Abstract
When a dielectric object is placed between two opposed, nonfocused laser beams, the total force acting on the object is zero but the surface forces are additive, thus leading to a stretching of the object along the axis of the beams. Using this principle, we have constructed a device, called an optical stretcher, that can be used to measure the viscoelastic properties of dielectric materials, including biologic materials such as cells, with the sensitivity necessary to distinguish even between different individual cytoskeletal phenotypes. We have successfully used the optical stretcher to deform human erythrocytes and mouse fibroblasts. In the optical stretcher, no focusing is required, thus radiation damage is minimized and the surface forces are not limited by the light power. The magnitude of the deforming forces in the optical stretcher thus bridges the gap between optical tweezers and atomic force microscopy for the study of biologic materials.
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- Adelman M. R., Borisy G. G., Shelanski M. L., Weisenberg R. C., Taylor E. W. Cytoplasmic filaments and tubules. Fed Proc. 1968 Sep-Oct;27(5):1186–1193. [PubMed] [Google Scholar]
- Aebi U., Cohn J., Buhle L., Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature. 1986 Oct 9;323(6088):560–564. doi: 10.1038/323560a0. [DOI] [PubMed] [Google Scholar]
- Allen P. G., Janmey P. A. Gelsolin displaces phalloidin from actin filaments. A new fluorescence method shows that both Ca2+ and Mg2+ affect the rate at which gelsolin severs F-actin. J Biol Chem. 1994 Dec 30;269(52):32916–32923. [PubMed] [Google Scholar]
- Ashkin A., Dziedzic J. M. Optical trapping and manipulation of viruses and bacteria. Science. 1987 Mar 20;235(4795):1517–1520. doi: 10.1126/science.3547653. [DOI] [PubMed] [Google Scholar]
- Ashkin A., Dziedzic J. M., Yamane T. Optical trapping and manipulation of single cells using infrared laser beams. Nature. 1987 Dec 24;330(6150):769–771. doi: 10.1038/330769a0. [DOI] [PubMed] [Google Scholar]
- Bennett V. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol Rev. 1990 Oct;70(4):1029–1065. doi: 10.1152/physrev.1990.70.4.1029. [DOI] [PubMed] [Google Scholar]
- Bennett V. The membrane skeleton of human erythrocytes and its implications for more complex cells. Annu Rev Biochem. 1985;54:273–304. doi: 10.1146/annurev.bi.54.070185.001421. [DOI] [PubMed] [Google Scholar]
- Block S. M., Goldstein L. S., Schnapp B. J. Bead movement by single kinesin molecules studied with optical tweezers. Nature. 1990 Nov 22;348(6299):348–352. doi: 10.1038/348348a0. [DOI] [PubMed] [Google Scholar]
- Carlier M. F. Control of actin dynamics. Curr Opin Cell Biol. 1998 Feb;10(1):45–51. doi: 10.1016/s0955-0674(98)80085-9. [DOI] [PubMed] [Google Scholar]
- Chaponnier C., Gabbiani G. Gelsolin modulation in epithelial and stromal cells of mammary carcinoma. Am J Pathol. 1989 Mar;134(3):597–603. [PMC free article] [PubMed] [Google Scholar]
- Chu S. Laser manipulation of atoms and particles. Science. 1991 Aug 23;253(5022):861–866. doi: 10.1126/science.253.5022.861. [DOI] [PubMed] [Google Scholar]
- Colon J. M., Sarosi P., McGovern P. G., Askin A., Dziedzic J. M., Skurnick J., Weiss G., Bonder E. M. Controlled micromanipulation of human sperm in three dimensions with an infrared laser optical trap: effect on sperm velocity. Fertil Steril. 1992 Mar;57(3):695–698. doi: 10.1016/s0015-0282(16)54926-7. [DOI] [PubMed] [Google Scholar]
- Cooper J. A., Bryan J., Schwab B., 3rd, Frieden C., Loftus D. J., Elson E. L. Microinjection of gelsolin into living cells. J Cell Biol. 1987 Mar;104(3):491–501. doi: 10.1083/jcb.104.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cunningham C. C., Gorlin J. B., Kwiatkowski D. J., Hartwig J. H., Janmey P. A., Byers H. R., Stossel T. P. Actin-binding protein requirement for cortical stability and efficient locomotion. Science. 1992 Jan 17;255(5042):325–327. doi: 10.1126/science.1549777. [DOI] [PubMed] [Google Scholar]
- Daily B., Elson E. L., Zahalak G. I. Cell poking. Determination of the elastic area compressibility modulus of the erythrocyte membrane. Biophys J. 1984 Apr;45(4):671–682. doi: 10.1016/S0006-3495(84)84209-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Discher D. E., Mohandas N., Evans E. A. Molecular maps of red cell deformation: hidden elasticity and in situ connectivity. Science. 1994 Nov 11;266(5187):1032–1035. doi: 10.1126/science.7973655. [DOI] [PubMed] [Google Scholar]
- Dunphy C. H., Ramos R. Combining fine-needle aspiration and flow cytometric immunophenotyping in evaluation of nodal and extranodal sites for possible lymphoma: a retrospective review. Diagn Cytopathol. 1997 Mar;16(3):200–206. doi: 10.1002/(sici)1097-0339(199703)16:3<200::aid-dc2>3.0.co;2-j. [DOI] [PubMed] [Google Scholar]
- Eichinger L., Köppel B., Noegel A. A., Schleicher M., Schliwa M., Weijer K., Witke W., Janmey P. A. Mechanical perturbation elicits a phenotypic difference between Dictyostelium wild-type cells and cytoskeletal mutants. Biophys J. 1996 Feb;70(2):1054–1060. doi: 10.1016/S0006-3495(96)79651-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elson E. L. Cellular mechanics as an indicator of cytoskeletal structure and function. Annu Rev Biophys Biophys Chem. 1988;17:397–430. doi: 10.1146/annurev.bb.17.060188.002145. [DOI] [PubMed] [Google Scholar]
- Evans E., Fung Y. C. Improved measurements of the erythrocyte geometry. Microvasc Res. 1972 Oct;4(4):335–347. doi: 10.1016/0026-2862(72)90069-6. [DOI] [PubMed] [Google Scholar]
- Fajardo L. L., DeAngelis G. A. The role of stereotactic biopsy in abnormal mammograms. Surg Oncol Clin N Am. 1997 Apr;6(2):285–299. [PubMed] [Google Scholar]
- Felder S., Elson E. L. Mechanics of fibroblast locomotion: quantitative analysis of forces and motions at the leading lamellas of fibroblasts. J Cell Biol. 1990 Dec;111(6 Pt 1):2513–2526. doi: 10.1083/jcb.111.6.2513. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldstein D., Djeu J., Latter G., Burbeck S., Leavitt J. Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes. Cancer Res. 1985 Nov;45(11 Pt 2):5643–5647. [PubMed] [Google Scholar]
- Guck J., Ananthakrishnan R., Moon T. J., Cunningham C. C., Käs J. Optical deformability of soft biological dielectrics. Phys Rev Lett. 2000 Jun 5;84(23):5451–5454. doi: 10.1103/PhysRevLett.84.5451. [DOI] [PubMed] [Google Scholar]
- Heidemann S. R., Kaech S., Buxbaum R. E., Matus A. Direct observations of the mechanical behaviors of the cytoskeleton in living fibroblasts. J Cell Biol. 1999 Apr 5;145(1):109–122. doi: 10.1083/jcb.145.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrmann H., Aebi U. Structure, assembly, and dynamics of intermediate filaments. Subcell Biochem. 1998;31:319–362. [PubMed] [Google Scholar]
- Hochmuth R. M. Measuring the mechanical properties of individual human blood cells. J Biomech Eng. 1993 Nov;115(4B):515–519. doi: 10.1115/1.2895533. [DOI] [PubMed] [Google Scholar]
- Hénon S., Lenormand G., Richert A., Gallet F. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J. 1999 Feb;76(2):1145–1151. doi: 10.1016/S0006-3495(99)77279-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janmey P. A., Euteneuer U., Traub P., Schliwa M. Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol. 1991 Apr;113(1):155–160. doi: 10.1083/jcb.113.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janmey P. A. Mechanical properties of cytoskeletal polymers. Curr Opin Cell Biol. 1991 Feb;3(1):4–11. doi: 10.1016/0955-0674(91)90159-v. [DOI] [PubMed] [Google Scholar]
- Janmey P. A., Peetermans J., Zaner K. S., Stossel T. P., Tanaka T. Structure and mobility of actin filaments as measured by quasielastic light scattering, viscometry, and electron microscopy. J Biol Chem. 1986 Jun 25;261(18):8357–8362. [PubMed] [Google Scholar]
- Janmey P. A., Shah J. V., Janssen K. P., Schliwa M. Viscoelasticity of intermediate filament networks. Subcell Biochem. 1998;31:381–397. [PubMed] [Google Scholar]
- Koffer A., Daridan M., Clarke G. D. Regulation of the microfilament system in normal and polyoma virus transformed cultured (BHK) cells. Tissue Cell. 1985;17(2):147–159. doi: 10.1016/0040-8166(85)90084-9. [DOI] [PubMed] [Google Scholar]
- Kuo S. C., Sheetz M. P. Force of single kinesin molecules measured with optical tweezers. Science. 1993 Apr 9;260(5105):232–234. doi: 10.1126/science.8469975. [DOI] [PubMed] [Google Scholar]
- Kuo S. C., Sheetz M. P. Optical tweezers in cell biology. Trends Cell Biol. 1992 Apr;2(4):116–118. doi: 10.1016/0962-8924(92)90016-g. [DOI] [PubMed] [Google Scholar]
- Käs J., Strey H., Tang J. X., Finger D., Ezzell R., Sackmann E., Janmey P. A. F-actin, a model polymer for semiflexible chains in dilute, semidilute, and liquid crystalline solutions. Biophys J. 1996 Feb;70(2):609–625. doi: 10.1016/S0006-3495(96)79630-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leavitt J., Latter G., Lutomski L., Goldstein D., Burbeck S. Tropomyosin isoform switching in tumorigenic human fibroblasts. Mol Cell Biol. 1986 Jul;6(7):2721–2726. doi: 10.1128/mcb.6.7.2721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu Y., Sonek G. J., Berns M. W., Tromberg B. J. Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry. Biophys J. 1996 Oct;71(4):2158–2167. doi: 10.1016/S0006-3495(96)79417-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacKintosh FC, Käs J, Janmey PA. Elasticity of semiflexible biopolymer networks. Phys Rev Lett. 1995 Dec 11;75(24):4425–4428. doi: 10.1103/PhysRevLett.75.4425. [DOI] [PubMed] [Google Scholar]
- Mahaffy R. E., Shih C. K., MacKintosh F. C., Käs J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys Rev Lett. 2000 Jul 24;85(4):880–883. doi: 10.1103/PhysRevLett.85.880. [DOI] [PubMed] [Google Scholar]
- Mitchison T. J. Compare and contrast actin filaments and microtubules. Mol Biol Cell. 1992 Dec;3(12):1309–1315. doi: 10.1091/mbc.3.12.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitchison T., Evans L., Schulze E., Kirschner M. Sites of microtubule assembly and disassembly in the mitotic spindle. Cell. 1986 May 23;45(4):515–527. doi: 10.1016/0092-8674(86)90283-7. [DOI] [PubMed] [Google Scholar]
- Mohandas N., Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu Rev Biophys Biomol Struct. 1994;23:787–818. doi: 10.1146/annurev.bb.23.060194.004035. [DOI] [PubMed] [Google Scholar]
- Neuman K. C., Chadd E. H., Liou G. F., Bergman K., Block S. M. Characterization of photodamage to Escherichia coli in optical traps. Biophys J. 1999 Nov;77(5):2856–2863. doi: 10.1016/S0006-3495(99)77117-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pasternak C., Elson E. L. Lymphocyte mechanical response triggered by cross-linking surface receptors. J Cell Biol. 1985 Mar;100(3):860–872. doi: 10.1083/jcb.100.3.860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petersen N. O., McConnaughey W. B., Elson E. L. Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5327–5331. doi: 10.1073/pnas.79.17.5327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pollard T. D. Assembly and dynamics of the actin filament system in nonmuscle cells. J Cell Biochem. 1986;31(2):87–95. doi: 10.1002/jcb.240310202. [DOI] [PubMed] [Google Scholar]
- Pollard T. D. Molecular architecture of the cytoplasmic matrix. Kroc Found Ser. 1984;16:75–86. [PubMed] [Google Scholar]
- Radmacher M., Fritz M., Kacher C. M., Cleveland J. P., Hansma P. K. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J. 1996 Jan;70(1):556–567. doi: 10.1016/S0006-3495(96)79602-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rotsch C., Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys J. 2000 Jan;78(1):520–535. doi: 10.1016/S0006-3495(00)76614-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sato M., Levesque M. J., Nerem R. M. An application of the micropipette technique to the measurement of the mechanical properties of cultured bovine aortic endothelial cells. J Biomech Eng. 1987 Feb;109(1):27–34. doi: 10.1115/1.3138638. [DOI] [PubMed] [Google Scholar]
- Schönle A., Hell S. W. Heating by absorption in the focus of an objective lens. Opt Lett. 1998 Mar 1;23(5):325–327. doi: 10.1364/ol.23.000325. [DOI] [PubMed] [Google Scholar]
- Shepherd G. M., Corey D. P., Block S. M. Actin cores of hair-cell stereocilia support myosin motility. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8627–8631. doi: 10.1073/pnas.87.21.8627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sidransky D. Advances in cancer detection. Sci Am. 1996 Sep;275(3):104–109. doi: 10.1038/scientificamerican0996-104. [DOI] [PubMed] [Google Scholar]
- Sleep J., Wilson D., Simmons R., Gratzer W. Elasticity of the red cell membrane and its relation to hemolytic disorders: an optical tweezers study. Biophys J. 1999 Dec;77(6):3085–3095. doi: 10.1016/S0006-3495(99)77139-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stossel T. P. Contribution of actin to the structure of the cytoplasmic matrix. J Cell Biol. 1984 Jul;99(1 Pt 2):15s–21s. doi: 10.1083/jcb.99.1.15s. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stossel T. P., Hartwig J. H., Janmey P. A., Kwiatkowski D. J. Cell crawling two decades after Abercrombie. Biochem Soc Symp. 1999;65:267–280. [PubMed] [Google Scholar]
- Strey H., Peterson M., Sackmann E. Measurement of erythrocyte membrane elasticity by flicker eigenmode decomposition. Biophys J. 1995 Aug;69(2):478–488. doi: 10.1016/S0006-3495(95)79921-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Svoboda K., Block S. M. Biological applications of optical forces. Annu Rev Biophys Biomol Struct. 1994;23:247–285. doi: 10.1146/annurev.bb.23.060194.001335. [DOI] [PubMed] [Google Scholar]
- Svoboda K., Schmidt C. F., Schnapp B. J., Block S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature. 1993 Oct 21;365(6448):721–727. doi: 10.1038/365721a0. [DOI] [PubMed] [Google Scholar]
- Tadir Y., Wright W. H., Vafa O., Ord T., Asch R. H., Berns M. W. Force generated by human sperm correlated to velocity and determined using a laser generated optical trap. Fertil Steril. 1990 May;53(5):944–947. doi: 10.1016/s0015-0282(16)53539-0. [DOI] [PubMed] [Google Scholar]
- Takahashi K., Heine U. I., Junker J. L., Colburn N. H., Rice J. M. Role of cytoskeleton changes and expression of the H-ras oncogene during promotion of neoplastic transformation in mouse epidermal JB6 cells. Cancer Res. 1986 Nov;46(11):5923–5932. [PubMed] [Google Scholar]
- Taniguchi S., Kawano T., Kakunaga T., Baba T. Differences in expression of a variant actin between low and high metastatic B16 melanoma. J Biol Chem. 1986 May 5;261(13):6100–6106. [PubMed] [Google Scholar]
- Thoumine O., Ott A. Time scale dependent viscoelastic and contractile regimes in fibroblasts probed by microplate manipulation. J Cell Sci. 1997 Sep;110(Pt 17):2109–2116. doi: 10.1242/jcs.110.17.2109. [DOI] [PubMed] [Google Scholar]
- Wang E., Goldberg A. R. Changes in microfilament organization and surface topogrophy upon transformation of chick embryo fibroblasts with Rous sarcoma virus. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4065–4069. doi: 10.1073/pnas.73.11.4065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang N., Butler J. P., Ingber D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 1993 May 21;260(5111):1124–1127. doi: 10.1126/science.7684161. [DOI] [PubMed] [Google Scholar]
- Wang N., Stamenović D. Contribution of intermediate filaments to cell stiffness, stiffening, and growth. Am J Physiol Cell Physiol. 2000 Jul;279(1):C188–C194. doi: 10.1152/ajpcell.2000.279.1.C188. [DOI] [PubMed] [Google Scholar]