Skeletal muscle tissue engineering: A maturation model promoting long-term survival of myotubes, structural development of the excitation-contraction coupling apparatus and neonatal myosin heavy chain expression

Biomaterials

Volumn 30, Issue 29, 2009, Pages 5392-5402

  Das, Mainak ^a   Rumsey, John W ^a   Bhargava, Neelima ^a   Stancescu, Maria ^a   Hickman, James J ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Cell culture; In vitro test; Muscle; Silane; Surface analysis; Surface modification

Indexed keywords

BAND FORMATIONS; CELL TYPES; CLASS-SWITCHING; DIHYDROPYRIDINES; EXCITATION-CONTRACTION COUPLING; HIGH-THROUGHPUT SCREENING; IN VITRO TEST; IN-VITRO; LARGE PARTS; MODEL SYSTEM; MYOSIN HEAVY CHAIN; MYOTUBES; PHYSIOLOGICAL CHARACTERISTICS; RAT HIND LIMB; REGENERATIVE MEDICINE; RYANODINE RECEPTORS; SKELETAL MUSCLE; STRUCTURAL DEVELOPMENT; SURFACE MODIFICATION;

CELL CULTURE; CELL MEMBRANES; PHYSIOLOGICAL MODELS; SCREENS (SIZING); SHRINKAGE; SILANES; SURFACE ANALYSIS; SURFACE TREATMENT; TISSUE ENGINEERING;

MUSCLE;

MAJOR HISTOCOMPATIBILITY ANTIGEN; MYOSIN HEAVY CHAIN; RYANODINE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; EXCITATION CONTRACTION COUPLING; FETUS; IMMUNOCYTOCHEMISTRY; MUSCLE DEVELOPMENT; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SARCOMERE; SKELETAL MUSCLE; TISSUE ENGINEERING; TISSUE SURVIVAL;

ANIMALS; ANIMALS, NEWBORN; BIOCOMPATIBLE MATERIALS; CELL SURVIVAL; CELLS, CULTURED; MATERIALS TESTING; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; RATS; TISSUE ENGINEERING;

RATTUS;

EID: 68549126727     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.05.081     Document Type: Article

References (63)

1. Arnold H.H., and Winter B. Muscle differentiation: more complexity to the network of myogenic regulators. Curr Opin Genet Dev 8 5 (1998) 539-544
2. Li L., and Olson E.N. Regulation of muscle cell growth and differentiation by the MyoD family of helix-loop-helix proteins. Adv Cancer Res 58 (1992) 95-119
3. Brand-Saberi B. Genetic and epigenetic control of skeletal muscle development. Ann Anat 187 3 (2005) 199-207
4. Christ B., and Brand-Saberi B. Limb muscle development. Int J Dev Biol 46 7 (2002) 905-914
5. Dutton E.K., Uhm C.S., Samuelsson S.J., Schaffner A.E., Fitzgerald S.C., and Daniels M.P. Acetylcholine receptor aggregation at nerve-muscle contacts in mammalian cultures: induction by ventral spinal cord neurons is specific to axons. J Neurosci 15 11 (1995) 7401-7416
6. Daniels M.P., Lowe B.T., Shah S., Ma J., Samuelsson S.J., Lugo B., et al. Rodent nerve-muscle cell culture system for studies of neuromuscular junction development: refinements and applications. Microsc Res Tech 49 1 (2000) 26-37
7. Kucera J., Walro J.M., and Reichler J. Role of nerve and muscle factors in the development of rat muscle spindles. Am J Anat 186 2 (1989) 144-160
8. Flucher B.E., Andrews S.B., and Daniels M.P. Molecular organization of transverse tubule/sarcoplasmic reticulum junctions during development of excitation-contraction coupling in skeletal muscle. Mol Biol Cell 5 10 (1994) 1105-1118
9. Flucher B.E., Terasaki M., Chin H.M., Beeler T.J., and Daniels M.P. Biogenesis of transverse tubules in skeletal muscle in vitro. Dev Biol 145 1 (1991) 77-90
10. Schaffner A.E., Barker J.L., Stenger D.A., and Hickman J.J. Investigation of the factors necessary for growth of hippocampal neurons in a defined system. J Neurosci Methods 62 1-2 (1995) 111-119
11. Das M., Bhargava N., Bhalkikar A., Kang J.F., and Hickman J.J. Temporal neurotransmitter conditioning restores the functional activity of adult spinal cord neurons in long-term culture. Exp Neurol 209 1 (2008) 171-180
12. Das M., Gregory C.A., Molnar P., Riedel L.M., Wilson K., and Hickman J.J. A defined system to allow skeletal muscle differentiation and subsequent integration with silicon microstructures. Biomaterials 27 24 (2006) 4374-4380
13. Das M., Molnar P., Devaraj H., Poeta M., and Hickman J.J. Electrophysiological and morphological characterization of rat embryonic motoneurons in a defined system. Biotechnol Prog 19 6 (2003) 1756-1761
14. Das M., Rumsey J.W., Gregory C.A., Bhargava N., Kang J.F., Molnar P., et al. Embryonic motoneuron-skeletal muscle co-culture in a defined system. Neuroscience 146 2 (2007) 481-488
15. Das M., Wilson K., Molnar P., and Hickman J.J. Differentiation of skeletal muscle and integration of myotubes with silicon microstructures using serum-free medium and a synthetic silane substrate. Nat Protoc 2 7 (2007) 1795-1801
16. Hickman J.J., Bhatia S.K., Quong J.N., Shoen P., Stenger D.A., Pike C.J., et al. Rational pattern design for in-vitro cellular networks using surface photochemistry. J Vac Sci Technol A 12 3 (1994) 607-616
17. Ravenscroft M.S., Bateman K.E., Shaffer K.M., Schessler H.M., Jung D.R., Schneider T.W., et al. Developmental neurobiology implications from fabrication and analysis of hippocampal neuronal networks on patterned silane-modified surfaces. J Am Chem Soc 120 47 (1998) 12169-12177
18. Das M., Molnar P., Gregory C., Riedel L., Jamshidi A., and Hickman J.J. Long-term culture of embryonic rat cardiomyocytes on an organosilane surface in a serum-free medium. Biomaterials 25 25 (2004) 5643-5647
19. Wilson K., Molnar P., and Hickman J. Integration of functional myotubes with a Bio-MEMS device for non-invasive interrogation. Lab Chip 7 7 (2007) 920-922
20. Rumsey J.W., Das M., Kang J.F., Wagner R., Molnar P., and Hickman J.J. Tissue engineering intrafusal fibers: dose- and time-dependent differentiation of nuclear bag fibers in a defined in vitro system using neuregulin 1-beta-1. Biomaterials 29 8 (2008) 994-1004
21. Brewer G.J., Boehler M.D., Jones T.T., and Wheeler B.C. NbActiv4 medium improvement to Neurobasal/B27 increases neuron synapse densities and network spike rates on multielectrode arrays. J Neurosci Methods 170 2 (2008) 181-187
22. Stenger D.A., Georger J.H., Dulcey C.S., Hickman J.J., Rudolph A.S., Nielsen T.B., et al. Coplanar molecular assemblies of aminoalkylsilane and perfluorinated alkylsilane - characterization and geometric definition of mammalian-cell adhesion and growth. J Am Chem Soc 114 22 (1992) 8435-8442
23. Flucher B.E., Phillips J.L., Powell J.A., Andrews S.B., and Daniels M.P. Coordinated development of myofibrils, sarcoplasmic reticulum and transverse tubules in normal and dysgenic mouse skeletal muscle, in vivo and in vitro. Dev Biol 150 2 (1992) 266-280
24. Flucher B.E., Morton M.E., Froehner S.C., and Daniels M.P. Localization of the alpha 1 and alpha 2 subunits of the dihydropyridine receptor and ankyrin in skeletal muscle triads. Neuron 5 3 (1990) 339-351
25. Olson E.N. Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol 154 2 (1992) 261-272
26. Torgan C.E., and Daniels M.P. Regulation of myosin heavy chain expression during rat skeletal muscle development in vitro. Mol Biol Cell 12 5 (2001) 1499-1508
27. Ruegg J. Calcium in muscle activation (1988), Springer Verlag, Berlin
28. Franzini-Armstrong C., and Protasi F. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77 3 (1997) 699-729
29. 2+ current and charge movements in skeletal myotubes promoted by the beta-subunit of the dihydropyridine receptor in the absence of ryanodine receptor type 1. Biophys J 84 2 Pt 1 (2003) 942-959
30. 2+-dependent excitation-contraction coupling triggered by the heterologous cardiac/brain DHPR beta2a-subunit in skeletal myotubes. Biophys J 85 6 (2003) 3739-3757
31. Brewer G.J., Torricelli J.R., Evege E.K., and Price P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35 5 (1993) 567-576
32. Alterio J., Courtois Y., Robelin J., Bechet D., and Martelly I. Acidic and basic fibroblast growth factor mRNAs are expressed by skeletal muscle satellite cells. Biochem Biophys Res Commun 166 3 (1990) 1205-1212
33. Anderson J.E., Liu L., and Kardami E. Distinctive patterns of basic fibroblast growth factor (bFGF) distribution in degenerating and regenerating areas of dystrophic (mdx) striated muscles. Dev Biol 147 1 (1991) 96-109
34. Arsic N., Zacchigna S., Zentilin L., Ramirez-Correa G., Pattarini L., Salvi A., et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther 10 5 (2004) 844-854
35. Dusterhoft S., and Pette D. Evidence that acidic fibroblast growth factor promotes maturation of rat satellite-cell-derived myotubes in vitro. Differentiation 65 3 (1999) 161-169
36. Fu X., Cuevas P., Gimenez-Gallego G., Sheng Z., and Tian H. Acidic fibroblast growth factor reduces rat skeletal muscle damage caused by ischemia and reperfusion. Chin Med J (Engl) 108 3 (1995) 209-214
37. Olwin B.B., and Rapraeger A. Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J Cell Biol 118 3 (1992) 631-639
38. Husmann I., Soulet L., Gautron J., Martelly I., and Barritault D. Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev 7 3 (1996) 249-258
39. Vakakis N., Bower J., and Austin L. In vitro myoblast to myotube transformations in the presence of leukemia inhibitory factor. Neurochem Int 27 4-5 (1995) 329-335
40. Biesecker G. The complement SC5b-9 complex mediates cell adhesion through a vitronectin receptor. J Immunol 145 1 (1990) 209-214
41. Gullberg D., Sjoberg G., Velling T., and Sejersen T. Analysis of fibronectin and vitronectin receptors on human fetal skeletal muscle cells upon differentiation. Exp Cell Res 220 1 (1995) 112-123
42. Wang X., Wu H., Zhang Z., Liu S., Yang J., Chen X., et al. Effects of interleukin-6, leukemia inhibitory factor, and ciliary neurotrophic factor on the proliferation and differentiation of adult human myoblasts. Cell Mol Neurobiol 28 1 (2008) 113-124
43. Chen X., Mao Z., Liu S., Liu H., Wang X., Wu H., et al. Dedifferentiation of adult human myoblasts induced by ciliary neurotrophic factor in vitro. Mol Biol Cell 16 7 (2005) 3140-3151
44. Oakley R.A., Lefcort F.B., Clary D.O., Reichardt L.F., Prevette D., Oppenheim R.W., et al. Neurotrophin-3 promotes the differentiation of muscle spindle afferents in the absence of peripheral targets. J Neurosci 17 11 (1997) 4262-4274
45. Carrasco D.I., and English A.W. Neurotrophin 4/5 is required for the normal development of the slow muscle fiber phenotype in the rat soleus. J Exp Biol 206 Pt 13 (2003) 2191-2200
46. Yang L.X., and Nelson P.G. Glia cell line-derived neurotrophic factor regulates the distribution of acetylcholine receptors in mouse primary skeletal muscle cells. Neuroscience 128 3 (2004) 497-509
47. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., et al. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266 5187 (1994) 1062-1064
48. Heinrich G.A. novel BDNF gene promoter directs expression to skeletal muscle. BMC Neurosci 4 (2003) 11
49. Sheng Z., Pennica D., Wood W.I., and Chien K.R. Cardiotrophin-1 displays early expression in the murine heart tube and promotes cardiac myocyte survival. Development 122 2 (1996) 419-428
50. Jaworska-Wilczynska M., Wilczynski G.M., Engel W.K., Strickland D.K., Weisgraber K.H., and Askanas V. Three lipoprotein receptors and cholesterol in inclusion-body myositis muscle. Neurology 58 3 (2002) 438-445
51. Caratsch C.G., Santoni A., and Eusebi F. Interferon-alpha, beta and tumor necrosis factor-alpha enhance the frequency of miniature end-plate potentials at rat neuromuscular junction. Neurosci Lett 166 1 (1994) 97-100
52. Jin P., Sejersen T., and Ringertz N.R. Recombinant platelet-derived growth factor-BB stimulates growth and inhibits differentiation of rat L6 myoblasts. J Biol Chem 266 2 (1991) 1245-1249
53. Gold M.R. The effects of vasoactive intestinal peptide on neuromuscular transmission in the frog. J Physiol 327 (1982) 325-335
54. Zorzano A., Kaliman P., Guma A., and Palacin M. Intracellular signals involved in the effects of insulin-like growth factors and neuregulins on myofibre formation. Cell Signal 15 2 (2003) 141-149
55. Gozes I., Steingart R.A., and Spier A.D. NAP mechanisms of neuroprotection. J Mol Neurosci 24 1 (2004) 67-72
56. Robertson T.A., Dutton N.S., Martins R.N., Taddei K., and Papadimitriou J.M. Comparison of astrocytic and myocytic metabolic dysregulation in apolipoprotein E deficient and human apolipoprotein E transgenic mice. Neuroscience 98 2 (2000) 353-359
57. Langen R.C., Schols A.M., Kelders M.C., Wouters E.F., and Janssen-Heininger Y.M. Enhanced myogenic differentiation by extracellular matrix is regulated at the early stages of myogenesis. In Vitro Cell Dev Biol Anim 39 3-4 (2003) 163-169
58. Foster R.F., Thompson J.M., and Kaufman S.J. A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using antidesmin and anti-BrdUrd monoclonal antibodies. Dev Biol 122 1 (1987) 11-20
59. Wang P., Yang G., Mosier D.R., Chang P., Zaidi T., Gong Y.D., et al. Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J Neurosci 25 5 (2005) 1219-1225
60. Hall B.K., and Miyake T. All for one and one for all: condensations and the initiation of skeletal development. Bioessays 22 2 (2000) 138-147
61. Elia D., Madhala D., Ardon E., Reshef R., and Halevy O. Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta 1773 9 (2007) 1438-1446
62. Koleva M., Kappler R., Vogler M., Herwig A., Fulda S., and Hahn H. Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell Mol Life Sci 62 16 (2005) 1863-1870
63. Bandi E., Jevsek M., Mars T., Jurdana M., Formaggio E., Sciancalepore M., et al. Neural agrin controls maturation of the excitation-contraction coupling mechanism in human myotubes developing in vitro. Am J Physiol Cell Physiol 294 1 (2008) C66-C73