Modelling in vivo skeletal muscle ageing in vitro using three-dimensional bioengineered constructs

Aging Cell

Volumn 11, Issue 6, 2012, Pages 986-995

  Sharples, Adam P ^a,b   Player, Darren J ^a,b   Martin, Neil R W ^a,b   Mudera, Vivek ^d   Stewart, Claire E ^c   Lewis, Mark P ^a,b,e,f  

^a UNIVERSITY OF BEDFORDSHIRE   (United Kingdom)

^b LOUGHBOROUGH UNIVERSITY   (United Kingdom)

^c MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e CRANFIELD UNIVERSITY   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

IGF I; IGFBP; MRF; Myostatin; Satellite cell; TNF

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; GELATINASE A; GELATINASE B; GROWTH FACTOR; INSULIN LIKE GROWTH FACTOR 1 EA; MATRIX METALLOPROTEINASE; MECHANO GROWTH FACTOR; MESSENGER RNA; MYOSTATIN; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG;

AGED; ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOENGINEERING; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; ELECTROSTIMULATION; EXERCISE; EXTRACELLULAR MATRIX; FORCE; GENE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE ATROPHY; MUSCLE STRETCHING; MUSCLE TONE; MYOBLAST; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKELETAL MUSCLE;

AGED; AGING; ANIMALS; CELL DIFFERENTIATION; COLLAGEN TYPE I; GENE EXPRESSION REGULATION; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; MYOBLASTS; MYOSTATIN; SARCOPENIA; SOMATOMEDINS; TISSUE CULTURE TECHNIQUES; TISSUE ENGINEERING;

MURINAE;

EID: 84869188273     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2012.00869.x     Document Type: Article

References (61)

1. Al-Shanti N, Stewart CE (2008) PD98059 enhances C2 myoblast differentiation through p38 MAPK activation: a novel role for PD98059. J. Endocrinol.198, 243-252.
2. Barton-Davis ER, Shoturma DI, Musaro A, Rosenthal N, Sweeney HL (1998) Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc. Natl. Acad. Sci. U S A95, 15603-15607.
3. Beccafico S, Riuzzi F, Puglielli C, Mancinelli R, Fulle S, Sorci G, Donato R (2010) Human muscle satellite cells show age-related differential expression of S100B protein and RAGE. Age (Dordr)33, 523-541.
4. Benbassat CA, Maki KC, Unterman TG (1997) Circulating levels of insulin-like growth factor (IGF) binding protein-1 and -3 in aging men: relationships to insulin, glucose, IGF, and dehydroepiandrosterone sulfate levels and anthropometric measures. J. Clin. Endocrinol. Metab.82, 1484-1491.
5. Berkes CA, Tapscott SJ (2005) MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol.16, 585-595.
6. Bigot A, Jacquemin V, Debacq-Chainiaux F, Butler-Browne GS, Toussaint O, Furling D, Mouly V (2008) Replicative aging down-regulates the myogenic regulatory factors in human myoblasts. Biol. Cell100, 189-199.
7. Binkert C, Landwehr J, Mary JL, Schwander J, Heinrich G (1989) Cloning, sequence analysis and expression of a cDNA encoding a novel insulin-like growth factor binding protein (IGFBP-2). EMBO J.8, 2497-2502.
8. Blau HM, Pavlath GK, Hardeman EC, Chiu CP, Silberstein L, Webster SG, Miller SC, Webster C (1985) Plasticity of the differentiated state. Science230, 758-766.
9. Cheema U, Yang SY, Mudera V, Goldspink GG, Brown RA (2003) 3-D in vitro model of early skeletal muscle development. Cell Motil Cytoskeleton54, 226-236.
10. Cheema U, Brown R, Mudera V, Yang SY, McGrouther G, Goldspink G (2005) Mechanical signals and IGF-I gene splicing in vitro in relation to development of skeletal muscle. J. Cell. Physiol.202, 67-75.
11. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR (1997) The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem.272, 6653-6662.
12. Cruz-Jentoft AJ, Landi F, Topinkova E, Michel JP (2010) Understanding sarcopenia as a geriatric syndrome. Curr. Opin. Clin. Nutr. Metab. Care.13, 1-7.
13. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ (2005) Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. Faseb J19, 422-424.
14. Degens H, Erskine R, Morse CI (2009) Disproportionate changes in skeletal muscle strength and size with resistance training and ageing9, pp. 123-129.
15. Eastwood M, McGrouther DA, Brown RA (1994) A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix mechanical signalling. Biochim. Biophys. Acta1201, 186-192.
16. Edstrom E, Ulfhake B (2005) Sarcopenia is not due to lack of regenerative drive in senescent skeletal muscle. Aging Cell4, 65-77.
17. Ernst CW, McCusker RH, White ME (1992) Gene expression and secretion of insulin-like growth factor-binding proteins during myoblast differentiation. Endocrinology130, 607-615.
18. Ferri P, Barbieri E, Burattini S, Guescini M, D'Emilio A, Biagiotti L, Del Grande P, De Luca A, Stocchi V, Falcieri E (2009) Expression and subcellular localization of myogenic regulatory factors during the differentiation of skeletal muscle C2C12 myoblasts. J. Cell. Biochem.108, 1302-1317.
19. Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr. Rev.17, 481-517.
20. Gillies AR, Lieber RL (2011) Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve44, 318-331.
21. Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD (2003) Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J. Physiol.547, 247-254.
22. Hameed M, Lange KH, Andersen JL, Schjerling P, Kjaer M, Harridge SD, Goldspink G (2004) The effect of recombinant human growth hormone and resistance training on IGF-I mRNA expression in the muscles of elderly men. J. Physiol.555, 231-240.
23. Heron-Milhavet L, Mamaeva D, LeRoith D, Lamb NJ, Fernandez A (2010) Impaired muscle regeneration and myoblast differentiation in mice with a muscle-specific KO of IGF-IR. J. Cell. Physiol.225, 1-6.
24. Hidestrand M, Richards-Malcolm S, Gurley CM, Nolen G, Grimes B, Waterstrat A, Zant GV, Peterson CA (2008) Sca-1-expressing nonmyogenic cells contribute to fibrosis in aged skeletal muscle. J. Gerontol. A Biol. Sci. Med. Sci.63, 566-579.
25. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, Fiatarone Singh MA (2001) Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J. Gerontol. Series A Biol. Sci. Med. Sci.56, B209-B217.
26. Jacquemin V, Furling D, Bigot A, Butler-Browne GS, Mouly V (2004) IGF-1 induces human myotube hypertrophy by increasing cell recruitment. Exp. Cell Res.299, 148-158.
27. Leger B, Derave W, De Bock K, Hespel P, Russell AP (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res.11, 163-175B.
28. Lewis MP, Tippett HL, Sinanan AC, Morgan MJ, Hunt NP (2000) Gelatinase-B (matrix metalloproteinase-9; MMP-9) secretion is involved in the migratory phase of human and murine muscle cell cultures. J. Muscle Res. Cell Motil.21, 223-233.
29. Mauro A (1961) Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol.9, 493-495.
30. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R (2006) Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J. Cell. Physiol.209, 501-514.
31. McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. U S A94, 12457-12461.
32. Miyazaki M, McCarthy JJ, Fedele MJ, Esser KA (2011) Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J. Physiol.589, 1831-1846.
33. Morgan J, Rouche A, Bausero P, Houssaini A, Gross J, Fiszman MY, Alameddine HS (2010) MMP-9 overexpression improves myogenic cell migration and engraftment. Muscle Nerve42, 584-595.
34. Morse CI, Thom JM, Birch KM, Narici MV (2005a) Changes in triceps surae muscle architecture with sarcopenia. Acta Physiol. Scand.183, 291-298.
35. Morse CI, Thom JM, Reeves ND, Birch KM, Narici MV (2005b) In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J. Appl. Physiol.99, 1050-1055.
36. Mouly V, Aamiri A, Bigot A, Cooper RN, Di Donna S, Furling D, Gidaro T, Jacquemin V, Mamchaoui K, Negroni E, Perie S, Renault V, Silva-Barbosa SD, Butler-Browne GS (2005) The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy. Acta Physiol. Scand.184, 3-15.
37. Mu X, Urso ML, Murray K, Fu F, Li Y (2010) Relaxin regulates MMP expression and promotes satellite cell mobilization during muscle healing in both young and aged mice. Am. J. Pathol.177, 2399-2410.
38. Mudera V, Smith AS, Brady MA, Lewis MP (2010) The effect of cell density on the maturation and contractile ability of muscle derived cells in a 3D tissue-engineered skeletal muscle model and determination of the cellular and mechanical stimuli required for the synthesis of a postural phenotype. J. Cell. Physiol.225, 646-653.
39. O'Connor MS, Carlson ME, Conboy IM (2009) Differentiation rather than aging of muscle stem cells abolishes their telomerase activity. Biotechnol. Prog.25, 1130-1137.
40. Owino V, Yang SY, Goldspink G (2001) Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett.505, 259-263.
41. Pietrangelo T, Puglielli C, Mancinelli R, Beccafico S, Fano G, Fulle S (2009) Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp. Gerontol.44, 523-531.
42. Player DJ, Martin NRW, Castle PC, Sharples AP, Passey S, Mudera V, Lewis MP (2011) A putative model of endurance exercise using bio-engineered skeletal muscle. Proc. Physiol. Soc.23, PC333.
43. Quinn LS, Anderson BG, Plymate SR (2007) Muscle-specific overexpression of the type 1 IGF receptor results in myoblast-independent muscle hypertrophy via PI3K, and not calcineurin, signaling. Am. J. Physiol. Endocrinol. Metab.293, E1538-E1551.
44. Rantanen T, Harris T, Leveille SG, Visser M, Foley D, Masaki K, Guralnik JM (2000) Muscle strength and body mass index as long-term predictors of mortality in initially healthy men. J. Gerontol. A Biol. Sci. Med. Sci.55, M168-73.
45. Ratkevicius A, Joyson A, Selmer I, Dhanani T, Grierson C, Tommasi AM, DeVries A, Rauchhaus P, Crowther D, Alesci S, Yaworsky P, Gilbert F, Redpath TW, Brady J, Fearon KC, Reid DM, Greig CA, Wackerhage H (2011) Serum concentrations of myostatin and myostatin-interacting proteins do not differ between young and sarcopenic elderly men. J. Gerontol. A Biol. Sci. Med. Sci.66, 620-626.
46. Rosenberg IH (1997) Sarcopenia: origins and clinical relevance. J. Nutr.127 (5 Suppl), 990S-991S.
47. Russ DW, Lanza IR (2011) The impact of old age on skeletal muscle energetics: supply and demand. Curr. Aging Sci.4, 234-247.
48. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc.3, 1101-1108.
49. Sharples AP, Stewart CE (2011) Myoblast models of skeletal muscle hypertrophy and atrophy. Curr. Opin. Clin. Nutr. Metab. Care14, 230-236.
50. Sharples AP, Al-Shanti N, Stewart CE (2010) C2 and C2C12 murine skeletal myoblast models of atrophic and hypertrophic potential: relevance to disease and ageing?J. Cell. Physiol.225, 240-250.
51. Sharples AP, Al-Shanti N, Lewis MP, Stewart CE (2011) Reduction of myoblast differentiation following multiple population doublings in mouse C(2) C(12) cells: a model to investigate ageing?J. Cell. Biochem.112, 3773-3785.
52. Smith AS, Passey S, Greensmith L, Mudera V, Lewis MP (2011) Characterisation and optimisation of a simple, repeatable system for the long term in vitro culture of aligned myotubes in 3D. J. Cell. Biochem.113, 1044-1053.
53. Spangenburg EE, Le Roith D, Ward CW, Bodine SC (2008) A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy. J. Physiol.586, 283-291.
54. Stewart CE, Rotwein P (1996) Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol. Rev.76, 1005-1026.
55. Stewart CE, Newcomb PV, Holly JM (2004) Multifaceted roles of TNF-alpha in myoblast destruction: a multitude of signal transduction pathways. J. Cell. Physiol.198, 237-247.
56. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ (2009) Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am. J. Physiol. Cell Physiol.296, C1258-C1270.
57. Welle S, Bhatt K, Shah B, Thornton C (2002) Insulin-like growth factor-1 and myostatin mRNA expression in muscle: comparison between 62-77 and 21-31yr old men. Exp. Gerontol.37, 833-839.
58. Wheatcroft SB, Kearney MT (2009) IGF-dependent and IGF-independent actions of IGF-binding protein-1 and -2: implications for metabolic homeostasis. Trends Endocrinol. Metab.20, 153-162.
59. Whittemore LA, Song K, Li X, Aghajanian J, Davies M, Girgenrath S, Hill JJ, Jalenak M, Kelley P, Knight A, Maylor R, O'Hara D, Pearson A, Quazi A, Ryerson S, Tan XY, Tomkinson KN, Veldman GM, Widom A, Wright JF, Wudyka S, Zhao L, Wolfman NM (2003) Inhibition of myostatin in adult mice increases skeletal muscle mass and strength. Biochem. Biophys. Res. Commun.300, 965-971.
60. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature270, 725-727.
61. Yang SY, Goldspink G (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett.522, 156-160.