Mammary epithelial cell adhesion, viability, and infiltration on blended or coated silk fibroin-collagen type i electrospun scaffolds

Materials Science and Engineering C

Volumn 43, Issue , 2014, Pages 37-44

  Maghdouri White, Yas ^a,b   Bowlin, Gary L ^c   Lemmon, Christopher A ^b   Dréau, Didier ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b Virginia Commonwealth University   (United States)

^c University of Memphis   (United States)

Author keywords

Cell adhesion; Cell viability; Electrospun scaffolds; Mechanical properties; Silk fibroin; Type I collagen

Indexed keywords

ANIMALS; BIOCOMPATIBILITY; BIOMECHANICS; BLENDING; CELL ADHESION; CELLS; COLLAGEN; MECHANICAL PROPERTIES; TISSUE;

CELL VIABILITY; ELECTROSPUN SCAFFOLDS; EXTRACELLULAR MATRICES; MAMMARY EPITHELIAL CELLS; PHYSICAL AND MECHANICAL PROPERTIES; RECOGNITION SEQUENCE; SILK FIBROIN; TYPE I COLLAGEN;

SCAFFOLDS (BIOLOGY);

COLLAGEN TYPE 1; FIBROIN; SILK;

CELL ADHESION; CELL LINE; CYTOLOGY; HUMAN; MAMMARY GLAND; TISSUE SCAFFOLD;

CELL ADHESION; CELL LINE; COLLAGEN TYPE I; FIBROINS; HUMANS; MAMMARY GLANDS, HUMAN; SILK; TISSUE SCAFFOLDS;

EID: 84904563515     PISSN: 09284931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.msec.2014.06.037     Document Type: Article

References (73)

1. M.J. Bissell, D.C. Radisky, A. Rizki, V.M. Weaver, and O.W. Petersen The organizing principle: microenvironmental influences in the normal and malignant breast Differentiation 70 2002 537 546 (Pubitemid 36194318)
2. F. Pampaloni, E.G. Reynaud, and E.H.K. Stelzer The third dimension bridges the gap between cell culture and live tissue Nature reviews Mol. Cell. Biol. 8 2007 839 845 (Pubitemid 47462131)
3. T. Jacks, and R.A. Weinberg Taking the study of cancer cell survival to a new dimension Cell 111 2002 923 925 (Pubitemid 36044684)
4. U. Boudriot, R. Dersch, A. Greiner, and J.H. Wendorff Electrospinning approaches toward scaffold engineering - a brief overview Artif. Organs 30 2006 785 792 (Pubitemid 44521370)
5. Y. Cao, and B. Wang Biodegradation of silk biomaterials Int. J. Mol. Sci. 10 2009 1514 1524
6. X. Wang, X. Zhang, L. Sun, B. Subramanian, M.V. Maffini, and A. Soto et al. Preadipocytes stimulate ductal morphogenesis and functional differentiation of human mammary epithelial cells on 3D silk scaffolds Tissue Eng. A 15 2009 3087 3098
7. N. Minoura, S.I. Aiba, M. Higuchi, Y. Gotoh, M. Tsukada, and Y. Imai Attachment and growth of fibroblast cells on silk fibroin Biochem. Biophys. Res. Commun. 208 1995 511 516
8. Y. Wang, H. Kim, G. Vunjak-Novakovic, and D.L. Kaplan Stem cell-based tissue engineering with silk biomaterials Biomaterials 27 2006 6064 6082 (Pubitemid 44437574)
9. G.H. Altman, F. Diaz, C. Jakuba, T. Calabro, R.L. Horan, and J. Chen et al. Silk-based biomaterials Biomaterials 24 2003 401 416 (Pubitemid 35291198)
10. M.D. Pierschbacher, and E. Ruoslahti Variants of the cell recognition site of fibronectin that retain attachment-promoting activity Proc. Natl. Acad. Sci. U. S. A. 81 1984 5985 5988 (Pubitemid 15219582)
11. M.D. Pierschbacher, and E. Ruoslahti Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule Nature 309 1984 30 33 (Pubitemid 14134132)
12. E. Ruoslahti, and M.D. Pierschbacher New perspectives in cell adhesion: RGD and integrins Science 238 1987 491 497 (Pubitemid 17147032)
13. J. Chen, G.H. Altman, V. Karageorgiou, R. Horan, A. Collette, and V. Volloch et al. Human bone marrow stromal cell and ligament fibroblast responses on RGD-modified silk fibers J. Biomed. Mater. Res. Part A 67 2003 559 570 (Pubitemid 37522463)
14. Q. Zhang, S. Yan, and M. Li Silk fibroin based porous materials Materials 2 2009 2276 2295
15. S. Wohlrab, S. Müller, A. Schmidt, S. Neubauer, H. Kessler, and A. Leal-Egaña et al. Cell adhesion and proliferation on RGD-modified recombinant spider silk proteins Biomaterials 33 2012 6650 6659
16. R.E. Unger, K. Peters, M. Wolf, A. Motta, C. Migliaresi, and C.J. Kirkpatrick Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of human endothelial cells Biomaterials 25 2004 5137 5146 (Pubitemid 38510399)
17. T. Asakura, H. Nishi, A. Nagano, A. Yoshida, Y. Nakazawa, and M. Kamiya et al. NMR analysis of the fibronectin cell-adhesive sequence, Arg-Gly-Asp, in a recombinant silk-like protein and a model peptide Biomacromolecules 12 2011 3910 3916
18. B. Min, L. Jeong, Y.S. Nam, J. Kim, J.Y. Kim, and W.H. Park Formation of silk fibroin matrices with different texture and its cellular response to normal human keratinocytes Int. J. Biol. Macromol. 34 2004 223 230 (Pubitemid 39535653)
19. S.A. Sell, M.J. McClure, K. Garg, P.S. Wolfe, and G.L. Bowlin Electrospinning of collagen/biopolymers for regenerative medicine and cardiovascular tissue engineering Adv. Drug Deliv. Rev. 61 2009 1007 1019
20. C.B. Weinberg, and E. Bell A blood vessel model constructed from collagen and cultured vascular cells Science 231 1986 397 400 (Pubitemid 16108649)
21. U. Nöth, K. Schupp, A. Heymer, S. Kall, F. Jakob, and N. Schütze et al. Anterior cruciate ligament constructs fabricated from human mesenchymal stem cells in a collagen type I hydrogel Cytotherapy 7 2005 447 455 (Pubitemid 41671631)
22. S. Nehrer, H.A. Breinan, A. Ramappa, S. Shortkroff, G. Young, and T. Minas et al. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro J. Biomed. Mater. Res. 38 1997 95 104 (Pubitemid 27233097)
23. S.D. Gorham, T.P. Hyland, D.A. French, and M.J. Willins Cellular invasion and breakdown of three different collagen films in the lumbar muscle of the rat Biomaterials 11 1990 113 118 (Pubitemid 20119320)
24. C.V.M. Rodrigues, P. Serricella, A.B.R. Linhares, R.M. Guerdes, R. Borojevic, and M.A. Rossi et al. Characterization of a bovine collagen-hydroxyapatite composite scaffold for bone tissue engineering Biomaterials 24 2003 4987 4997 (Pubitemid 37237629)
25. S.R. Frenkel, B. Toolan, D. Menche, M.I. Pitman, and J.M. Pachence Chondrocyte transplantation using a collagen bilayer matrix for cartilage repair J. Bone Joint Surg. Br. Vol. 79 1997 831 836 (Pubitemid 27434509)
26. A.E. Sams, and A.J. Nixon Chondrocyte-laden collagen scaffolds for resurfacing extensive articular cartilage defects Osteoarthr. Cartil. 3 1995 47 59
27. W. Friess Collagen - biomaterial for drug delivery Eur. J. Pharm. Biopharm. 45 1998 113 136 (Pubitemid 28167739)
28. J. Beier, D. Klumpp, M. Rudisile, R. Dersch, J. Wendorff, and O. Bleiziffer et al. Collagen matrices from sponge to nano: new perspectives for tissue engineering of skeletal muscle BMC Biotechnol. 9 2009 34
29. P.P. Provenzano, K.W. Eliceiri, J.M. Campbell, D.R. Inman, J.G. White, and P.J. Keely Collagen reorganization at the tumor-stromal interface facilitates local invasion BMC Med. 4 2006 10.1186/1741-7015-4-38 (Pubitemid 46210997)
30. L. Ma, C. Gao, Z. Mao, J. Zhou, J. Shen, and X. Hu et al. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering Biomaterials 24 2003 4833
31. C.E. Butler, I.V. Yannas, C.C. Compton, C.A. Correia, and D.P. Orgill Comparison of cultured and uncultured keratinocytes seeded into a collagen-GAG matrix for skin replacements Br. J. Plast. Surg. 52 1999 127 132 (Pubitemid 29179105)
32. N.-. Dai, M.R. Williamson, N. Khammo, E.F. Adams, and A.G.A. Coombes Composite cell support membranes based on collagen and polycaprolactone for tissue engineering of skin Biomaterials 25 2004 4263 4271 (Pubitemid 38388587)
33. E.D. Boland, J.A. Matthews, K.J. Pawlowski, D.G. Simpson, G.E. Wnek, and G.L. Bowlin Electrospinning collagen and elastin: preliminary vascular tissue engineering Front. Biosci. 9 2004 1422 1432 (Pubitemid 39060854)
34. K.S. Rho, L. Jeong, G. Lee, B. Seo, Y.J. Park, and S. Hong et al. Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing Biomaterials 27 2006 1452 1461 (Pubitemid 41739571)
35. J. Chen, G. Chang, and J. Chen Electrospun collagen/chitosan nanofibrous membrane as wound dressing Colloids Surf. A Physicochem. Eng. Asp. 313-314 2008 183 188 (Pubitemid 350299894)
36. Y. Pang, X. Wang, A.A. Ucuzian, E.M. Brey, W.H. Burgess, and K.J. Jones et al. Local delivery of a collagen-binding FGF-1 chimera to smooth muscle cells in collagen scaffolds for vascular tissue engineering Biomaterials 31 2010 878 885
37. J. Emerman, and D. Pitelka Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes In Vitro. 13 5 1977 316 328 (Pubitemid 8118093)
38. 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
39. A. Sionkowska Current research on the blends of natural and synthetic polymers as new biomaterials: review Prog. Polym. Sci. 36 2011 1254 1276
40. W. He, T. Yong, W.E. Teo, Z. Ma, and S. Ramakrishna Fabrication and endothelialization of collagen-blended biodegradable polymer nanofibers: potential vascular graft for blood vessel tissue engineering Tissue Eng. 11 2005 1574 1588 (Pubitemid 41636442)
41. W. He, Z. Ma, T. Yong, W.E. Teo, and S. Ramakrishna Fabrication of collagen-coated biodegradable polymer nanofiber mesh and its potential for endothelial cells growth Biomaterials 26 2005 7606 7615 (Pubitemid 41187560)
42. H.K. Noh, S.W. Lee, J. Kim, J. Oh, K. Kim, and C. Chung et al. Electrospinning of chitin nanofibers: degradation behavior and cellular response to normal human keratinocytes and fibroblasts Biomaterials 27 2006 3934 3944
43. D.N. Rockwood, R.C. Preda, T. Yücel, X. Wang, M.L. Lovett, and D.L. Kaplan Materials fabrication from Bombyx mori silk fibroin Nat. Protoc. 6 2011 1612 1631
44. S. Sofia, M.B. McCarthy, G. Gronowicz, and D.L. Kaplan Functionalized silk-based biomaterials for bone formation J. Biomed. Mater. Res. 54 2001 139 148
45. M.J. McClure, P.S. Wolfe, D.G. Simpson, S.A. Sell, and G.L. Bowlin The use of air-flow impedance to control fiber deposition patterns during electrospinning Biomaterials 33 2012 771 779
46. Y. Maghdouri-White, L.W. Elmore, G.L. Bowlin, and D. Dréau Breast epithelial cell infiltration in enhanced electrospun silk scaffolds J. Tissue Eng. Regen. Med. 2013 10.1002/term.1778 [Epub ahead of print] PMID:23798502
47. J.A. Matthews, G.E. Wnek, D.G. Simpson, and G.L. Bowlin Electrospinning of collagen nanofibers Biomacromolecules 3 2002 232 238 (Pubitemid 34257140)
48. M. Li, M.J. Mondrinos, M.R. Gandhi, F.K. Ko, A.S. Weiss, and P.I. Lelkes Electrospun protein fibers as matrices for tissue engineering Biomaterials 26 2005 5999 6008 (Pubitemid 40805606)
49. Y. Wang, D.D. Rudym, A. Walsh, L. Abrahamsen, H. Kim, and H.S. Kim et al. In vivo degradation of three-dimensional silk fibroin scaffolds Biomaterials 29 2008 3415 3428
50. X. Zhang, M.R. Reagan, and D.L. Kaplan Electrospun silk biomaterial scaffolds for regenerative medicine Adv. Drug Deliv. Rev. 61 2009 988 1006
51. A.W. Morgan, K.E. Roskov, S. Lin-Gibson, D.L. Kaplan, M.L. Becker, and C.G. Simon et al. Characterization and optimization of RGD-containing silk blends to support osteoblastic differentiation Biomaterials 29 16 2008 2556 2563 10.1016/j.biomaterials.2008.02.007
52. H. Jin, S.V. Fridrikh, G.C. Rutledge, and D.L. Kaplan Electrospinning Bombyx mori silk with poly(ethylene oxide) Biomacromolecules 3 2002 1233 1239 (Pubitemid 35428773)
53. S. Talukdar, M. Mandal, D.W. Hutmacher, P.J. Russell, C. Soekmadji, and S.C. Kundu Engineered silk fibroin protein 3D matrices for in vitro tumor model Biomaterials 32 2011 2149 2159
54. B. Min, G. Lee, S.H. Kim, Y.S. Nam, T.S. Lee, and W.H. Park Electrospinning of silk fibroin nanofibers and its effect on the adhesion and spreading of normal human keratinocytes and fibroblasts in vitro Biomaterials 25 2004 1289
55. V. Kearns, A. MacIntosh, A. Crawford, and P. Hatton Silk-based biomaterials for tissue engineering Top. Tissue Eng. 4 2008 1 19
56. J. Debnath, S.K. Muthuswamy, and J.S. Brugge Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures Methods 30 2003 256 268 (Pubitemid 36677560)
57. C.T. Hanks Insulin and hydrocortisone influences on cultured rat tongue epithelium Arch. Oral Biol. 24 1979 765 776 (Pubitemid 10151546)
58. A. Bollig-Fischer, T.G. Dewey, S.P. Ethier, and I. Agoulnik Oncogene activation induces metabolic transformation resulting in insulin-independence in human breast cancer cells PLoS One 6 2011
59. P.I. Nedvetsky, S. Kwon, J. Debnath, and K.E. Mostov Cyclic AMP regulates formation of mammary epithelial acini in vitro Mol. Biol. Cell 23 2012 2973 2981
60. L. Bacakova, E. Filova, F. Rypacek, V. Svorcik, and V. Stary Cell adhesion on artificial materials for tissue engineering Physiol. Res. 53 2004 S35 S45
61. S.N. Krylov, and N.J. Dovichi Single-cell analysis using capillary electrophoresis: influence of surface support properties on cell injection into the capillary Electrophoresis 21 2000 767 773 (Pubitemid 30163402)
62. A. Lance, C. Yang, M. Swamydas, D. Dean, S. Deitch, and K.J.L. Burg et al. Increased extracellular matrix density decreases MCF10A breast cell acinus formation in 3D culture conditions J. Tissue Eng. Regen. Med. 2014 10.1002/term.1675
63. X. Wang, L. Sun, M.V. Maffini, A. Soto, C. Sonnenschein, and D.L. Kaplan A complex 3D human tissue culture system based on mammary stromal cells and silk scaffolds for modeling breast morphogenesis and function Biomaterials 31 2010 3920 3929
64. C.P. Barnes, S.A. Sell, E.D. Boland, D.G. Simpson, and G.L. Bowlin Nanofiber technology: designing the next generation of tissue engineering scaffolds Adv. Drug Deliv. Rev. 59 2007 1413 1433 (Pubitemid 350122771)
65. J. Venugopal, L.L. Ma, T. Yong, and S. Ramakrishna In vitro study of smooth muscle cells on polycaprolactone and collagen nanofibrous matrices Cell Biol. Int. 29 2005 861 867 (Pubitemid 41368055)
66. H.R. Pant, K. Nam, H. Oh, G. Panthi, H. Kim, and B. Kim et al. Effect of polymer molecular weight on the fiber morphology of electrospun mats J. Colloid Interface Sci. 364 2011 107 111
67. H.J. Cho, C.S. Ki, H. Oh, K.H. Lee, and I.C. Um Molecular weight distribution and solution properties of silk fibroins with different dissolution conditions Int. J. Biol. Macromol. 51 2012 336 341
68. A.G. Kanani, and S.H. Bahrami Review on electrospun nanofibers scaffold and biomedical applications Trends Biomater. Artif. Organs 24 2010 93 115
69. M.A. Meyers, P. Chen, A.Y. Lin, and Y. Seki Biological materials: structure and mechanical properties Prog. Mater. Sci. 53 2008 1 206 (Pubitemid 350017839)
70. C.M. Murphy, M.G. Haugh, and F.J. O'Brien The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering Biomaterials 31 2010 461 466
71. Y. Zhang, H. Ouyang, C.T. Lim, S. Ramakrishna, and Z. Huang Electrospinning of gelatin fibers and gelatin/PCL composite fibrous scaffolds J. Biomed. Mater. Res. B Appl. Biomater. 72 2004 156 165
72. P. Chomchalao, S. Pongcharoen, M. Sutheerawattananonda, and W. Tiyaboonchai Fibroin and fibroin blended three-dimensional scaffolds for rat chondrocyte culture Biomed. Eng. Online 12 2013 28
73. W. Tiyaboonchai, P. Chomchalao, S. Pongcharoen, M. Sutheerawattananonda, and P. Sobhon Preparation and characterization of blended Bombyx mori silk fibroin scaffolds Fibers Polym. 12 2011 324 333