Directing nuclear deformation on micropillared surfaces by substrate geometry and cytoskeleton organization

Biomaterials

Volumn 34, Issue 12, 2013, Pages 2991-3001

  Badique, Florent ^a   Stamov, Dimitar R ^b   Davidson, Patricia M ^a,c   Veuillet, Matthieu ^a   Reiter, Günter ^c   Freund, Jean Noël ^d   Franz, Clemens M ^b   Anselme, Karine ^a  

^a UNIVERSITÉ DE HAUTE ALSACE   (France)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

AFM (atomic force microscopy); Cancer cells; Cell deformation; Cell nucleus; Confocal microscopy; Cytoskeleton

Indexed keywords

AFM; CANCER CELLS; CELL DEFORMATION; CELL NUCLEUS; CYTOSKELETONS;

ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL CULTURE; CELLS; CONFOCAL MICROSCOPY; LACTIC ACID; PROTEINS; STIFFNESS; SURFACE RECONSTRUCTION;

DEFORMATION;

ACTIN; DIMETICONE; POLYLACTIC ACID; VIMENTIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CANCER CELL CULTURE; CELL FUNCTION; CELL NUCLEUS; CELL TYPE; CYTOSKELETON; ELASTICITY; GEOMETRY; MICROTUBULE; OSTEOSARCOMA CELL; PRIORITY JOURNAL; RIGIDITY; SCANNING ELECTRON MICROSCOPY; SURFACE PROPERTY;

CELL LINE, TUMOR; CELL NUCLEUS; CYTOSKELETON; DIMETHYLPOLYSILOXANES; HUMANS; LACTIC ACID; MICROSCOPY, ATOMIC FORCE; POLYMERS; SURFACE PROPERTIES;

EID: 84873422264     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.01.018     Document Type: Article

References (55)

1. Davidson P., özçelik H., Hasirci V., Reiter G., Anselme K. Micro-structured surfaces cause severe but non-detrimental deformation of the cell nucleus. Adv Mater 2009, 21:3586-3590.
2. Davidson P., Fromigue O., Marie P., Hasirci V., Reiter G., Anselme K. Topographically induced self-deformation of the nuclei of cells: dependence on cell type and proposed mechanisms. J Mat Sci Mater Med 2010, 31:939-946.
3. Pan Z., Yan C., Peng R., Zhao Y.C., He Y., Ding J.D. Control of cell nucleus shapes via micropillar patterns. Biomaterials 2012, 33:1730-1735.
4. Poulouin L., Gallet O., Rouahi M., Imhoff J.M. Purification and stability of human plasma fibronectin. Protein Express Purif 1999, 17:146-152.
5. Anselme K., Ploux L., Ponche A. Cell/material interfaces: influence of surface chemistry and surface topography on cell adhesion. J Adhes Sci Technol 2010, 24:831-852.
6. Anselme K., Ponche A., Bigerelle M. Relative influence of surface topography and surface chemistry on cell response to bone implant materials. 2. Biological aspects. P I Mech Eng H 2010, 224:1487-1507.
7. Anselme K., Bigerelle M. Role of materials surface topography on mammalian cell response. Int Mater Rev 2011, 56:243-266.
8. Walboomers X.F., Croes H.J.E., Ginsel L.A., Jansen J.A. Growth behavior of fibroblasts on microgrooved polystyrene. Biomaterials 1998, 19:1861-1868.
9. Matsuzaka K., Walboomers X.F., De Ruijter J.E., Jansen J.A. The effect of poly-L-lactic acid with parallel surface micro groove on osteoblast-like cells in vitro. Biomaterials 1999, 20:1293-1301.
10. Teixeira A.I., Abrams G.A., Bertics P.J., Murphy C.J., Nealey P.F. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci 2003, 116:1881-1892.
11. Moroni L., Lee L.P. Micropatterned hot-embossed polymeric surfaces influence cell proliferation and alignment. J Biomed Mater Res A 2009, 88A:644-653.
12. Charest J.L., Garcia A.J., King W.P. Myoblast alignment and differentiation on cell culture substrates with microscale topography and model chemistries. Biomaterials 2007, 28:2202-2210.
13. Dalby M.J., Riehle M.O., Yarwood S.J., Wilkinson C.D., Curtis A.S. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res 2003, 284:274-282.
14. McNamara L.E., Burchmore R., Riehle M.O., Herzyk P., Biggs M.J.P., Wilkinson C.D.W., et al. The role of microtopography in cellular mechanotransduction. Biomaterials 2012, 33:2835-2847.
15. Albini A., Benelli R. The chemoinvasion assay: a method to assess tumor and endothelial cell invasion and its modulation. Nat Protoc 2007, 2:504-511.
16. Tzvetkova-Chevolleau T., Stephanou A., Fuard D., Ohayon J., Schiavone P., Tracqui P. The motility of normal and cancer cells in response to the combined influence of the substrate rigidity and anisotropic microstructure. Biomaterials 2008, 29:1541-1551.
17. Brunette D.M., Chehroudi B. The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. J Biomech Eng 1999, 121:49-57.
18. Bettinger C.J., Langer R., Borenstein J.T. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Edit 2009, 48:5406-5415.
19. Chaw K.C., Manimaran M., Tay F.E.H., Swaminathan S. Matrigel coated polydimethylsiloxane based microfluidic devices for studying metastatic and non-metastatic cancer cell invasion and migration. Biomed Microdevices 2007, 9:597-602.
20. Breckenridge M.T., Egelhoff T.T., Baskaran H. A microfluidic imaging chamber for the direct observation of chemotactic transmigration. Biomed Microdevices 2010, 12:543-553.
21. Rolli C.G., Seufferlein T., Kemkemer R., Spatz J.P. Impact of tumor cell cytoskeleton organization on invasiveness and migration: a microchannel-based approach. Plos One 2010, 5:e8726.
22. Walter N., Micoulet A., Seufferlein T., Spatz J.P. Direct assessment of living cell mechanical responses during deformation inside microchannel restrictions. Biointerphases 2011, 6:117-125.
23. 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.
24. 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.
25. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
26. Ghibaudo M., Saez A., Trichet L., Xayaphoummine A., Browaeys J., Silberzan P., et al. Traction forces and rigidity sensing regulate cell functions. Soft Matter 2008, 4:1836-1843.
27. Rehfledt F., Engler A.J., Eckardt A., Ahmed F., Discher D.E. Cell responses to the mechanochemical microenvironment - Implications for regenerative medicine and drug delivery. Adv Drug Deliver Rev 2007, 59:1329-1339.
28. Levy-Mishali M., Zoldan J., Levenberg S. Effect of scaffold stiffness on myoblast differentiation. Tissue Eng Part A 2009, 15:935-944.
29. Tilghman R.W., Cowan C.R., Mih J.D., Koryakina Y., Gioeli D., Slack-Davis J.K., et al. Matrix rigidity regulates cancer cell growth and cellular phenotype. Plos One 2010, 5:e12905.
30. Trappmann B., Gautrot J.E., Connelly J.T., Strange D.G.T., Li Y., Oyen M.L., et al. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 2012, 11:642-649.
31. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci U S A 2003, 100:1484-1489.
32. Steinberg T., Schultz S., Spatz J.P., Grabe N., Mussig E., Kohl A., et al. Early keratinocyte differentiation on micropillar interfaces. Nano Lett 2007, 7:287-294.
33. Mussig E., Schulz S., Spatz J.P., Ziegler N., Tomakidi P., Steinberg T. Soft micropillar interfaces of distinct biomechanics govern behaviour of periodontal cells. Eur J Cell Biol 2010, 89:315-325.
34. Ochsner M., Textor M., Vogel V., Smith M.L. Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape. Plos One 2010, 5:e9445.
35. Domke J., Dannöhl S., Parak W.J., Müller O., Aicher W.K., Radmacher M. Substrate dependent differences in morphology and elasticity of living osteoblasts investigated by atomic force microscopy. Colloid Surface B 2000, 19:367-379.
36. Docheva D., Padula D., Popov C., Mutschler W., Clausen-Schaumann H., Schieker M. Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J Cell Mol Med 2008, 12:537-552.
37. Rotsch C., Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys J 2000, 78:520-535.
38. Khatau S.B., Kim D.-H., Hale C.M., Bloom R.J., Wirtz D. The perinuclear actin cap in health and disease. Nucleus 2010, 1:337-342.
39. Khatau S.B., Hale C.M., Stewart-Hutchinson P.J., Patel M.S., Stewart C.L., Searson P.C., et al. A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci U S A 2009, 106:19017-19022.
40. Dupin I., Sakamoto Y., Etienne-Manneville S. Cytoplasmic intermediate filaments mediate actin-driven positioning of the nucleus. J Cell Sci 2011, 124:865-872.
41. Dupin I., Etienne-Manneville S. Nuclear positioning: mechanisms and functions. Int J Biochem Cell Biol 2011, 43:1698-1707.
42. Levy J.R., Holzbaur E.L.F. Dynein drives nuclear rotation during forward progression of motile fibroblasts. J Cell Sci 2008, 121:3187-3195.
43. Mellad J.A., Warren D.T., Shanahan C.M. Nesprins LINC the nucleus and cytoskeleton. Curr Opin Cell Biol 2011, 23:47-54.
44. Shimi T., Butin-Israeli V., Goldman R.D. The functions of the nuclear envelope in mediating the molecular crosstalk between the nucleus and the cytoplasm. Curr Opin Cell Biol 2012, 24:71-78.
45. Lammerding J. Mechanics of the nucleus. Comprehensive Physiology 2011, 1:783-807.
46. Spencer V.A., Samuel S.K., Davie J.R. Nuclear matrix proteins associated with DNA in situ in hormone-dependent and hormone-independent human breast cancer cell lines. Cancer Res 2000, 60:288-292.
47. Georgatos S.D. Blobel G Lamin B constitutes an intermediate filaments attachment site at the nuclear envelope. J Cell Biol 1987, 105:117-125.
48. Shivashankar G.V. Mechanosignaling to the cell nucleus and gene regulation. Annu Rev Biophys 2011, 40:361-378.
49. Reddy K.L., Zullo J.M., Bertolino E., Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 2008, 452:243-247.
50. Ruault M., Dubarry M., Taddei A. Re-positioning genes to the nuclear envelope in mammalian cells: impact on transcription. Trends Genet 2008, 24:574-581.
51. Dahl K.N., Booth-Gauthier E.A., Ladoux B. In the middle of it all: mutual mechanical regulation between the nucleus and the cytoskeleton. J Biomech 2010, 43:2-8.
52. Spencer V.A., Xu R., Bissell M.J. Gene expression in the third dimension: the ECM-nucleus connection. J Mam Gland Biol Neoplasia 2010, 15:65-71.
53. Thomas C.H., Collier J.H., Sfeir C.S., Healy K.E. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc Natl Acad Sci U S A 2002, 99:1972-1977.
54. Ben-Ze'ev A. The cytoskeleton in cancer cells. BBA 1985, 780:197-212.
55. Bidwell J.P., Fey E.G., Vanwijnen A.J., Penman S., Stein J.L., Lian J.B., et al. Nuclear matrix proteins distinguish normal diploid osteoblasts from osteosarcoma cells. Cancer Res 1994, 54:28-32.