Mechanical dynamics of single cells during early apoptosis

Cell Motility and the Cytoskeleton

Volumn 66, Issue 7, 2009, Pages 409-422

  Pelling, Andrew E ^a,b   Veraitch, Farlan S ^a   Chu, Carol Pui Kei ^a   Mason, Chris ^a   Horton, Michael A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Atomic force microscopy; Cytoskeleton; Elasticity; Laser scanning confocal microscopy; Viscosity

Indexed keywords

CASPASE; HYBRID PROTEIN; STAUROSPORINE;

APOPTOSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL KINETICS; CELL NUCLEUS; CONFOCAL MICROSCOPY; CYTOSKELETON; ELASTICITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; VISCOSITY; YOUNG MODULUS;

ACTINS; APOPTOSIS; CELL LINE; CELL NUCLEUS; CYTOCHALASIN D; CYTOSKELETON; ENZYME INHIBITORS; FIBROBLASTS; HUMANS; LAMIN TYPE A; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; NOCODAZOLE; NUCLEIC ACID SYNTHESIS INHIBITORS; STAUROSPORINE; STRESS, MECHANICAL; TRANSFECTION; TUBULIN; TUBULIN MODULATORS;

EID: 67650138619     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20391     Document Type: Article

References (58)

1. Aho S. 2004. Plakin proteins are coordinately cleaved during apoptosis but preferentially through the action of different caspases. Exp Dermatol 13(11):700-707. (Pubitemid 39481023)
2. Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y, Kaibuchi K. 1997. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275(5304):1308-1311. (Pubitemid 27114159)
3. Andra K, Nikolic B, Stocher M, Drenckhahn D, Wiche G. 1998. Not just scaffolding: Plectin regulates actin dynamics in cultured cells. Genes Dev 12(21):3442-3451. (Pubitemid 28520991)
4. Belmokhtar CA, Hillion J, Segal-Bendirdjian E. 2001. Staurosporine induces apoptosis through both caspase-dependent and caspase- independent mechanisms. Oncogene 20(26):3354-3362. (Pubitemid 32588984)
5. Binnig G, Quate CF, Gerber C. 1986. Atomic force microscope. Phys Rev Lett 56(9):930-933.
6. Borner C, Monney L. 1999. Apoptosis without caspases: An inefficient molecular guillotine? Cell Death Differ 6(6): 497-507.
7. Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J, Mahadevan L, Parker KK, Ingber DE, Weitz DA. 2006. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J Cell Biol 173(5):733-741. (Pubitemid 46165581)
8. Chang L, Goldman RD. 2004. Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol 5(8):601-613. (Pubitemid 39025061)
9. Charras GT, Horton MA. 2002. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys J 82(6):2970-2981. (Pubitemid 34547640)
10. Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ. 2005. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435(7040):365-369. (Pubitemid 40745547)
11. Charras GT, Hu CK, Coughlin M, Mitchison TJ. 2006. Reassembly of contractile actin cortex in cell blebs. J Cell Biol 175(3): 477-490. (Pubitemid 44708071)
12. Darling EM, Zauscher S, Guilak F. 2006. Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritis Cartilage 14(6):571-579. (Pubitemid 43758550)
13. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126(4):677-689.
14. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE. 2008. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scarlike rigidity inhibits beating. J Cell Sci 121(Pt 22):3794-3802.
15. Gurland G, Gundersen GG. 1995. Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J Cell Biol 131(5):1275-1290.
16. Gyoeva FK, Gelfand VI. 1991. Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353(6343):445-448. (Pubitemid 21912534)
17. Haupt BJ, Pelling AE, Horton MA. 2006. Integrated confocal and scanning probe microscopy for biomedical research. Scientific World J 6:1609-1618. (Pubitemid 46045430)
18. Heidemann SR, Kaech S, Buxbaum RE, Matus A. 1999. Direct observations of the mechanical behaviors of the cytoskeleton in living fibroblasts. J Cell Biol 145(1):109-122. (Pubitemid 29177679)
19. Herrmann H, Bar H, Kreplak L, Strelkov SV, Aebi U. 2007. Intermediate filaments: From cell architecture to nanomechanics. Nat Rev Mol Cell Biol 8(7):562-573. (Pubitemid 46985377)
20. Hessler JA, Budor A, Putchakayala K, Mecke A, Rieger D, Banaszak Holl MM, Orr BG, Bielinska A, Beals J, Baker J, Jr. 2005. Atomic force microscopy study of early morphological changes during apoptosis. Langmuir 21(20):9280-9286.
21. Hipfner DR, Cohen SM. 2004. Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol 5(10):805-815. (Pubitemid 39336274)
22. Huang H, Kamm RD, Lee RT. 2004. Cell mechanics and mechanotransduction: Pathways, probes, and physiology. Am J Physiol Cell Physiol 287(1):C1-C11. (Pubitemid 38780146)
23. Jefferson JJ, Leung CL, Liem RK. 2004. Plakins: Goliaths that link cell junctions and the cytoskeleton. Nat Rev Mol Cell Biol 5(7):542-553. (Pubitemid 38868583)
24. Krieg M, Arboleda-Estudillo Y, Puech PH, Kafer J, Graner F, Muller DJ, Heisenberg CP. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10(4):429-436.
25. Kunda P, Pelling AE, Liu T, Baum B. 2008. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 18(2):91-101.
26. Lam WA, Rosenbluth MJ, Fletcher DA. 2007. Chemotherapy exposure increases leukemia cell stiffness. Blood 109(8):3505-3508. (Pubitemid 46572542)
27. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT. 2004. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113(3):370-378. (Pubitemid 38544181)
28. Lee J. 2007. The use of gelatin substrates for traction force microscopy in rapidly moving cells. Methods Cell Biol 83:297-312.
29. Leung CL, Green KJ, Liem RK. 2002. Plakins: A family of versatile cytolinker proteins. Trends Cell Biol 12(1):37-45. (Pubitemid 34164155)
30. Mannherz HG, Gonsior SM, Wu X, Polzar B, Pope BJ, Wartosch L, Weeds AG. 2006. Dual effects of staurosporine on A431 and NRK cells: Microfilament disassembly and uncoordinated lamellipodial activity followed by cell death. Eur J Cell Biol 85(8):785-802. (Pubitemid 44070572)
31. Martens JC, Radmacher M. 2008. Softening of the actin cytoskeleton by inhibition of myosin II. Pflugers Arch 456(1):95-100.
32. Matzke R, Jacobson K, Radmacher M. 2001. Direct, high-resolution measurement of furrow stiffening during division of adherent cells. Nat Cell Biol 3(6):607-610. (Pubitemid 32536859)
33. McCarthy NJ, Whyte MK, Gilbert CS, Evan GI. 1997. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J Cell Biol 136(1):215-227. (Pubitemid 27044816)
34. Omelchenko T, Vasiliev JM, Gelfand IM, Feder HH, Bonder EM. 2002. Mechanisms of polarization of the shape of fibroblasts and epitheliocytes: Separation of the roles of microtubules and Rho-dependent actin-myosin contractility. Proc Natl Acad Sci USA 99(16):1045210457. (Pubitemid 34906997)
35. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE. 2007. Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA 104(40):15619-15624.
36. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241-254.
37. Pelling AE, Horton MA. 2008. An historical perspective on cell mechanics. Pflugers Arch 456(1):3-12.
38. Pelling AE, Dawson DW, Carreon DM, Christiansen JJ, Shen RR, Teitell MA, Gimzewski JK. 2007a. Distinct contributions of microtubule subtypes to cell membrane shape and stability. Nanomedicine 3:43-52. (Pubitemid 46428186)
39. Pelling AE, Nicholls BM, Silberberg YS, Horton MA. 2007b. Approaches for investigating mechanobiologial dynamics in living cells with combined fluorescence and atomic force microscopies. In: Méndez-Vilas A, D́az J, editors. Modern Research and Educational Topics on Microscopy. Badajoz: Formatex. pp 3-10.
40. Pelling AE, Veraitch FS, Pui-Kei Chu C, Nicholls BM, Hemsley AL, Mason C, Horton MA. 2007c. Mapping correlated membrane pulsations and fluctuations in human cells. J Mol Recognit 20(6):467-475.
41. Riedl SJ, Shi Y. 2004. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5(11):897-907. (Pubitemid 39486541)
42. Rolls MM, Stein PA, Taylor SS, Ha E, McKeon F, Rapoport TA. 1999. A visual screen of a GFP-fusion library identifies a new type of nuclear envelope membrane protein. J Cell Biol 146(1):29-44. (Pubitemid 29349962)
43. Rotsch C, Radmacher M. 2000. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys J 78(1):520-535. (Pubitemid 30207160)
44. Ruchaud S, Korfali N, Villa P, Kottke TJ, Dingwall C, Kaufmann SH, Earnshaw WC. 2002. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J 21(8):19671977. (Pubitemid 34437194)
45. Schafer A, Radmacher M. 2005. Influence of myosin II activity on stiffness of fibroblast cells. Acta Biomater 1(3):273-280. (Pubitemid 43348787)
46. Stegh AH, Herrmann H, Lampel S, Weisenberger D, Andra K, Seper M, Wiche G, Krammer PH, Peter ME. 2000. Identification of the cytolinker plectin as a major early in vivo substrate for caspase 8 during CD95 and tumor necrosis factor receptor-mediated apoptosis. Mol Cell Biol 20(15):5665-5679. (Pubitemid 30482900)
47. Stolz M, Raiteri R, Daniels AU, VanLandingham MR, Baschong W, Aebi U. 2004. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys J 86(5):3269-3283. (Pubitemid 38552726)
48. Svitkina TM, Verkhovsky AB, Borisy GG. 1996. Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J Cell Biol 135(4):991-1007. (Pubitemid 26403774)
49. Taylor RC, Cullen SP, Martin SJ. 2008. Apoptosis: Controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9:231-241. (Pubitemid 351301823)
50. Thompson CB. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267(5203):1456-1462.
51. Thornberry NA, Lazebnik Y. 1998. Caspases: Enemies within. Science 281(5381):1312-1316.
52. Wiche G. 1998. Role of plectin in cytoskeleton organization and dynamics. J Cell Sci 111(Pt 17):2477-2486. (Pubitemid 28474951)
53. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A. 2005. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 171(5):799-810. (Pubitemid 41746582)
54. Yang RS, Lu KS, Fu WM, Liu TK, Lin-Shiau SY. 1993. Staurosporine- induced morphological changes in the rat osteoblasts. Cell Biol Int 17(1):75-82. (Pubitemid 23121721)
55. Yoon M, Moir RD, Prahlad V, Goldman RD. 1998. Motile properties of vimentin intermediate filament networks in living cells. J Cell Biol 143(1):147-157. (Pubitemid 28480524)
56. 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(5):473-481. (Pubitemid 35333789)
57. Zhang XD, Gillespie SK, Hersey P. 2004. Staurosporine induces apoptosis of melanoma by both caspase-dependent and -independent apoptotic pathways. Mol Cancer Ther 3(2):187-197. (Pubitemid 39193693)
58. Zhu C, Bao G, Wang N. 2000. Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu Rev Biomed Eng 2:189-226.