A novel approach that preserved most mesenchymal stem cell (MSC) characteristics was developed using MSC encapsulation in a hydrogel based on hyaluronic acid (HA). An optimized HA–hydrogel composition, whose characteristics were assessed by scanning electron microscopy and viscoelastic property analyses, as well as the more favorable MSC seeding density, was established. These optimal three-dimensional MSC culture conditions allowed morphological cell remodeling, maintained the expression of stem cell markers over 28 days of culture, and preserved MSC differentiation plasticity. In addition, MSCs in HA–hydrogel submitted for 7 days to mechanical constraint that aimed at mimicking in vivo cardiac beat displayed enhanced cell survival by more than 40% compared to static culture conditions. Thus, the optimized HA-based hydrogel provides a niche for MSCs, which preserves their properties and opens ways for cell therapy, in particular in aortic repair medicine.
PampaloniF., ReynaudE.G., StelzerE.H.The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol, 8:839. 2007.
5.
SahaK., PollockJ.F., SchafferD.V., HealyK.E.Designing synthetic materials to control stem cell phenotype. Curr Opin Chem Biol, 11:381. 2007.
6.
DawsonE., MapiliG., EricksonK., TaqviS., RoyK.Biomaterials for stem cell differentiation. Adv Drug Deliv Rev, 60:215. 2008.
7.
FacchiniA., LisignoliG., CristinoS., RosetiL., De FranceschiL., MarconiE.et al.Human chondrocytes and mesenchymal stem cells grown onto engineered scaffold. Biorheology, 43:471. 2006.
8.
Garcia-FuentesM., MeinelA.J., HilbeM., MeinelL., MerkleH.P.Silk fibroin/hyaluronan scaffolds for human mesenchymal stem cell culture in tissue engineering. Biomaterials, 30:5068. 2009.
9.
CristinoS., GrassiF., ToneguzziS., PiacentiniA., GrigoloB., SantiS.et al.Analysis of mesenchymal stem cells grown on a three-dimensional HYAFF 11-based prototype ligament scaffold. J Biomed Mater Res A, 73:275. 2005.
10.
GerechtS., BurdickJ.A., FerreiraL.S., TownsendS.A., LangerR., Vunjak-NovakovicG.Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci U S A, 104:11298. 2007.
11.
KuttyJ.K., ChoE., Soo LeeJ., VyavahareN.R., WebbK.The effect of hyaluronic acid incorporation on fibroblast spreading and proliferation within PEG-diacrylate based semi-interpenetrating networks. Biomaterials, 28:4928. 2007.
HuntN.C., GroverL.M.Cell encapsulation using biopolymer gels for regenerative medicine. Biotechnol Lett, 32:733. 2010.
17.
WoerlyS., PinetE., De RobertisL., BousminaM., LarocheG., RoitbackT.et al.Heterogeneous PHPMA hydrogels for tissue repair and axonal regeneration in the injured spinal cord. J Biomater Sci Polym Ed, 9:681. 1998.
18.
DobsonK.R., ReadingL., HabereyM., MarineX., ScuttA.Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int, 65:411. 1999.
19.
JeonE.S., MoonH.J., LeeM.J., SongH.Y., KimY.M., BaeY.C.et al.Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-beta-dependent mechanism. J Cell Sci, 119:4994. 2006.
20.
LiX., FengQ., WangW., CuiF.Chemical characteristics and cytocompatibility of collagen-based scaffold reinforced by chitin fibers for bone tissue engineering. J Biomed Mater Res B Appl Biomater, 77:219. 2006.
21.
MahoneyM.J., AnsethK.S.Three-dimensional growth and function of neural tissue in degradable polyethylene glycol hydrogels. Biomaterials, 27:2265. 2006.
22.
WeberL.M., HaydaK.N., AnsethK.S.Cell-matrix interactions improve beta-cell survival and insulin secretion in three-dimensional culture. Tissue Eng Part A, 14:1959. 2008.
23.
FrithJ.E., ThomsonB., GeneverP.G.Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng Part C Methods, 16:735. 2010.
24.
GumbinerB.M.Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell, 84:345. 1996.
25.
LeeS.B., JeonH.W., LeeY.W., ChoS.K., LeeY.M., SongK.W., Hwa HongM.H.P.Artificial dermis composed of gelatin, hyaluronic acid and (1–3),(1–6)-b-glucan. Macromol Res, 11:368. 2003.
26.
LiuY., Zheng ShuX., PrestwichG.D.Biocompatibility and stability of disulfide-crosslinked hyaluronan films. Biomaterials, 26:4737. 2005.
PrestwichG.D., LiuY., YuB., ShuX.Z., ScottA.3-D culture in synthetic extracellular matrices: new tissue models for drug toxicology and cancer drug discovery. Adv Enzyme Regul, 47:196. 2007.
29.
GhoshK., RenX.D., ShuX.Z., PrestwichG.D., ClarkR.A.Fibronectin functional domains coupled to hyaluronan stimulate adult human dermal fibroblast responses critical for wound healing. Tissue Eng, 12:601. 2006.
30.
ShuX.Z., AhmadS., LiuY., PrestwichG.D.Synthesis and evaluation of injectable, in situ crosslinkable synthetic extracellular matrices for tissue engineering. J Biomed Mater Res A, 79:902. 2006.
31.
ShuX.Z., LiuY., PalumboF., PrestwichG.D.Disulfide-crosslinked hyaluronan-gelatin hydrogel films: a covalent mimic of the extracellular matrix for in vitro cell growth. Biomaterials, 24:3825. 2003.
32.
ZhangF., HeC., CaoL., FengW., WangH., MoX.et al.Fabrication of gelatin-hyaluronic acid hybrid scaffolds with tunable porous structures for soft tissue engineering. Int J Biol Macromol, 48:474. 2011.
33.
WatanabeK., NakamuraM., OkanoH., ToyamaY.Establishment of three-dimensional culture of neural stem/progenitor cells in collagen type-1 gel. Restor Neurol Neurosci, 25:109. 2007.
LeeM., WuB.M., DunnJ.C.Effect of scaffold architecture and pore size on smooth muscle cell growth. J Biomed Mater Res A, 87:1010. 2008.
39.
LeeS.T., YunJ.I., JoY.S., MochizukiM., van der VliesA.J., KontosS.et al.Engineering integrin signaling for promoting embryonic stem cell self-renewal in a precisely defined niche. Biomaterials, 31:1219. 2010.
40.
GhoshK., PanZ., GuanE., GeS., LiuY., NakamuraT.et al.Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials, 28:671. 2007.
41.
WengL., ChenX., ChenW.Rheological characterization of in situ crosslinkable hydrogels formulated from oxidized dextran and N-carboxyethyl chitosan. Biomacromolecules, 8:1109. 2007.
42.
LiY.J., ChungE.H., RodriguezR.T., FirpoM.T., HealyK.E.Hydrogels as artificial matrices for human embryonic stem cell self-renewal. J Biomed Mater Res A, 79:1. 2006.
43.
FlynnL., PrestwichG.D., SempleJ.L., WoodhouseK.A.Adipose tissue engineering with naturally derived scaffolds and adipose-derived stem cells. Biomaterials, 28:3834. 2007.
CimettaE., FlaibaniM., MellaM., SerenaE., BoldrinL., De CoppiP.et al.Enhancement of viability of muscle precursor cells on 3D scaffold in a perfusion bioreactor. Int J Artif Organs, 30:415. 2007.
50.
TiituV., PulkkinenH.J., ValonenP., PulliainenO., KellomakiM., LammiM.J.et al.Bioreactor improves the growth and viability of chondrocytes in the knitted poly-L,D-lactide scaffold. Biorheology, 45:539. 2008.
51.
LiY., ZhaoZ., SongJ., FengY., WangY., LiX.et al.Cyclic force upregulates mechano-growth factor and elevates cell proliferation in 3D cultured skeletal myoblasts. Arch Biochem Biophys, 490:171. 2009.
52.
ButcherJ.T., BarrettB.C., NeremR.M.Equibiaxial strain stimulates fibroblastic phenotype shift in smooth muscle cells in an engineered tissue model of the aortic wall. Biomaterials, 27:5252. 2006.
