Effect of membrane stiffness and cytoskeletal element density on mechanical stimuli within cells: an analysis of the consequences of ageing in cells

Computer Methods in Biomechanics and Biomedical Engineering

Volumn 18, Issue 5, 2015, Pages 468-476

  Xue, Feng ^a   Lennon, Alex B ^a   McKayed, Katey K ^a,b   Campbell, Veronica A ^a,b   Prendergast, Patrick J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

ageing; cell mechanics; cytoskeleton; nucleoskeleton; tensegrity

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOPHYSICS; CELLS; CYTOLOGY; MEMBRANES; PHYSIOLOGICAL MODELS; PROTEINS; STIFFNESS; VISCOELASTICITY;

AGEING; CELL MECHANICS; CYTOSKELETONS; NUCLEOSKELETON; TENSEGRITIES;

FINITE ELEMENT METHOD;

AGING; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL AGING; CELL DENSITY; CELL MEMBRANE; CELL MEMBRANE STIFFNESS; COMPUTER MODEL; CONTROLLED STUDY; FINITE ELEMENT ANALYSIS; INDENTATION TONOMETER; INTERMEDIATE FILAMENT; MATHEMATICAL ANALYSIS; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; VALIDATION PROCESS; BIOLOGICAL MODEL; BIOMECHANICS; CELL NUCLEUS; COMPUTER SIMULATION; CYTOSKELETON; ELASTICITY; MECHANICAL STRESS; METABOLISM; MICROTUBULE; PHYSIOLOGY; VISCOSITY;

BIOMECHANICAL PHENOMENA; CELL AGING; CELL MEMBRANE; CELL NUCLEUS; COMPUTER SIMULATION; CYTOSKELETON; ELASTICITY; MICROSCOPY, ATOMIC FORCE; MICROTUBULES; MODELS, BIOLOGICAL; STRESS, MECHANICAL; VISCOSITY;

EID: 84911989193     PISSN: 10255842     EISSN: 14768259     Source Type: Journal    
DOI: 10.1080/10255842.2013.811234     Document Type: Article

References (48)

1. AjmaniRS, MeterEJ, JaykumarR, IngramDK, SpanglerEL, AbugoOO, RifkindJM. 2000. Hemodynamic changes during aging associated with cerebral blood flow and impaired cognitive function. Neurobiol Aging.21(2):257–269.
2. AzelogluU, BhattacharyaJ, CostaKD. 2008. Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness. J Appl Physiol.105(2):652–661.
3. BertaudJ, QinZ, BuehlerMJ. 2010. Intermediate filament-deficient cells are mechanically softer at large deformation: a multi-scale simulation study. Acta Biomater.6(7):2457–2466.
4. CharrasGT, HortonMA. 2002a. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys J.82(6):2970–2981.
5. CharrasGT, HortonMA. 2002b. Determination of cellular strains by combined atomic force microscopy and finite element modeling. Biophys J.83(2):858–879.
6. CharrasGT, WilliamsBA, SimsSM, HortonMA. 2004. Estimating the sensitivity of mechanosensitive ion channels to membrane strain and tension. Biophys J.87(4):2870–2884.
7. CollinsworthAM, ZhangS, KrausWE, TruskeyGA. 2002. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol Cell Physiol.283(4):1219–1227.
8. CoughlinMF, StamenovicD. 1998. A tensegrity model of the cytoskeleton in spread and round cells. J Biomech Eng.120(6):770–777.
9. DahlKN, Booth-GauthierEA, LadouxB. 2010. In the middle of it all: mutual mechanical regulation between the nucleus and the cytoskeleton. J Biomech.43(1):2–8.
10. DahlKN, KahnSM, WilsonKL, DischerDE. 2004. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J Cell Sci.117(20):4779–4786.
11. DalbyMJ. 2005. Topographically induced direct cell mechanotransduction. Med Eng Phys.27(9):730–742.
12. De SantisG, LennonAB, BoschettiF, VerheggheB, VerdonckP, PrendergastPJ. 2011. How can cells sense the elasticity of a substrate? An analysis using a cell tensegrity model. Eur Cell Mater.22:202–213.
13. DeguchiS, OhashiT, SatoM. 2005. Evaluation of tension in actin bundle of endothelial cells based on preexisting strain and tensile properties measurements. Mol Cell Biomech.2(3):125–133.
14. EvansE, YeungA. 1989. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J.56(1):151–160.
15. FrischT, ThoumineO. 2002. Predicting the kinetics of cell spreading. J Biomech.35(8):1137–1141.
16. GittesF, MickeyB, NettletonJ, HowardJ. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol.120(4):923–934.
17. GuilakF, TedrowJR, BurgkartR. 2000. Viscoelastic properties of the cell nucleus. Biochem Biophys Res Commun.269(3):781–786.
18. HaleJP, WinloveCP, PetrovPG. 2011. Effect of hydroperoxides on red blood cell membrane mechanical properties. Biophys J. 11(8):1921–1929.
19. IngberDE. 1997. Tensegrity: the architectural basis of cellular mechanotransduction. Ann Rev Physiol.59:575–599.
20. IngberDE. 2008. Tensegrity-based mechanosensing from macro to micro. Prog Biophys Mol Biol.97(2–3):163–179.
21. IngberDE. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci.104(3):613–627.
22. KammRD, McVittieAK, BatheM. 2000. On the role of continuum models in mechanobiology. ASME Int Congr Mech Biol.242:1–9.
23. KarcherH, LammerdingJ, HuangH, LeeRT, KammRD, Kaazempur-MofradMR. 2003. A three-dimensional viscoelastic model for cell deformation with experimental verification. Biophys J.85(5):3336–3349.
24. KellyGM, KilpatrickJI, van EsMH, WeaferPP, PrendergastPJ, JarvisSP. 2011. Bone cell elasticity and morphology changes during the cell cycle. J Biomech.44(8):1484–1490.
25. MaguireP, KilpatrickJI, KellyGM, PrendergastPJ, CampbellVA, O'ConnellBC, JarvisSP. 2007. Direct mechanical measurement of geodesic structures in rat mesenchymal stem cells. HFSP J.1(3):181–191.
26. MazumderA, ShivashankarGV. 2010. Emergence of a prestressed eukaryotic nucleus during cellular differentiation and development. J Roy Soc Interface.7(3):321–330.
27. McGarryJG, PrendergastPJ. 2004. A three-dimensional finite element model of an adherent eukaryotic cell. Eur Cell Mater.7:27–33.
28. McGarryJG, Klein-NulendJ, MullenderMG, PrendergastPJ. 2005. A comparison of strain and fluid shear stress in stimulating bone cell responses – a computational and experimental study. FASEB J.19(3):482–484.
29. McKayed KK, Campbell VA, Prendergast PJ. 2010. The influence of age on mesenchymal stem cell mechanoresponsiveness to tensile strain. Paper presented at: ESB 2010.Proceedings of the 17th Congress of European Society of Biomechanics, July 5–8; University of Edinburgh, Edinburgh, UK.
30. MoeendarbaryE, ValonL, FritzscheM, HarrisAR, MouldingDA, ThrasherAJ, StrideE, MahadevanL, CharrasGT. 2013. The cytoplasm of living cells behaves as a poroelastic material. Nat Mater.12:253–261.
31. MorrisR, CoxH, MombelliE, QuinnPJ. 2004. Rafts, little caves and large potholes: how lipid structure interacts with membrane proteins to create functionally diverse membrane environments. Subcell Biochem.37:35–118.
32. MuellerSM, GlowackiJ. 2001. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem.82(4):583–590.
33. NgL, HungH, SpruntA, ChubinskyaS, OrtizC, GrodzinskyA. 2007. Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J Biomech.40:1011–1023.
34. OhashiT, IshiiY, IshikawaY, MatsumotoT, SatoM. 2002. Experimental and numerical analyses of local mechanical properties measured by atomic force microscopy for sheared endothelial cells. Biomed Mater Eng.12(3):319–327.
35. RadmacherM, ClevelandJP, FritzM, HansmaHG, HansmaPK. 1994. Mapping interaction forces with the atomic force microscope. Biophys J.66(6):2159–2165.
36. ShinD, AthanasiouK. 1999. Cytoindentation for obtaining cell biomechanical properties. J Orthop Res.17:880–890.
37. SmithSB, CuiY, BustamanteC. 1996. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science.271(5250):795–799.
38. StamenovicD, CoughlinMF. 1999. The role of prestress and architecture of the cytoskeleton and deformability of cytoskeletal filaments in mechanics of adherent cells: a quantitative analysis. J Theor Biol.201(1):63–74.
39. StamenovicD, FredbergJJ, WangN, ButlerJP, IngberDE. 1996. A microstructural approach to cytoskeletal mechanics based on tensegrity. J Theor Biol.181(2):125–136.
40. StarodubtsevaMN. 2011. Mechanical properties of cells and ageing. Ageing Res Rev.10(1):16–25.
41. SteinGS, LianJB, van WijnenAJ, SteinJL, JavedA, MontecinoM, ChoiJ, VradiiD, ZaidiSK, PratapJ, YoungD. 2007. Organization of transcriptional regulatory machinery in nuclear microenvironments: implications for biological control and cancer. Adv Enzyme Regul.47:242–250.
42. WangN, StamenovicD. 2000. Contribution of intermediate filaments to cell stiffness, stiffening, and growth. Am J Physiol Cell Physiol.279(1):188–194.
43. WangN, StamenovicD. 2002. Mechanics of vimentin intermediate filaments. J Muscle Res Cell Motil.23(5-6):535–540.
44. WangN, NaruseK, StamenovicD, FredbergJJ, MijailovichSM, Tolic-NorrelykkeIM, PolteT, MannixR, IngberDE. 2001. Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci USA.98(14):7765–7770.
45. WangN, TytellJD, IngberDE. 2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol.10(1):75–82.
46. WaughRE, AgreP. 1988. Reductions of erythrocyte membrane viscoelastic coefficients reflect spectrin deficiencies in hereditary spherocytosis. J Clin Invest.81(1):133–141.
47. WendlingS, OddouC, IsabeyD. 1999. Stiffening response of a cellular tensegrity model. J Theor Biol.196(3):309–325.
48. ZhengH, MartinJA, DuwayriY, FalconG, BuckwalterJA. 2007. Impact of aging on rat bone marrow-derived stem cell chondrogenesis. J Gerontol Biol Sci Med Sci.62(2):136–148.