The involvement of integrin β1 signaling in the migration and myofibroblastic differentiation of skin fibroblasts on anisotropic collagen-containing nanofibers

Biomaterials

Volumn 33, Issue 6, 2012, Pages 1791-1800

  Huang, Chengyang ^a   Fu, Xiaoling ^a   Liu, Jie ^b   Qi, Yanmei ^b   Li, Shaohua ^b   Wang, Hongjun ^a  

^a Stevens Institute of Technology   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Anisotropic nanofibers; Fibroblast to myofibroblast differentiation; Integrin 1 signaling; Normal human dermal fibroblasts

Indexed keywords

ANISOTROPIC MATRICES; CELL BEHAVIORS; CELL MORPHOLOGY; FIBER ORGANIZATION; FOCAL ADHESION KINASE; FOCAL ADHESIONS; IMMUNOSTAINING; INTEGRINS; INTRACELLULAR SIGNALING PATHWAYS; MOLECULAR ANALYSIS; NATIVE EXTRACELLULAR MATRIX; NEUTRALIZING ANTIBODIES; NORMAL HUMAN DERMAL FIBROBLASTS; PHENOTYPIC EXPRESSION; SIGNALING PATHWAYS; SKIN GRAFT; SKIN REGENERATION; WOUND HEALING PROCESS; WOUND REPAIR;

ADHESION; ALIGNMENT; ANISOTROPY; BIOMATERIALS; CELL CULTURE; COLLAGEN; ENZYME ACTIVITY; FIBERS; FIBROBLASTS; PHOSPHORYLATION; PIGMENTS; SIGNALING; TISSUE;

NANOFIBERS;

BETA1 INTEGRIN; NANOFIBER;

ANISOTROPY; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN FIBROBLAST;

ANISOTROPY; ANTIGENS, CD29; CELL DIFFERENTIATION; CELL MOVEMENT; COLLAGEN; FIBROBLASTS; HUMANS; MICROSCOPY, FLUORESCENCE; MYOFIBROBLASTS; NANOFIBERS; NANOTECHNOLOGY; PHENOTYPE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN; WOUND HEALING;

EID: 83555176263     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.11.025     Document Type: Article

References (45)

1. MacNeil S. Progress and opportunities for tissue-engineered skin. Nature 2007, 445:874-880.
2. Ma Z., Kotaki M., Inai R., Ramakrishna S. Potential of nanofiber matrix as tissue-engineering scaffolds. Tissue Eng 2005, 11:101-109.
3. Kumbar S.G., James R., Nukavarapu S.P., Laurencin C.T. Electrospun nanofiber scaffolds: engineering soft tissues. Biomed Mater 2008, 3:034002.
4. Venugopal J., Ramakrishna S. Biocompatible nanofiber matrices for the engineering of a dermal substitute for skin regeneration. Tissue Eng 2005, 11:847-854.
5. Yang X., Shah J.D., Wang H. Nanofiber enabled layer-by-layer approach toward three-dimensional tissue formation. Tissue Eng Part A 2009, 15:945-956.
6. Miyata T., Taira T., Noishiki Y. Collagen engineering for biomaterial use. Clin Mater 1992, 9:139-148.
7. Powell H.M., Supp D.M., Boyce S.T. Influence of electrospun collagen on wound contraction of engineered skin substitutes. Biomaterials 2008, 29:834-843.
8. Yang X., Ogbolu K.R., Wang H. Multifunctional nanofibrous scaffold for tissue engineering. J Exp Nanosci 2008, 3:329-345.
9. Dalby M.J., Riehle M.O., Johnstone H.J., Affrossman S., Curtis A.S. Polymer-demixed nanotopography: control of fibroblast spreading and proliferation. Tissue Eng 2002, 8:1099-1108.
10. Venugopal J.R., Zhang Y., Ramakrishna S. In vitro culture of human dermal fibroblasts on electrospun polycaprolactone collagen nanofibrous membrane. Artif Organs 2006, 30:440-446.
11. Zhang Y.Z., Venugopal J., Huang Z.M., Lim C.T., Ramakrishna S. Characterization of the surface biocompatibility of the electrospun PCL-collagen nanofibers using fibroblasts. Biomacromolecules 2005, 6:2583-2589.
12. Xie J., Macewan M.R., Ray W.Z., Liu W., Siewe D.Y., Xia Y. Radially aligned, electrospun nanofibers as dural substitutes for wound closure and tissue regeneration applications. ACS Nano 2010, 4:5027-5036.
13. Fu X, Wang H. Spatial arrangement of polycaprolatonec/collagen nanofibrous scaffolds regulates the wound-healing related behaviors of human adipose stromal cells. Tissue Eng Part A Epub ahead of print.
14. Yang X., Wang H. Electrospun functional nanofibrous scaffolds for tissue engineering. Tissue engineering 2010, 159-176. InTech, Croatia. D. Eberli (Ed.).
15. Martin P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276:75-81.
16. Singer A.J., Clark R.A. Cutaneous wound healing. N Engl J Med 1999, 341:738-746.
17. Darby I.A., Hewitson T.D. Fibroblast differentiation in wound healing and fibrosis. Int Rev Cytol 2007, 257:143-179.
18. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 2007, 127:526-537.
19. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993, 122:103-111.
20. Vi L., de Lasa C., DiGuglielmo G.M., Dagnino L. Integrin-linked kinase is required for TGF-beta1 induction of dermal myofibroblast differentiation. J Invest Dermatol 2011, 131:586-593.
21. Li Z., Dranoff J.A., Chan E.P., Uemura M., Sevigny J., Wells R.G. Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture. Hepatology 2007, 46:1246-1256.
22. Ayres C., Bowlin G.L., Henderson S.C., Taylor L., Shultz J., Alexander J., et al. Modulation of anisotropy in electrospun tissue-engineering scaffolds: analysis of fiber alignment by the fast Fourier transform. Biomaterials 2006, 27:5524-5534.
23. Eisenbarth E., Meyle J., Nachtigall W., Breme J. Influence of the surface structure of titanium materials on the adhesion of fibroblasts. Biomaterials 1996, 17:1399-1403.
24. Hansen M.B., Nielsen S.E., Kurt B. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Methods 1989, 119(2):203-210.
25. Yuan J.S., Reed A., Chen F., Stewart C.N. Statistical analysis of real-time PCR data. BMC Bioinform 2006, 7:85.
26. Webster T.J., Ergun C., Doremus R.H., Siegel R.W., Bizios R. Enhanced osteoclast-like cell functions on nanophase ceramics. Biomaterials 2001, 22:1327-1333.
27. Dalby M.J., Di Silvio L., Gurav N., Annaz B., Kayser M.V., Bonfield W. Optimizing HAPEX topography influences osteoblast response. Tissue Eng 2002, 8:453-467.
28. Dalby M.J. Topographically induced direct cell mechanotransduction. Med Eng Phys 2005, 27:730-742.
29. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 1999, 112(16):2677-2691.
30. Schlaepfer D.D., Mitra S.K. Multiple connections link FAK to cell motility and invasion. Curr Opin Genet Dev 2004, 14:92-101.
31. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006, 18:516-523.
32. Palecek S.P., Loftus J.C., Ginsberg M.H., Lauffenburger D.A., Horwitz A.F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 1997, 385:537-540.
33. Giancotti F.G., Ruoslahti E. Integrin signaling. Science 1999, 285:1028-1032.
34. Harburger D.S., Calderwood D.A. Integrin signalling at a glance. J Cell Sci 2009, 122:159-163.
35. Palecek S.P., Schmidt C.E., Lauffenburger D.A., Horwitz A.F. Integrin dynamics on the tail region of migrating fibroblasts. J Cell Sci 1996, 109:941-952.
36. Yamada K.M., Miyamoto S. Integrin transmembrane signaling and cytoskeletal control. Curr Opin Cell Biol 1995, 7:681-689.
37. Takagi J., Petre B.M., Walz T., Springer T.A. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 2002, 110:599-611.
38. Hamadi A., Bouali M., Dontenwill M., Stoeckel H., Takeda K., Ronde P. Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 2005, 118:4415-4425.
39. Vaughan M.B., Howard E.W., Tomasek J.J. Transforming growth factor-beta1 promotes the morphological and functional differentiation of the myofibroblast. Exp Cell Res 2000, 257:180-189.
40. Chan M.W., Chaudary F., Lee W., Copeland J.W., McCulloch C.A. Force-induced myofibroblast differentiation through collagen receptors is dependent on mammalian diaphanous (mDia). J Biol Chem 2010, 285:9273-9281.
41. Hinz B., Mastrangelo D., Iselin C.E., Chaponnier C., Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am J Pathol 2001, 159:1009-1020.
42. Ding Q., Gladson C.L., Wu H., Hayasaka H., Olman M.A. Focal adhesion kinase (FAK)-related non-kinase inhibits myofibroblast differentiation through differential MAPK activation in a FAK-dependent manner. J Biol Chem 2008, 283:26839-26849.
43. Dugina V., Fontao L., Chaponnier C., Vasiliev J., Gabbiani G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J Cell Sci 2001, 114:3285-3296.
44. Ng C.P., Hinz B., Swartz M.A. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 2005, 118:4731-4739.
45. Lee C.H., Shin H.J., Cho I.H., Kang Y.M., Kim I.A., Park K.D., et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 2005, 26:1261-1270.