Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds

Biomaterials

Volumn 73, Issue , 2015, Pages 23-31

  Chen, Shangwu ^a,b   Nakamoto, Tomoko ^a   Kawazoe, Naoki ^a   Chen, Guoping ^a,b  

^a NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Collagen scaffold; Microgroove; Micropattern; Muscle tissue engineering; Myoblast

Indexed keywords

ALIGNMENT; CELLS; COLLAGEN; CYTOLOGY; HISTOLOGY; SCAFFOLDS (BIOLOGY); TOPOGRAPHY;

COLLAGEN SCAFFOLDS; MICRO PATTERN; MICROGROOVE; MUSCLE TISSUES; MYOBLASTS;

MUSCLE;

COLLAGEN; MYOSIN HEAVY CHAIN; SCLEROPROTEIN; ACTIN;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CELL INTERACTION; CELL STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION; MUSCLE TISSUE; MYOBLAST; NONHUMAN; POROSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SCANNING ELECTRON MICROSCOPY; SKELETAL MUSCLE; TISSUE ENGINEERING; TISSUE SCAFFOLD; ANIMAL; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE CELL;

ACTINS; ANIMALS; CELLS, CULTURED; COLLAGEN; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOBLASTS; MYOSIN HEAVY CHAINS; POROSITY; RATS; REAL-TIME POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84943560250     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.09.010     Document Type: Article

References (49)

1. Friedebo G., Groher W. Sprains and other sports-injuries of muscles and tendons. Z Orthop. Grenzgeb. 1972, 110:647-653.
2. Moller P., Bergstrom J., Furst P., Hellstrom K. Effect of aging on energy-rich phosphagens in human skeletal-muscles. Clin. Sci. 1980, 58:553-555.
3. Tournadre A., Dubost J.J., Soubrier M. Treatment of inflammatory muscle disease in adults. Jt. Bone Spine 2010, 77:390-394.
4. Campbell K.P., Stull J.T. Skeletal muscle basement membrane-sarcolemma-cytoskeleton interaction minireview series. J. Biol. Chem. 2003, 278:12599-12600.
5. Sanes J.R. The basement membrane/basal lamina of skeletal muscle. J. Biol. Chem. 2003, 278:12601-12604.
6. Ayaz H.G.S., Perets A., Ayaz H., Gilroy K.D., Govindaraj M., Brookstein D., et al. Textile-templated electrospun anisotropic scaffolds for regenerative cardiac tissue engineering. Biomaterials 2014, 35:8540-8552.
7. Choi J.S., Lee S.J., Christ G.J., Atala A., Yoo J.J. The influence of electrospun aligned poly(epsilon-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes. Biomaterials 2008, 29:2899-2906.
8. Cooper A., Jana S., Bhattarai N., Zhang M.Q. Aligned chitosan-based nanofibers for enhanced myogenesis. J. Mater Chem. 2010, 20:8904-8911.
9. Clark P., Coles D., Peckham M. Preferential adhesion to and survival on patterned laminin organizes myogenesis in vitro. Exp. Cell Res. 1997, 230:275-283.
10. Clark P., Dunn G.A., Knibbs A., Peckham M. Alignment of myoblasts on ultrafine gratings inhibits fusion in vitro. Int. J. Biochem. Cell B 2002, 34:816-825.
11. Salick M.R., Napiwocki B.N., Sha J., Knight G.T., Chindhy S.A., Kamp T.J., et al. Micropattern width dependent sarcomere development in human ESC-derived cardiomyocytes. Biomaterials 2014, 35:4454-4464.
12. Shi X.T., Fujie T., Saito A., Takeoka S., Hou Y., Shu Y.W., et al. Periosteum-mimetic structures made from freestanding microgrooved nanosheets. Adv. Mater. 2014, 26:3290-3296.
13. Zorlutuna P., Annabi N., Camci-Unal G., Nikkhah M., Cha J.M., Nichol J.W., et al. Microfabricated biomaterials for engineering 3D tissues. Adv. Mater. 2012, 24:1782-1804.
14. Fujie T., Ahadian S., Liu H., Chang H.X., Ostrovidov S., Wu H.K., et al. Engineered nanomembranes for directing cellular organization toward flexible biodevices. Nano Lett. 2013, 13:3185-3192.
15. Nakamoto T., Wang X.L., Kawazoe N.P., Chen G. Influence of micropattern width on differentiation of human mesenchymal stem cells to vascular smooth muscle cells. Colloid Surf. B 2014, 122:316-323.
16. Evans D.J.R., Britland S., Wigmore P.M. Differential response of fetal and neonatal myoblasts to topographical guidance cues in vitro. Dev. Genes Evol. 1999, 209:438-442.
17. Huang N.F., Lee R.J., Li S. Engineering of aligned skeletal muscle by micropatterning. Am. J. Transl. Res. 2010, 2:43-55.
18. Lam M.T., Sim S., Zhu X.Y., Takayama S. The effect of continuous wavy micropatterns on silicone substrates on the alignment of skeletal muscle myoblasts and myotubes. Biomaterials 2006, 27:4340-4347.
19. Takahashi H., Shimizu T., Nakayama M., Yamato M., Okano T. The use of anisotropic cell sheets to control orientation during the self-organization of 3D muscle tissue. Biomaterials 2013, 34:7372-7380.
20. Oh H.H., Ko Y.G., Lu H.X., Kawazoe N., Chen G.P. Preparation of porous collagen scaffolds with micropatterned structures. Adv. Mater. 2012, 24:4311-4316.
21. Caldwell C.J., Mattey D.L., Weller R.O. Role of the basement-membrane in the regeneration of skeletal-muscle. Neuropath Appl. Neuro 1990, 16:225-238.
22. Caldwell C.J., Weller R.O. The role of the basement-membrane in regeneration of skeletal-muscle. Neuropath Appl. Neuro 1987, 13:492-493.
23. Hurd S.A., Bhatti N.M., Walker A.M., Kasukonis B.M., Wolchok J.C. Development of a biological scaffold engineered using the extracellular matrix secreted by skeletal muscle cells. Biomaterials 2015, 49:9-17.
24. Jiang X.Y., Takayama S., Qian X.P., Ostuni E., Wu H.K., Bowden N., et al. Controlling mammalian cell spreading and cytoskeletal arrangement with conveniently fabricated continuous wavy features on poly(dimethylsiloxane). Langmuir 2002, 18:3273-3280.
25. Kolewe M.E., Park H., Gray C., Ye X.F., Langer R., Freed L.E. 3D structural patterns in scalable, elastomeric scaffolds guide engineered tissue architecture. Adv. Mater. 2013, 25:4459-4465.
26. Li G.C., Zhao X.Y., Zhao W.X., Zhang L.Z., Wang C.P., Jiang M.R., et al. Porous chitosan scaffolds with surface micropatterning and inner porosity and their effects on Schwann cells. Biomaterials 2014, 35:8503-8513.
27. Patz T.M., Doraiswamy A., Narayan R.J., Modi R., Chrisey D.B. Two-dimensional differential adherence and alignment of C2C12 myoblasts. Mat. Sci. Eng. B-Solid 2005, 123:242-247.
28. Ramon-Azcon J., Ahadian S., Estili M., Liang X.B., Ostrovidov S., Kaji H., et al. Dielectrophoretically aligned carbon nanotubes to control electrical and mechanical properties of hydrogels to fabricate contractile muscle myofibers. Adv. Mater. 2013, 25:4028-4034.
29. Shen J.Y., Chan-Park M.B.E., Feng Z.Q., Chan V., Feng Z.W. UV-embossed microchannel in biocompatible polymeric film: application to control of cell shape and orientation of muscle cells. J. Biomed. Mater Res. B 2006, 77B:423-430.
30. Ye X.F., Lu L., Kolewe M.E., Hearon K., Fischer K.M., Coppeta J., et al. Scalable units for building cardiac tissue. Adv. Mater. 2014, 26:7202-7208.
31. Guillame-Gentil O., Semenov O., Roca A.S., Groth T., Zahn R., Voros J., et al. Engineering the extracellular environment: strategies for building 2D and 3D cellular structures. Adv. Mater. 2010, 22:5443-5462.
32. Kurland N.E., Dey T., Kundu S.C., Yadavalli V.K. Precise patterning of silk microstructures using photolithography. Adv. Mater. 2013, 25:6207-6212.
33. Yao X., Peng R., Ding J.D. Cell-material interactions revealed via material techniques of surface patterning. Adv. Mater. 2013, 25:5257-5286.
34. Chen S.W., Zhang Q., Nakamoto T., Kawazoe N., Chen G.P. Highly active porous scaffolds of collagen and hyaluronic acid prepared by suppression of polyion complex formation. J. Mater Chem. B 2014, 2:5612-5619.
35. Zhang Q., Lu H.X., Kawazoe N., Chen G.P. Pore size effect of collagen scaffolds on cartilage regeneration. Acta Biomater. 2014, 10:2005-2013.
36. Hosseini V., Ahadian S., Ostrovidov S., Camci-Unal G., Chen S., Kaji H., et al. Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate. Tissue Eng. Pt A 2012, 18:2453-2465.
37. Flynn J.M., Meadows E., Fiorotto M., Klein W.H. Myogenin regulates exercise capacity and skeletal muscle metabolism in the adult mouse. Plos One 2010, 5:e13535.
38. Macfelda K., Kapeller B., Wilbacher I., Losert U.M. Behavior of cardiomyocytes and skeletal muscle cells on different extracellular matrix components - relevance for cardiac tissue engineering. Artif. Organ. 2007, 31:4-12.
39. Charest J.L., Garcia A.J., King W.P. Myoblast alignment and differentiation on cell culture substrates with microscale topography and model chemistries. Biomaterials 2007, 28:2202-2210.
40. Yang H.S., Ieronimakis N., Tsui J.H., Kim H.N., Suh K.Y., Reyes M., et al. Nanopatterned muscle cell patches for enhanced myogenesis and dystrophin expression in a mouse model of muscular dystrophy. Biomaterials 2014, 35:1478-1486.
41. Fujie T., Shi X., Ostrovidov S., Liang X., Nakajima K., Chen Y., et al. Spatial coordination of cell orientation directed by nanoribbon sheets. Biomaterials 2015, 53:86-94.
42. Jiao A., Trosper N.E., Yang H.S., Kim J., Tsui J.H., Frankel S.D., et al. Thermoresponsive nanofabricated substratum for the engineering of three-dimensional tissues with layer-by-layer architectural control. Acs Nano 2014, 8:4430-4439.
43. Sasagawa T., Shimizu T., Sekiya S., Haraguchi Y., Yamato M., Sawa Y., et al. Design of prevascularized three-dimensional cell-dense tissues using a cell sheet stacking manipulation technology. Biomaterials 2010, 31:1646-1654.
44. Hume S.L., Hoyt S.M., Walker J.S., Sridhar B.V., Ashley J.F., Bowman C.N., et al. Alignment of multi-layered muscle cells within three-dimensional hydrogel macrochannels. Acta Biomater. 2012, 8:2193-2202.
45. VanDusen K.W., Syverud B.C., Williams M.L., Lee J.D., Larkin L.M. Engineered skeletal muscle units for repair of volumetric muscle loss in the tibialis anterior muscle of a rat. Tissue Eng. Pt A 2014, 20:2920-2930.
46. Juhas M., Engelmayr G.C., Fontanella A.N., Palmer G.M., Bursac N. Biomimetic engineered muscle with capacity for vascular integration and functional maturation in vivo. P. Natl. Acad. Sci. U. S. A. 2014, 111:5508-5513.
47. Hinds S., Bian W.N., Dennis R.G., Bursac N. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 2011, 32:3575-3583.
48. Juhas M., Bursac N. Roles of adherent myogenic cells and dynamic culture in engineered muscle function and maintenance of satellite cells. Biomaterials 2014, 35:9438-9446.
49. Harridge S.D.R., Bottinelli R., Canepari M., Pellegrino M.A., Reggiani C., Esbjornsson M., et al. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflug Arch. Eur. J. Phys. 1996, 432:913-920.