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Single-molecule fluorescence to study molecular motors

Published online by Cambridge University Press:  31 July 2007

Hyokeun Park ,
Erdal Toprak  and
Paul R. Selvin
Hyokeun Park
Affiliation:
Department of Chemistry, University of Illinois, Urbana, IL, USA
Erdal Toprak
Affiliation:
Center for Biophysics and Computational Biology, University of Illinois, Urbana, IL, USA
Paul R. Selvin*
Affiliation:
Center for Biophysics and Computational Biology, University of Illinois, Urbana, IL, USA Department of Physics, University of Illinois, Urbana, IL, USA
*
*Author for correspondence: Dr P. R. Selvin, Physics Department, 1110 West Green Street, Loomis Laboratory, University of Illinois, Urbana, IL 61801, USA. Tel.: 217-244-3371; Fax: 217-244-7559; E-mail: [email protected]
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Abstract

Molecular motors, which use energy from ATP hydrolysis to take nanometer-scale steps with run-lengths on the order of micrometers, have important roles in areas such as transport and mitosis in living organisms. New techniques have recently been developed to measure these small movements at the single-molecule level. In particular, fluorescence imaging has contributed to the accurate measurement of this tiny movement. We introduce three single-molecule fluorescence imaging techniques which can find the position of a fluorophore with accuracy in the range of a few nanometers. These techniques are named after Hollywood animation characters: Fluorescence Imaging with One Nanometer Accuracy (FIONA), Single-molecule High-REsolution Colocalization (SHREC), and Defocused Orientation and Position Imaging (DOPI). We explain new understanding of molecular motors obtained from measurements using these techniques.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 40 , Issue 1 , February 2007 , pp. 87 - 111
Copyright
Copyright © Cambridge University Press 2007

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References

7. References

Adams, S. R., Campbell, R. E., Gross, L. A., Martin, B. R., Walkup, G. K., Yao, Y., Llopis, J. & Tsien, R. Y. (2002). New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. Journal of the American Chemical Society 124, 6063–6076.CrossRefGoogle ScholarPubMed
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. & Walter, P. (2002). Molecular Biology of the Cell, 4th edn. New York: Garland Science.Google Scholar
Asbury, C. L., Fehr, A. N. & Block, S. M. (2003). Kinesin moves by an asymmetric hand-over hand mechanism. Science 302, 2130–2134.CrossRefGoogle ScholarPubMed
Avraham, K. B., Hasson, T., Sobe, T., Balsara, B., Testa, J. R., Skvorak, A. B., Morton, C. C., Copeland, N. G. & Jenkins, N. A. (1997). Characterization of unconventional MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice. Human Molecular Genetics 6, 1225–1231.CrossRefGoogle ScholarPubMed
Avraham, K. B., Hasson, T., Steel, K. P., Kingsley, D. M., Russell, L. B., Mooseker, M. S., Copeland, N. G. & Jenkins, N. A. (1995). The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nature Genetics 11, 369–375.CrossRefGoogle ScholarPubMed
Bahloul, A., Chevreux, G., Wells, A. L., Martin, D., Nolt, J., Yang, Z., Chen, L.-Q., Potier, N., Van Dorsselaer, A., Rosenfeld, S., Houdusse, A. & Sweeney, H. L. (2004). The unique insert in myosin VI is a structural calcium-calmodulin binding site. Proceedings of the National Academy of Sciences USA 101, 4787–4792.CrossRefGoogle ScholarPubMed
Balci, H., Ha, T., Sweeney, H. L. & Selvin, P. R. (2005). Interhead distance measurements in myosin VI via SHRImP support a simplified hand-over-hand model. Biophysical Journal 89, 413–417.CrossRefGoogle ScholarPubMed
Bartko, A. P. & Dickson, R. M. (1999). Three-dimensional orientations of polymer-bound single molecules. Journal of Physical Chemistry B 103, 3053–3056.CrossRefGoogle Scholar
Berg, J. S., Powell, B. C. & Cheney, R. E. (2001). A millennial myosin census. Molecular Biology of the Cell 12, 780–794.CrossRefGoogle ScholarPubMed
Bobroff, N. (1986). Position measurement with a resolution and noise-limited instrument. Review of Scientific Instruments 57, 1152–1157.CrossRefGoogle Scholar
Böhmer, M. & Enderlein, J. (2003). Orientation imaging of single molecules by wide-field epi-fluorescence microscopy. Journal of the Optical Society of America B 20, 554–559.CrossRefGoogle Scholar
Burgess, S., Walker, M., Wang, F., Sellers, J. R., White, H. D., Knight, P. J. & Trinick, J. (2002). The prepower stroke conformation of myosin V. Journal of Cell Biology 159, 983–991.CrossRefGoogle ScholarPubMed
Buss, F., Spudich, G. & Kendrick-Jones, J. (2004). Myosin VI: cellular functions and motor properties. Annual Review of Cell Developmental Biology 20, 649–676.CrossRefGoogle ScholarPubMed
Cheezum, M. K., Walker, W. F. & Guilford, W. H. (2001). Quantitative comparison of algorithms for tracking single fluorescent particles. Biophysical Journal 81, 2378–2388.CrossRefGoogle ScholarPubMed
Chevreux, G., Potier, N., Van Dorsselaer, A., Bahloul, A., Houdusse, A., Wells, A. & Sweeney, H. L. (2005). Electrospray ionization mass spectrometry studies of noncovalent myosin VI complexes reveal a new specific calmodulin binding site. Journal of the American Society for Mass Spectrometry 16, 1367–1376.CrossRefGoogle ScholarPubMed
Churchman, L. S., Okten, Z., Rock, R. S., Dawson, J. F. & Spudich, J. A. (2005). Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proceedings of the National Academy of Sciences USA 102, 1419–1423.CrossRefGoogle ScholarPubMed
Dahan, M., Levi, S., Luccardini, C., Rostaing, P., Riveau, B. & Triller, A. (2003). Diffusion dynamics of glycine receptors revealed by single quantum dot tracking. Science 302, 442–445.CrossRefGoogle ScholarPubMed
Enderlein, J., Toprak, E. & Selvin, P. R. (2006). Polarization effect on position accuracy of fluorophore localization. Optics Express 14, 8111–8120.CrossRefGoogle ScholarPubMed
Forkey, J. N., Quinlan, M. E., Shaw, M. A., Corrie, J. E. & Goldman, Y. E. (2003). Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization. Nature 422, 399–404.CrossRefGoogle ScholarPubMed
Geisbrecht, E. R. & Montell, D. J. (2002). Myosin VI is required for E-cadherin-mediated border cell migration. Nature Cell Biology 4, 616–620.CrossRefGoogle ScholarPubMed
Gibbons, I. R., Gibbons, B. H., Mocz, G. & Asai, D. J. (1991). Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain. Nature 352, 640–643.CrossRefGoogle ScholarPubMed
Gibbons, I. R., Lee-Eiford, A., Mocz, G., Phillipson, C. A., Tang, W. T. & Gibbons, B. H. (1987). Photosensitized cleavage of dynein heavy chains. Cleavage at the ‘V1 site’ by irradiation at 365 nm in the presence of ATP and vanadate. Journal of Biological Chemistry 262, 2780–2786.CrossRefGoogle ScholarPubMed
Gordon, M. P., Ha, T. & Selvin, P. R. (2004). Single-molecule high-resolution imaging with photobleaching. Proceedings of the National Academy of Sciences USA 101, 6462–6465.CrossRefGoogle ScholarPubMed
Ha, T., Enderle, T., Chemla, S., Selvin, R. & Weiss, S. (1996). Single molecule dynamics studied by polarization modulation. Physical Review Letters 77, 3979–3982.CrossRefGoogle ScholarPubMed
Hasson, T. (2003). Myosin VI: two distinct roles in endocytosis. Journal of Cell Science 116, 3453–3461.CrossRefGoogle ScholarPubMed
Hirokawa, N. & Takemura, R. (2004). Molecular motors in neuronal development, intracellular transport and diseases. Current Opinion in Neurobiology 14, 564–573.CrossRefGoogle ScholarPubMed
Hu, J., Li, L., Yang, W., Manna, L., Wang, L. & Alivisatos, A. P. (2001). Linearly polarized emission from colloidal semiconductor quantum rods. Science 292, 2060–2063.CrossRefGoogle ScholarPubMed
Hua, W., Young, E. C., Fleming, M. L. & Gelles, J. (1997). Coupling of kinesin step to ATP hydrolysis. Nature 388, 390–393.CrossRefGoogle ScholarPubMed
Hua, W., Chung, J. & Gelles, J. (2002). Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements. Science 295, 844–848.CrossRefGoogle ScholarPubMed
Hurd, D. D. & Saxton, W. M. (1996). Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144, 1075–1085.CrossRefGoogle ScholarPubMed
Jaiswal, J. D. & Simon, S. M. (2007). Imaging single events at the cell membrane. Nature Chemical Biology 3, 92–98.CrossRefGoogle ScholarPubMed
Kaseda, K., Higuchi, H. & Hirose, K. (2003). Alternate fast and slow stepping of a heterodimeric kinesin molecule. Nature Cell Biology 5, 1079–1082.CrossRefGoogle ScholarPubMed
Kellerman, K. A. & Miller, K. G. (1992). An unconventional myosin heavy chain gene from Drosophila melanogaster. Journal of Cell Biology 119, 823–834.CrossRefGoogle ScholarPubMed
King, S. J., Bonilla, M., Rodgers, M. E. & Schroer, T. A. (2002). Subunit organization in cytoplasmic dynein subcomplexes. Protein Science 11, 1239–1250.CrossRefGoogle ScholarPubMed
Kinosita, K. Jr., Itoh, H., Ishiwata, S., Hirano, K., Nishizaka, T. & Hayakawa, T. (1991). Dual-view microscopy with a single camera: real-time imaging of molecular orientations and calcium. Journal of Cell Biology 115, 67–73.CrossRefGoogle ScholarPubMed
Kinosita, K. Jr., Yasuda, R., Noji, H., Ishiwata, S. & Yoshida, M. (1998). F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 93, 21–24.CrossRefGoogle Scholar
Kon, T., Mogami, T., Ohkura, R., Nishiura, M. & Sutoh, K. (2005). ATP hydrolysis cycle-dependent tail motions in cytoplasmic dynein. Nature Structural & Molecular Biology 12, 513–519.CrossRefGoogle ScholarPubMed
Koonce, M. P. (1997). Identification of a microtubule-binding domain in a cytoplasmic dynein heavy chain. Journal of Biological Chemistry 272, 19714–19718.CrossRefGoogle Scholar
Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V. I. & Selvin, P. R. (2005). Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308, 1469–1472.CrossRefGoogle ScholarPubMed
Lister, I., Schmitz, S., Walker, M., Trinick, J., Buss, F., Veigel, C. & Kendrick-Jones, J. (2004). A monomeric myosin VI with a large working stroke. EMBO Journal 23, 1729–1738.Google Scholar
Mallik, R. & Gross, S. P. (2004). Molecular motors: strategies to get along. Current Biology 14, R971–R982.CrossRefGoogle ScholarPubMed
Mehta, A. D., Rock, R. S., Rief, M., Spudich, J. A., Mooseker, M. S. & Cheney, R. E. (1999). Myosin-V is a processive actin-based motor. Nature 400, 590–593.CrossRefGoogle ScholarPubMed
Melchionda, S., Ahituv, N., Bisceglia, L., Sobe, T., Glaser, F., Rabionet, R., Arbones, M. L., Notarangelo, A., Iorio, E. D., Carella, M., Zelante, L., Estivill, X., Avraham, K. B. & Gasparini, P. (2001). MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss. American Journal of Human Genetics 69, 635–640.CrossRefGoogle ScholarPubMed
Ménétrey, J., Bahloul, A., Wells, A. L., Yengo, C. M., Morris, C. A., Sweeney, H. L. & Houdusse, A. (2005). The structure of the myosin VI motor reveals the mechanism of directionality reversal. Nature 435, 779–785.CrossRefGoogle ScholarPubMed
Milescu, L. S., Yildiz, A., Selvin, P. R. & Sachs, F. (2006). Extracting dwell time sequences from processive molecular motor data. Biophysical Journal 91, 3135–3150.CrossRefGoogle ScholarPubMed
Miller, K. E. & Sheetz, M. P. (2000). Characterization of myosin V binding to brain vesicles. Journal of Biological Chemistry 275, 2598–2606.CrossRefGoogle ScholarPubMed
Millo, H., Leaper, K., Lazou, V. & Bownes, M. (2004). Myosin VI plays a role in cell-cell adhesion during epithelial morphogenesis. Mechanisms of Development 121, 1335–1351.CrossRefGoogle Scholar
Moerner, W. E. & Fromm, D. P. (2003). Methods of single-molecule fluorescence spectroscopy and microscopy. Review of Scientific Instruments 74, 3597–3619.CrossRefGoogle Scholar
Nan, X., Sims, P. A., Chen, P. & Xie, X. S. (2005). Observation of individual microtubule in living cells with endocytosed quantum dots. Journal of Physical Chemistry 109, 24220–24224.Google Scholar
Ogawa, K. (1991). Four ATP-binding sites in the midregion of the beta heavy chain of dynein. Nature 352, 643–645.CrossRefGoogle ScholarPubMed
Okten, Z., Churchman, L. S., Rock, R. S. & Spudich, J. A. (2004). Myosin VI walks hand-over-hand along actin. Nature Structural & Molecular Biology 11, 884–887.CrossRefGoogle ScholarPubMed
Park, H., Hanson, G., Duff, S. & Selvin, P. R. (2004). Nanometre localization of single ReAsH molecules. Journal of Microscopy 216, 199–205.CrossRefGoogle ScholarPubMed
Park, H., Li, A., Chen, L.-Q., Houdusse, A., Selvin, P. R. & Sweeney, H. L. (2007). The unique inset at the end of the myosin VI motor is the sole determinant of directionality. Proceedings of the National Academy of Sciences USA 104, 778–783.CrossRefGoogle Scholar
Park, H., Ramamurthy, B., Safer, D., Travaglia, M., Chen, L.-Q., Franzini-Armstrong, C., Selvin, P. R. & Sweeney, H. L. (2006). Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Molecular Cell 21, 331–336.CrossRefGoogle ScholarPubMed
Paschal, B. M. & Vallee, R. B. (1987). Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181–183.CrossRefGoogle ScholarPubMed
Patra, D., Gregor, I. & Enderlein, J. (2004). Image analysis of defocused single-molecule images for three-dimensional molecule orientation studies. Journal of Physical Chemistry A 108, 6836–6841.CrossRefGoogle Scholar
Peterman, E. J. G., Sosa, H. & Moerner, W. E. (2004). Single-molecule fluorescence spectroscopy and microscopy of biomolecular motors. Annual Review of Physical Chemistry 55, 79–96.CrossRefGoogle ScholarPubMed
Qu, X., Wu, D., Mets, L. & Scherer, N. F. (2004). Nanometer-localized multiple single-molecule fluorescence microscopy. Proceedings of the National Academy of Sciences USA 101, 11298–11303.CrossRefGoogle ScholarPubMed
Rasnik, I., McKinney, S. A. & Ha, T. (2006). Nonblinking and long-lasting single molecule fluorescence imaging. Nature Methods 3, 891–893.Google Scholar
Reck-Peterson, S. L., Provance, D. W., Mooseker, M. S. & Mercer, J. A. (2000). Review: class V myosins. Biochimica et Biophysica Acta 1496, 36–51.CrossRefGoogle ScholarPubMed
Reck-Peterson, S. L., Yildiz, A., Carter, A. P., Gennerich, A., Zhang, N. & Vale, R. D. (2006). Single-molecule analysis of dynein processivity and stepping behavior. Cell 126, 335–348.CrossRefGoogle ScholarPubMed
Reid, E., Kloos, M., Ashley-Koch, A., Hughes, L., Bevan, S., Svenson, I. K., Graham, F. L., Gaskell, P. C., Dearlove, A., Pericak-Vance, M. A., Rubinsztein, D. C. & Marchuk, D. A. (2002). A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). American Journal of Human Genetics. 71, 1189–1194.CrossRefGoogle ScholarPubMed
Rock, R. S., Ramamurthy, B., Dunn, A. R., Beccafico, S., Morris, C., Spink, B., Rami, B., Franzini-Armstrong, C., Spudich, J. A. & Sweeney, H. L. (2005). A flexible domain is essential for the large step size and processivity of myosin VI. Molecular Cell 17, 603–609.Google Scholar
Rock, R. S., Rice, S. E., Wells, A. L., Purcell, T. J., Spudich, J. A. & Sweeney, H. L. (2001). Myosin VI is a processive motor with a large step size. Proceedings of the National Academy of Sciences USA 98, 13655–13659.CrossRefGoogle ScholarPubMed
Sakamoto, T., Amitani, I., Yokota, E. & Ando, T. (2000). Direct observation of processive movement by individual myosin V molecules. Biochemical and Biophysical Research Communication 272, 586–590.CrossRefGoogle ScholarPubMed
Saunders, W. S., Koshland, D., Eshel, D., Gibbons, I. R. & Hoyt, M. A. (1995). Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. Journal of Cell Biology 128, 617–624.CrossRefGoogle ScholarPubMed
Schliwa, M. & Woehlke, G. (2003). Molecular motors. Nature 422, 759–765.CrossRefGoogle ScholarPubMed
Schnitzer, M. J. & Block, S. M. (1997). Kinesin hydrolyses one ATP per 8-nm step. Nature 388, 386–390.CrossRefGoogle ScholarPubMed
Schoch, C. L., Aist, J. R., Yoder, O. C. & Turgeon, B. G. (2003). A complete inventory of fungal kinesins in representative filamentous ascomycetes. Fungal Genetics and Biology 39, 1–15.CrossRefGoogle ScholarPubMed
Selvin, P. R. (2003). Lighting up single ion channels. Biophysical Journal 84, 1–2.CrossRefGoogle ScholarPubMed
Sharp, D. J., Rogers, G. C. & Scholey, J. M. (2000). Microtubule motors in mitosis. Nature 407, 41–47.CrossRefGoogle ScholarPubMed
Snyder, G. E., Sakamoto, T., Hammer, J. A. 3rd, Sellers, J. R. & Selvin, P. R. (2004). Nanometer localization of single green fluorescent proteins: evidence that myosin V walks hand-over-hand via telemark configuration. Biophysical Journal 87, 1776–1783.CrossRefGoogle ScholarPubMed
Spudich, J. A. (1994). How molecular motors work. Nature 372, 515–518.CrossRefGoogle ScholarPubMed
Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. (1993). Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721–727.CrossRefGoogle ScholarPubMed
Syed, S., Snyder, G. E., Franzini-Armstrong, C., Selvin, P. R. & Goldman, Y. E. (2006). Simultaneous detection of the position and structural dynamics of myosin V. EMBO Journal 25, 1795–1803.CrossRefGoogle ScholarPubMed
Thompson, R. E., Larson, D. R. & Webb, W. W. (2002). Precise nanometer localization analysis for individual fluorescent probes. Biophysical Journal 82, 2775–2783.CrossRefGoogle ScholarPubMed
Toprak, E., Enderlein, J., Syed, S., McKinney, S. A., Petschek, R. G., Ha, T., Goldman, Y. E. & Selvin, P. R. (2006). Defocused orientation and position imaging (DOPI) of myosin V. Proceedings of the National Academy of Sciences USA 103, 6495–6499.CrossRefGoogle ScholarPubMed
Vale, R. D. (2003a). Myosin V motor proteins: marching stepwise towards a mechanism. Journal of Cell Biology 163, 445–450.CrossRefGoogle ScholarPubMed
Vale, R. D. (2003b). The molecular motor toolbox for intracellular transport. Cell 112, 467–480.Google Scholar
Vaisberg, E. A., Koonce, M. P. & McIntosh, J. R. (1993). Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. Journal of Cell Biology 123, 849–858.CrossRefGoogle Scholar
Vallee, R. B., Williams, J. C., Varma, D. & Barnhart, L. E. (2004). Dynein: an ancient motor protein involved in multiple modes of transport. Journal of Neurobiology 58, 189–200.CrossRefGoogle ScholarPubMed
Warshaw, D. W., Kennedy, G. G., Work, S. S., Krementsova, E. B., Beck, S. & Trybus, K. M. (2005). Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity. Biophysical Journal 88, L30–L32.CrossRefGoogle ScholarPubMed
Wells, A. L., Lin, A. W., Chen, L.-Q., Safer, D., Cain, S. M., Hasson, T., Carragher, B. O., Milligan, R. A. & Sweeney, H. L. (1999). Myosin VI is an actin-based motor that moves backwards. Nature 401, 505–508.Google Scholar
Yildiz, A., Forkey, J. N., McKinney, S. A., Ha, T., Goldman, Y. E. & Selvin, P. R. (2003). Myosin V walks hand-over-hand: Single fluorophore imaging with 1·5 nm localization. Science 300, 2061–2065.CrossRefGoogle ScholarPubMed
Yildiz, A., Park, H., Safer, D., Yang, Z., Chen, L.-Q., Selvin, P. R. & Sweeney, H. L. (2004a). Myosin VI steps via a hand-over-hand mechanism with its lever arm undergoing fluctuations when attached to actin. Journal of Biological Chemistry 279, 37223–37226.CrossRefGoogle Scholar
Yildiz, A., Tomishige, M., Vale, R. D. & Selvin, P. R. (2004b). Kinesin walks hand-over-hand. Science 303, 676–678.Google Scholar