Effect of RGD functionalization and stiffness modulation of polyelectrolyte multilayer films on muscle cell differentiation

Acta Biomaterialia

Volumn 9, Issue 5, 2013, Pages 6468-6480

  Gribova, Varvara ^a,b   Gauthier Rouvière, Cécile ^c   Albigès Rizo, Corinne ^b   Auzely Velty, Rachel ^b   Picart, Catherine ^a  

^a GRENOBLE INSTITUTE OF TECHNOLOGY   (France)

^b UNIV GRENOBLE ALPES   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

Arginylglycylaspartic acid; Extracellular matrix; Myogenesis; Polyelectrolyte multilayer films; Substrate stiffness

Indexed keywords

CELL ADHESION; CELL ENGINEERING; MULTILAYER FILMS; MULTILAYERS; MUSCLE; PEPTIDES; PHASE LOCKED LOOPS; POLYELECTROLYTES; SCAFFOLDS (BIOLOGY); STIFFNESS; STIFFNESS MATRIX; SUBSTRATES;

ARGINYLGLYCYLASPARTIC ACID; EXTRACELLULAR MATRICES; MUSCLE TISSUES; MYOGENESIS; MYOGENIC DIFFERENTIATIONS; POLYELECTROLYTE MULTILAYER FILM; RGD PEPTIDE; SOFT FILM; SUBSTRATE STIFFNESS; TISSUES ENGINEERINGS;

AMINO ACIDS;

ARGINYLGLYCYLASPARTIC ACID; INTEGRIN; POLYELECTROLYTE; POLYGLUTAMIC ACID; POLYLYSINE;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; MUSCLE CELL; MYOBLAST; PRIORITY JOURNAL; RIGIDITY;

EID: 84879886648     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.12.015     Document Type: Article

References (67)

1. R. Bischoff Regeneration of single skeletal muscle fibers in vitro Anat Rec 182 1975 215 235
2. S. Le Ricousse-Roussanne, J. Larghero, J.M. Zini, V. Barateau, P. Foubert, and G. Uzan Ex vivo generation of mature and functional human smooth muscle cells differentiated from skeletal myoblasts Exp Cell Res 313 2007 1337 1346
3. T. Katagiri, A. Yamaguchi, M. Komaki, E. Abe, N. Takahashi, and T. Ikeda Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage J Cell Biol 127 1994 1755 1766
4. A. Schindeler, R. Liu, and D.G. Little The contribution of different cell lineages to bone repair: exploring a role for muscle stem cells Differentiation 77 2009 12 18
5. L. Teboul, D. Gaillard, L. Staccini, H. Inadera, E.Z. Amri, and P.A. Grimaldi Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells J Biol Chem 270 1995 28183 28187
6. M.R. Wada, M. Inagawa-Ogashiwa, S. Shimizu, S. Yasumoto, and N. Hashimoto Generation of different fates from multipotent muscle stem cells Development 129 2002 2987 2995
7. V. Andres, and K. Walsh Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis J Cell Biol 132 1996 657 666
8. B.D. Cosgrove, A. Sacco, P.M. Gilbert, and H.M. Blau A home away from home: challenges and opportunities in engineering in vitro muscle satellite cell niches Differentiation 78 2009 185 194
9. S. Thorsteinsdottir, M. Deries, A.S. Cachaco, and F. Bajanca The extracellular matrix dimension of skeletal muscle development Dev Biol 354 2011 191 207
10. R.D. Cohn, M.D. Henry, D.E. Michele, R. Barresi, F. Saito, and S.A. Moore Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration Cell 110 2002 639 648
11. R. Han, M. Kanagawa, T. Yoshida-Moriguchi, E.P. Rader, R.A. Ng, and D.E. Michele Basal lamina strengthens cell membrane integrity via the laminin G domain-binding motif of alpha-dystroglycan Proc Natl Acad Sci USA 106 2009 12573 12579
12. R.O. Hynes Integrins: bidirectional, allosteric signaling machines Cell 110 2002 673 687
13. U. Mayer Integrins: redundant or important players in skeletal muscle? J Biol Chem 278 2003 14587 14590
14. A.D. Perkins, S.J. Ellis, P. Asghari, A. Shamsian, E.D. Moore, and G. Tanentzapf Integrin-mediated adhesion maintains sarcomeric integrity Dev Biol 338 2010 15 27
15. E. Ruoslahti RGD and other recognition sequences for integrins Annu Rev Cell Dev Biol 12 1996 697 715
16. V. Gribova, T. Crouzier, and C. Picart A material's point of view on recent developments of polymeric biomaterials: control of mechanical and biochemical properties J Mater Chem 21 2011 14354 14366
17. U. Hersel, C. Dahmen, and H. Kessler RGD modified polymers: biomaterials for stimulated cell adhesion and beyond Biomaterials 24 2003 4385 4415
18. D.S. Benoit, and K.S. Anseth The effect on osteoblast function of colocalized RGD and PHSRN epitopes on PEG surfaces Biomaterials 26 2005 5209 5220
19. Y. Hirano, Y. Kando, T. Hayashi, K. Goto, and A. Nakajima Synthesis and cell attachment activity of bioactive oligopeptides: RGD, RGDS, RGDV, and RGDT J Biomed Mater Res 25 1991 1523 1534
20. H.B. Lin, C. Garcia-Echeverria, S. Asakura, W. Sun, D.F. Mosher, and S.L. Cooper Endothelial cell adhesion on polyurethanes containing covalently attached RGD-peptides Biomaterials 13 1992 905 914
21. B.T. Houseman, and M. Mrksich The microenvironment of immobilized Arg-Gly-Asp peptides is an important determinant of cell adhesion Biomaterials 22 2001 943 955
22. J.T. Koepsel, and W.L. Murphy Patterning discrete stem cell culture environments via localized self-assembled monolayer replacement Langmuir 25 2009 12825 12834
23. J.T. Koepsel, S.G. Loveland, M.P. Schwartz, S. Zorn, D.G. Belair, and N.N. Le A chemically-defined screening platform reveals behavioral similarities between primary human mesenchymal stem cells and endothelial cells Integr Biol (Camb) 4 2012 1508 1521
24. P. Bajaj, B. Reddy Jr., L. Millet, C. Wei, P. Zorlutuna, and G. Bao Patterning the differentiation of C2C12 skeletal myoblasts Integr Biol 3 2011 897 909
25. E. Serena, S. Zatti, E. Reghelin, A. Pasut, E. Cimetta, and N. Elvassore Soft substrates drive optimal differentiation of human healthy and dystrophic myotubes Integr Biol 2 2010 193 201
26. A.J. Engler, M.A. Griffin, S. Sen, C.G. Bonnemann, H.L. Sweeney, and D.E. Discher Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments J Cell Biol 166 2004 877 887
27. T. Boontheekul, E.E. Hill, H.J. Kong, and D.J. Mooney Regulating myoblast phenotype through controlled gel stiffness and degradation Tissue Eng 13 2007 1431 1442
28. W.L. Chen, and C.A. Simmons Lessons from (patho)physiological tissue stiffness and their implications for drug screening, drug delivery and regenerative medicine Adv Drug Deliv Rev 63 2011 269 276
29. D.E. Discher, P. Janmey, and Y.L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143
30. H.H. Stedman, H.L. Sweeney, J.B. Shrager, H.C. Maguire, R.A. Panettieri, and B. Petrof The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy Nature 352 1991 536 539
31. P.M. Gilbert, K.L. Havenstrite, K.E. Magnusson, A. Sacco, N.A. Leonardi, and P. Kraft Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture Science 329 2010 1078 1081
32. K. Ren, T. Crouzier, C. Roy, and C. Picart Polyelectrolyte multilayer films of controlled stiffness modulate myoblast cells differentiation Adv Funct Mater 18 2008 1378 1389
33. K.J. Boonen, K.Y. Rosaria-Chak, F.P. Baaijens, D.W. van der Schaft, and M.J. Post Essential environmental cues from the satellite cell niche: optimizing proliferation and differentiation Am J Physiol Cell Physiol 296 2009 C1338 C1345
34. G. Decher Fuzzy nanoassemblies: toward layered polymeric multicomposites Science 277 1997 1232 1237
35. G.-K. Tan, D.L.M. Dinnes, L.N. Butler, and J.J. Cooper-White Interactions between meniscal cells and a self assembled biomimetic surface composed of hyaluronic acid, chitosan and meniscal extracellular matrix molecules Biomaterials 31 2010 6104 6118
36. R.E. Samuel, A. Shukla, D.H. Paik, M.X. Wang, J.C. Fang, and D.J. Schmidt Osteoconductive protamine-based polyelectrolyte multilayer functionalized surfaces Biomaterials 32 2011 7491 7502
37. T. Boudou, T. Crouzier, K. Ren, G. Blin, and C. Picart Multiple functionalities of polyelectrolyte multilayer films: new biomedical applications Adv Mater 22 2010 441 467
38. M.C. Berg, S.Y. Yang, P.T. Hammond, and M.F. Rubner Controlling mammalian cell interactions on patterned polyelectrolyte multilayer surfaces Langmuir 20 2004 1362 1368
39. H.W. Chien, T.Y. Chang, and W.B. Tsai Spatial control of cellular adhesion using photo-crosslinked micropatterned polyelectrolyte multilayer films Biomaterials 30 2009 2209 2218
40. C. Monge, K. Ren, K. Berton, R. Guillot, D. Peyrade, and C. Picart Engineering muscle tissues on microstructured polyelectrolyte multilayer films Tissue Eng 18 2012 1664 1676
41. A. Schneider, A.L. Bolcato-Bellemin, G. Francius, J. Jedrzejwska, P. Schaaf, and J.C. Voegel Glycated polyelectrolyte multilayer films: differential adhesion of primary versus tumor cells Biomacromolecules 7 2006 2882 2889
42. P. Tryoen-Toth, D. Vautier, Y. Haikel, J.C. Voegel, P. Schaaf, and J. Chluba Viability, adhesion, and bone phenotype of osteoblast-like cells on polyelectrolyte multilayer films J Biomed Mater Res 60 2002 657 667
43. C. Picart, R. Elkaim, L. Richert, F. Audoin, Y. Arntz, and M. Da Silva Cardoso Primary cell adhesion on RGD-functionalized and covalently crosslinked thin polyelectrolyte multilayer films Adv Funct Mater 15 2005 83 94
44. T. Crouzier, and C. Picart Ion pairing and hydration in polyelectrolyte multilayer films containing polysaccharides Biomacromolecules 10 2009 433 442
45. S. Charrasse, F. Comunale, M. Fortier, E. Portales-Casamar, A. Debant, and C. Gauthier-Rouviere M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion Mol Biol Cell 18 2007 1734 1743
46. M.V. Voinova, M. Rodahl, M. Jonson, and B. Kasemo Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: continuum mechanics approach Phys Scr 59 1999 391
47. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat Rev Mol Cell Biol 10 2009 21 33
48. A.J. Garcia, M.D. Vega, and D. Boettiger Modulation of cell proliferation and differentiation through substrate-dependent changes in fibronectin conformation Mol Biol Cell 10 1999 785 798
49. E. Zamir, and B. Geiger Molecular complexity and dynamics of cell-matrix adhesions J Cell Sci 114 2001 3583 3590
50. N. Ozeki, P. Jethanandani, H. Nakamura, B.L. Ziober, and R.H. Kramer Modulation of satellite cell adhesion and motility following BMP2-induced differentiation to osteoblast lineage Biochem Biophys Res Commun 353 2007 54 59
51. H. Liu, A. Niu, S.E. Chen, and Y.P. Li Beta3-integrin mediates satellite cell differentiation in regenerating mouse muscle FASEB J 25 2011 1914 1921
52. A.D. Bach, J.P. Beier, J. Stern-Staeter, and R.E. Horch Skeletal muscle tissue engineering J Cell Mol Med 8 2004 413 422
53. T. Nishiyama, I. Kii, and A. Kudo Inactivation of Rho/ROCK signaling is crucial for the nuclear accumulation of FKHR and myoblast fusion J Biol Chem 279 2004 47311 47319
54. L. Castellani, E. Salvati, S. Alema, and G. Falcone Fine regulation of RhoA and Rock is required for skeletal muscle differentiation J Biol Chem 281 2006 15249 15257
55. S. Nemir, and J.L. West Synthetic materials in the study of cell response to substrate rigidity Ann Biomed Eng 38 2010 2 20
56. K. Ren, L. Fourel, C.G. Rouviere, C. Albiges-Rizo, and C. Picart Manipulation of the adhesive behaviour of skeletal muscle cells on soft and stiff polyelectrolyte multilayers Acta Biomater 6 2010 4238 4248
57. J.A. Rowley, and D.J. Mooney Alginate type and RGD density control myoblast phenotype J Biomed Mater Res 60 2002 217 223
58. P.Y. Wang, H. Thissen, and W.B. Tsai The roles of RGD and grooved topography in the adhesion, morphology, and differentiation of C2C12 skeletal myoblasts Biotechnol Bioeng 109 2012 2104 2115
59. E.H. Danen, J. van Rheenen, W. Franken, S. Huveneers, P. Sonneveld, and K. Jalink Integrins control motile strategy through a Rho-cofilin pathway J Cell Biol 169 2005 515 526
60. E. Hirsch, L. Lohikangas, D. Gullberg, S. Johansson, and R. Fassler Mouse myoblasts can fuse and form a normal sarcomere in the absence of beta1 integrin expression J Cell Sci 111 16 1998 2397 2409
61. O.T. Fackler, and R. Grosse Cell motility through plasma membrane blebbing J Cell Biol 181 2008 879 884
62. S. Charrasse, F. Comunale, Y. Grumbach, F. Poulat, A. Blangy, and C. Gauthier-Rouviere RhoA GTPase regulates M-cadherin activity and myoblast fusion Mol Biol Cell 17 2006 749 759
63. M. Fortier, F. Comunale, J. Kucharczak, A. Blangy, S. Charrasse, and C. Gauthier-Rouviere RhoE controls myoblast alignment prior fusion through RhoA and ROCK Cell Death Differ 15 2008 1221 1231
64. A. Mammoto, and D.E. Ingber Cytoskeletal control of growth and cell fate switching Curr Opin Cell Biol 21 2009 864 870
65. M.D. Schaller Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions J Cell Sci 123 2010 1007 1013
66. S. Narumiya, M. Tanji, and T. Ishizaki Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion Cancer Metastasis Rev 28 2009 65 76
67. K.R. Levental, H. Yu, L. Kass, J.N. Lakins, M. Egeblad, and J.T. Erler Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 2009 891 906