Evaluation systems of generated forces of skeletal muscle cell-based bio-actuators

Journal of Bioscience and Bioengineering

Volumn 115, Issue 2, 2013, Pages 115-121

  Shimizu, Kazunori ^a,b   Fujita, Hideaki ^c,d   Nagamori, Eiji ^e  

^a KYOTO UNIVERSITY   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

^c RIKEN   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

Author keywords

Active force; Myoblasts; Myotubes; Screening system; Skeletal muscle; Tetanus; Twitch

Indexed keywords

ACTIVE FORCES; MYOBLASTS; MYOTUBES; SCREENING SYSTEM; SKELETAL MUSCLE; TETANUS; TWITCH;

CELLS; PHYSIOLOGY;

MUSCLE;

ANIMAL CELL; CELL CULTURE; CONTROLLED STUDY; CYTOLOGY; HUMAN; IN VITRO STUDY; MOLECULAR BIOLOGY; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE STRENGTH; MUSCLE TONE; MYOTUBE; NANODEVICE; NANOFABRICATION; NONHUMAN; REVIEW; SKELETAL MUSCLE; TISSUE ENGINEERING;

ANIMALS; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; HUMANS; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; TISSUE ENGINEERING;

EID: 84871929442     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2012.08.024     Document Type: Review

References (85)

1. Cohn R.D., Campbell K.P. Molecular basis of muscular dystrophies. Muscle Nerve 2000, 23:1456-1471.
2. Henriksen E.J. Exercise effects of muscle insulin signaling and action - invited review: effects of acute exercise and exercise training on insulin resistance. J. Appl. Physiol. 2002, 93:788-796.
3. Glass D.J. Skeletal muscle hypertrophy and atrophy signaling pathways. Int. J. Biochem. Cell Biol. 2005, 37:1974-1984.
4. Kelley D.E., Goodpaster B.H. Skeletal muscle triglyceride - an aspect of regional adiposity and insulin resistance. Diabetes Care 2001, 24:933-941.
5. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270:725-727.
6. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc. Natl. Acad. Sci. USA 1968, 61:477-483.
7. Yanagida T., Nakase M., Nishiyama K., Oosawa F. Direct observation of motion of single F-actin filaments in the presence of myosin. Nature 1984, 307:58-60.
8. Finer J.T., Simmons R.M., Spudich J.A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 1994, 368:113-119.
9. Ishijima A., Kojima H., Higuchi H., Harada Y., Funatsu T., Yanagida T. Multiple- and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: unitary steps and forces. Biophys. J. 1996, 70:383-400.
10. Natori R. The electric potential change of internal membrane during propagation of contraction in skinned fibre of toad skeletal muscle. Jpn. J. Physiol. 1975, 25:51-63.
11. Higuchi S., Tsukasaki Y., Fukuda N., Kurihara S., Fujita H. Thin filament-reconstituted skinned muscle fibers for the study of muscle physiology. J. Biomed. Biotechnol. 2011, 2011:486021.
12. Tanaka Y., Sato K., Shimizu T., Yamato M., Okano T., Kitamori T. Biological cells on microchips: new technologies and applications. Biosens. Bioelectron. 2007, 23:449-458.
13. Pilarek M., Neubauer P., Marx U. Biological cardio-micro-pumps for microbioreactors and analytical micro-systems. Sens. Actuators B Chem 2011, 156:517-526.
14. Liu H.Q., Schmidt J.J., Bachand G.D., Rizk S.S., Looger L.L., Hellinga H.W., Montemagno C.D. Control of a biomolecular motor-powered nanodevice with an engineered chemical switch. Nat. Mater. 2002, 1:173-177.
15. Soong R.K., Bachand G.D., Neves H.P., Olkhovets A.G., Craighead H.G., Montemagno C.D. Powering an inorganic nanodevice with a biomolecular motor. Science 2000, 290:1555-1558.
16. Tarhan M.C., Yokokawa R., Bottier C., Collard D., Fujita H. A nano-needle/microtubule composite gliding on a kinesin-coated surface for target molecule transport. Lab Chip 2010, 10:86-91.
17. Nagai M., Ryu S., Thorsen T., Matsudaira P., Fujita H. Chemical control of Vorticella bioactuator using microfluidics. Lab Chip 2010, 10:1574-1578.
18. Hiratsuka Y., Miyata M., Tada T., Uyeda T.Q.P. A microrotary motor powered by bacteria. Proc. Natl. Acad. Sci. USA 2006, 103:13618-13623.
19. Park S.J., Bae H., Kim J., Lim B., Park J., Park S. Motility enhancement of bacteria actuated microstructures using selective bacteria adhesion. Lab Chip 2010, 10:1706-1711.
20. Akiyama Y., Iwabuchi K., Furukawa Y., Morishima K. Culture of insect cells contracting spontaneously; research moving toward an environmentally robust hybrid robotic system. J. Biotechnol. 2008, 133:261-266.
21. Akiyama Y., Iwabuchi K., Furukawa Y., Morishima K. Electrical stimulation of cultured lepidopteran dorsal vessel tissue: an experiment for development of bioactuators. In Vitro Cell. Dev. Biol. Anim. 2010, 46:411-415.
22. Baryshyan A.L., Woods W., Trimmer B.A., Kaplan D.L. Isolation and maintenance-free culture of contractile myotubes from Manduca sexta embryos. PLoS ONE 2012, 7:e31598.
23. Akiyama Y., Iwabuchi K., Furukawa Y., Morishima K. Long-term and room temperature operable bioactuator powered by insect dorsal vessel tissue. Lab Chip 2009, 9:140-144.
24. Kubo H., Shimizu T., Yamato M., Fujimoto T., Okano T. Creation of myocardial tubes using cardiomyocyte sheets and an in vitro cell sheet-wrapping device. Biomaterials 2007, 28:3508-3516.
25. Morishima K., Tanaka Y., Ebara M., Shimizu T., Kikuchi A., Yamato M., Okano T., Kitamori T. Demonstration of a bio-microactuator powered by cultured cardiomyocytes coupled to hydrogel micropillars. Sens. Actuators B Chem. 2006, 119:345-350.
26. Tanaka Y., Morishima K., Shimizu T., Kikuchi A., Yamato M., Okano T., Kitamori T. Demonstration of a PDMS-based bio-microactuator using cultured cardiomyocytes to drive polymer micropillars. Lab Chip 2006, 6:230-235.
27. Horiguchi H., Imagawa K., Hoshino T., Akiyama Y., Morishima K. Fabrication and evaluation of reconstructed cardiac tissue and its application to bio-actuated microdevices. IEEE Trans. Nanobioscience 2009, 8:349-355.
28. Kim D.H., Park J., Suh K.Y., Kim P., Choi S.K., Ryu S., Park S., Lee S.H., Kim B. Fabrication of patterned micromuscles with high activity for powering biohybrid microdevices. Sens. Actuators B Chem. 2006, 117:391-400.
29. Tanaka Y., Yanagisawa Y., Kitamori T. Fluid actuation for a bio-micropump powered by previously frozen cardiomyocytes directly seeded on a diagonally stretched thin membrane. Sens. Actuators B Chem. 2011, 156:494-498.
30. Tanaka Y., Sato K., Shimizu T., Yamato M., Okano T., Kitamori T. A micro-spherical heart pump powered by cultured cardiomyocytes. Lab Chip 2007, 7:207-212.
31. Xi J., Schmidt J.J., Montemagno C.D. Self-assembled microdevices driven by muscle. Nat. Mater. 2005, 4:180-184.
32. Feinberg A.W., Feigel A., Shevkoplyas S.S., Sheehy S., Whitesides G.M., Parker K.K. Muscular thin films for building actuators and powering devices. Science 2007, 317:1366-1370.
33. Chan V., Jeong J.H., Bajaj P., Collens M., Saif T., Kong H., Bashir R. Multi-material bio-fabrication of hydrogel cantilevers and actuators with stereolithography. Lab Chip 2012, 12:88-98.
34. Tanaka Y., Sato K., Shimizu T., Yamato M., Okano T., Manabe I., Nagai R., Kitamori T. Demonstration of a bio-microactuator powered by vascular smooth muscle cells coupled to polymer micropillars. Lab Chip 2008, 8:58-61.
35. Haas S., Jahnke H.G., Glass M., Azendorf R., Schmidt S., Robitzki A.A. Real-time monitoring of relaxation and contractility of smooth muscle cells on a novel biohybrid chip. Lab Chip 2010, 10:2965-2971.
36. Shimizu K., Sasaki H., Hida H., Fujita H., Obinata K., Shikida M., Nagamori E. Assembly of skeletal muscle cells on a Si-MEMS device and their generative force measurement. Biomed. Microdevices 2010, 12:247-252.
37. Wilson K., Das M., Wahl K.J., Colton R.J., Hickman J. Measurement of contractile stress generated by cultured rat muscle on silicon cantilevers for toxin detection and muscle performance enhancement. PLoS ONE 2010, 5:e11042.
38. Wilson K., Molnar P., Hickman J.J. Integration of functional myotubes with a Bio-MEMS device for non-invasive interrogation. Lab Chip 2007, 7:920-922.
39. Das M., Gregory C.A., Molnara P., Riedela L.M., Wilsona K., Hickman J.J. A defined system to allow skeletal muscle differentiation and subsequent integration with silicon microstructures. Biomaterials 2006, 27:4374-4380.
40. Das M., Wilson K., Molnar P., 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. 2007, 2:1795-1801.
41. Shimizu K., Fujita H., Nagamori E. Micropatterning of single myotubes on a thermoresponsive culture surface using elastic stencil membranes for single-cell analysis. J. Biosci. Bioeng. 2010, 109:174-178.
42. Fujita H., Endo A., Shimizu K., Nagamori E. Evaluation of serum-free differentiation conditions for C2C12 myoblast cells assessed as to active tension generation capability. Biotechnol. Bioeng. 2010, 107:894-901.
43. Fujita H., Hirano M., Shimizu K., Nagamori E. Rapid decrease in active tension generated by C2C12 myotubes after termination of artificial exercise. J. Muscle Res. Cell Motil. 2010, 31:279-288.
44. Fujita H., Nedachi T., Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp. Cell Res. 2007, 313:1853-1865.
45. Fujita H., Shimizu K., Morioka Y., Nagamori E. Enhancement of C2C12 differentiation by perfluorocarbon-mediated oxygen delivery. J. Biosci. Bioeng. 2010, 110:359-362.
46. Fujita H., Shimizu K., Nagamori E. Novel method for measuring active tension generation by C2C12 myotube using UV-Crosslinked collagen film. Biotechnol. Bioeng. 2010, 106:482-489.
47. Fujita H., Van T.D., Shimizu K., Hatsuda R., Sugiyama S., Nagamori E. Designing of a Si-MEMS device with an integrated skeletal muscle cell-based bio-actuator. Biomed. Microdevices 2011, 13:123-129.
48. Dennis R.G., Kosnik P.E. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 2000, 36:327-335.
49. Huang Y.C., Dennis R.G., Baar K. Cultured slow vs. fast skeletal muscle cells differ in physiology and responsiveness to stimulation. Am. J. Physiol. Cell Physiol. 2006, 291:11-17.
50. Dennis R.G., Dow D.E. Excitability of skeletal muscle during development, denervation, and tissue culture. Tissue Eng. 2007, 13:2395-2404.
51. Dennis R.G., Kosnik P.E., Gilbert M.E., Faulkner J.A. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am. J. Physiol. Cell Physiol. 2001, 280:288-295.
52. Fujita H., Shimizu K., Nagamori E. Novel method for fabrication of skeletal muscle construct from the C2C12 myoblast cell line using serum-free medium AIM-V. Biotechnol. Bioeng. 2009, 103:1034-1041.
53. Huang Y.C., Dennis R.G., Larkin L., Baar K. Rapid formation of functional muscle in vitro using fibrin gels. J. Appl. Physiol. 2005, 98:706-713.
54. Khodabukus A., Baar K. Regulating fibrinolysis to engineer skeletal muscle from the C2C12 cell line. Tissue Eng. Part C Methods 2009, 15:501-511.
55. Donnelly K., Khodabukus A., Philp A., Deldicque L., Dennis R.G., Baar K. A novel bioreactor for stimulating skeletal muscle in vitro. Tissue Eng. Part C Methods 2010, 16:711-718.
56. Khodabukus A., Baar K. Defined electrical stimulation emphasizing excitability for the development and testing of engineered skeletal muscle. Tissue Eng. Part C Methods 2012, 18:349-357.
57. Hinds S., Bian W., Dennis R.G., Bursac N. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 2011, 32:3575-3583.
58. Cheema U., Yang S.Y., Mudera V., Goldspink G.G., Brown R.A. 3-D in vitro model of early skeletal muscle development. Cell Motil. Cytoskeleton 2003, 54:226-236.
59. Brady M.A., Lewis M.P., Mudera V. Synergy between myogenic and non-myogenic cells in a 3D tissue-engineered craniofacial skeletal muscle construct. J. Tissue Eng. Regen. Med. 2008, 2:408-417.
60. Mudera V., Smith A.S.T., Brady M.A., Lewis M.P. 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. 2010, 225:646-653.
61. Vandenburgh H., Swasdison S., Karlisch P. Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. FASEB J. 1991, 5:2860-2867.
62. Powell C.A., Smiley B.L., Mills J., Vandenburgh H.H. Mechanical stimulation improves tissue-engineered human skeletal muscle. Am. J. Physiol. Cell Physiol. 2002, 283:C1557-C1565.
63. Yamasaki K., Hayashi H., Nishiyama K., Kobayashi H., Uto S., Kondo H., Hashimoto S., Fujisato T. Control of myotube contraction using electrical pulse stimulation for bio-actuator. J. Artif. Organs 2009, 12:131-137.
64. Smith A.S.T., Passey S., Greensmith L., Mudera V., Lewis M.P. Characterization and optimization of a simple, repeatable system for the long term in vitro culture of aligned myotubes in 3D. J. Cell. Biochem. 2012, 113:1044-1053.
65. Gawlitta D., Boonen K.J.M., Oomens C.W.J., Baaijens F.P.T., Bouten C.V.C. The influence of serum-free culture conditions on skeletal muscle differentiation in a tissue-engineered model. Tissue Eng. Part A 2008, 14:161-171.
66. Sato M., Ito A., Kawabe Y., Nagamori E., Kamihira M. Enhanced contractile force generation by artificial skeletal muscle tissues using IGF-I gene-engineered myoblast cells. J. Biosci. Bioeng. 2011, 112:273-278.
67. Okano T., Matsuda T. Tissue engineered skeletal muscle: preparation of highly dense, highly oriented hybrid muscular tissues. Cell Transplant. 1998, 7:71-82.
68. Bian W.N., Bursac N. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials 2009, 30:1401-1412.
69. Bian W.N., Juhas M., Pfeiler T.W., Bursac N. Local tissue geometry determines contractile force generation of engineered muscle networks. Tissue Eng. Part A 2012, 18:957-967.
70. Bian W., Liau B., Badie N., Bursac N. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat. Protoc. 2009, 4:1522-1534.
71. Vandenburgh H., Shansky J., Benesch-Lee F., Barbata V., Reid J., Thorrez L., Valentini R., Crawford G. Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 2008, 37:438-447.
72. Vandenburgh H., Shansky J., Benesch-Lee F., Skelly K., Spinazzola J.M., Saponjian Y., Tseng B.S. Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts. FASEB J. 2009, 23:3325-3334.
73. Yamamoto Y., Ito A., Kato M., Kawabe Y., Shimizu K., Fujita H., Nagamori E., Kamihira M. Preparation of artificial skeletal muscle tissues by a magnetic force-based tissue engineering technique. J. Biosci. Bioeng. 2009, 108:538-543.
74. Yamamoto Y., Ito A., Fujita H., Nagamori E., Kawabe Y., Kamihira M. Functional evaluation of artificial skeletal muscle tissue constructs fabricated by a magnetic force-based tissue engineering technique. Tissue Eng. Part A 2011, 17:107-114.
75. Fujita H., Shimizu K., Yamamoto Y., Ito A., Kamihira M., Nagamori E. Fabrication of scaffold-free contractile skeletal muscle tissue using magnetite-incorporated myogenic C2C12 cells. J. Tissue Eng. Regen. Med. 2010, 4:437-443.
76. Ito A., Jitsunobu H., Kawabe Y., Karnihira M. Construction of heterotypic cell sheets by magnetic force-based 3-D coculture of HepG2 and NIH3T3 cells. J. Biosci. Bioeng. 2007, 104:371-378.
77. Ito A., Takizawa Y., Honda H., Hata K.I., Kagami H., Ueda M., Kobayashi T. Tissue engineering using magnetite nanoparticles and magnetic force: heterotypic layers of cocultured hepatocytes and endothelial cells. Tissue Eng. 2004, 10:833-840.
78. Ito A., Ino K., Hayashida M., Kobayashi T., Matsunuma H., Kagami H., Ueda M., Honda H. Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force. Tissue Eng. 2005, 11:1553-1561.
79. Shimizu K., Ito A., Arinobe M., Murase Y., Iwata Y., Narita Y., Kagami H., Ueda M., Honda H. Effective cell-seeding technique using magnetite nanoparticles and magnetic force onto decellularized blood vessels for vascular tissue engineering. J. Biosci. Bioeng. 2007, 103:472-478.
80. Shimizu K., Ito A., Honda H. Mag-seeding of rat bone marrow stromal cells into porous hydroxyapatite scaffolds for bone tissue engineering. J. Biosci. Bioeng. 2007, 104:171-177.
81. Shimizu K., Ito A., Yoshida T., Yamada Y., Ueda M., Honda H. Bone tissue engineering with human mesenchymal stem cell sheets constructed using magnetite nanoparticles and magnetic force. J. Biomed. Mater. Res. Part B 2007, 82B:471-480.
82. Akiyama H., Ito A., Sato M., Kawabe Y., Kamihira M. Construction of cardiac tissue rings using a magnetic tissue fabrication technique. Int. J. Mol. Sci. 2010, 11:2910-2920.
83. Shimizu K., Ito A., Lee J.K., Yoshida T., Miwa K., Ishiguro H., Numaguchi Y., Murohara T., Kodama I., Honda H. Construction of multi-layered cardiomyocyte sheets using magnetite nanoparticles and magnetic force. Biotechnol. Bioeng. 2007, 96:803-809.
84. Asano T., Ishizua T., Yawo H. Optically controlled contraction of photosensitive skeletal muscle cells. Biotechnol. Bioeng. 2012, 109:199-204.
85. Darabi R., Arpke R.W., Irion S., Dimos J.T., Grskovic M., Kyba M., Perlingeiro R.C.R. Human ES- and iPS-derived myogenic progenitors restore dystrophin and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 2012, 10:610-619.