Scaffolds for tissue engineering must be designed to direct desired events such as cell attachment, growth, and differentiation. The incorporation of extracellular matrix-derived peptides into biomaterials has been proposed to mimic biochemical signals. In this study, three synthetic fragments of fibronectin, vitronectin, and stromal-derived factor-1 were investigated for the first time as potential adhesive sequences for cardiomyocytes (CMs) compared to smooth muscle cells. CMs are responsive to all peptides to differing degrees, demonstrating the existence of diverse adhesion mechanisms. The pretreatment of nontissue culture well surfaces with the (Arginine-Glycine-Aspartic Acid) RGD sequence anticipated the appearance of CMs' contractility compared to the control (fibronectin-coated well) and doubled the length of cell viability. Future prospects are the inclusion of these sequences into biomaterial formulation with the improvement in cell adhesion that could play an important role in cell retention during dynamic cell seeding.
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References
1.
RadisicM., ParkH., GenechtS., CannizzaroC., LangerR., Vunjak- NovakovicG.Biomimetic approach to cardiac tissue engineering. Philos Trans R Soc Lond B Biol Sci, 362:1357. 2007.
2.
KyleS., AggeliA., InghamE., McPhersonM.J.Recombinant self-assembling peptides as biomaterials for tissue engineering. Biomaterials, 31:9395. 2010.
3.
Von der MarkK., ParkJ., BauerS., SchmukiP.Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res, 339:1531. 2010.
ShiJ., VotrubaA.R., FarokhzadO.C., LangerR.Nanotechnology in drug delivery and tissue engineering: from discovery to applications. Nano Lett, 10:3223. 2010.
7.
RomanoN.H., SenguptaD., ChungC., HeilshornS.C.Protein-engineered biomaterials: nanoscale mimics of the extracellular matrix. Biochim Biophys Acta, 1810:339. 2011.
HumphriesM.J., TravisM.A., ClarkK., MouldA.P.Mechanisms of integration of cells and extracellular matrices by integrins. Mould Biochem Soc Trans, 32:822. 2004.
10.
JeonW.B., ParkB.H., WeiJ., ParkR.W.Stimulation of fibroblasts and neuroblasts on a biomimetic extracellular matrix consisting of tandem repeats of the elastic VGVPG domain and RGD motif. J Biomed Mater Res A, 97:152. 2011.
11.
ShekaranA., GarciaA.J.Nanoscale engineering of extracellular matrix-mimetic bioadhesive surfaces and implants for tissue engineering. Biochim Biophys Acta, 1810:350. 2011.
12.
PierschbacherM.D., RuoslahtiE.Variants of the cell recognition site of fibronectin that retain attachment-promoting activity. Proc Natl Acad Sci U S A, 1:5985. 1984.
13.
PytelaR., PierschbacherM.D., RuoslahtiE.Identification and isolation of a 140 kDa cell surface glycoprotein with properties expected of a fibronectin receptor. Cell, 40:191. 1985.
14.
LeissM., BeckmannK., GirósA., CostellM., FässlerR.The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr Opin Cell Biol, 20:502. 2008.
15.
BacakovaL., FilovaE., KubiesD., MachovaL., ProksV., MalinovaV., LisaV., RypacekF.Adhesion and growth of vascular smooth muscle cells in cultures on bioactive RGD peptide-carrying polylactides. J Mater Sci Mater Med, 18:1317. 2007.
16.
MannB.K., GobinA.S., TsaiA.T., SchmedlenR.H., WestJ.L.Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and protolytically degradable domains: synthetic ECM analogs for tissue engineering. Biomaterials, 22:3045. 2001.
17.
ShacharM., Tsur-GangO., DvirT., LeorJ., CohenS.The effect of immobilized RGD peptide in alginate scaffolds on cardiac tissue engineering. Acta Biomater, 7:152. 2010.
18.
DettinM., ConconiM.T., GambarettoR., BagnoA., Di BelloC., MentiA.M., GrandiC., ParnigottoP.P.Effect of synthetic peptides on osteoblast adhesion. Biomaterials, 26:4507. 2005.
19.
SchvartzI., SegerD., ShaltielS.Vitronectin. Int J Biochem Cell Biol, 31:539. 1999.
20.
DettinM., BagnoA., MorpurgoM., CacchioliA., ConconiM.T., Di BelloC., GabbiC., GambarettoR., ParnigottoP.P., PizzinatoS., RavanettiF., GuglielmiM.Evaluation of silicon dioxide-based coating enriched with bioactive peptides mapped on human vitronectin and fibronectin: in vitro and in vivo assays. Tissue Eng, 12:3509. 2006.
21.
MichelJ.B.Anoikis in the cardiovascular system: known and unknown extracellular mediators. Arterioscler Thromb Vasc Biol, 23:2146. 2003.
OrbachR., Adler-AbramovichL., ZigersonS., Mironi-HarpazI., SeliktarD., GazitE.Self-assembled Fmoc-peptides as a platform for the formation of nanostructures and hydrogels. Biomacromolecules, 10:2646. 2009.
24.
DettinM., PasquatoA., ScarinciC., ZanchettaM., De RossiA., Di BelloC.Anti-HIV activity and conformational studies of peptides derived from the C-terminal sequenze of SDF-1. J Med Chem, 47:3058. 2004.
25.
OakesB.W., BattyA.C., HandleyC.J., SandbergL.B.The synthesis of elastin, collagen, and glycosaminoglycans by high density primary cultures of neonatal rat aortic smooth muscle. An ultrastructural and biochemical study. Eur J Cell Biol, 27:34. 1982.
26.
RapuanoB.E., WuC., MacDonaldD.E.Osteoblast-like cell adhesion to bone sialoprotein peptides. J Orthop Res, 22:353. 2004.
27.
WallukatG., NissenE., NeichelD., HarrisJ.Spontaneously beating neonatal rat heart myocyte culture-a model to characterize angiotensin II at(1) receptor autoantibodies in patients with preeclampsia. In Vitro Cell Dev Biol Anim, 38:376. 2002.
28.
WeikertC., Eppenberger-EberhardtM., EppenbergerH.M.Cellular engineering of ventricular adult rat cardiomyocytes. Cardiovasc Res, 59:874. 2003.
29.
LandegrenU.Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens. J Immunol Methods, 67:379. 1984.
30.
BoatengS.Y., LateefS.S., MosleyW., HartmanT.J., HanleyL., RussellB.RGD and YIGSR synthetic peptides facilitate cellular adhesion identical to that of laminin and fibronectin but alter the physiology of neonatal cardiac myocytes. Am J Physiol Cell Physiol, 288:C30. 2005.
31.
CushingM.C., JaeggliM.P., MastersK.S., LeinwandL.A., AnsethK.S.Serum deprivation improves seeding and repopulation of acellular matrices with valvular interstitial cells. J Biomed Mater Res A, 75:232. 2005.
32.
MannB.K., WestJ.L.Cell adhesion peptides alter smooth muscle cell adhesion, proliferation, migration, and matrix protein synthesis on modified surfaces and in polymer scaffolds. J Biomed Mater Res, 60:86. 2002.
33.
CarragherN.O., LevkauB., RossR., RainesE.W.Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesions that correlates with cleavage of pp125(FAK), paxillin, and talin. J Cell Biol, 147:619. 1999.
34.
SandemanS.R., LloydA.W., TigheB.J., FranklinV., LiJ., LydonF., LiuC.S., MannD.J., JamesS.E., MartinR.A model for the preliminary biological screening of potential keratoprosthetic biomaterials. Biomaterials, 24:4729. 2003.
ConconiM.T., GhezzoF., DettinM., UrbaniL., GrandiC., GuidolinD., NicoB., Di BelloC., RibattiD., ParnigottoP.P.Effects on in vitro and in vivo angiogenesis induced by small peptides carrying adhesion sequences. J Pept Sci, 16:349. 2010.
40.
ChillakuriC.R., JonesC., MardonH.J.Heparin binding domain in vitronectin is required for oligomerization and thus enhances integrin mediated cell adhesion and spreading. FEBS Lett, 584:3287. 2010.
41.
PettyJ.M., LenoxC.C., WeissD.J., PoynterM.E., SurattB.T.Crosstalk between CXCR4/stromal derived factor-1 and VLA-4/VCAM-1 pathways regulates neutrophil retention in the bone marrow. J Immunol, 182:604. 2009.
42.
Iwai-KanaiE., YuanH., HuangC., SayenM.R., Perry-GarzaC.N., KimL., GottliebR.A.A method to measure cardiac autophagic flux in vivo. Autophagy, 4:322. 2008.
43.
ThybergJ.Caveolae and cholesterol distribution in vascular smooth muscle cells of different phenotypes. J Histochem Cytochem, 50:185. 2002.
44.
DongY., LiP., ChenC.B., WangZ.H., MaP., ChenG.Q.The improvement of fibroblast growth on hydrophobic biopolyesters by coating with polyhydroxyalkanoate granule binding protein PhaP fused with cell adhesion motif RGD. Biomaterials, 31:8921. 2010.
45.
LuchiniA.Transcriptional analysis of osteoblast-biomaterial interaction [Ph.D. thesis]Bioengineering, University of Padova, 2005.
46.
KaoW.J., LeeD., SchenseJ.C., HubbellJ.A.Fibronectin modulates macrophage adhesion and FBGC formation: the role of RGD, PHSRN, and PRRARV domains. J Biomed Mater Res, 55:79. 2001.
47.
HilfikerA., KasperC., HassR., HaverichA.Mesenchymal stem cells and progenitor cells in connective tissue engineering and regenerative medicine: is there a future for transplantation?Langenbecks Arch Surg, 396:489. 2011.
48.
HeldmanA.W., ZambranoJ.P., HareJ.M.Cell therapy for heart disease: where are we in 2011?J Am Coll Cardiol, 57:466. 2011.
49.
GabrielM., AmerongenG.P., Van HinsberghV.W., AmerongenA.V., ZentnerA.Direct grafting of RGD-motif-containing peptide on the surface of polycaprolactone films. J Biomater Sci Polym Ed, 17:567. 2006.
50.
BlitP.H., ShenY.H., ErnstingM.J., WoodhouseK.A., SanterreJ.P.Bioactivation of porous polyurethane scaffolds using fluorinated RGD surface modifiers. J Biomed Mater Res A, 94:1226. 2010.
51.
MassiaS.P., HubbellJ.A.Covalently attached GRGD on polymer surfaces promotes biospecific adhesion of mammalian cells. Ann N Y Acad Sci, 589:261. 1990.
52.
LiJ., DingM., FuQ., TanH., XieX., ZhongY.A novel strategy to graft RGD peptide on biomaterials surfaces for endothelization of small-diamater vascular grafts and tissue engineering blood vessel. J Mater Sci Mater Med, 19:2595. 2008.
53.
KumarP., PillayV., ModiG., ChoonaraY.E., du ToitL.C., NaidooD.Self-assembling peptides: implications for patenting in drug delivery and tissue engineering. Recent Pat Drug Deliv Formul, 5:24. 2011.
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