Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells

Biophysical Journal

Volumn 101, Issue 9, 2011, Pages 2139-2146

  McKee, Clayton T ^a   Raghunathan, Vijay K ^a   Nealey, Paul F ^b   Russell, Paul ^a   Murphy, Christopher J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Wisconsin Madison   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL NUCLEUS; CONFOCAL MICROSCOPY; CYTOLOGY; CYTOSKELETON; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; NUCLEAR SHAPE; YOUNG MODULUS;

CELL NUCLEUS; CELL NUCLEUS SHAPE; CYTOSKELETON; ELASTIC MODULUS; EPITHELIAL CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE;

EID: 80455143353     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.09.042     Document Type: Article

References (48)

1. P. Russell, and J.Z. Gasiorowski C.J. Murphy Response of human trabecular meshwork cells to topographic cues on the nanoscale level Invest. Ophthalmol. Vis. Sci. 49 2008 629 635
2. J.C. Hansen, and J.Y. Lim H.J. Donahue Effect of surface nanoscale topography on elastic modulus of individual osteoblastic cells as determined by atomic force microscopy J. Biomech. 40 2007 2865 2871 (Pubitemid 47385816)
3. G. McPhee, and M.J. Dalby H. Yin Can common adhesion molecules and microtopography affect cellular elasticity? A combined atomic force microscopy and optical study Med. Biol. Eng. Comput. 48 2010 1043 1053
4. C.T. McKee, and J.A. Wood P. Russell The effect of biophysical attributes of the ocular trabecular meshwork associated with glaucoma on the cell response to therapeutic agents Biomaterials 32 2011 2417 2423
5. B.C. Isenberg, and P.A. Dimilla J.Y. Wong Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength Biophys. J. 97 2009 1313 1322
6. P. Uttayarat, and M. Chen P.I. Lelkes Microtopography and flow modulate the direction of endothelial cell migration Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1027 H1035
7. E. Hadjipanayi, V. Mudera, and R.A. Brown Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness J. Tissue Eng. Regen. Med. 3 2009 77 84
8. S.J. Liliensiek, and J.A. Wood C.J. Murphy Modulation of human vascular endothelial cell behaviors by nanotopographic cues Biomaterials 31 2010 5418 5426
9. N.D. Leipzig, and M.S. Shoichet The effect of substrate stiffness on adult neural stem cell behavior Biomaterials 30 2009 6867 6878
10. O. Zinger, and G. Zhao B. Boyan Differential regulation of osteoblasts by substrate microstructural features Biomaterials 26 2005 1837 1847 (Pubitemid 39575326)
11. R.J. Pelham Jr., and Y. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. USA 94 1997 13661 13665 (Pubitemid 28009639)
12. E.K. Yim, and R.M. Reano K.W. Leong Nanopattern-induced changes in morphology and motility of smooth muscle cells Biomaterials 26 2005 5405 5413 (Pubitemid 40462355)
13. M.J. Dalby, and M.O. Riehle A.S. Curtis Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography Exp. Cell Res. 284 2003 274 282 (Pubitemid 36324534)
14. J.Z. Gasiorowski, and S.J. Liliensiek C.J. Murphy Alterations in gene expression of human vascular endothelial cells associated with nanotopographic cues Biomaterials 31 2010 8882 8888
15. M. Radmacher, and R.W. Tillamnn H.E. Gaub From molecules to cells: imaging soft samples with the atomic force microscope Science 257 1992 1900 1905 (Pubitemid 23604211)
16. J.C. Martens, and M. Radmacher Softening of the actin cytoskeleton by inhibition of myosin II Pflugers Arch. 456 2008 95 100
17. A.B. Mathur, G.A. Truskey, and W.M. Reichert Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells Biophys. J. 78 2000 1725 1735 (Pubitemid 30183571)
18. U.G. Hofmann, and C. Rotsch M. Radmacher Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope J. Struct. Biol. 119 1997 84 91 (Pubitemid 27325781)
19. F. Guilak Compression-induced changes in the shape and volume of the chondrocyte nucleus J. Biomech. 28 1995 1529 1541 (Pubitemid 26004298)
20. N. Caille, Y. Tardy, and J.J. Meister Assessment of strain field in endothelial cells subjected to uniaxial deformation of their substrate Ann. Biomed. Eng. 26 1998 409 416 (Pubitemid 128609282)
21. J.R. Sims, S. Karp, and D.E. Ingber Altering the cellular mechanical force balance results in integrated changes in cell, cytoskeletal and nuclear shape J. Cell Sci. 103 1992 1215 1222 (Pubitemid 23042264)
22. D.E. Ingber Tensegrity I. Cell structure and hierarchical systems biology J. Cell Sci. 116 2003 1157 1173 (Pubitemid 36410656)
23. T.J. Chancellor, and J. Lee T. Lele Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation Biophys. J. 99 2010 115 123
24. D.A. Starr, and M. Han Role of ANC-1 in tethering nuclei to the actin cytoskeleton Science 298 2002 406 409 (Pubitemid 35176347)
25. T.G. Kuznetsova, and M.N. Starodubtseva R.I. Zhdanov Atomic force microscopy probing of cell elasticity Micron 38 2007 824 833 (Pubitemid 47554622)
26. J. Lammerding, and K.N. Dahl R.D. Kamm Nuclear mechanics and methods Methods Cell Biol. 83 2007 269 294
27. R.M. Hochmuth Micropipette aspiration of living cells J. Biomech. 33 2000 15 22
28. A.I. Teixeira, and G.A. Abrams P.F. Nealey Epithelial contact guidance on well-defined micro- and nanostructured substrates J. Cell Sci. 116 2003 1881 1892 (Pubitemid 36622287)
29. S.J. Liliensiek, and S. Campbell C.J. Murphy The scale of substratum topographic features modulates proliferation of corneal epithelial cells and corneal fibroblasts J. Biomed. Mater. Res. A 79 2006 185 192 (Pubitemid 44452869)
30. C. Rotsch, and M. Radmacher Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study Biophys. J. 78 2000 520 535 (Pubitemid 30207160)
31. Q. Zhang, and C. Ragnauth R.G. Roberts The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300 Genomics 80 2002 473 481 (Pubitemid 35333789)
32. N.W. Karuri, and S. Liliensiek C.J. Murphy Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells J. Cell Sci. 117 2004 3153 3164 (Pubitemid 39139902)
33. A.I. Teixeira, and G.A. McKie C.J. Murphy The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography Biomaterials 27 2006 3945 3954
34. D.M. Robertson, and L. Li J.V. Jester Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line Invest. Ophthalmol. Vis. Sci. 46 2005 470 478 (Pubitemid 40270324)
35. M. Radmacher, and M. Fritz P.K. Hansma Measuring the viscoelastic properties of human platelets with the atomic force microscope Biophys. J. 70 1996 556 567 (Pubitemid 26021495)
36. M. Radmacher Studying the mechanics of cellular processes by atomic force microscopy Methods Cell Biol. 83 2007 347 372
37. J.L. Hutter, and J. Bechhoefer Calibration of atomic force microscope tips Rev. Sci. Instrum. 64 1993 1868 1873 erratum 64:3342
38. A.E.H. Love Boussinesq's problem for a rigid cone Q. J. Math. 10 1939 161 175
39. R.E. Mahaffy, and C.K. Shih J. Käs Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells Phys. Rev. Lett. 85 2000 880 883
40. E.K. Yim, and E.M. Darling K.W. Leong Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells Biomaterials 31 2010 1299 1306
41. R.J. Truscott Presbyopia. Emerging from a blur towards an understanding of the molecular basis for this most common eye condition Exp. Eye Res. 88 2009 241 247
42. J.A. Last, and T. Pan P. Russell Elastic modulus determination of normal and glaucomatous human trabecular meshwork Invest. Ophthalmol. Vis. Sci. 52 2011 2147 2152
43. T. Matsumoto, and H. Abe M. Sato Local elastic modulus of atherosclerotic lesions of rabbit thoracic aortas measured by pipette aspiration method Physiol. Meas. 23 2002 635 648 (Pubitemid 35386572)
44. G. Kymionis, and D. Portaliou Corneal crosslinking with riboflavin and UVA for the treatment of keratoconus J. Cataract Refract. Surg. 33 2007 1143 1144 author reply 1144 (Pubitemid 46936159)
45. P. Roca-Cusachs, and J. Alcaraz D. Navajas Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation Biophys. J. 94 2008 4984 4995
46. F.A. Saad, and M. Torres L. Graham Intracellular lysyl oxidase: effect of a specific inhibitor on nuclear mass in proliferating cells Biochem. Biophys. Res. Commun. 396 2010 944 949
47. M. Webster, K.L. Witkin, and O. Cohen-Fix Sizing up the nucleus: nuclear shape, size and nuclear-envelope assembly J. Cell Sci. 122 2009 1477 1486
48. K.N. Dahl, A.J.S. Ribeiro, and J. Lammerding Nuclear shape, mechanics, and mechanotransduction Circ. Res. 102 2008 1307 1318