Influence of the stiffness of three-dimensional alginate/collagen-I interpenetrating networks on fibroblast biology

Biomaterials

Volumn 35, Issue 32, 2014, Pages 8927-8936

  Branco da Cunha, Cristiana ^a,b,c,d,e   Klumpers, Darinka D ^a,b,f   Li, Weiwei A ^a,b   Koshy, Sandeep T ^a,b,g   Weaver, James C ^b   Chaudhuri, Ovijit ^h   Granja, Pedro L ^c,d   Mooney, David J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF PORTO   (Portugal)

^d INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^e University of Porto   (Portugal)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^g HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^h Stanford University   (United States)

Author keywords

ECM (extracellular matrix); Inflammation; Interpenetrating networks (IPNs); Mechanical properties; Wound dressing biomaterial; Wound healing

Indexed keywords

BIOLOGICAL MATERIALS; BIOMATERIALS; BIOMECHANICS; CELL CULTURE; FIBROBLASTS; MECHANICAL PROPERTIES; PATHOLOGY; REPAIR;

BIOACTIVE MOLECULES; DERMAL FIBROBLASTS; ECM (EXTRACELLULAR MATRIX); INFLAMMATION; POLYMER CONCENTRATIONS; THREE-DIMENSIONAL CULTURE; WOUND DRESSINGS; WOUND HEALING;

STIFFNESS;

ALGINIC ACID; COLLAGEN TYPE 1; CYCLOOXYGENASE 2; INTERLEUKIN 10; POLYMER; BIOMATERIAL; GLUCURONIC ACID; HEXURONIC ACID; PTGS2 PROTEIN, HUMAN;

ADULT; ARTICLE; CELL ENCAPSULATION; CELL STRUCTURE; CYTOLOGY; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; NANOFABRICATION; PRIORITY JOURNAL; RIGIDITY; SKIN FIBROBLAST; UPREGULATION; WOUND DRESSING; BIOLOGICAL DRESSING; CELL ADHESION; CELL CULTURE; CHEMISTRY; FIBROBLAST; GENETICS; METABOLISM; REGENERATION; SCANNING ELECTRON MICROSCOPY; TISSUE SCAFFOLD; WOUND HEALING;

ALGINATES; BIOCOMPATIBLE MATERIALS; BIOLOGICAL DRESSINGS; CELL ADHESION; CELLS, CULTURED; COLLAGEN TYPE I; CYCLOOXYGENASE 2; FIBROBLASTS; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; INTERLEUKIN-10; MICROSCOPY, ELECTRON, SCANNING; POLYMERS; REGENERATION; TISSUE SCAFFOLDS; UP-REGULATION; WOUND HEALING;

EID: 84905723265     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.06.047     Document Type: Article

References (62)

1. Singer A.J., Clark R.A.F. Cutaneous wound healing. NEngl J Med 1999, 341(10):738-746.
2. Martin P. Wound healing - aiming for perfect skin regeneration. Science 1997, 276(5309):75-81.
3. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005, 366(9498):1736-1743.
4. Menke N.B., Ward K.R., Witten T.M., Bonchev D.G., Diegelmann R.F. Impaired wound healing. Clin Dermatol 2007, 25(1):19-25.
5. Clark R.A.F., Ghosh K., Tonnesen M.G. Tissue engineering for cutaneous wounds. JInvest Dermatol 2007, 127(5):1018-1029.
6. Bell E., Ehrlich H.P., Buttle D.J., Nakatsuji T. Living tissue formed invitro and accepted as skin-equivalent tissue of full thickness. Science 1981, 211(4486):1052-1054.
7. Yannas I.V., Burke J.F., Orgill D.P., Skrabut E.M. Wound tissue can utilize a polymeric template to synthesize a functional extension of skin. Science 1982, 215(4529):174-176.
8. Yannas I.V., Lee E., Orgill D.P., Skrabut E.M., Murphy G.F. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc Natl Acad Sci USA 1989, 86(3):933-937.
9. Zahedi P., Rezaeian I., Ranaei-Siadat S.-O., Jafari S.-H., Supaphol P. Areview on wound dressings with an emphasis on electrospun nanofibrous polymeric bandages. Polym Adv Technol 2010, 21(2):77-95.
10. Boateng J.S., Matthews K.H., Stevens H.N.E., Eccleston G.M. Wound healing dressings and drug delivery systems: a review. JPharm Sci 2008, 97(8):2892-2923.
11. Wong V.W., Akaishi S., Longaker M.T., Gurtner G.C. Pushing back: wound mechanotransduction in repair and regeneration. JInvest Dermatol 2011, 131(11):2186-2196.
12. Wong V.W., Paterno J., Sorkin M., Glotzbach J.P., Levi K., Januszyk M., et al. Mechanical force prolongs acute inflammation via T-cell-dependent pathways during scar formation. FASEB J 2011, 25(12):4498-4510.
13. Wipff P.-J., Rifkin D.B., Meister J.-J., Hinz B. Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. JCell Biol 2007, 179(6):1311-1323.
14. Zhang H., Landmann F., Zahreddine H., Rodriguez D., Koch M., Labouesse M. Atension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 2011, 471(7336):99-103.
15. Boerckel J.D., Uhrig B.A., Willett N.J., Huebsch N., Guldberg R.E. Mechanical regulation of vascular growth and tissue regeneration invivo. Proc Natl Acad Sci USA 2011, 108(37):674-680.
16. Lo C.-M., Wang H.-B., Dembo M. Wang Y-l. Cell movement is guided by the rigidity of the substrate. Biophys J 2000, 79(1):144-152.
17. Gardel M.L., Sabass B., Ji L., Danuser G., Schwarz U.S., Waterman C.M. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. JCell Biol 2008, 183(6):999-1005.
18. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689.
19. Huebsch N., Arany P.R., Mao A.S., Shvartsman D., Ali O.A., Bencherif S.A., et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010, 9(6):518-526.
20. McNaught A.D., Wilkinson A.I.U.P.A.C. Compendium of chemical terminology 1997, UK Blackwell Scientific Publications, Oxford. 2nd ed.
21. Rowley J.A., Madlambayan G., Mooney D.J. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 1999, 20(1):45-53.
22. Chaudhuri O., Koshy S.T., Branco da Cunha C., Shin J.-W., Verbeke C.S., Allison K.H., et al. Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium. Nat Mater 2014, http://dx.doi.org/10.1038/nmat4009 [Epub ahead of print], PMID: 24930031.
23. Chaudhuri O., Parekh S.H., Fletcher D.A. Reversible stress softening of actin networks. Nature 2007, 445(7125):295-298.
24. Fabry B., Maksym G.N., Butler J.P., Glogauer M., Navajas D., Fredberg J.J. Scaling the microrheology of living cells. Phys Rev Lett 2001, 87(14):148102.
25. Crank J. The mathematics of diffusion 1979, Clarendon Press, Oxford University Press. 2nd ed.
26. Jokinen J., Dadu E., Nykvist P., Käpylä J., White D.J., Ivaska J., et al. Integrin-mediated cell adhesion to type I collagen fibrils. JBiol Chem 2004, 279(30):31956-31963.
27. Khetan S., Guvendiren M., Legant W.R., Cohen D.M., Chen C.S., Burdick J.A. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat Mater 2013, 12(5):458-465.
28. Peyton S.R., Raub C.B., Keschrumrus V.P., Putnam A.J. The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 2006, 27(28):4881-4893.
29. Kloxin A.M., Kasko A.M., Salinas C.N., Anseth K.S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 2009, 324(5923):59-63.
30. Trappmann B., Chen C.S. How cells sense extracellular matrix stiffness: a material's perspective. Curr Opin Biotechnol 2013, 24(5):948-953.
31. Park Y.D., Tirelli N., Hubbell J.A. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials 2003, 24(6):893-900.
32. Suri S., Schmidt C.E. Photopatterned collagen-hyaluronic acid interpenetrating polymer network hydrogels. Acta Biomater 2009, 5(7):2385-2397.
33. Akpalo E.B.L., Boissière M., Vancaeyzeele C., Fichet O., Larreta-Garde V. Fibrin-polyethylene oxide interpenetrating polymer networks: new selfsupported biomaterials combining the properties of both protein gel and synthetic polymer. Acta Biomater 2011, 7(24):2418-2427.
34. Sun J., Xiao W., Tang Y., Li K., Fan H. Biomimetic interpenetrating polymer network hydrogels based on methacrylated alginate and collagen for 3D pre-osteoblast spreading and osteogenic differentiation. Soft Matter 2012, 8:2398-2404.
35. Tong X., Yang F. Engineering interpenetrating network hydrogels as biomimetic cell niche with independently tunable biochemical and mechanical properties. Biomaterials 2014, 35(6):1807-1815.
36. Ulrich T.A., Jain A., Tanner K., MacKay J.L., Kumar S. Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 2010, 31(7):1875-1884.
37. Wen C., Lu L., Li X. Mechanically robust gelatin-alginate IPN hydrogels by a combination of enzymatic and ionic crosslinking approaches. Macromol Mater Eng 2013, 229(4):504-513.
38. Edwards C., Marks R. Evaluation of biomechanical properties of human skin. Clin Dermatol 1995, 13(4):375-380.
39. Y-l Yang, Leone L.M., Kaufman L.J. Elastic moduli of collagen gels can be predicted from two-dimensional confocal microscopy. Biophys J 2009, 97(7):2051-2060.
40. Wu C.-C., Ding S.-J., Wang Y.-H., Tang M.-J., Chang H.-C. Mechanical properties of collagen gels derived from rats of different ages. JBiomater Sci Polym Ed 2005, 16(10):1261-1275.
41. Arevalo R.C., Urbach J.S., Blair D.L. Size-dependent rheology of type-I collagen networks. Biophys J 2010, 99(8):L65-L67.
42. Achilli M., Mantovani D. Tailoring mechanical properties of collagen-based scaffolds for vascular tissue engineering: the effects of pH, temperature and ionic strength on gelation. Polymers 2010, 2:664-680.
43. Discher D.E., Janmey P. Wang Y-l. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310(5751):1139-1143.
44. Solon J., Levental I., Sengupta K., Georges P.C., Janmey P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 2007, 93(12):4453-4461.
45. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. JCell Biol 1972, 54(3):626-637.
46. Grinnell F. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol 2000, 10(9):362-365.
47. Tamariz E., Grinnell F. Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. Mol Biol Cell 2002, 13(11):3915-3929.
48. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 2003, 13(5):264-269.
49. Miron-Mendoza M., Seemann J., Grinnell F. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 2010, 31(25):6425-6435.
50. Dallon J.C., Ehrlich H.P. Areview of fibroblast-populated collagen lattices. Wound Repair Regen 2008, 16(4):472-479.
51. Jiang H., Grinnell F. Cell-matrix entanglement and mechanical anchorage of fibroblasts in three-dimensional collagen matrices. Mol Biol Cell 2005, 16(11):5070-5076.
52. Freyman T.M., Yannas I.V., Pek Y.-S., Yokoo R., Gibson L.J. Micromechanics of fibroblast contraction of a collagen-GAG matrix. Exp Cell Res 2001, 269(1):140-153.
53. Eastwood M., Porter R., Khan U., McGrouther G., Brown R. Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology. JCell Physiol 1996, 166(1):33-42.
54. Maia F.R., Fonseca K.B., Rodrigues G., Granja P.L., Barrias C.C. Matrix-driven formation of mesenchymal stem cell-extracellular matrix microtissues on soft alginate hydrogels. Acta Biomater 2014, 10(7):3197-3208.
55. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130(4):601-610.
56. Schwartz M.A., Chen C.S. Deconstructing dimensionality. Science 2013, 339(6118):402-404.
57. Wong V.W., Rustad K.C., Akaishi S., Sorkin M., Glotzbach J.P., Januszyk M., et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med 2011, 18(1):148-152.
58. Warner T.D., Mitchell J.A. Cyclooxygenases: new forms, new inhibitors, and lessons from the clinic. FASEB J 2004, 18(7):790-804.
59. Berg D.J., Zhang J., Lauricell D.M., Moore S.A. IL-10 is a central regulator of cyclooxygenase-2 expression and prostaglandin production. JImmunol 2001, 166(4):2674-2680.
60. Eming S.A., Krieg Thomas, Davidson Jeffrey M. Inflammation in wound repair: molecular and cellular mechanisms. JInvest Dermatol 2007, 127(3):514-525.
61. MacNeil S. Progress and opportunities for tissue-engineered skin. Nature 2007, 445(7130):874-880.
62. Kearney C.J., Mooney D.J. Macroscale delivery systems for molecular and cellular payloads. Nat Mater 2013, 12(11):1004-1017.