Layer-by-layer films as biomaterials: bioactivity and mechanics

References

• Decher G. Fuzzy nanoassemblies: toward layered polymeric multicomposites. Science. 1997;277:1232–1237.
   Web of Science ®Google Scholar
• Hammond PT. Form and function in multilayer assembly: new applications at the nanoscale. Adv. Mater. 2004;16:1271–1293.
   Web of Science ®Google Scholar
• Hammond PT. Engineering materials layer-by-layer: challenges and opportunities in multilayer assembly. AIChE J. 2011;57:2928–2940.
   Web of Science ®Google Scholar
• Tang ZY, Wang Y, Podsiadlo P, Kotov NA. Biomedical applications of layer-by-layer assembly: from biomimetics to tissue engineering. Adv. Mater. 2006;18:3203–3224.
   Web of Science ®Google Scholar
• Picart C. Polyelectrolyte multilayer films: from physico-chemical properties to the control of cellular processes. Curr. Med. Chem. 2008;15:685–697.
   PubMed Web of Science ®Google Scholar
• Boudou T, Crouzier T, Ren KF, Blin G, Picart C. Multiple functionalities of polyelectrolyte multilayer films: new biomedical applications. Adv. Mater. 2010;22:441–467.
   PubMed Web of Science ®Google Scholar
• Gribova V, Auzely-Velty R, Picart C. Polyelectrolyte multilayer assemblies on materials surfaces: from cell adhesion to tissue engineering. Chem. Mater. 2012;24:854–869.
   PubMed Web of Science ®Google Scholar
• Jessel N, Atalar F, Lavalle P, Mutterer J, Decher G, Schaaf P, Voegel JC, Ogier J. Bioactive coatings based on a polyelectrolyte multilayer architecture functionalized by embedded proteins. Adv. Mater. 2003;15:692–695.
   Web of Science ®Google Scholar
• Benkirane-Jessel N, Lavalle P, Meyer F, Audouin F, Frisch B, Schaaf P, Ogier J, Decher G, Voegel JC. Control of monocyte morphology on and response to model surfaces for implants equipped with anti-inflammatory agent. Adv. Mater. 2004;16:1507–1511.
   Web of Science ®Google Scholar
• Berg MC, Yang SY, Hammond PT, Rubner MF. Controlling mammalian cell interactions on patterned polyelectrolyte multilayer surfaces. Langmuir. 2004;20:1362–1368.
   PubMed Web of Science ®Google Scholar
• Benkirane-Jessel N, Lavalle P, Hubsch E, Holl V, Senger B, Haikel Y, Voegel JC, Ogier J, Schaaf P. Short-time tuning of the biological activity of functionalized polyelectrolyte multilayers. Adv. Funct. Mater. 2005;15:648–654.
   Web of Science ®Google Scholar
• Olenych SG, Moussallem MD, Salloum DS, Schlenoff JB, Keller TCS. Fibronectin and cell attachment to cell and protein resistant polyelectrolyte surfaces. Biomacromolecules. 2005;6:3252–3258.
   PubMed Web of Science ®Google Scholar
• Picart C, Elkaim R, Richert L, Audoin T, Arntz Y, Cardoso MD, Schaaf P, Voegel JC, Frisch B. Primary cell adhesion on RGD-functionalized and covalently crosslinked thin polyelectrolyte multilayer films. Adv. Funct. Mater. 2005;15:83–94.
   Web of Science ®Google Scholar
• Jessel N, Oulad-Abdelghani M, Meyer F, Lavalle P, Haikel Y, Schaaf P, Voegel JC. Multiple and time-scheduled in situ DNA delivery mediated by beta-cyclodextrin embedded in a polyelectrolyte multilayer. Proc. Nat. Acad. Sci. 2006;103:8618–8621.
   PubMed Web of Science ®Google Scholar
• Vodouhê C, Le Guen E, Garza JM, Francius G, Déjugnat C, Ogier J, Schaaf P, Voegel JC, Lavalle P. Control of drug accessibility on functional polyelectrolyte multilayer films. Biomaterials. 2006;27:4149–4156.
   PubMed Web of Science ®Google Scholar
• Wood KC, Chuang HF, Batten RD, Lynn DM, Hammond PT. Controlling interlayer diffusion to achieve sustained, multiagent delivery from layer-by-layer thin films. Proc. Nat. Acad. Sci. 2006;103:10207–10212.
   PubMed Web of Science ®Google Scholar
• Wittmer CR, Phelps JA, Saltzman WM, Van Tassel PR. Fibronectin terminated multilayer films: protein adsorption and cell attachment studies. Biomaterials. 2007;28:851–860.
   PubMed Web of Science ®Google Scholar
• Schneider A, Vodouhe C, Richert L, Francius G, Le Guen E, Schaaf P, Voegel JC, Frisch B, Picart C. Multifunctional polyelectrolyte multilayer films: combining mechanical resistance, biodegradability, and bioactivity. Biomacromolecules. 2007;8:139–145.
   PubMed Web of Science ®Google Scholar
• Nadiri A, Kuchler-Bopp S, Mjahed H, Hu B, Haikel Y, Schaaf P, Voegel J-C, Benkirane-Jessel N. Cell apoptosis control using BMP4 and noggin embedded in a polyelectrolyte multilayer film. Small. 2007;3:1577–1583.
   PubMed Web of Science ®Google Scholar
• Wittmer CR, Phelps JA, Lepus CM, Saltzman WM, Harding MJ, Van Tassel PR. Multilayer nanofilms as substrates for hepatocellular applications. Biomaterials. 2008;29:4082–4090.
   PubMed Web of Science ®Google Scholar
• Jewell CM, Lynn DM. Multilayered polyelectrolyte assemblies as platforms for the delivery of DNA and other nucleic acid-based therapeutics. Adv. Drug Delivery Rev. 2008;60:979–999.
   Web of Science ®Google Scholar
• Liu XH, Zhang JT, Lynn DM. Ultrathin multilayered films that promote the release of two DNA constructs with separate and distinct release profiles. Adv. Mater. 2008;20:4148–4153.
   PubMed Web of Science ®Google Scholar
• Chen AA, Khetani SR, Lee S, Bhatia SN, Van Vliet KJ. Modulation of hepatocyte phenotype in vitro via chemomechanical tuning of polyelectrolyte multilayers. Biomaterials. 2009;30:1113–1120.
   Google Scholar
• Seo J, Lee H, Jeon J, Jang Y, Kim R, Char K, Nam J-M. Tunable layer-by-layer polyelectrolyte platforms for comparative cell assays. Biomacromolecules. 2009;10:2254–2260.
   Google Scholar
• Crouzier T, Ren K, Nicolas C, Roy C, Picart C. Layer-by-layer films as a biomimetic reservoir for rhBMP-2 delivery: controlled differentiation of myoblasts to osteoblasts. Small. 2009;5:598–608.
   PubMedGoogle Scholar
• Crouzier T, Szarpak A, Boudou T, Auzely-Velty R, Picart C. Polysaccharide-blend multi layers containing hyaluronan and heparin as a delivery system for rhBMP-2. Small. 2010;6:651–662.
   Google Scholar
• Macdonald ML, Rodriguez NM, Shah NJ, Hammond PT. Characterization of tunable FGF-2 releasing polyelectrolyte multilayers. Biomacromolecules. 2010;11:2053–2059.
   PubMed Web of Science ®Google Scholar
• Macdonald ML, Samuel RE, Shah NJ, Padera RF, Beben YM, Hammond PT. Tissue integration of growth factor-eluting layer-by-layer polyelectrolyte multilayer coated implants. Biomaterials. 2011;32:1446–1453.
   PubMed Web of Science ®Google Scholar
• Flessner RM, Yu Y, Lynn DM. Rapid release of plasmid DNA from polyelectrolyte multilayers: a weak poly(acid) approach. Chem. Commun. 2011;47:550–552.
   PubMed Web of Science ®Google Scholar
• Crouzier T, Fourel L, Boudou T, Albiges-Rizo C, Picart C. Presentation of BMP-2 from a soft biopolymeric film unveils its activity on cell adhesion and migration. Adv. Mater. 2011;23:H111–H118.
   Google Scholar
• Crouzier T, Sailhan F, Becquart P, Guillot R, Logeart-Avramoglou D, Picart C. The performance of BMP-2 loaded TCP/HAP porous ceramics with a polyelectrolyte multilayer film coating. Biomaterials. 2011;32:7543–7554.
   PubMed Web of Science ®Google Scholar
• Pavlukhina S, Sukhishvili S. Polymer assemblies for controlled delivery of bioactive molecules from surfaces. Adv. Drug Delivery Rev. 2011;63:822–836.
   PubMed Web of Science ®Google Scholar
• Shah NJ, Hong J, Hyder MN, Hammond PT. Osteophilic multilayer coatings for accelerated bone tissue growth. Adv. Mater. 2012;24:1445–1450.
   PubMed Web of Science ®Google Scholar
• Keeney M, Mathur M, Cheng E, Tong XM, Yang F. Effects of polymer end-group chemistry and order of deposition on controlled protein delivery from layer-by-layer assembly. Biomacromolecules. 2013;14:794–800.
   Google Scholar
• Guillot R, Gilde F, Becquart P, Sailhan F, Lapeyrere A, Logeart-Avramoglou D, Picart C. The stability of BMP loaded polyelectrolyte multilayer coatings on titanium. Biomaterials. 2013;34:5737–5746.
   Google Scholar
• Shah NJ, Hyder MN, Moskowitz JS, Quadir MA, Morton SW, Seeherman HJ, Padera RF, Spector M, Hammond PT. Surface-mediated bone tissue morphogenesis from tunable nanolayered implant coatings. Sci. Transl. Med. 2013;5:ra83.
   Web of Science ®Google Scholar
• Almodovar J, Crouzier T, Selimovic S, Boudou T, Khademhosseini A, Picart C. Gradients of physical and biochemical cues on polyelectrolyte multilayer films generated via microfluidics. Lab Chip. 2013;13:1562–1570.
   Google Scholar
• Bechler SL, Si Y, Yu Y, Ren J, Liu B, Lynn DM. Reduction of intimal hyperplasia in injured rat arteries promoted by catheter balloons coated with polyelectrolyte multilayers that contain plasmid DNA encoding PKC delta. Biomaterials. 2013;34:226–236.
   Google Scholar
• Saurer EM, Jewell CM, Roenneburg DA, Bechler SL, Torrealba JR, Hacker TA, Lynn DM. Polyelectrolyte multilayers promote stent-mediated delivery of DNA to vascular tissue. Biomacromolecules. 2013;14:1696–1704.
   Google Scholar
• Min J, Braatz RD, Hammond PT. Tunable staged release of therapeutics from layer-by-layer coatings with clay interlayer barrier. Biomaterials. 2014;35:2507–2517.
   PubMedGoogle Scholar
• Manna U, Kratochvil MJ, Lynn DM. Superhydrophobic polymer multilayers that promote the extended, long-term release of embedded water-soluble agents. Adv. Mater. 2013;25:6405–6409.
   Google Scholar
• Vrana NE, Erdemli O, Francius G, Fahs A, Rabineau M, Debry C, Tezcaner A, Keskin D, Lavalle P. Double entrapment of growth factors by nanoparticles loaded into polyelectrolyte multilayer films. J. Mater. Chem. B. 2014;2:999–1008.
   Google Scholar
• Harris JJ, DeRose PM, Bruening ML. Synthesis of passivating, nylon-like coatings through cross-linking of ultrathin polyelectrolyte films. J. Am. Chem. Soc. 1999;121:1978–1979.
   Web of Science ®Google Scholar
• Mendelsohn JD, Yang SY, Hiller J, Hochbaum AI, Rubner MF. Rational design of cytophilic and cytophobic polyelectrolyte multilayer thin films. Biomacromolecules. 2003;4:96–106.
   PubMed Web of Science ®Google Scholar
• Schuetz P, Caruso F. Copper-assisted weak polyelectrolyte multilayer formation on microspheres and subsequent film crosslinking. Adv. Funct. Mater. 2003;13:929–937.
   Web of Science ®Google Scholar
• Richert L, Boulmedais F, Lavalle P, Mutterer J, Ferreux E, Decher G, Schaaf P, Voegel JC, Picart C. Improvement of stability and cell adhesion properties of polyelectrolyte multilayer films by chemical cross-linking. Biomacromolecules. 2004;5:284–294.
   PubMed Web of Science ®Google Scholar
• Richert L, Engler AJ, Discher DE, Picart C. Elasticity of native and cross-linked polyelectrolyte multilayer films. Biomacromolecules. 2004;5:1908–1916.
   PubMed Web of Science ®Google Scholar
• Thompson MT, Berg MC, Tobias IS, Rubner MF, Van Vliet KJ. Tuning compliance of nanoscale polyelectrolyte multilayers to modulate cell adhesion. Biomaterials. 2005;26:6836–6845.
   PubMed Web of Science ®Google Scholar
• Schneider A, Francius G, Obeid R, Schwinte P, Hemmerle J, Frisch B, Schaaf P, Voegel JC, Senger B, Picart C. Polyelectrolyte multilayers with a tunable Young's modulus: influence of film stiffness on cell adhesion. Langmuir. 2006;22:1193–1200.
   PubMedGoogle Scholar
• Francius G, Hemmerle J, Ohayon J, Schaaf P, Voegel JC, Picart C, Senger B. Effect of crosslinking on the elasticity of polyelectrolyte multilayer films measured by colloidal probe AFM. Microsc. Res. Tech. 2006;69:84–92.
   PubMed Web of Science ®Google Scholar
• Schneider A, Richert L, Francius G, Voegel JC, Picart C. Elasticity, biodegradability and cell adhesive properties of chitosan/hyaluronan multilayer films. Biomed. Mater. 2007;2:S45–S51.
   PubMed Web of Science ®Google Scholar
• Ren KF, Crouzier T, Roy C, Picart C. Polyelectrolyte multilayer films of controlled stiffness modulate myoblast cell differentiation. Adv. Funct. Mater. 2008;18:1378–1389.
   PubMedGoogle Scholar
• Hillberg AL, Holmes CA, Tabrizian M. Effect of genipin cross-linking on the cellular adhesion properties of layer-by-layer assembled polyelectrolyte films. Biomaterials. 2009;30:4463–4470.
   PubMed Web of Science ®Google Scholar
• Blacklock J, Sievers TK, Handa H, You YZ, Oupicky D, Mao GZ, Mohwald H. Cross-linked bioreducible layer-by-layer films for increased cell adhesion and transgene expression. J. Phys. Chem. B. 2010;114:5283–5291.
   Google Scholar
• Blacklock J, Vetter A, Lankenau A, Oupicky D, Mohwald H. Tuning the mechanical properties of bioreducible multilayer films for improved cell adhesion and transfection activity. Biomaterials. 2010;31:7167–7174.
   Google Scholar
• Mehrotra S, Hunley SC, Pawelec KM, Zhang LX, Lee I, Baek S, Chan C. Cell adhesive behavior on thin polyelectrolyte multilayers: cells attempt to achieve homeostasis of its adhesion energy. Langmuir. 2010;26:12794–12802.
   PubMed Web of Science ®Google Scholar
• Larkin AL, Davis RM, Rajagopalan P. Biocompatible, detachable, and free-standing polyelectrolyte multilayer films. Biomacromolecules. 2010;11:2788–2796.
   Google Scholar
• Boudou T, Crouzier T, Nicolas C, Ren K, Picart C. Polyelectrolyte multilayer nanofilms used as thin materials for cell mechano-sensitivity studies. Macromol. Biosci. 2011;11:77–89.
   Google Scholar
• Phelps JA, Morisse S, Hindie M, Degat MC, Pauthe E, Van Tassel PR. Nanofilm biomaterials: localized cross-linking to optimize mechanical rigidity and bioactivity. Langmuir. 2011;27:1123–1130.
   Google Scholar
• Chaubaroux C, Vrana E, Debry C, Schaaf P, Senger B, Voegel J-C, Haikel Y, Ringwald C, Hemmerle J, Lavalle P, Boulmedais F. Collagen-based fibrillar multilayer films cross-linked by a natural agent. Biomacromolecules. 2012;13:2128–2135.
   Google Scholar
• Pelham RJ, Wang YL. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Nat. Acad. Sci. 1997;94:13661–13665.
   PubMed Web of Science ®Google Scholar
• Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 2004;86:617–628.
   PubMed Web of Science ®Google Scholar
• Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310:1139–1143.
   PubMed Web of Science ®Google Scholar
• Semler EJ, Lancin PA, Dasgupta A, Moghe PV. Engineering hepatocellular morphogenesis and function via ligand-presenting hydrogels with graded mechanical compliance. Biotechnol. Bioeng. 2005;89:296–307.
   Google Scholar
• Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–689.
   PubMed Web of Science ®Google Scholar
• Buxboim A, Rajagopal K, Brown AEX, Discher DE. How deeply cells feel: methods for thin gels. J. Phys Condens. Matter. 2010;22:194116.
   PubMed Web of Science ®Google Scholar
• Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA. Optimal matrix rigidity for stress-fibre polarization in stem cells. Nature Phys. 2010;6:468–473.
   PubMed Web of Science ®Google Scholar
• Potts JR, Campbell ID. Structure and function of fibronectin modules. Matrix Biol. 1996;15:313–320.
   PubMed Web of Science ®Google Scholar
• Etienne O, Schneider A, Taddei C, Richert L, Schaaf P, Voegel JC, Egles C, Picart C. Degradability of polysaccharides multilayer films in the oral environment: an in vitro and in vivo study. Biomacromolecules. 2005;6:726–733.
   PubMed Web of Science ®Google Scholar
• Picart C, Schneider A, Etienne O, Mutterer J, Schaaf P, Egles C, Jessel N, Voegel JC. Controlled degradability of polysaccharide multilayer films in vitro and in vivo. Adv. Funct. Mater. 2005;15:1771–1780.
   Web of Science ®Google Scholar
• Wu C, Aslan S, Gand A, Wolenski JS, Pauthe E, Van Tassel PR. Porous nanofilm biomaterials via templated layer-by-layer assembly. Adv. Funct. Mater. 2013;23:67–74.
   Google Scholar
• Ricotti L, Taccola S, Bernardeschi I, Pensabene V, Dario P, Menciassi A. Quantification of growth and differentiation of C2C12 skeletal muscle cells on PSS-PAH-based polyelectrolyte layer-by-layer nanofilms. Biomed. Mater. 2011;6:031001.
   Web of Science ®Google Scholar
• Hu X, Park SH, Gil ES, Xia XX, Weiss AS, Kaplan DL. The influence of elasticity and surface roughness on myogenic and osteogenic-differentiation of cells on silk-elastin biomaterials. Biomaterials. 2011;32:8979–8989.
   PubMedGoogle Scholar
• Logeart-Avramoglou D, Bourguignon M, Oudina K, Ten Dijke P, Petite H. An assay for the determination of biologically active bone morphogenetic proteins using cells transfected with an inhibitor of differentiation promoter-luciferase construct. Anal. Biochem. 2006;349:78–86.
   Google Scholar
• Gand A, Hindie M, Chacon D, Van Tassel PR, Pauthe E. Nanotemplated polyelectrolyte films as porous biomolecular delivery systems: application to the growth factor BMP-2. BioMatter. 2014;4. doi:10.4161/biom.28823.
   Google Scholar
• Iwasaki S, Tsuruoka N, Hattori A, Sato M, Tsujimoto M, Kohno M. Distribution and characterization of specific cellular-binding proteins for bone morphogenetic protein-2. J. Biol. Chem. 1995;270:5476–5482.
   PubMed Web of Science ®Google Scholar
• Sun XJ, Peng W, Yang ZL, Ren ML, Zhang SC, Zhang WG, Zhang LY, Xiao K, Wang ZG, Zhang B, Wang J. Heparin-Chitosan-coated acellular bone matrix enhances perfusion of blood and vascularization in bone tissue engineering scaffolds. Tissue Eng. Part A. 2011;17:2369–2378.
   Google Scholar
• He LM, Shi YF, Han Q, Zuo QH, Ramakrishna S, Xue W, Zhou LB. Surface modification of electrospun nanofibrous scaffolds via polysaccharide-protein assembly multilayer for neurite outgrowth. J. Mater. Chem. 2012;22:13187–13196.
   Web of Science ®Google Scholar