Control of cell adhesion by mechanical reinforcement of soft polyelectrolyte films with nanoparticles

Langmuir

Volumn 28, Issue 18, 2012, Pages 7249-7257

  Schmidt, Stephan ^a,b   Madaboosi, Narayanan ^a,b   Uhlig, Katja ^a   Köhler, Dorothee ^b   Skirtach, André ^b,c   Duschl, Claus ^a   Möhwald, Helmuth ^b   Volodkin, Dmitry V ^a  

^a FRAUNHOFER INSTITUTE FOR BIOMEDICAL ENGINEERING   (Germany)

^b MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMEDICAL APPLICATIONS; CHEMICAL CROSS-LINKING; CRITICAL SURFACES; ENGINEERING APPLICATIONS; FILM SURFACES; FORM CLUSTERS; GOLD NANOPARTICLE; HYALURONIC ACIDS; MATERIAL DENSITY; MECHANICAL PROPERTIES OF POLYMERS; MECHANICAL REINFORCEMENT; PERCOLATION THRESHOLDS; POLY-L-LYSINE; POLYELECTROLYTE FILMS; PROTEIN INTERACTION; SURFACE PARAMETER; SWELLING RATIO;

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; CELL CULTURE; CROSSLINKING; ELASTIC MODULI; FUNCTIONAL POLYMERS; MEDICAL APPLICATIONS; NANOPARTICLES; OPTIMIZATION; POLYELECTROLYTES; STIFFNESS; SURFACE ROUGHNESS; SURFACES;

CELL ADHESION;

ELECTROLYTE; GOLD; HYALURONIC ACID; METAL NANOPARTICLE; POLYLYSINE;

ANIMAL; ARTICLE; ARTIFICIAL MEMBRANE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CHEMISTRY; CYTOLOGY; FIBROBLAST; MOUSE; PARTICLE SIZE; SURFACE PROPERTY;

ANIMALS; CELL ADHESION; ELECTROLYTES; FIBROBLASTS; GOLD; HYALURONIC ACID; MEMBRANES, ARTIFICIAL; METAL NANOPARTICLES; MICE; MICROSCOPY, ATOMIC FORCE; PARTICLE SIZE; POLYLYSINE; SURFACE PROPERTIES;

EID: 84860720211     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la300635z     Document Type: Article

References (67)

1. von der Mark, K.; Park, J.; Bauer, S.; Schmuki, P. Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix Cell Tissue Res. 2010, 339, 131-153
2. Alves, N. M.; Pashkuleva, I.; Reis, R. L.; Mano, J. F. Controlling Cell Behavior Through the Design of Polymer Surfaces Small 2010, 6, 2208-2220
3. Lutolf, M. P. Integration column: Artificial ECM: expanding the cell biology toolbox in 3D Integr. Biol. 2009, 1, 235-241
4. Rehfeldt, F.; Engler, A. J.; Eckhardt, A.; Ahmed, F.; Discher, D. E. Cell responses to the mechanochemical microenvironment - Implications for regenerative medicine and drug delivery Adv. Drug Delivery Rev. 2007, 59, 1329-1339 (Pubitemid 350088256)
5. Volodkin, D. V.; Madaboosi, N.; Blacklock, J.; Skirtach, A. G.; Mohwald, H. Surface-Supported Multilayers Decorated with Bio-active Material Aimed at Light-Triggered Drug Delivery Langmuir 2009, 25, 14037-14043
6. Skirtach, A. G.; Volodkin, D. V.; Mohwald, H. Bio-interfaces-Interaction of PLL/HA Thick Films with Nanoparticles and Microcapsules ChemPhysChem 2010, 11, 822-829
7. Dubiel, E. A.; Martin, Y.; Vermette, P. Bridging the Gap Between Physicochemistry and Interpretation Prevalent in Cell-Surface Interactions Chem. Rev. 2011, 111, 2900-2936
8. Geiger, B.; Spatz, J. P.; Bershadsky, A. D. Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 2009, 10, 21-33
9. Discher, D. E.; Janmey, P.; Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate Science 2005, 310, 1139-1143 (Pubitemid 41681732)
10. Saha, K.; Keung, A. J.; Irwin, E. F.; Li, Y.; Little, L.; Schaffer, D. V.; Healy, K. E. Substrate Modulus Directs Neural Stem Cell Behavior Biophys. J. 2008, 95, 4426-4438
11. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification Cell 2006, 126, 677-689 (Pubitemid 44233625)
12. Tay, C. Y.; Irvine, S. A.; Boey, F. Y. C.; Tan, L. P.; Venkatraman, S. Micro-/Nano-engineered Cellular Responses for Soft Tissue Engineering and Biomedical Applications Small 2011, 7, 1361-1378
13. Decher, G.; Hong, J. D.; Schmitt, J. uildup of Ultrathin Multilayer Films by a Self-. Assembly Process 0.3. Consecutively Alternating Adsorption of Anionic and. Cationic Polyelectrolytes on Charged Surfaces Thin Solid Films 1992, 210, 831-835
14. Decher, G. Fuzzy nanoassemblies: Toward layered polymeric multicomposites Science 1997, 277, 1232-1237 (Pubitemid 27449063)
15. Boudou, T.; Crouzier, T.; Ren, K. F.; Blin, G.; Picart, C. Multiple Functionalities of Polyelectrolyte Multilayer Films: New Biomedical Applications Adv. Mater. 2010, 22, 441-467
16. Picart, C. Polyelectrolyte multilayer films: From physico-chemical properties to the control of cellular processes Curr. Med. Chem. 2008, 15, 685-697 (Pubitemid 351516804)
17. Rinaudo, M. Main properties and current applications of some polysaccharides as biomaterials Polym. Int. 2008, 57, 397-430 (Pubitemid 351283101)
18. Zelikin, A. N., Drug Releasing Polymer Thin Films: New Era of Surface-Mediated Drug Delivery. ACS Nano 4, 2494-2509.
19. Jan, E.; Kotov, N. A. Successful Differentiation of Mouse Neural Stem Cells on Layer-by-Layer Assembled Single-Walled Carbon Nanotube Composite Nano Lett. 2007, 7, 1123-1128 (Pubitemid 46834384)
20. Kommireddy, D. S.; Sriram, S. M.; Lvov, Y. M.; Mills, D. K. Stem cell attachment to layer-by-layer assembled TiO2 nanoparticle thin films Biomaterials 2006, 27, 4296-4303 (Pubitemid 43674177)
21. Kommireddy, D. S.; Ichinose, I.; Lvov, Y. M.; Mills, D. K. Nanoparticle Multilayers: Surface Modification for Cell Attachment and Growth J. Biomed. Nanotechnol. 2005, 1, 286-290
22. Picart, C.; Lavalle, P.; Hubert, P.; Cuisinier, F. J. G.; Decher, G.; Schaaf, P.; Voegel, J. C. Buildup mechanism for poly(L-lysine)/hyaluronic acid films onto a solid surface Langmuir 2001, 17, 7414-7424 (Pubitemid 35338225)
23. Sorrenti, E.; Ball, V.; Del Frari, D.; Arnoult, C.; Toniazzo, V.; Ruch, D., Incorporation of Copper (II) Phtalocyanines as Model Dyes in Exponentially Growing Polyelectrolyte Multilayer Films: A Multiparametric Investigation. J. Phys. Chem. C 115, 8248-8259.
24. Wang, X. F.; Ji, J. Postdiffusion of Oligo-Peptide within Exponential Growth Multilayer Films for Localized Peptide Delivery Langmuir 2009, 25, 11664-11671
25. Srivastava, S.; Podsiadlo, P.; Critchley, K.; Zhu, J.; Qin, M.; Shim, B. S.; Kotov, N. A. Single-Walled Carbon Nanotubes Spontaneous Loading into Exponentially Grown LBL Films Chem. Mater. 2009, 21, 4397-4400
26. Srivastava, S.; Ball, V.; Podsiadlo, P.; Lee, J.; Ho, P.; Kotov, N. A. Reversible Loading and Unloading of Nanoparticles in 'Exponentially' Growing Polyelectrolyte LBL Films J. Am. Chem. Soc. 2008, 130, 3748-3749 (Pubitemid 351429830)
27. Volodkin, D. V.; Delcea, M.; MoÌ̂hwald, H.; Skirtach, A. G. Remote Near-IR Light Activation of a Hyaluronic Acid/Poly(l-lysine) Multilayered Film and Film-Entrapped Microcapsules ACS Appl. Mater. Interfaces 2009, 1, 1705-1710
28. Podsiadlo, P.; Michel, M.; Lee, J.; Verploegen, E.; Kam, N. W. S.; Ball, V.; Qi, Y.; Hart, A. J.; Hammond, P. T.; Kotov, N. A. Exponential growth of LBL films with incorporated inorganic sheets Nano Lett. 2008, 8, 1762-1770
29. Volodkin, D.; Arntz, Y.; Schaaf, P.; Moehwald, H.; Voegel, J. C.; Ball, V. Composite multilayered biocompatible polyelectrolyte films with intact liposomes: stability and temperature triggered dye release Soft Matter 2008, 4, 122-130 (Pubitemid 350255989)
30. Volodkin, D. V.; Schaaf, P.; Mohwald, H.; Voegel, J. C.; Ball, V. Effective embedding of liposomes into polyelectrolyte multilayered films: the relative importance of lipid-polyelectrolyte and interpolyelectrolyte interactions Soft Matter 2009, 5, 1394-1405
31. Zhang, X.; Sharma, K. K.; Boeglin, M.; Ogier, J.; Mainard, D.; Voegel, J. C.; Mely, Y.; Benkirane-Jessel, N. Transfection ability and intracellular DNA pathway of nanostructured gene-delivery systems Nano Lett. 2008, 8, 2432-2436
32. Vodouhê, C.; Guen, E. L.; Garza, J. M.; Francius, G.; Déjugnat, C.; Ogier, J.; Schaaf, P.; Voegel, J.-C.; Lavalle, P. Control of drug accessibility on functional polyelectrolyte multilayer films Biomaterials 2006, 27, 4149-4156
33. Schneider, A.; Francius, G.; Obeid, R.; Schwinte, P.; Hemmerle, J.; Frisch, B.; Schaaf, P.; Voegel, J. C.; Senger, B.; Picart, C. Polyelectrolyte multilayers with a tunable Young's modulus: Influence of film stiffness on cell adhesion Langmuir 2006, 22, 1193-1200 (Pubitemid 43282178)
34. Ren, K. F.; Fourel, L.; Rouviere, C. G.; Albiges-Rizo, C.; Picart, C., Manipulation of the adhesive behaviour of skeletal muscle cells on soft and stiff polyelectrolyte multilayers. Acta Biomater. 6, 4238-4248.
35. Richert, L.; Boulmedais, F.; Lavalle, P.; Mutterer, J.; Ferreux, E.; Decher, G.; Schaaf, P.; Voegel, J. C.; Picart, C. Improvement of stability and cell adhesion properties of polyelectrolyte multilayer films by chemical cross-linking Biomacromolecules 2004, 5, 284-294 (Pubitemid 38404462)
36. Jessel, N.; Atalar, F.; Lavalle, P.; Mutterer, J.; Decher, G.; Schaaf, P.; Voegel, J. C.; Ogier, J. Bioactive Coatings Based on a Polyelectrolyte Multilayer Architecture Functionalized by Embedded Proteins Adv. Mater. 2003, 15, 692-695
37. Thierry, B.; Winnik, F. o. M.; Merhi, Y.; Silver, J.; Tabrizian, M. Bioactive Coatings of Endovascular Stents Based on Polyelectrolyte Multilayers Biomacromolecules 2003, 4, 1564-1571 (Pubitemid 37455567)
38. Phelps, J. A.; Morisse, S.; Hindie, M.; Degat, M. C.; Pauthe, E.; Van Tassel, P. R., Nanofilm Biomaterials: Localized Cross-Linking To Optimize Mechanical Rigidity and Bioactivity. Langmuir 27, 1123-1130.
39. Etienne, O.; Schneider, A.; Taddei, C.; Richert, L.; Schaaf, P.; Voegel, J.-C.; 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 (Pubitemid 40467814)
40. Podsiadlo, P.; Kaushik, A. K.; Arruda, E. M.; Waas, A. M.; Shim, B. S.; Xu, J. D.; Nandivada, H.; Pumplin, B. G.; Lahann, J.; Ramamoorthy, A.; Kotov, N. A. Ultrastrong and stiff layered polymer nanocomposites Science 2007, 318, 80-83 (Pubitemid 47538034)
41. Fiedler, B.; Gojny, F. H.; Wichmann, M. H. G.; Nolte, M. C. M.; Schulte, K. Fundamental aspects of nano-reinforced composites Compos. Sci. Technol. 2006, 66, 3115-3125 (Pubitemid 44529218)
42. Zhang, Q.; Archer, L. A. Poly(ethylene oxide)/silica nanocomposites: Structure and rheology Langmuir 2002, 18, 10435-10442
43. Francius, G.; Hemmerle, J.; Ball, V.; Lavalle, P.; Picart, C.; Voegel, J. C.; Schaaf, P.; Senger, B. Stiffening of soft polyelectrolyte architectures by multilayer capping evidenced by viscoelastic analysis of AFM indentation measurements J. Phys. Chem. C 2007, 111, 8299-8306 (Pubitemid 47012684)
44. Lavalle, P.; Picart, C.; Mutterer, J. r.; Gergely, C.; Reiss, H.; Voegel, J.-C.; Senger, B.; Schaaf, P. Modeling the Buildup of Polyelectrolyte Multilayer Films Having Exponential Growth J. Phys. Chem. B 2003, 108, 635-648
45. Dimitriadis, E. K.; Horkay, F.; Maresca, J.; Kachar, B.; Chadwick, R. S. Determination of elastic moduli of thin layers of soft material using the atomic force microscope Biophys. J. 2002, 82, 2798-2810 (Pubitemid 34441316)
46. Richert, L.; Schneider, A.; Vautier, D.; Vodouhe, C.; Jessel, N.; Payan, E.; Schaaf, P.; Voegel, J. C.; Picart, C. Imaging cell interactions with native and crosslinked polyelectrolyte multilayers Cell Biochem. Biophys. 2006, 44, 273-285 (Pubitemid 43172324)
47. Semenov, O. V.; Malek, A.; Bittermann, A. G.; Voros, J.; Zisch, A. H. Engineered Polyelectrolyte Multilayer Substrates for Adhesion, Proliferation, and Differentiation of Human Mesenchymal Stem Cells Tissue Eng. Part A 2009, 15, 2977-2990
48. Picart, C.; Mutterer, J.; Richert, L.; Luo, Y.; Prestwich, G. D.; Schaaf, P.; Voegel, J. C.; Lavalle, P. Molecular basis for the explanation of the exponential growth of polyelectrolyte multilayers Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12531-12535
49. Lee, H.; Jang, Y.; Seo, J.; Nam, J. M.; Char, K. Nanoparticle- Functionalized Polymer Platform for Controlling Metastatic Cancer Cell Adhesion, Shape, and Motility ACS Nano 2011, 5, 5444-5456
50. Coletti, D.; Scaramuzz, F. A.; Montemiglio, L. C.; Pristera, A.; Teodori, L.; Adamo, S.; Barteri, M. Culture of skeletal muscle cells in unprecedented proximity to a gold surface J. Biomed. Mater. Res. Part A 2009, 91A, 370-377
51. Wittmer, C. R.; Phelps, J. A.; Saltzman, W. M.; Van Tassel, P. R. Fibronectin terminated multilayer films: Protein adsorption and cell attachment studies Biomaterials 2007, 28, 851-860 (Pubitemid 44667023)
52. Gentsch, R.; Pippig, F.; Schmidt, S.; Cernoch, P.; Polleux, J.; Borner, H. G., Single-Step Electrospinning to Bioactive Polymer Nanofibers. Macromolecules 44, 453-461.
53. Karuri, N. W.; Liliensiek, S.; Teixeira, A. I.; Abrams, G.; Campbell, S.; Nealey, P. F.; Murphy, C. J. Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells J. Cell Sci. 2004, 117, 3153-3164 (Pubitemid 39139902)
54. Brunetti, V.; Maiorano, G.; Rizzello, L.; Sorce, B.; Sabella, S.; Cingolani, R.; Pompa, P. P., Neurons sense nanoscale roughness with nanometer sensitivity. Proc. Natl. Acad. Sci. U.S.A. 107, 6264-6269.
55. 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, 144-152 (Pubitemid 30436733)
56. Pelham, R. J.; Wang, Y. L. Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 13661-13665
57. Schmidt, S.; Zeiser, M.; Hellweg, T.; Duschl, C.; Fery, A.; Mohwald, H. Adhesion and Mechanical Properties of PNIPAM Microgel Films and Their Potential Use as Switchable Cell Culture Substrates Adv. Funct. Mater. 2010, 20, 3235-3243
58. Schulte, V. A.; DiÌez, M.; MoÌ̂ller, M.; Lensen, M. C. Surface Topography Induces Fibroblast Adhesion on Intrinsically Nonadhesive Poly(ethylene glycol) Substrates Biomacromolecules 2009, 10, 2795-2801
59. Kirkpatrick, S. Percolation and Conduction Rev. Mod. Phys. 1973, 45, 574
60. Yanagioka, M.; Frank, C. W. Defect Generation Surrounding Nanoparticles in a Cross-Linked Hydrogel Network Langmuir 2009, 25, 5927-5939
61. Kohler, D.; Madaboosi, N.; Delcea, M.; Schmidt, S.; De Geest, B. G.; Volodkin, D. V.; Möhwald, H.; Skirtach, A. G. Patchiness of Embedded Particles and Film Stiffness Control Through Concentration of Gold Nanoparticles Adv. Mater. 2012, 24, 1095-1100
62. Delcea, M.; Madaboosi, N.; Yashchenok, A. M.; Subedi, P.; Volodkin, D. V.; De Geest, B. G.; Mohwald, H.; Skirtach, A. G. Anisotropic multicompartment micro- and nano-capsules produced via embedding into biocompatible PLL/HA films Chem. Commun. 2011, 47, 2098-2100
63. Garza, J. M. n.; Schaaf, P.; Muller, S.; Ball, V.; Stoltz, J.-F. o.; Voegel, J.-C.; Lavalle, P. Multicompartment Films Made of Alternate Polyelectrolyte Multilayers of Exponential and Linear Growth Langmuir 2004, 20, 7298-7302
64. v. Klitzing, R. Internal structure of polyelectrolyte multilayer assemblies Phys. Chem. Chem. Phys. 2006, 8, 5012-5033
65. Crouzier, T.; Picart, C. Ion Pairing and Hydration in Polyelectrolyte Multilayer Films Containing Polysaccharides Biomacromolecules 2009, 10, 433-442
66. Hicks, J. F.; Seok-Shon, Y.; Murray, R. W. Layer-by-layer growth of polymer/nanoparticle films containing monolayer-protected gold clusters Langmuir 2002, 18, 2288-2294 (Pubitemid 35383916)
67. Skirtach, A. G.; Dejugnat, C.; Braun, D.; Susha, A. S.; Rogach, A. L.; Parak, W. J.; Mohwald, H.; Sukhorukov, G. B. The role of metal nanoparticles in remote release of encapsulated materials Nano Lett. 2005, 5, 1371-1377 (Pubitemid 41084419)