profiling reveals heightened apoptosis and supports fiber size economy in the murine muscles of mastication. Physiol Genomics 35, 86-95.
22. Ferrando AA, Stuart CA, Brunder DG, et al. (1995) Magnetic resonance imaging quantitation of changes in muscle volume during 7 days of strict bed rest. Av Space Environ Med 66, 976-981.
23. Fitts RH, Riley DR, Widrick JJ (2001) Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204, 3201-3208.
24. Fluck M, Carson JA, Gordon SE, et al. (1999) Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am J Physiol Cell Physiol 277, C152-C162.
25. Fluck M, Ziemiecki A, Billeter R, et al. (2002) Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration. J Exp Biol 205, 2337-2348.
26. Fluck M, Chiquet M, Schmutz S, et al. (2003) Reloading of atrophied rat soleus muscle induces tenascin-C expression around damaged muscle fibers. Am J Physiol 284, R792-R801.
27. Flueck M, Goldspink G (2010) Point: Counterpoint "IGF is not the major physiological regulator of muscle mass". J Appl Physiol 108:1823-1824 and 1833 .
28. Flueck M, Eyeang-Bekale N, Heraud A, et al. (2011) Load-sensitive adhesion factor expression in the elderly with skiing: relation to fiber type and muscle strength. Scand J Med Sci Sports 21(Suppl), 29-38.
29. Fry AC (2004) The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 34, 663-679.
30. Gordon SE, Fluck M, Booth FW (2001) Selected contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J Appl Physiol 90, 1174-1183.
31. Grounds MD, Sorokin L, White J (2005) Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 15, 381-391.
32. Gullberg D, Velling T, Lohikangas L, et al. (1998) Integrins during muscle development and in muscular dystrophies. Front Biosci 3, D1039-D1050.
33. Hackney KJ, Ploutz-Snyder LL (2012) Unilateral lower limb suspension: integrative physiological knowledge from the past 20 years (1991-2011). Eur J Appl Physiol 112, 9-22.
34. Huijing PA (1999) Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J Biomech 32, 329-345.
35. Ilic D, Furuta Y, Kanazawa S, et al. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 388, 539-544.
36. Klossner S, Durieux AC, Freyssenet D, et al. (2009) Mechano-transduction to muscle protein synthesis is modulated by FAK. Eur J Appl Physiol 106, 389-398.
37. Konieczny P, Fuchs P, Reipert S, et al. (2008) Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J Cell Biol 181, 667-681.
38. Lal H, Verma SK, Smith M, et al. (2007) Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta1-integrin and focal adhesion kinase. J Mol Cell Cardiol 43, 137-147.
39. Li S, Kim M, Hu YL, et al. (1997) Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J Biol Chem 272, 30455-30462.
40. Loughna P, Goldspink G, Goldspink DF (1986) Effect of inactivity and passive stretch on protein turnover in phasic and postural rat muscles. J Appl Physiol 61, 173-179.
41. Luthi JM, Howald H, Claassen H, et al. (1986) Structural changes in skeletal muscle tissue with heavy-resistance exercise. Int J Sports Med 7, 123-127.
42. McCarthy JJ, Esser KA (2010) Anabolic and catabolic pathways regulating skeletal muscle mass. Cur Op Clin Nutr Metab Care 13, 230-235.
43. Miyamoto S, Teramoto H, Coso OA, et al. (1995) Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131, 791-805.
44. Narici MV, Maganaris CN (2007) Plasticity of the muscle-tendon complex with disuse and aging. Exerc Sport Sci Rev 35, 126-134.
45. Pardo JV, Siliciano JD, Craig SW (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 80, 1008-1012.
46. Quach NL, Rando TA (2006) Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev Biol 293, 38-52.
47. Ramaswamy KS, Palmer ML, van der Meulen JH, et al. (2011) Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats. J Physiol 589, 1195-1208.
48. Salanova M, Schiffl G, Puttmann B, et al. (2008) Molecular biomarkers monitoring human skeletal muscle fibres and microvasculature following long-term bed rest with and without countermeasures. J Anat 212, 306-318.
49. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1, 4.
50. Schlaepfer DD, Hauck CR, Sieg DJ (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71, 435-478.
51. Schlaepfer DD, Mitra SK, Ilic D (2004) Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 1692, 77-102.
52. Schröder R, Mundegar R, Treusch M, et al. (1997) Altered distribution of plectin/HD1 in dystrophinopathies. Eur J Cell Biol 74, 165-171.
53. Seynnes OR, de Boer M, Narici MV (2007) Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 102, 368-373.
54. Shear CR, Bloch RJ (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J Cell Biol 101, 240-256.
55. Terzis G, Georgiadis G, Stratakos G, et al. (2008) Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects. Eur J Appl Physiol 102, 145-152.
56. Thoss F, Dietrich F, Punkt K, et al. (2013) Metavinculin: new insights into functional properties of a muscle adhesion protein. Biochem Biophys Res Commun 430, 7-13.
57. Torsoni AS, Constancio SS, Nadruz W Jr, et al. (2003) Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ Res 93, 140-147.
58. Trimarchi F, Favaloro A, Fulle S, et al. (2006) Culture of human skeletal muscle myoblasts: timing appearance and localization of dystrophin-glycoprotein complex and vinculin-talin-integrin complex. Cells Tissues Organs 183, 87-98.
59. West DW, Burd NA, Tang JE, et al. (2010) Elevations in ostensibly anabolic hormones with resistance exercise enhance neither training-induced muscle hypertrophy nor strength of the elbow flexors. J Appl Physiol 108, 60-67.
60. Wilkinson SB, Phillips SM, Atherton PJ, et al. (2008) Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586, 3701-3717.
61. Williams M, Resneck W, Bloch R (2000) Membrane skeleton of innervated and denervated fast- and slow-twitch muscle. Muscle Nerve 23, 590-599.
62. Williamson DL, Gallagher PM, Carroll CC, et al. (2001) Reduction in hybrid single muscle fiber proportions with resistance training in humans. J Appl Physiol 91, 1955-1961.