The influence of serum-free culture conditions on skeletal muscle differentiation in a tissue-engineered model

Tissue Engineering - Part A.

Volumn 14, Issue 1, 2008, Pages 161-171

  Gawlitta, Debby ^a   Boonen, Kristel J M ^a   Oomens, Cees W J ^a   Baaijens, Frank P T ^a   Bouten, Carlijn V C ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CELL GROWTH; CELL PROLIFERATION; MONOLAYERS; TISSUE ENGINEERING; CELL CULTURE; MUSCLE; PROTEINS;

CREATINE KINASE ACTIVITY; MYOBLAST DIFFERENTIATION; SERUM FREE CULTURE MEDIUM; TISSUE VIABILITY; HORSE SERUM;

CELL CULTURE; TISSUE ENGINEERING;

CREATINE KINASE; PROTEIN; SOMATOMEDIN C; ULTROSER G; BLOOD SUBSTITUTE; MUSCLE PROTEIN; ORGANIC COMPOUND;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL CULTURE; CELL VIABILITY; CULTURE MEDIUM; ENZYME ACTIVITY; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SERUM; SKELETAL MUSCLE; TISSUE ENGINEERING; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECT; METABOLISM; METHODOLOGY; CELL PROLIFERATION; EXPERIMENTAL MODEL; GOLD STANDARD; PROTEIN CONTENT;

EQUIDAE; MURINAE;

ANIMALS; BLOOD SUBSTITUTES; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CREATINE KINASE; CULTURE MEDIA, SERUM-FREE; INSULIN-LIKE GROWTH FACTOR I; MICE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; ORGANIC CHEMICALS; TISSUE ENGINEERING;

EID: 38349090769     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.a.2007.0095     Document Type: Article

References (60)

1. Yaffe, D., and Saxel, O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725, 1977.
2. Blau, H.M., Chiu, C.P., and Webster, C. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32, 1171, 1983.
3. Kubo, Y. Comparison of initial stages of muscle differentiation in rat and mouse myoblastic and mouse mesodermal stem cell lines. J Physiol 442, 743, 1991.
4. Andres, V., and Walsh, K. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol 132, 657, 1996.
5. Shimokawa, T., Kato, M., Ezaki, O., and Hashimoto, S. Transcriptional regulation of muscle-specific genes during myoblast differentiation. Biochem Biophys Res Commun 246, 287, 1998.
6. Lawson, M.A. and Purslow, P.P. Differentiation of myoblasts in serum-free media: effects of modified media are cell linespecific. Cells Tissues Organs 167, 130, 2000.
7. Delgado, I., Huang, X., Jones, S., Zhang, L., Hatcher, R., Gao, B., and Zhang, P. Dynamic gene expression during the onset of myoblast differentiation in vitro. Genomics 82, 109, 2003.
8. Shen, X., Collier, J.M., Hlaing, M., Zhang, L., Delshad, E.H., Bristow, J., and Bernstein, H.S. Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Dev Dyn 226, 128, 2003.
9. Burattini, S., Ferri, P., Battistelli, M., Curci, R., Luchetti, F., and Falcieri, E. C2C12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization. Eur J Histochem 48, 223, 2004.
10. Tannu, N.S., Rao, V.K., Chaudhary, R.M., Giorgianni, F., Saeed, A.E., Gao, Y., and Raghow, R. Comparative proteomes of the proliferating C(2)C(12) myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol Cell Proteomics 3, 1065, 2004.
11. Okano, T. and Matsuda, T. Hybrid muscular tissues: preparation of skeletal muscle cell-incorporated collagen gels. Cell Transplant 6, 109, 1997.
12. Okano, T. and Matsuda, T. Tissue engineered skeletal muscle: preparation of highly dense, highly oriented hybrid muscular tissues. Cell Transplant 7, 71, 1998.
13. Okano, T. and Matsuda, T. Muscular tissue engineering: capillary-incorporated hybrid muscular tissues in vivo tissue culture. Cell Transplant 7, 435, 1998.
14. Dennis, R.G. and Kosnik, P.E. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell Dev Biol Anim 36, 327, 2000.
15. Dennis, R.G., Kosnik, P.E., Gilbert, M.E., and Faulkner, J.A. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am J Physiol Cell Physiol 280, C288, 2001.
16. Srikakulam, R. and Winkelmann, D.A. Chaperone-mediated folding and assembly of myosin in striated muscle. J Cell Sci 117, 641, 2004.
17. Furst, D.O., Osborn, M., and Weber, K. Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol 109, 517, 1989.
18. Lin, Z., Lu, M.H., Schultheiss, T., Choi, J., Holtzer, S., DiLullo, C., Fischman, D.A., and Holtzer, H. Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil Cytoskeleton 29, 1, 1994.
19. Begum, S., Komiyama, M., Toyota, N., Obinata, T., Maruyama, K., and Shimada, Y. Differentiation of muscle-specific proteins in chicken somites as studied by immunofluorescence microscopy. Cell Tissue Res 293, 305, 1998.
20. Sanger, J.W., Chowrashi, P., Shaner, N.C., Spalthoff, S., Wang, J., Freeman, N.L., and Sanger, J.M. Myofibrillogenesis in skeletal muscle cells. Clin Orthop Relat Res S153, 2002.
21. Portier, G.L., Benders, A.G., Oosterhof, A., Veerkamp, J.H., and van Kuppevelt, T.H. Differentiation markers of mouse C2C12 and rat L6 myogenic cell lines and the effect of the differentiation medium. In Vitro Cell Dev Biol Anim 35, 219, 1999.
22. Ewton, D.Z., Roof, S.L., Magri, K.A., McWade, F.J., and Florini, J.R. IGF-II is more active than IGF-I in stimulating L6A1 myogenesis: greater mitogenic actions of IGF-I delay differentiation. J Cell Physiol 161, 277, 1994.
23. Bach, L.A., Salemi, R., and Leeding, K.S. Roles of insulin-like growth factor (IGF) receptors and IGF-binding proteins in IGF-II-induced proliferation and differentiation of L6A1 rat myoblasts. Endocrinology 136, 5061, 1995.
24. Coolican, S.A., Samuel, D.S., Ewton, D.Z., McWade, F.J., and Florini, J.R. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272, 6653, 1997.
25. Conejo, R., Valverde, A.M., Benito, M., and Lorenzo, M. Insulin produces myogenesis in C2C12 myoblasts by induction of NF-kappaB and downregulation of AP-1 activities. J Cell Physiol 186, 82, 2001.
26. Takahashi, A., Kureishi, Y., Yang, J., Luo, Z., Guo, K., Mukhopadhyay, D., Ivashchenko, Y., Branellec, D., and Walsh, K. Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol Cell Biol 22, 4803, 2002.
27. Yang, S.Y. and Goldspink, G. Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522, 156, 2002.
28. Hill, M. and Goldspink, G. Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J Physiol 549, 409, 2003.
29. Rabinovsky, E.D., Gelir, E., Gelir, S., Lui, H., Kattash, M., DeMayo, F.J., Shenaq, S.M., and Schwartz, R.J. Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEB J 17, 53, 2003.
30. Musaro, A., Giacinti, C., Borsellino, G., Dobrowolny, G., Pelosi, L., Cairns, L., Ottolenghi, S., Cossu, G., Bernardi, G., Battistini, L., Molinaro, M., and Rosenthal, N. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc Natl Acad Sci U S A 101, 1206, 2004.
31. Cheema, U., Brown, R., Mudera, V., Yang, S.Y., McGrouther, G., and Goldspink, G. Mechanical signals and IGF-I gene splicing in vitro in relation to development of skeletal muscle. J Cell Physiol 202, 67, 2005.
32. Benders, A.A., van Kuppevelt, T.H., Oosterhof, A., and Veerkamp, J.H. The biochemical and structural maturation of human skeletal muscle cells in culture: the effect of the serum substitute Ultroser G. Exp Cell Res 195, 284, 1991.
33. Jacobs, A.E., Benders, A.A., Oosterhof, A., and Veerkamp, J.H. Effects of growth medium, electrical stimulation and paralysis on various enzyme activities in cultured rat muscle cells. Comparison with activities in rat muscles in vivo. Int J Biochem 24, 751, 1992.
34. van Kuppevelt, T.H., Benders, A.A., Versteeg, E.M., and Veerkamp, J.H. Ultroser G and brain extract induce a continuous basement membrane with specific synaptic elements in aneurally cultured human skeletal muscle cells. Exp Cell Res 200, 306, 1992.
35. Sultan, K.R., Henkel, B., Terlou, M., and Haagsman, H.P. Quantification of hormone-induced atrophy of large myotubes from C2C12 and L6 cells: atrophy-inducible and atrophyresistant C2C12 myotubes. Am J Physiol Cell Physiol 290, C650, 2006.
36. Vandenburgh, H., Del Tatto, M., Shansky, J., Lemaire, J., Chang, A., Payumo, F., Lee, P., Goodyear, A., and Raven, L. Tissue-engineered skeletal muscle organoids for reversible gene therapy. Hum Gene Ther 7, 2195, 1996.
37. Breuls, R.G.M., Bouten, C.V.C., Oomens, C.W.J., Bader, D.L., and Baaijens, F.P.T. Compression induced cell damage in engineered muscle tissue: an in vitro model to study pressure ulcer aetiology. Ann Biomed Eng 31, 1357, 2003.
38. van Wachem, P.B., van Luyn, M.J., and da Costa, M.L. Myoblast seeding in a collagen matrix evaluated in vitro. J Biomed Mater Res 30, 353, 1996.
39. Shansky, J., Del Tatto, M., Chromiak, J., and Vandenburgh, H. A simplified method for tissue engineering skeletal muscle organoids in vitro. In Vitro Cell Dev Biol Anim 33, 659, 1997.
40. Vandenburgh, H.H., Swasdison, S., and Karlisch, P. Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. FASEB J 5, 2860, 1991.
41. Strohman, R.C., Bayne, E., Spector, D., Obinata, T., Micou-Eastwood, J., and Maniotis, A. Myogenesis and histogenesis of skeletal muscle on flexible membranes in vitro. In Vitro Cell Dev Biol 26, 201, 1990.
42. Engler, A.J., Griffin, M.A., Sen, S., Bonnemann, C.G., Sweeney, H.L., and Discher, D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166, 877, 2004.
43. Griffin, M.A., Sen, S., Sweeney, H.L., and Discher, D.E. Adhesion-contractile balance in myocyte differentiation. J Cell Sci 117, 5855, 2004.
44. Swasdison, S. and Mayne, R. Formation of highly organized skeletal muscle fibers in vitro. Comparison with muscle development in vivo. J Cell Sci 102 (Pt 3), 643, 1992.
45. Vandenburgh, H., Shansky, J., Del Tatto, M., and Chromiak, J. Organogenesis of Skeletal Muscle in Tissue Culture. In: Morgan, J.R., and Yarmush, M.L., eds. Tissue Engineering. Humana Press, Totowa, NJ, 1998, pp. 217-226.
46. Dusterhoft, S. and Pette, D. Satellite cells from slow rat muscle express slow myosin under appropriate culture conditions. Differentiation 53, 25, 1993.
47. Maley, M.A., Davies, M.J., and Grounds, M.D. Extracellular matrix, growth factors, genetics: their influence on cell proliferation and myotube formation in primary cultures of adult mouse skeletal muscle. Exp Cell Res 219, 169, 1995.
48. Langen, R.C.J., Schols, A.M.W.J., Kelders, M.C.J.M., Wouters, E.F.M., and Janssen-Heininger, Y.M.W. Enhanced myogenic differentiation by extracellular matrix is regulated at the early stages of myogenesis. In Vitro Cell Dev Biol Anim 39, 163, 2003.
49. Page, S., Jackson, M.J., Coakley, J., and Edwards, R.H. Isoforms of creatine kinase: MM in the study of skeletal muscle damage. Eur J Clin Invest 19, 185, 1989.
50. McArdle, A., Maglara, A., Appleton, P., Watson, A.J., Grierson, I., and Jackson, M.J. Apoptosis in multinucleated skeletal muscle myotubes. Lab Invest 79, 1069, 1999.
51. Lin, Z.X., Eshelman, J.R., Forry-Schaudies, S., Duran, S., Lessard, J.L., and Holtzer, H. Sequential disassembly of myofibrils induced by myristate acetate in cultured myotubes. J Cell Biol 105, 1365, 1987.
52. Yotov, W.V. and St Arnaud, R. Differential splicing-in of a proline-rich exon converts alphaNAC into a muscle-specific transcription factor. Genes Dev 10, 1763, 1996.
53. Palmer, S., Groves, N., Schindeler, A., Yeoh, T., Biben, C., Wang, C.C., Sparrow, D.B., Barnett, L., Jenkins, N.A., Copeland, N.G., Koentgen, F., Mohun, T., and Harvey, R.P. The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an insulin-like growth factor 1-dependent manner. J Cell Biol 153, 985, 2001.
54. Florini, J.R., Ewton, D.Z., and Coolican, S.A. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17, 481, 1996.
55. Spangenburg, E.E., Bowles, D.K., and Booth, F.W. Insulin-like growth factor-induced transcriptional activity of the skeletal alpha-actin gene is regulated by signaling mechanisms linked to voltage-gated calcium channels during myoblast differentiation. Endocrinology 145, 2054, 2004.
56. Semsarian, C., Sutrave, P., Richmond, D.R., and Graham, R.M. Insulin-like growth factor (IGF-I) induces myotube hypertrophy associated with an increase in anaerobic glycolysis in a clonal skeletal-muscle cell model. Biochem J 339 (Pt 2), 443, 1999.
57. Napier, J.R., Thomas, M.F., Sharma, M., Hodgkinson, S.C., Bass, J.J. Insulin-like growth factor-I protects myoblasts from apoptosis but requires other factors to stimulate proliferation. J Endocrinol 163, 63, 1999.
58. Florini, J.R., Ewton, D.Z., Falen, S.L., Van Wyk, J.J. Biphasic concentration dependency of stimulation of myoblast differentiation by somatomedins. Am J Physiol 250(5 Pt 1), C771, 1986.
59. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E.S., Kohane, D.S., Darland, D.C., Marini, R., van Blitterswijk, C.A., Mulligan, R.C., D'Amore, P.A., and Langer, R. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23, 879, 2005.
60. De Coppi, P., Delo, D., Farrugia, L., Udompanyanan, K., Yoo, J.J., Nomi, M., Atala, A., and Soker, S. Angiogenic gene-modified muscle cells for enhancement of tissue formation. Tissue Eng 11, 1034, 2005.