The Influence of Physical and Physiological Cues on Atomic Force Microscopy-Based Cell Stiffness Assessment

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Chiou, Yu Wei ^a   Lin, Hsiu Kuan ^a   Tang, Ming Jer ^a   Lin, Hsi Hui ^a   Yeh, Ming Long ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; ASSOCIATION; ATOMIC FORCE MICROSCOPY; CELL AGING; CELL CULTURE; CELL STIFFNESS; CELL STRUCTURE; CELLULAR PARAMETERS; CONTROLLED STUDY; DENSITY; ELASTICITY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; MDCK CELL; MOUSE; NONHUMAN; PHENOTYPE; STEM CELL; TEMPERATURE; YOUNG MODULUS; ANIMAL; BIOMECHANICS; BOVINAE; CELL COUNT; CYTOLOGY; DOG; FLUORESCENT ANTIBODY TECHNIQUE; KIDNEY; MDCK CELL LINE; METABOLISM; PHYSIOLOGY; PROCEDURES;

ACTIN CYTOSKELETON; ANIMALS; BIOMECHANICAL PHENOMENA; CATTLE; CELL COUNT; DOGS; ELASTICITY; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; KIDNEY; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROSCOPY, ATOMIC FORCE; STEM CELLS;

EID: 84885990063     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077384     Document Type: Article

References (67)

1. Stossel TP, (1993) On the crawling of animal cells. Science 260: 1086-1094.
2. Guck J, Lautenschlager F, Paschke S, Beil M, (2010) Critical review: cellular mechanobiology and amoeboid migration. Integr Biol (Camb) 2: 575-583.
3. Provenzano PP, Keely PJ, (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J Cell Sci 124: 1195-1205.
4. Chen CS, Tan J, Tien J, (2004) Mechanotransduction at cell-matrix and cell-cell contacts. Annu Rev Biomed Eng 6: 275-302.
5. Takai E, Costa KD, Shaheen A, Hung CT, Guo XE, (2005) Osteoblast elastic modulus measured by atomic force microscopy is substrate dependent. Ann Biomed Eng 33: 963-971.
6. Ketene AN, Roberts PC, Shea AA, Schmelz EM, Agah M, (2012) Actin filaments play a primary role for structural integrity and viscoelastic response in cells. Integr Biol (Camb) 4: 540-549.
7. Rotsch C, Radmacher M, (2000) Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys J 78: 520-535.
8. Dominguez R, Holmes KC, (2011) Actin structure and function. Annu Rev Biophys 40: 169-186.
9. Lu L, Oswald SJ, Ngu H, Yin FC, (2008) Mechanical properties of actin stress fibers in living cells. Biophys J 95: 6060-6071.
10. Kidoaki S, Matsuda T, (2007) Shape-engineered fibroblasts: cell elasticity and actin cytoskeletal features characterized by fluorescence and atomic force microscopy. J Biomed Mater Res A 81: 803-810.
11. Pawlak G, Helfman DM, (2001) Cytoskeletal changes in cell transformation and tumorigenesis. Curr Opin Genet Dev 11: 41-47.
12. Schwartz MA, (2010) Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb Perspect Biol 2: a005066.
13. Clark EA, Hynes RO, (1996) Ras activation is necessary for integrin-mediated activation of extracellular signal-regulated kinase 2 and cytosolic phospholipase A2 but not for cytoskeletal organization. J Biol Chem 271: 14814-14818.
14. Niessen CM, (2007) Tight junctions/adherens junctions: basic structure and function. J Invest Dermatol 127: 2525-2532.
15. Schmalhofer O, Brabletz S, Brabletz T, (2009) E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 28: 151-166.
16. Zhang Q, Ragnauth C, Greener MJ, Shanahan CM, Roberts RG, (2002) The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 80: 473-481.
17. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, et al. (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172: 41-53.
18. Stewart-Hutchinson PJ, Hale CM, Wirtz D, Hodzic D, (2008) Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp Cell Res 314: 1892-1905.
19. Chancellor TJ, Lee J, Thodeti CK, Lele T, (2010) Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 99: 115-123.
20. Naumanen P, Lappalainen P, Hotulainen P, (2008) Mechanisms of actin stress fibre assembly. J Microsc 231: 446-454.
21. Miyake Y, Inoue N, Nishimura K, Kinoshita N, Hosoya H, et al. (2006) Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp Cell Res 312: 1637-1650.
22. Muller DJ, Dufrene YF, (2008) Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat Nanotechnol 3: 261-269.
23. Lulevich V, Zink T, Chen HY, Liu FT, Liu GY, (2006) Cell mechanics using atomic force microscopy-based single-cell compression. Langmuir 22: 8151-8155.
24. Sirghi L, Ponti J, Broggi F, Rossi F, (2008) Probing elasticity and adhesion of live cells by atomic force microscopy indentation. Eur Biophys J 37: 935-945.
25. Roduit C, Sekatski S, Dietler G, Catsicas S, Lafont F, et al. (2009) Stiffness tomography by atomic force microscopy. Biophys J 97: 674-677.
26. Alonso JL, Goldmann WH, (2003) Feeling the forces: atomic force microscopy in cell biology. Life Sci 72: 2553-2560.
27. Bouchiat C, Wang MD, Allemand J, Strick T, Block SM, et al. (1999) Estimating the persistence length of a worm-like chain molecule from force-extension measurements. Biophys J 76: 409-413.
28. Rico F, Roca-Cusachs P, Gavara N, Farre R, Rotger M, et al. (2005) Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Phys Rev E Stat Nonlin Soft Matter Phys 72: 021914.
29. Bilodeau GG, (1992) Regular Pyramid Punch Problem. Journal of Applied Mechanics-Transactions of the Asme 59: 519-523.
30. Sokolov I (2007) Atomic Force Microscopy in Cancer Cell Research. Cancer Nanotechnology: 1-17.
31. Docheva D, Padula D, Popov C, Mutschler W, Clausen-Schaumann H, et al. (2008) Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J Cell Mol Med 12: 537-552.
32. Pelling AE, Dawson DW, Carreon DM, Christiansen JJ, Shen RR, et al. (2007) Distinct contributions of microtubule subtypes to cell membrane shape and stability. Nanomedicine 3: 43-52.
33. Rotsch C, Braet F, Wisse E, Radmacher M, (1997) AFM imaging and elasticity measurements on living rat liver macrophages. Cell Biol Int 21: 685-696.
34. Mahaffy RE, Park S, Gerde E, Kas J, Shih CK, (2004) Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophys J 86: 1777-1793.
35. Sunyer R, Trepat X, Fredberg JJ, Farre R, Navajas D, (2009) The temperature dependence of cell mechanics measured by atomic force microscopy. Phys Biol 6: 025009.
36. Ferri A, Grazi E, (1982) Mechano-chemical energy transduction in biological systems. The effect of mechanical stimulation on the polymerization of actin: a kinetic study. Biochem J 205: 281-284.
37. Kuznetsova TG, Starodubtseva MN, Yegorenkov NI, Chizhik SA, Zhdanov RI, (2007) Atomic force microscopy probing of cell elasticity. Micron 38: 824-833.
38. Wang YK, Lin HH, Tang MJ, (2001) Collagen gel overlay induces two phases of apoptosis in MDCK cells. Am J Physiol Cell Physiol 280: C1440-1448.
39. Lee PT, Lin HH, Jiang ST, Lu PJ, Chou KJ, et al. (2010) Mouse kidney progenitor cells accelerate renal regeneration and prolong survival after ischemic injury. Stem Cells 28: 573-584.
40. Wang YH, Chiu WT, Wang YK, Wu CC, Chen TL, et al. (2007) Deregulation of AP-1 proteins in collagen gel-induced epithelial cell apoptosis mediated by low substratum rigidity. J Biol Chem 282: 752-763.
41. Costa KD, Sim AJ, Yin FC, (2006) Non-Hertzian approach to analyzing mechanical properties of endothelial cells probed by atomic force microscopy. J Biomech Eng 128: 176-184.
42. Trickey WR, Baaijens FP, Laursen TA, Alexopoulos LG, Guilak F, (2006) Determination of the Poisson's ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. J Biomech 39: 78-87.
43. Ketene AN, Schmelz EM, Roberts PC, Agah M, (2012) The effects of cancer progression on the viscoelasticity of ovarian cell cytoskeleton structures. Nanomedicine 8: 93-102.
44. Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA, (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J Biomech 34: 1545-1553.
45. Lu YB, Franze K, Seifert G, Steinhauser C, Kirchhoff F, et al. (2006) Viscoelastic properties of individual glial cells and neurons in the CNS. Proc Natl Acad Sci U S A 103: 17759-17764.
46. Lekka M, Laidler P, Gil D, Lekki J, Stachura Z, et al. (1999) Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 28: 312-316.
47. Obataya I, Nakamura C, Han S, Nakamura N, Miyake J, (2005) Nanoscale operation of a living cell using an atomic force microscope with a nanoneedle. Nano Lett 5: 27-30.
48. Goncalves RP, Agnus G, Sens P, Houssin C, Bartenlian B, et al. (2006) Two-chamber AFM: probing membrane proteins separating two aqueous compartments. Nat Methods 3: 1007-1012.
49. Cuerrier CM, Lebel R, Grandbois M, (2007) Single cell transfection using plasmid decorated AFM probes. Biochem Biophys Res Commun 355: 632-636.
50. Hategan A, Law R, Kahn S, Discher DE, (2003) Adhesively-tensed cell membranes: lysis kinetics and atomic force microscopy probing. Biophys J 85: 2746-2759.
51. Li QS, Lee GY, Ong CN, Lim CT, (2008) AFM indentation study of breast cancer cells. Biochem Biophys Res Commun 374: 609-613.
52. Welch WJ, Suhan JP, (1985) Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol 101: 1198-1211.
53. Shyy TT, Asch BB, Asch HL, (1989) Concurrent collapse of keratin filaments, aggregation of organelles, and inhibition of protein synthesis during the heat shock response in mammary epithelial cells. J Cell Biol 108: 997-1008.
54. Mounier N, Arrigo AP, (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7: 167-176.
55. Chrzanowska-Wodnicka M, Burridge K, (1994) Tyrosine phosphorylation is involved in reorganization of the actin cytoskeleton in response to serum or LPA stimulation. J Cell Sci 107 (Pt 12): 3643-3654.
56. Battista PJ, DiSorbo DM, Weiss SA (1991) Development of a carbon dioxide independent medium. In Vitro Cell Dev Biol 27.
57. Lim SM, Kreipe BA, Trzeciakowski J, Dangott L, Trache A, (2010) Extracellular matrix effect on RhoA signaling modulation in vascular smooth muscle cells. Exp Cell Res 316: 2833-2848.
58. Tojkander S, Gateva G, Lappalainen P, (2012) Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 125: 1855-1864.
59. Razafsky D, Hodzic D, (2009) Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186: 461-472.
60. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL, et al. (2009) A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci U S A 106: 19017-19022.
61. Kim DH, Khatau SB, Feng Y, Walcott S, Sun SX, et al. (2012) Actin cap associated focal adhesions and their distinct role in cellular mechanosensing. Sci Rep 2: 555.
62. Wei WC, Lin HH, Shen MR, Tang MJ, (2008) Mechanosensing machinery for cells under low substratum rigidity. Am J Physiol Cell Physiol 295: C1579-1589.
63. Berdyyeva TK, Woodworth CD, Sokolov I, (2005) Human epithelial cells increase their rigidity with ageing in vitro: direct measurements. Phys Med Biol 50: 81-92.
64. Zeng X, (2007) Human embryonic stem cells: mechanisms to escape replicative senescence? Stem Cell Rev 3: 270-279.
65. Koch CM, Reck K, Shao K, Lin Q, Joussen S, et al. (2013) Pluripotent stem cells escape from senescence-associated DNA methylation changes. Genome Res 23: 248-259.
66. Farhadifar R, Roper JC, Aigouy B, Eaton S, Julicher F, (2007) The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17: 2095-2104.
67. Califano JP, Reinhart-King CA, (2010) Substrate Stiffness and Cell Area Predict Cellular Traction Stresses in Single Cells and Cells in Contact. Cell Mol Bioeng 3: 68-75.