Selective and uncoupled role of substrate elasticity in the regulation of replication and transcription in epithelial cells

Journal of Cell Science

Volumn 123, Issue 1, 2010, Pages 29-39

  Kocgozlu, Leyla ^a,b,c   Lavalle, Phillippe ^a,b,d   Koenig, Géraldine ^a,b   Senger, Bernard ^a,b   Haikel, Youssef ^a,b,c   Schaaf, Pierre ^e   Voegel, Jean Claude ^a,b,c   Tenenbaum, Henri ^a,b,c   Vautier, Dominique ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Unité 977   (France)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^e CNRS   (France)

Author keywords

Actin; Integrin; Rac1; Replication; Substrate elasticity; Transcription; Vinculin

Indexed keywords

CD51 ANTIGEN; FOCAL ADHESION KINASE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HISTONE H3; PHOSPHATIDYLSERINE; RAC1 PROTEIN; TYROSINE; VINCULIN;

ACETYLATION; ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CELL ADHESION; CELL SPREADING; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; CYTOSKELETON; EPITHELIUM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE REPLICATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ACTINS; ANIMALS; APOPTOSIS; CELL ADHESION; CELL LINE; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; ELASTICITY; EPITHELIAL CELLS; FOCAL ADHESIONS; HISTONES; INTEGRIN ALPHA CHAINS; MICROFILAMENTS; MOTION PICTURES AS TOPIC; RAC1 GTP-BINDING PROTEIN; RATS; TRANSCRIPTIONAL ACTIVATION; VINCULIN;

EID: 72449160313     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.053520     Document Type: Article

References (57)

1. Assoian, R. K. (1997). Anchorage-dependent cell cycle progression. J. Cell Biol. 136, 1-4.
2. Balby, M. J., Gadegaard, N., Herzyl, P., Sutherland, D., Agheli, H., Wilkinson, C. D. and Curtis, A. S. (2007). Nanomechanotransduction and interphase nuclear organization influence on genomic control. J. Cell Biochem. 102, 1234-1244.
3. Biggs, M. J., Richards, R. G., Gadegaard, N., Wilkinson, C. D. and Dalby, M. J. (2007). Regulation of implant surface cell adhesion: characterization and quantification of S-phase primary osteoblast adhesions on biomimetic nanoscale substrates. J. Orthop. Res. 25, 273-282.
4. Boura, C., Muller, S., Vautier, D., Dumas, D., Schaaf, P., Voegel, J. C., Stoltz, J. F. and Menu, P. (2005). Endothelial cell-interactions with polyelectrolyte multilayer films. Biomaterials 22, 4568-4575.
5. Burridge, A. D. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
6. Decher, G. (1997). Fuzzy nanoassemblies: Toward layered polymeric multicomposites. Science 277, 1232-1237.
7. Discher, D. E., Janmey, P. and Wang, Y. L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143.
8. Dreyfuss, G., Matunis, M. J., Piñol-Roma, S. and Burd, C. G. (1993). hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62, 289-321.
9. Dubreuil, F., Elsner, N. and Fery, A. (2003). Elastic properties of polyelectrolyte capsules studies by atomic-force microscopy and RICM. Eur. Phys. J. E 12, 215-221.
10. Engler, A. J., Griffin, M. A., Sen, S., Bonnemann, C. G., Sweeney, H. L. and Discher, D. E. (2004). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887.
11. Engler, A. J., Sen, S., Sweeney, H. L. and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
12. Engler, A. J., Carag-Krieger, C., Johnson, C. P., Raab, M., Tang, H. Y., Speicher, D. W., Sanger, J. W., Sanger, J. M. and Discher, D. E. (2008). Embryonic cardiomyocytes beat best on a matrix with heaet-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121, 3794-3802.
13. Ferreira, J. A., Carmo-Fonseca, M. and Lamond, A. I. (1994). Differential interaction of splicing snRNPs with coiled bodies and interchromatin granules during mitosis and assembly of daughter cell nuclei. J. Cell Biol. 126, 11-23.
14. Ferreira, J., Paolella, G., Ramos, C. and Lamond, A. I. (1997). Spatial organization of large-scale chromatin domains in the nucleus: a magnified view of single chromosome territories. J. Cell Biol. 139, 1597-1610.
15. Francius, G., Hemmerle, J., Ohayon, J., Schaaf, P., Voegel, J. C., Picart, C. and Senger, B. (2006). Effect of crosslinking on the elasticity of polyelectrolyte multilayer films measured by colloidal probe AFM. Microsc. Res. Tech. 69, 84-92.
16. Francius, G., Hemmerle, J., Ball, V., Lavalle, P., Picart, C., Voegel, J. C., Schaaf, P. and Senger, B. (2007). Stiffening of soft polyelectrolyte architectures by multilayer capping evidenced by viscoelastic analysis of AFM indentation measurements. J. Phys. Chem. C 111, 8299-8306.
17. Garza, J. M., Schaaf, P., Muller, S., Ball, V., Stoltz, J. F., Voegel, J. C. and Lavalle, P. (2004). Multicompartment films made of alternate polyelectrolyte multilayers of exponential and linear growth. Langmuir 20, 7298-7302.
18. Georges, P. C., Miller, W. J., Meaney, D. F., Sawyer, E. S. and Janmey, P. A. (2006). Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012-3018.
19. Giannone, G. and Sheetz, M. P. (2006). Substrate rigidity and force define form through tyrosine phosphatise and kinase pathways. Trends Cell Biol. 16, 213-223.
20. Gieni, S. and Hendzel, M. J. (2008). Mechanotransduction from the ECM to the Genome: are the pieces now in place? J. Cell Biochem. 104, 1964-1987.
21. Gross, I., Duluc, I., Benameur, T., Calon, A., Martin, E., Brabletz, T., Kedinger, M., Domon-Dell, C. and Freund, J. N. (2008). The intestine-specific homeobox gene Cdx2 decreases mobility and antagonizes dissemination of colon cancer cells. Oncogene 27, 107-115.
22. Hassan, A., Errington, R. J., White, N. S., Jackson, D. A. and Cook, P. R. 1994. Replication and transcription sites are colocalized in human cells. J. Cell Sci. 107, 425-434.
23. Huang, C., Jacobson, K. and Schaller, M. D. (2004). MAP kinases and cell migration. J. Cell Sci. 117, 4619-4628.
24. Kim, W., Kook, S., Kim, D. J., Teodorof, C. and Song, W. K. (2004). The 31-kDa caspase-generated cleavage product of p130cas functions as a transcriptional repressor of E2A in apoptotic cells. J. Biol. Chem. 279, 8333-8342.
25. Kohzaki, H. and Murakami, Y. (2005). Transcription factors and DNA replication origin selection. BioEssays 27, 1107-1116.
26. Kornberg, L. J., Earp, H. S., Turner, C. E., Prockop, C. and Juliano, R. L. (1991). Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins. Proc. Natl. Acad. Sci. USA 88, 8392-8396.
27. Kurdistani, S. K., Tavazoie, S. and Grunstein, M. (2004). Mapping global histone acetylation patterns to gene expression. Cell 117, 721-733.
28. Le Beyec, J., Wu, R., Lee, S. Y., Nelson, C. M., Rizki, A., Alcaraz, J. and Bissell, M. J. (2007). Cell shape regulates global histone acetylation in human mammary epithelial cells. Exp. Cell Res. 313, 3066-3075.
29. Levental, I., Georges, P. C. and Janmey, P. A. (2007). Soft biological materials and their impact on cell function. Soft Matter 3, 299-306.
30. Lo, C. M., Wang, H. B., Dembo, M. and Wang, Y. L. (2000). Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152.
31. Margadant, C., van Opstal, A. and Boonstra, J. (2007). Focal adhesion signalling and actin stress fibers are dispensable for progression through the ongoing cell cycle. J. Cell Sci. 120, 66-76.
32. Maxwell, C. A. and Hendzel, M. J. (2001). The integration of tissue structure and nuclear function. Biochem. Cell Biol. 79, 267-274.
33. Mendelsohn, J. D., Yang, S. Y., Hiller, Y., Hochbaum, A. I. and Rubner, M. F. (2003). Rational design of cytophilic and cytophobic polyelectrolyte multilayer thin films. Biomacromolecules 4, 96-106.
34. Meredith, D. O., Owen, G. R., ap Gwynn, I. and Richards, R. G. (2004). Variation in cell-substratum adhesion in relation to cell cycle phases. Exp. Cell Res. 293, 58-67.
35. Mitchison, J. M. (1971). The biology of the cell cycle. Cambridge University Press: Cambridge.
36. Nobes, C. D. and Hall, A. (1995). Rho, Rac and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, Lamelliopodia, and filopodia. Cell 81, 53-62.
37. Pardee, A. B. (1989). G1 events and regulation of cell proliferation. Science 246, 603-608.
38. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D. et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell. 8, 241-254.
39. Pelham, R. J., Jr and Wang, Y. L. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94, 13661-13665.
40. Picart, C., Senger, B., Sengupa, K., Dubreuil, F. and Fery, A. (2007). Measuring mechanical properties of polyelectrolyte multilayer thin films: novel methods based on AFM and optical techniques. Colloids and Surfaces A 303, 30-36.
41. Piñol-Roma, S. and Dreyfuss, G. (1991). Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science 253, 312-314.
42. Ren, K. F., Crouzier, T., Roy, C. and Picart, C. (2008). Polyelectrolyte multilayer films of controlled stiffness modulate myoblast cell differentiation. Adv. Funct. Mater. 18, 1378-1389.
43. Richert, L., Engler, A. J., Discher, D. E. and Picart, C. (2004). Elasticity of native and cross-linked polyelectrolyte multilayer films. Biomacromolecules 5, 1908-1916.
44. Rizzi, S. C., Ehrbar, M., Halstenberg, S., Raeber, G. P., Schmoekel, H. G., Hagenmuller, H., Muller, R., Weber, F. E. and Hubbell, J. A. (2006). Recombinant protein-co-PEG networks as cell-adhesive proteolytically degradable hydrogel matrixes. Part II: Biofunctional characteristics. Biomacromolecules 7, 3019-3029.
45. Roovers, K. and Assoian, R. K. (2003). Effects of rho kinase and actin stress fibers on sustained extracellular signal-regulated kinase activity and activation of G(1) phase cyclin-dependent kinases. Mol. Cell. Biol. 23, 4283-4294.
46. Rose, J. L., Huang, H., Wray, S. F. and Hoyt, D. G. (2005). Integrin engagement increases histone H3 acetylation and reduces histone H1 association with DNA in murine Lung endothelial cells. Mol. Pharmacol. 68, 439-446.
47. Sauerbrey, G. Z. (1959). Verwendung von Schwingquartzen zur Wägung dünner Schichten und zur Mikrowägung. Phys. 155, 206-222.
48. Schaller, M. D., Hildebrand, J. D. and Parsons, J. T. (1999). Complex formation with focal adhesion kinase: a mechanism to regulate activity and subcellular localization of Src kinases. Mol. Biol. Cell 10, 3489-3505.
49. Snedeker, J. G., Barbezat, M., Niederer, P., Schmidlin, F. R. and Farshad, M. (2005). Strain energy density as a rupture criterion for the kidney: impact tests on porcine organs, finite element simulation, and a baseline comparison between human and porcine tissues. J. Biomech. 38, 993-1001.
50. Shimi, T., Pfleghaar, K., Kojima, S., Pack, C. G., Solovei, I., Goldman, A. E., Adam, S. A., Shumaker, D. K., Kinjo, M., Cremer, T. et al. (2008). The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev. 22, 3409-3421.
51. Vautier, D., Chesne, P., Cunha, C., Calado, A., Renard, J. P. and Carmo-Fonseca, M. (2001). Transcription-dependent nucleocytoplasmic distribution of hnRNP A1 protein in early mouse embryos. J. Cell Sci. 114, 1521-1531.
52. Wang, F., Weaver, V. M., Petersen, O. W., Larabell, C. A., Dedhar, S., Briand, P., Lupu, R. and Bissell, M. J. (1998). Reciprocal interaction between □1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc. Natl. Acad. Sci. USA 95, 14821-14826.
53. Wang, N., Tytell, J. D. and Ingber, D. E. (2009). Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell. Biol. 10, 75-82.
54. Wei, W. C., Lin, H. H., Shen, M. R. and Tang, M. J. (2008). Mechanosensing machinery for cells under low substratum rigidity. Am. J. Physiol. Cell Pysiol. 295, 1579-1589.
55. Wong, J. Y., Velasco, A., Rajagopalan, P. and Pham, Q. (2003). Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels. Langmuir 19, 1908-1913.
56. Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J. and Keely, P. J. (2003). ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163, 583-595.
57. Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V. and Janmey, P. A. (2005). Effects of substrate stiffness on cell morphology, cytoskeletal, and adhesion. Cell Motil. Cytoskeleton 60, 24-34.