Mechanical response of a living human epidermal keratinocyte sheet as measured in a composite diaphragm inflation experiment

Biorheology

Volumn 44, Issue 5-6, 2007, Pages 319-348

  Selby, John C ^a   Shannon, Mark A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Adherens junctions; Cell mechanics; Cytoskeleton; Desmosomes; Intermediate filaments; Microfilaments

Indexed keywords

DIMETICONE;

CELL CULTURE; CELL FUNCTION; CELL JUNCTION; CELL KINETICS; CELL STRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; DESMOSOME; FLOW KINETICS; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; LUNG INFLATION; REVIEW; VISCOELASTICITY; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; CYTOSKELETON; EPIDERMIS; FLUORESCENCE MICROSCOPY; MECHANICAL STRESS; MICROFILAMENT; PHYSIOLOGY;

CELL CULTURE TECHNIQUES; CYTOSKELETON; DESMOSOMES; DIMETHYLPOLYSILOXANES; EPIDERMIS; HUMANS; KERATINOCYTES; MICROFILAMENTS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; RHEOLOGY; STRESS, MECHANICAL;

EID: 58149123106     PISSN: 0006355X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (93)

1. J.E. Adkins and R.S. Rivlin, Large elastic deformations of isotropic materials. IX. The deformations of thin shells, Phil. Trans. Roy. Soc. Lond. Ser. A 244(1952), 505-531.
2. P. Agache, J.P. Boyer and R. Laurent, Biomechanical properties and microscopic morphology of human stratum corneum incubated on a wet pad in vitro, Arch. Dermatol. Res. 246(1973), 271-283.
3. N.Q. Balaban, U.S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, I. Sabanay, D. Mahalu, S. Safran, A. Bershadsky, L. Addadi and B. Geiger, Force and focal adhesion assembly: A close relationship studied using elastic micropatterned substrates, Nat. Cell Biol. 3(2001), 466-472.
4. A.J. Banes, J. Gilbert, D. Taylor and O. Monbureau, A new vacuum-operated stress-providing instrument that applies static or variable duration cyclic tension or compression to cells in vitro, J. Cell Sci. 75(1985), 35-42.
5. A.R. Bausch, W. Moller and E. Sackmann, Measurement of local viscoelasticity and forces in living cells by magnetic tweezers, Biophys. J. 76(1999), 573-579.
6. A.R. Bausch, F. Ziemann, A.A. Boulbitch, K. Jacobson and E. Sackmann, Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry, Biophys. J. 75(1998), 2038-2049.
7. T.D. Brown, Techniques for mechanical stimulation of cells in vitro:Areview, J. Biomech. 33(2000), 3-14.
8. T.D. Brown, M. Bottlang, D.R. Pedersen and A.J. Banes, Development and experimental validation of a fluid/structure- interaction finite element model of a vacuum-driven cell culture mechanostimulus system, Comput. Meth. Biomech. Bio-med. Eng. 3(2000), 65-78.
9. J.P. Butler and S.M. Kelly, A model for cytoplasmic rheology consistent with magnetic twisting cytometry, Biorheology 35(1998), 193-209.
10. E. Canetta, A. Duperray, A. Leyrat and C. Verdier, Measuring cell viscoelastic properties using a force-spectrometer:Influence of protein-cytoplasm interactions, Biorheology 42(2005), 321-333.
11. S.J. Chapman and R.A.J. Eady, Blistering in keratinocyte cultures: A regular phenomenon associated with differentiation, Eur. J. Cell Biol. 39(1985), 352-359.
12. S. Chien, Molecular basis of rheological modulation of endothelial functions: Importance of stress direction, Biorheology 43(2006), 95-116.
13. P. Chistolini, G. De Angelis, M. De Luca, G. Pellegrini and I. Ruspantini, Analysis of the mechanical properties of in vitro reconstructed epidermis: Preliminary results, Med. Biol. Eng. Comput. 37(1999), 670-672.
14. P.A. Coulombe, O. Bousquet, L.L. Ma, S. Yamada and D. Wirtz, The 'ins' and 'outs' of intermediate filament organization, Trends Cell Biol. 10(2000), 420-428.
15. P.A. Coulombe and P. Wong, Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds, Nat. Cell Biol. 6(2004), 699-706.
16. H.D. Crane, Switching properties in bubbles, balloons, capillaries and alveoli, J. Biomech. 6(1973), 411-414.
17. 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.
18. H. Fassihi, T. Wong, V. Wessagowit, J.A. McGrath and J.E. Mellerio, Target proteins in inherited and acquired blistering skin disorders, Clin. Exp. Dermatol. 31(2006), 252-259.
19. P. Fernandez, P.A. Pullarkat and A. Ott, A master relation defines the viscoelasticity of single fibroblasts, Biophys. J. 90(2006), 3796-3805.
20. E. Fuchs and C. Byrne, The epidermis: Rising to the surface, Curr. Opin. Genet. Dev. 4(1994), 725736. [21] E. Fuchs and D.W. Cleveland, A structural scaffolding of intermediate filaments in health and disease, Science 279(1998), 514-519.
21. D.S. Fudge, K.H. Gardner, V.T. Forsyth, C. Riekel and J.M. Gosline, The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads, Biophys. J. 85(2003), 2015-2027.
22. J.A. Gilbert, P.S. Weinhold, A.J. Banes, G.W. Link and G.L. Jones, Strain profiles for circular cell culture plates containing flexible surfaces employed to mechanically deform cells in vitro, J. Biomech. 27(1994), 1169-1177.
23. K.J. Green, B. Geiger, J.C.R. Jones, J.C. Talian and R.D. Goldman, The relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes, J. Cell Biol. 104(1987), 1389-1402.
24. M. Haftek, M.U. Hansen, H.W. Kaiser, H.W. Kreysel and D. Schmitt, Interkeratinocyte adherens junctions: Immuno-cytochemical visualization of cell-cell junctional structures, distinct from desmosomes, in human epidermis, J. Invest. Dermatol. 106(1996), 498-504.
25. H. Hennings and K.A. Holbrook, Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture - An ultrastructural-study, Exp. Cell Res. 143(1983), 127-142.
26. J.H. Hoh and C.A. Schoenenberger, Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy, J. Cell Sci. 107(1994), 1105-1114.
27. F.P.K. Hsu, A.M.C. Liu, J. Downs, D. Rigamonti and J.D. Humphrey, A triplane video-based experimental system for studying axisymmetrically inflated biomembranes, IEEE Trans. Biomed. Eng. 42(1995), 442-450.
28. F.P.K. Hsu, C. Schwab, D. Rigamonti and J.D. Humphrey, Identification of response functions from axisymmetrical membrane inflation tests - Implications for biomechanics, Int. J. Solid Struct. 31(1994), 3375-3386.
29. C. Jamora and E. Fuchs, Intercellular adhesion, signalling and the cytoskeleton, Nat. Cell Biol. 4(2002), E101-E108.
30. J.J. Jefferson, C.L. Leung and R.K.H. Liem, Plakins: Goliaths that link cell junctions and the cytoskeleton, Nat. Rev. Mol. Cell Biol. 5(2004), 542-553.
31. P.J. Jensen and M.J. Wheelock, The relationships among adhesion, stratification and differentiation in keratinocytes, Cell Death Differ. 3(1996), 357-371.
32. J.C.R. Jones and R.D. Goldman, Intermediate filaments and the initiation of desmosome assembly, J. Cell Biol. 101(1985), 506-517.
33. H.W. Kaiser, W. Ness, I. Jungblut, R.A. Briggaman, H.W. Kreysel and E.J. Okeefe, Adherens junctions - Demonstration in human epidermis, J. Invest. Dermatol. 100(1993), 180-185.
34. S. Kippenberger, A. Bernd, S. Loitsch, M. Guschel, J. Muller, J. Bereiter-Hahn and R. Kaufmann, Signaling of mechanical stretch in human keratinocytes via MAP kinases, J. Invest. Dermatol. 114(2000), 408-412.
35. W.W. Klingbeil and R.T. Shield, Some numerical investigations on empirical strain energy functions in the large axi- symmetric extensions of rubber membranes, ZAMP 15(1964), 608-629.
36. P.D. Kouklis, E. Hutton and E. Fuchs, Making a connection: Direct binding between keratin intermediate filaments and desmosomal proteins, J. Cell Biol. 127(1994), 1049-1060.
37. K.S. Koutroupi and J.C. Barbenel, Mechanical and failure behavior of the stratum corneum, J. Biomech. 23(1990), 281-287.
38. A.P. Kowalczyk, E.A. Bornslaeger, S.M. Norvell, H.L. Palka and K.J. Green, Desmosomes: Intercellular adhesive junctions specialized for attachment of intermediate filaments, Int. Rev. Cytol. 185(1999), 237-302.
39. L. Kreplak, H. Bar, J.F. Leterrier, H. Herrmann and U. Aebi, Exploring the mechanical behavior of single intermediate filaments, J. Mol. Biol. 354(2005), 569-577.
40. T.J. Kriewall, N. Akkas, D.L. Bylski, J.W. Melvin and B.A. Work, Mechanical behavior of fetal dura mater under large axisymmetric inflation, J. Biomech. Eng. 105(1983), 71-76.
41. S.K. Kyriacou, A.D. Shah and J.D. Humphrey, Inverse finite element characterization of hyperelastic membranes, J. Appl. Mech. 64(1997), 257-262.
42. E.B. Lane and W.H.I. McLean, Keratins and skin disorders, J. Pathol. 204(2004), 355-366.
43. E.B. Lane and M. Pekny, Stress models for the study of intermediate filament function, Meth. Cell Biol. 78(2004), 229-264.
44. V.M. Laurent, E. Planus, R. Fodil and D. Isabey, Mechanical assessment by magnetocytometry of the cytosolic and cortical cytoskeletal compartments in adherent epithelial cells, Biorheology 40(2003), 235-240.
45. J.E. Lewis, P.J. Jensen and M.J. Wheelock, Cadherin function is required for human keratinocytes to assemble desmosomes and stratify in response to calcium, J. Invest. Dermatol. 102(1994), 870-877.
46. L.L. Ma, J.Y. Xu, P.A. Coulombe and D. Wirtz, Keratin filament suspensions show unique micromechanical properties, J. Biol. Chem. 274(1999), 19145-19151.
47. D. Maier-Schneider, J. Maibach and E. Obermeier, Computer-aided characterization of the elastic properties of thin films, J. Micromech. Microeng. 2(1992), 173-175.
48. B.D. Matthews, D.R. Overby, F.J. Alenghat, J. Karavitis, Y. Numaguchi, P.G. Allen and D.E. Ingber, Mechanical properties of individual focal adhesions probed with a magnetic microneedle, Biochem. Biophys. Res. Commun. 313(2004), 758-764.
49. J.A. McGrath, Inherited disorders of desmosomes, Australas. J. Dermatol. 46(2005), 221-229.
50. C.S. Nicolopoulos, P.V. Giannoudis, K.D. Glaros and J.C. Barbenel, In vitro study of the failure of skin surface after influence of hydration and preconditioning, Arch. Dermatol. Res. 290(1998), 638-640.
51. C.J.M. Nolte, M.A. Oleson, P.R. Bilbo and N.L. Parenteau, Development of a stratum corneum and barrier function in an organotypic skin culture, Arch. Dermatol. Res. 285(1993), 466-474.
52. E.J. Okeefe, R.A. Briggaman and B. Herman, Calcium-induced assembly of adherens junctions in keratinocytes, J. Cell Biol. 105(1987), 807-817.
53. A.S. Payne, Y. Hanakawa, M. Amagai and J.R. Stanley, Desmosomes and disease: Pemphigus and bullous impetigo, Curr. Opin. Cell Biol. 16(2004), 536-543.
54. G.K. Ragsdale, J. Phelps and K. Luby-Phelps, Viscoelastic response of fibroblasts to tension transmitted through adherens junctions, Biophys. J. 73(1997), 2798-2808.
55. N. Rosenblatt, S. Hu, B. Suki, N. Wang and D. Stamenovic, Contributions of the active and passive components of the cytoskeletal prestress to stiffening of airway smooth muscle cells, Ann. Biomed. Eng. 35(2007), 224-234.
56. D. Russell, P.D. Andrews, J. James and E.B. Lane, Mechanical stress induces profound remodelling of keratin filaments
57. and cell junctions in epidermolysis bullosa simplex keratinocytes, J. Cell Sci. 117(2004), 5233-5243.
58. J.C. Selby, Composite diaphragm inflation: A method for probing the rheological functions of cell-cell anchoring junctions and cytoskeletal networks within a living normal human epidermal keratinocyte sheet, PhD dissertation, University of Illinois at Urbana-Champaign, 2007.
59. J.C. Selby, S.A. Boppart and M.A. Shannon, Anchoring junctions and cytoskeletal networks in an epithelial sheet: Mechanical characterization using elastic microfabricated membranes, in: Proceedings of the 2003 ASME Summer Bioengi-neering Conference, Key Biscayne, FL, 2003, pp. 885-886.
60. J.C. Selby, S.A. Boppart and M.A. Shannon, Cytoskeletal networks in an epithelial sheet: Mechanical characterization using composite diaphragm inflation, in: Third Annual IEEE/EMBS Special Topic Conference on Microtechnology in Medicine and Biology, Oahu, HA, 2005, pp. 201-204.
61. J.C. Selby and M.A. Shannon, A method to fabricate mesoscopic freestanding polydimethylsiloxane membranes used to probe the rheology of an epithelial sheet, J. Biochem. Biophys. Methods (2008), in press; doi: 10.1016/j.jbbm.2007.07.005.
62. J.C. Selby and M.A. Shannon, An apparatus for measuring the finite load-deformation behavior of a sheet of epithelial cells cultured on a mesoscopic freestanding elastomer membrane, Rev. Sci. Instrum. 78(2007), 094301.
63. E.A. Smith and E. Fuchs, Defining the interactions between intermediate filaments and desmosomes, J. Cell Biol. 141(1998), 1229-1241.
64. M. Sotoudeh, S. Jalali, S. Usami, J.Y.J. Shyy and S. Chien, A strain device imposing dynamic and uniform equi-biaxial strain to cultured cells, Ann. Biomed. Eng. 26(1998), 181-189.
65. S. Suresh, J. Spatz, J.P. Mills, A. Micoulet, M. Dao, C.T. Lim, M. Beil and T. Seufferlein, Connections between single-cell biomechanics and human disease states: Gastrointestinal cancer and malaria, Acta Biomater. 1(2005), 15-30.
66. T.M. Svitkina, A.B. Verkhovsky and G.G. Borisy, Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton, J. Cell Biol. 135(1996), 991-1007.
67. O. Tabata, K. Kawahata, S. Sugiyama and I. Igarashi, Mechanical property measurements of thin films using load- deflection of composite rectangular membranes, Sensor. Actuator. 20(1989), 135-141.
68. E. Takai, K.D. Costa, A. Shaheen, C.T. Hung and X.E. Guo, Osteoblast elastic modulus measured by atomic force microscopy is substrate dependent, Ann. Biomed. Eng. 33(2005), 963-971.
69. O. Thoumine, A. Ott, O. Cardoso and J.J. Meister, Microplates: A new tool for manipulation and mechanical perturbation of individual cells, J. Biochem. Biophys. Methods 39(1999), 47-62.
70. A.M. Tomson, J. Scholma and E.H. Blaauw, The effect of detachment of cultured epithelial sheets on cellular ultrastructure and organization, Epithelial Cell Biol. 4(1995), 43-51.
71. X. Trepat, M. Grabulosa, F. Puig, G.N. Maksym, D. Navajas and R. Farre, Viscoelasticity of human alveolar epithelial cells subjected to stretch, Am.J.Physiol. 287(2004), L1025-L1034.
72. J. Trzewik, A. Artmann-Temiz, P.T. Linder, T. Demirci, I. Digel and G.M. Artmann, Evaluation of lateral mechanical tension in thin-film tissue constructs, Ann. Biomed. Eng. 32(2004), 1243-1251.
73. D.J. Tschumperlin and S.S. Margulies, Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro, Am. J. Physiol. 19(1998), L1173-L1183.
74. H. Ura, F. Takeda and H. Okochi, An in vitro outgrowth culture system for normal human keratinocytes, J. Dermatol. Sci. 35(2004), 19-28.
75. V. Vasioukhin, C. Bauer, M. Yin and E. Fuchs, Directed actin polymerization is the driving force for epithelial cell-cell adhesion, Cell 100(2000), 209-219.
76. H.G. Vogel and K. Denkel, In vivo recovery of mechanical- properties in rat skin after repeated strain, Arch. Dermatol. Res. 277(1985), 484-488.
77. T. Wakatsuki, M.S. Kolodney, G.I. Zahalak and E.L. Elson, Cell mechanics studied by a reconstituted model tissue, Biophys. J. 79(2000), 2353-2368.
78. N. Wang, J.P. Butler and D.E. Ingber, Mechanotransduction across the cell surface and through the cytoskeleton, Science 260(1993), 1124-1127.
79. N. Wang, I.M. Tolic-Norrelykke, J.X. Chen, S.M. Mijailovich, J.P. Butler, J.J. Fredberg and D. Stamenovic, Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells, Am.J.Physiol .282(2002), C606-C616.
80. F.M. Watt, Selective migration of terminally differentiating cells from the basal layer of cultured human epidermis, J. Cell Biol. 98(1984), 16-21.
81. F.M. Watt, D.L. Mattey and D.R. Garrod, Calcium-induced reorganization of desmosomal components in cultured human keratinocytes, J. Cell Biol. 99(1984), 2211-2215.
82. C. Wiebe and G.W. Brodland, Tensile properties of embryonic epithelia measured using a novel instrument, J. Biomech. 38(2005), 2087-2094.
83. J.L. Williams, J.H. Chen and D.M. Belloli, Strain fields on cell stressing devices employing clamped circular elastic diaphragms as substrates, J. Biomech. Eng. 114(1992), 377-384.
84. A. Wineman, D. Wilson and J.W. Melvin, Material identification of soft tissue using membrane inflation, J. Biomech. 12(1979), 841-850.
85. F.K. Winston, E.J. Macarak, S.F. Gorfien and L.E. Thibault, A system to reproduce and quantify the biomechanical environment of the cell, J. Appl. Physiol. 67(1989), 397-405.
86. M.A. Wolfram, N.F. Wolejsza and K. Laden, Biomechanical properties of delipidized stratum corneum, J. Invest. Derma- tol. 59(1972), 421-426.
87. K.S. Wu, W.W. van Osdol and R.H. Dauskardt, Mechanical properties of human stratum corneum: Effects of temperature, hydration, and chemical treatment, Biomaterials 27(2006), 785-795.
88. S. Yang and T. Saif, Micromachined force sensors for the study of cell mechanics, Rev. Sci. Instrum. 76(2005), 044301.
89. S. Yang and T. Saif, Reversible and repeatable linear local cell force response under large stretches, Exp. Cell Res. 305(2005), 42-50.
90. W.H. Yang and W.W. Feng, On axisymmetrical deformations of nonlinear membranes, J. Appl. Mech. 37(1970), 1002-1011.
91. S. Yano, M. Komine, M. Fujimoto, H. Okochi and K. Tamaki, Mechanical stretching in vitro regulates signal transduction pathways and cellular proliferation in human epidermal keratinocytes, J. Invest. Dermatol. 122(2004), 783-790.
92. T. Yeung, P.C. Georges, L.A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W.Y. Ming, V. Weaver and P.A. Janmey, Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion, Cell Motil. Cytoskel. 60(2005), 24-34.
93. G.B. Zamansky, U. Nguyen and I.N. Chou, An immunofluorescence study of the calcium-induced coordinated reorganization of microfilaments, keratin intermediate filaments, and microtubules in cultured human epidermal keratinocytes, J. Invest. Dermatol. 97(1991), 985-994.