Tracking single Kinesin molecules in the cytoplasm of mammalian cells.

Understanding dynamic cellular processes requires precise knowledge of the distribution, transport, and interactions of individual molecules in living cells. Despite recent progress in in vivo imaging, it has not been possible to express and directly track single molecules in the cytoplasm of live cells. Here, we overcome these limitations by combining fluorescent protein-labeling with high resolution total internal reflection fluorescence microcopy, using the molecular motor Kinesin-1 as model system. First, we engineered a three-tandem monomeric Citrine tag for genetic labeling of individual molecules and expressed this motor in COS cells. Detailed analysis of the quantized photobleaching behavior of individual fluorescent spots demonstrates that we are indeed detecting single proteins in the cytoplasm of live cells. Tracking the movement of individual cytoplasmic molecules reveals that individual Kinesin-1 motors in vivo move with an average speed of 0.78 +/- 0.11 microm/s and display an average run length of 1.17 +/- 0.38 microm, which agrees well with in vitro measurements. Thus, Kinesin-1's speed and processivity are not upregulated or hindered by macromolecular crowding. Second, we demonstrate that standard deviation maps of the fluorescence intensity computed from single molecule image sequences can be used to reveal important physiological information about infrequent cellular events in the noisy fluorescence background of live cells. Finally, we show that tandem fluorescent protein tags enable single-molecule, in vitro analyses of extracted, mammalian-expressed proteins. Thus, by combining direct genetic labeling and single molecule imaging in vivo, our work establishes an important new biophysical method for observing single molecules expressed and localized in the mammalian cytoplasm.

[1]  Xiaolin Nan,et al.  Observation of individual microtubule motor steps in living cells with endocytosed quantum dots. , 2005, The journal of physical chemistry. B.

[2]  T. Yanagida,et al.  Movements of truncated kinesin fragments with a short or an artificial flexible neck. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  A Kusumi,et al.  Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. , 2001, Biophysical journal.

[4]  E. Meyhöfer,et al.  The E-hook of tubulin interacts with kinesin's head to increase processivity and speed. , 2005, Biophysical journal.

[5]  J. Gelles,et al.  Imaging of single-molecule translocation through nuclear pore complexes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Arne Seitz,et al.  Processive movement of single kinesins on crowded microtubules visualized using quantum dots , 2006, The EMBO journal.

[7]  Jonathon Howard,et al.  Processivity of the Motor Protein Kinesin Requires Two Heads , 1998, The Journal of cell biology.

[8]  Gerald Kada,et al.  Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy , 2000, The EMBO journal.

[9]  R. Tsien,et al.  Reducing the Environmental Sensitivity of Yellow Fluorescent Protein , 2001, The Journal of Biological Chemistry.

[10]  E. Meyhöfer,et al.  The force generated by a single kinesin molecule against an elastic load. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Ronald D. Vale,et al.  Single-Molecule Microscopy Reveals Plasma Membrane Microdomains Created by Protein-Protein Networks that Exclude or Trap Signaling Molecules in T Cells , 2005, Cell.

[12]  Paul R. Selvin,et al.  Kinesin and Dynein Move a Peroxisome in Vivo: A Tug-of-War or Coordinated Movement? , 2005, Science.

[13]  Vladimir Gelfand,et al.  Myosin cooperates with microtubule motors during organelle transport in melanophores , 1998, Current Biology.

[14]  S. Leibler,et al.  Porters versus rowers: a unified stochastic model of motor proteins , 1993, The Journal of cell biology.

[15]  Timothy J Mitchison,et al.  Single-Molecule Speckle Analysis of Actin Filament Turnover in Lamellipodia , 2002, Science.

[16]  Christoph F. Schmidt,et al.  Direct observation of kinesin stepping by optical trapping interferometry , 1993, Nature.

[17]  T. Yanagida,et al.  Single-molecule visualization in cell biology. , 2003, Nature reviews. Molecular cell biology.

[18]  A. Hudspeth,et al.  Movement of microtubules by single kinesin molecules , 1989, Nature.

[19]  G. Holzwarth,et al.  Fast vesicle transport in PC12 neurites: velocities and forces , 2004, European Biophysics Journal.

[20]  C. Kaether,et al.  Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. , 2000, Molecular biology of the cell.

[21]  S. Gambhir,et al.  Quantum Dots for Live Cells, in Vivo Imaging, and Diagnostics , 2005, Science.

[22]  T. Rapoport,et al.  Light Chain– dependent Regulation of Kinesin's Interaction with Microtubules , 1998, Journal of Cell Biology.

[23]  Enrico Gratton,et al.  Organelle transport along microtubules in Xenopus melanophores: evidence for cooperation between multiple motors. , 2006, Biophysical journal.

[24]  X. Xie,et al.  Living Cells as Test Tubes , 2006, Science.

[25]  G. A. Blab,et al.  Single-molecule imaging of l-type Ca(2+) channels in live cells. , 2001, Biophysical journal.

[26]  Yohanns Bellaiche,et al.  Tracking individual kinesin motors in living cells using single quantum-dot imaging. , 2006, Nano letters.

[27]  Michael Unser,et al.  Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics , 2005, IEEE Transactions on Image Processing.

[28]  Robert H Singer,et al.  Materials and Methods Som Text Figs. S1 to S8 References and Notes Dynamics of Single Mrnps in Nuclei of Living Cells , 2022 .

[29]  J. Howard,et al.  The force exerted by a single kinesin molecule against a viscous load. , 1994, Biophysical journal.

[30]  J. Swanson,et al.  Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells , 2007, The Journal of cell biology.

[31]  R. Tsien,et al.  On/off blinking and switching behaviour of single molecules of green fluorescent protein , 1997, Nature.