Silk scaffolds with tunable mechanical capability for cell differentiation

Acta Biomaterialia

Volumn 20, Issue , 2015, Pages 22-31

  Bai, Shumeng ^a   Han, Hongyan ^b   Huang, Xiaowei ^a   Xu, Weian ^b   Kaplan, David L ^a,c   Zhu, Hesun ^d   Lu, Qiang ^a  

^a SOOCHOW UNIVERSITY   (China)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c Tufts University   (United States)

^d BEIJING INSTITUTE OF TECHNOLOGY   (China)

Author keywords

Cell differentiation; Nanofibrous scaffolds; Silk fibroin; Tissue engineering

Indexed keywords

BIOMATERIALS; BIOMECHANICS; CELL CULTURE; CELL ENGINEERING; CELL SIGNALING; ENDOTHELIAL CELLS; SCAFFOLDS (BIOLOGY); SELF ASSEMBLY; STEM CELLS; STIFFNESS; TISSUE; TISSUE REGENERATION;

BOMBYX MORI SILK FIBROIN; CELL DIFFERENTIATION; INERT MATERIALS; MECHANICAL CAPABILITIES; NANOFIBROUS SCAFFOLDS; PEPTIDE DOMAINS; SILK FIBROIN; SILK SCAFFOLD; TISSUES ENGINEERINGS; TUNABLES;

NANOFIBERS;

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MOLECULAR SCAFFOLD; MYOD1 PROTEIN; NANOFIBER; SILK FIBROIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; BIOLOGICAL MARKER; BIOMATERIAL; FIBROIN; SILK;

ANIMAL CELL; ARTICLE; BETA SHEET; BIOCOMPATIBILITY; BOMBYX MORI; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; FREEZE DRYING; HYDROGEL; IN VITRO STUDY; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; RAT; RIGIDITY; TISSUE ENGINEERING; TISSUE REGENERATION; ANIMAL; BIOMECHANICS; BOMBYX; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; INFRARED SPECTROSCOPY; MATERIALS TESTING; MESENCHYMAL STROMA CELL; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD; ULTRASTRUCTURE; WETTABILITY; X RAY DIFFRACTION;

BOMBYX MORI; RATTUS;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMARKERS; BIOMECHANICAL PHENOMENA; BOMBYX; CELL DIFFERENTIATION; FIBROINS; MATERIALS TESTING; MESENCHYMAL STROMAL CELLS; NANOFIBERS; PROTEIN CONFORMATION; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SILK; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TISSUE SCAFFOLDS; WETTABILITY; X-RAY DIFFRACTION;

EID: 84929505568     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2015.04.004     Document Type: Article

References (58)

1. E. Cukierman, R. Pankov, D.R. Stevens, and K.M. Yamada Taking cell-matrix adhesions to the third dimension Science 23 2001 1708 1712
2. A. Abbott Cell culture: biology's new dimension Nature 424 2003 870 872
3. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689
4. H.N. Kim, A. Jiao, N.S. Hwang, M.S. Kim, D.H. Kang, and D.H. Kim Nanotopography-guided tissue engineering and regenerative medicine Adv Drug Deliver Rev 65 2013 536 558
5. C.C. Huang, S. Ravindran, Z. Yin, and A. George 3-D self-assembling leucine zipper hydrogel with tunable properties for tissue engineering Biomaterials 35 2014 5316 5326
6. D.S.W. Benoit, M.P. Schwartz, A.R. Durney, and K.S. Anseth Small function groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells Nat Mater 7 2008 816 823
7. J. Fu, Y.K. Wang, M.T. Yang, R.A. Desai, X. Yu, and Z. Liu Mechanical regulation of cell function with geometrically modulated elastomeric substrates Nat Methods 7 2010 733 736
8. X. Hu, S.H. Park, E.S. Gil, X.X. Xia, A.S. Weiss, and D.L. Kaplan The influence of elasticity and surface roughness on myogenic and osteogenic-differentiation of cells on silk-elastin biomaterials Biomaterials 32 2011 8979 8989
9. J.S. Park, J.S. Chu, A.D. Tsou, R. Diop, Z. Tang, and A. Wang The effect of matrix stiffness on the differentiation of mysenchymal stem cells in response to TGF-β Biomaterials 32 2011 3921 3930
10. A. Solanki, S.T.D. Chueng, P.T. Yin, R. Kappera, M. Chhowalla, and K.B. Lee Axonal alignment and enhanced neuronal differentiation of neural stem cells on graphene-nanoparticle hybrid structures Adv Mater 25 2013 5477 5482
11. G.H. Altman, F. Diaz, C. Jakuba, T. Calabro, R.L. Horan, and J.S. Chen Silk-based biomaterials Biomaterials 24 2003 401 416
12. Y. Wang, E. Bella, C.S.D. Lee, C. Migliaresi, L. Pelcastre, and Z. Schwartz The synergistic effects of 3-D porous silk fibroin matrix scaffold properties and hydrodynamic environment in cartilage tissue regeneration Biomaterials 31 2010 4672 4681
13. B.P. Partlow, C.W. Hanna, J. Rnjak-Kovacina, J.E. Moreau, M.B. Applegate, and K.A. Burke Highly tunable elastomeric silk biomaterials Adv Funct Mater 24 2014 4615 4624
14. J. Wu, J. Rnjak-Kovacina, Y. Du, M.L. Funderburgh, D.L. Kaplan, and J.L. Funderburgh Corneal stromal bioequivalents secreted on patterned silk substrates Biomaterials 35 2014 3744 3755
15. S.L. McNamara, J. Rnjak-Kovacina, D.F. Schmidt, T.J. Lo, and D.L. Kaplan Silk as a biocohesive sacrificial binder in the fabrication of hydroxyapatite load bearing scaffolds Biomaterials 35 2014 6941 6953
16. Z. Shao, and F. Vollrath Surprising strength of silkworm silk Nature 418 2002 741
17. L. Meinel, S. Hofmann, V. Karageorgiou, C. Kirker-Head, J. McCool, and G. Gronowicz The inflammatory responses to silk films in vitro and in vivo Biomaterials 26 2005 147 155
18. H.J. Kim, U.J. Kim, G. Vunjak-Novakovic, B.H. Min, and D.L. Kaplan Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells Biomaterials 26 2005 4442 4452
19. C. Jiang, X. Wang, R. Gunawidjaja, Y.H. Lin, M.K. Gupta, and D.L. Kaplan Mechanical properties of robust ultrathin silk fibroin films Adv Funct Mater 17 2007 2229 2237
20. Y. Wang, D.D. Rudym, A. Walsh, L. Abrahamsen, H.J. Kim, and H.S. Kim In vivo degradation of three-dimensional silk fibroin scaffolds Biomaterials 29 2008 3415 3428
21. A. Higuchi, Q.D. Ling, S.T. Hsu, and A. Umezawa Biomimetic cell culture proteins as extracellular matrices for stem cell differentiation Chem Rev 112 2012 4507 4540
22. P. Gong, W. Zheng, Z. Huang, W. Zhang, D. Xiao, and X. Jiang A strategy for the construction of controlled, three-dimensional, multilayered, tissue-like structures Adv Funct Mater 23 2013 42 46
23. S.S. Lee, B.J. Huang, S.R. Kaltz, S. Sur, C.J. Newcomb, and S.R. Stock Bone regeneration with low dose BMP-2 amplified by biomimetic supramolecular nanofibers within collagen scaffolds Biomaterials 34 2013 452 459
24. A. Li, A. Hokugo, A. Yalom, E.J. Berns, N. Stephanopoulos, and M.T. McClendon A bioengineered peripheral nerve construct using aligned peptide amphiphile nanofibers Biomaterials 35 2014 8780 8790
25. C. Cristalini, E.C. Rocchietti, L. Accomasso, A. Folino, C. Gallina, and L. Muratori The effect of bioartificial constructs that mimic myocardial structure and biomechanical properties on stem cell commitment towards cardiac lineage Biomaterials 35 2014 92 104
26. H. Liu, X. Li, G. Zhou, H. Fan, and Y. Fan Electrospun sulfated silk fibroin nanofibrous scaffolds for vascular tissue engineering Biomaterials 32 2011 3784 3793
27. X. Zhang, C.B. Baughman, and D.L. Kaplan In vitro evaluation of electrospun silk fibroin scaffolds for vascular cell growth Biomaterials 29 2008 2217 2227
28. M.P. Prabhakaran, J.R. Venugopal, and S. Ramakrishna Mesenchymal stem cell differentiation to neuronal cells on electrospun nanofibrous substrates for nerve tissue engineering Biomaterials 30 2009 4996 5003
29. A.J. Meinel, K.E. Kubow, E. Klotzsch, M. Garcia-Fuentes, M.L. Smith, and V. Vogel Optimization strategies for electrospun silk fibroin tissue engineering scaffolds Biomaterials 30 2009 3058 3067
30. Q. Lu, X. Wang, S. Lu, M. Li, D.L. Kaplan, and H. Zhu Nanofibrous architecture of silk fibroin scaffolds prepared with a mild self-assembly process Biomaterials 32 2011 1059 1067
31. J.M. Coburn, M. Gibson, S. Monagle, Z. Patterson, and J.H. Elisseeff Bioinspired nanofibers support chondrogenesis for articular cartilage repair Proc Natl Acad Sci USA 109 2012 10012 10017
32. D.N. Rockwood, R.C. Preda, T. Yucel, X. Wang, M.L. Lovett, and D.L. Kaplan Materials fabrication from Bombyx mori silk fibroin Nat Protoc 6 2011 1612 1631
33. D.Y. Yao, S. Dong, Q. Lu, X. Hu, D.L. Kaplan, and B.B. Zhang Salt-leached silk scaffolds with tunable mechanical properties Biomacromolecules 13 2012 3723 3729
34. S. Liu, C. Dong, G. Lu, Q. Lu, Z. Li, and D.L. Kaplan Bilayered vascular grafts based on silk proteins Acta Biomater 9 2013 8991 9003
35. U.J. Kim, J. Park, H.J. Kim, M. Wada, and D.L. Kaplan Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin Biomaterials 26 2005 2775 2785
36. R. Nazarov, H.J. Jin, and D.L. Kaplan Porous 3-D scaffolds from regenerated silk fibroin Biomacromolecules 5 2004 718 726
37. H.J. Jin, J. Park, V. Karageorgiou, U.J. Kim, R. Valluzzi, and P. Cebe Water-stable silk films with reduced β-sheet content Adv Funct Mater 15 2005 1241 1247
38. Q. Lu, H. Zhu, C. Zhang, F. Zhang, B. Zhang, and D.L. Kaplan Silk self-assembly mechanisms and control from thermodynamics to kinetics Biomacromolecules 13 2012 826 832
39. S. Bai, S. Liu, C. Zhang, W. Xu, Q. Lu, and H. Han Controllable transition of silk fibroin nanostructures: an insight into in vitro silk self-assembly process Acta Biomater 9 2013 7806 7813
40. S.S. Lin, G.Z. Lu, S.S. Liu, S.M. Bai, X. Liu, and Q. Lu Nanoscale control of silks for nanofibrous scaffold formation with an improved porous structure J Mater Chem B 2 2014 2622 2633
41. G.Z. Lu, S.S. Liu, S.S. Lin, D.L. Kaplan, and Q. Lu Silk porous scaffolds with nanofibrous microstructures and tunable properties Colloid Surf B 120 2014 28 37
42. F. Han, S. Liu, X. Liu, Y. Pei, S. Bai, and H. Zhao Woven silk fabric-reinforced silk nanofibrous scaffolds for regenerating load-bearing soft tissues Acta Biomater 10 2014 921 930
43. S. Bai, X. Zhang, Q. Lu, W. Sheng, L. Liu, and B. Dong Reversible hydrogel-solution system of silk with high beta-sheet content Biomacromolecules 15 2014 3044 3051
44. S.M. Bai, W.M. Zhang, Q. Lu, Q.H. Ma, D.L. Kaplan, and H.S. Zhu Silk nanofiber hydrogels with tunable modulus to regulate nerve stem cell fate J Mater Chem B 2 2014 6590 6600
45. J. Sun, D. Wei, Y. Zhu, M. Zhong, Y. Zuo, and H. Fan A spatial patternable macroporous hydrogel with cell-affinity domains to enhance cell spreading and differentiation Biomaterials 35 2014 4759 4768
46. K. Wingate, W. Bonani, Y. Tan, S.J. Bryant, and W. Tan Compressive elasticity of three-dimensional nanofiber matrix directs mesenchymal stem cell differentiation to vascular cells with endothelial or smooth muscle cell markers Acta Biomater 8 2012 1440 1449
47. M.T. Valarmathi, J.M. Davis, M.J. Yost, R.L. Goodwin, and J.D. Potts A three-dimensional model of vasculogenesis Biomaterials 30 2009 1098 1112
48. L.W. Dunne, T. Iyyanki, J. Hubenak, and A.B. Mathur Characterization of dielectrophoresis-aligned nanofibrous silk fibroin-chitosan scaffold and its interactions with endothelial cells for tissue engineering applications Acta Biomater 10 2014 3630 3640
49. N.F. Huang, J. Okogbaa, J.C. Lee, A. Jha, T.S. Zaitseva, and M.V. Paukshto The modulation of endothelial cell morphology, function, and survival using anisotropic nanofibrillar collagen scaffolds Biomaterials 34 2013 4038 4047
50. X. Wu, J. Hou, M. Li, J. Wang, D.L. Kaplan, and S. Lu Sodium dodecyl sulfate-induced rapid gelation of silk fibroin Acta Biomater 8 2012 2185 2192
51. A.B. Mathur, A.M. Collinsworth, W.M. Reichert, W.E. Kraus, and G.A. Truskey Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy J Biomech 34 2001 1545 1553
52. Y. Song, Y. Ju, G. Song, and Y. Morita In vitro proliferation and osteogenic differentiation of mesenchymal stem cells on nanoporous alumina Int J Nanomed 8 2013 2745 2756
53. S.J. Florczyk, D.J. Kim, D.L. Wood, and M. Zhang Influence of processing parameters on pore structure of 3D porous chitosan-alginate polyelectrolyte complex scaffolds J Biomed Mater Res A 98 2011 614 620
54. J. Zoldan, E.D. Karagiannis, C.Y. Lee, D.G. Anderson, R. Langer, and S. Levenberg The influence of scaffold elasticity on germ layer specification of human embryonic stem cells Biomaterials 32 2011 9612 9621
55. Y.S. Pek, A.C.A. Wan, and J.Y. Ying The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel Biomaterials 31 2010 385 391
56. C. Toma, M.F. Pittenger, K.S. Cahill, B.J. Byrne, and P.D. Kessler Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart Circulation 105 2002 93 98
57. C. Bardouille, J. Lehmann, P. Heimann, and H. Jockusch Growth and differentiation of permanent and secondary mouse myogenic cell lines on microcarriers Appl Microbiol Biotechnol 55 2001 556 562
58. J. Peloquin, J. Huynh, R.M. Williams, and C.A. Reinhart-King Indentation measurements of the subendothelial matrix in bovine carotid arteries J Biomech 44 2011 815 821