Abstract

The transport dynamics of endocytic vesicles in a living cell contains essential biomedical information. Although the movement mechanism of a vesicle by motor proteins has been revealed, understanding the precise movement of vesicles on the cytoskeleton in a living cell has been considered challenging, due to the complex 3D network of cytoskeletons. Here, we specify the shape of the 3D interaction between the vesicle and microtubule, based on the theoretically estimated location of the microtubule and the vesicle trajectory data acquired at high spatial and temporal precision. We detected that vesicles showed more frequent direction changes with either in very acute or in obtuse angles than right angles, on similar time scales in a microtubule network. Interestingly, when a vesicle interacted with a relatively longer (> 400 nm) microtubule filament, rotational movement along the axis of the microtubule was frequently observed. Our results are expected to give in-depth insight into understanding the actual 3D interactions between the intracellular molecule and complex cytoskeletal network.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (4)

Y. Gao, S. M. Anthony, Y. Yi, W. Li, Y. Yu, and Y. Yu, “Single-janus rod tracking reveals the “rock-and-roll”, of endosomes in living cells,” Langmuir 34(3), 1151–1158 (2018).
[Crossref]

J. P. Bergman, M. J. Bovyn, F. F. Doval, A. Sharma, M. V. Gudheti, S. P. Gross, J. F. Allard, and M. D. Vershinin, “Cargo navigation across 3d microtubule intersections,” Proc. Natl. Acad. Sci. 115(3), 537–542 (2018).
[Crossref]

S. Lee, H. Kim, and H. Higuchi, “Numerical method for vesicle movement analysis in a complex cytoskeleton network,” Opt. Express 26(13), 16236–16249 (2018).
[Crossref]

Y. Gao, S. M. Anthony, Y. Yu, Y. Yi, and Y. Yu, “Cargos rotate at microtubule intersections during intracellular trafficking,” Biophys. J. 114(12), 2900–2909 (2018).
[Crossref]

2017 (3)

O. Kučera, D. Havelka, and M. Cifra, “Vibrations of microtubules: Physics that has not met biology yet,” Wave Motion 72, 13–22 (2017).
[Crossref]

M. Liu, Q. Li, L. Liang, J. Li, K. Wang, J. Li, M. Lv, N. Chen, H. Song, J. Lee, J. Shi, L. Wang, R. Lal, and C. Fan, “Real-time visualization of clustering and intracellular transport of gold nanoparticles by correlative imaging,” Nat. Commun. 8:15646 (2017).
[Crossref] [PubMed]

I. Verdeny-Vilanova, F. Wehnekamp, N. Mohan, A. S. Alvarez, J. S. Borbely, J. J. Otterstrom, D. C. Lamb, and M. Lakadamyali, “3d motion of vesicles along microtubules helps them to circumvent obstacles in cells,” J. Cell Sci. 130(11), 1904–1916 (2017).
[Crossref]

2016 (2)

Y. Li, L. Shang, and G. U. Nienhaus, “Super-resolution imaging-based single particle tracking reveals dynamics of nanoparticle internalization by live cells,” Nanoscale 8(14), 7423–7429 (2016).
[Crossref]

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with imagej through super-resolution radial fluctuations,” Nat. Commun. 7(1), 12471 (2016).
[Crossref]

2015 (1)

O. Osunbayo, J. Butterfield, J. Bergman, L. Mershon, V. Rodionov, and M. Vershinin, “Cargo transport at microtubule crossings: evidence for prolonged tug-of-war between kinesin motors,” Biophys. J. 108(6), 1480–1483 (2015).
[Crossref]

2014 (3)

W. O. Hancock, “Bidirectional cargo transport: moving beyond tug of war,” Nat. Rev. Mol. Cell Biol. 15(9), 615–628 (2014).
[Crossref]

S. Can, M. A. Dewitt, and A. Yildiz, “Bidirectional helical motility of cytoplasmic dynein around microtubules,” eLife 3, 03205 (2014).
[Crossref]

M. E. Tanenbaum, L. A. Gilbert, L. S. Qi, J. S. Weissman, and R. D. Vale, “A protein-tagging system for signal amplification in gene expression and fluorescence imaging,” Cell 159(3), 635–646 (2014).
[Crossref]

2013 (4)

I. Kalinina, A. Nandi, P. Delivani, M. R. Chacón, A. H. Klemm, D. Ramunno-Johnson, A. Krull, B. Lindner, N. Pavin, and I. M. Tolić-Nørrelykke, “Pivoting of microtubules around the spindle pole accelerates kinetochore capture,” Nat. Cell Biol. 15(1), 82–87 (2013).
[Crossref]

A. Dupont, M. Gorelashvili, V. Schüller, F. Wehnekamp, D. Arcizet, Y. Katayama, D. Lamb, and D. Heinrich, “Three-dimensional single-particle tracking in live cells: news from the third dimension,” New J. Phys. 15(7), 075008 (2013).
[Crossref]

A. L. Zajac, Y. E. Goldman, E. L. Holzbaur, and E. M. Ostap, “Local cytoskeletal and organelle interactions impact molecular-motor-driven early endosomal trafficking,” Curr. Biol. 23(13), 1173–1180 (2013).
[Crossref]

Š. Bálint, I. V. Vilanova, Á. S. Álvarez, and M. Lakadamyali, “Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections,” Proc. Natl. Acad. Sci. 110(9), 3375–3380 (2013).
[Crossref]

2012 (1)

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “Nih image to imagej: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref]

2011 (3)

R. P. Erickson, Z. Jia, S. P. Gross, and C. Y. Clare, “How molecular motors are arranged on a cargo is important for vesicular transport,” PLoS Comput. Biol. 7(5), e1002032 (2011).
[Crossref]

J. Wu, K. C. Lee, R. B. Dickinson, and T. P. Lele, “How dynein and microtubules rotate the nucleus,” J. Cell. Physiol. 226(10), 2666–2674 (2011).
[Crossref]

J. H. Seo, K. Cho, S. Y. Lee, and S.-W. Joo, “Concentration-dependent fluorescence live-cell imaging and tracking of intracellular nanoparticles,” Nanotechnology 22(23), 235101 (2011).
[Crossref]

2010 (2)

Y. Xiao, S. P. Forry, X. Gao, R. D. Holbrook, W. G. Telford, and A. Tona, “Dynamics and mechanisms of quantum dot nanoparticle cellular uptake,” J. Nanobiotechnol. 8(1), 13 (2010).
[Crossref]

E. L. Holzbaur and Y. E. Goldman, “Coordination of molecular motors: from in vitro assays to intracellular dynamics,” Curr. Opin. Cell Biol. 22(1), 4–13 (2010).
[Crossref]

2009 (1)

L. W. Zhang and N. A. Monteiro-Riviere, “Mechanisms of quantum dot nanoparticle cellular uptake,” Toxicol. Sci. 110(1), 138–155 (2009).
[Crossref]

2008 (3)

D. Arcizet, B. Meier, E. Sackmann, J. O. Rädler, and D. Heinrich, “Temporal analysis of active and passive transport in living cells,” Phys. Rev. Lett. 101(24), 248103 (2008).
[Crossref]

M. J. Müller, S. Klumpp, and R. Lipowsky, “Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors,” Proc. Natl. Acad. Sci. 105(12), 4609–4614 (2008).
[Crossref]

R. Dixit, J. L. Ross, Y. E. Goldman, and E. L. Holzbaur, “Differential regulation of dynein and kinesin motor proteins by tau,” Science 319(5866), 1086–1089 (2008).
[Crossref]

2007 (3)

T. M. Watanabe, T. Sato, K. Gonda, and H. Higuchi, “Three-dimensional nanometry of vesicle transport in living cells using dual-focus imaging optics,” Biochem. Biophys. Res. Commun. 359(1), 1–7 (2007).
[Crossref]

T. Savin and P. S. Doyle, “Statistical and sampling issues when using multiple particle tracking,” Phys. Rev. E 76(2), 021501 (2007).
[Crossref]

T. M. Watanabe and H. Higuchi, “Stepwise movements in vesicle transport of her2 by motor proteins in living cells,” Biophys. J. 92(11), 4109–4120 (2007).
[Crossref]

2003 (1)

S. D. Conner and S. L. Schmid, “Regulated portals of entry into the cell,” Nature 422(6927), 37–44 (2003).
[Crossref]

2002 (2)

R. D. Minshall, C. Tiruppathi, S. M. Vogel, and A. B. Malik, “Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function,” Histochem. Cell Biol. 117(2), 105–112 (2002).
[Crossref]

A. Sorkin and M. von Zastrow, “Signal transduction and endocytosis: close encounters of many kinds,” Nat. Rev. Mol. Cell Biol. 3(8), 600–614 (2002).
[Crossref]

2001 (4)

S. Matveev, X. Li, W. Everson, and E. J. Smart, “The role of caveolae and caveolin in vesicle-dependent and vesicle-independent trafficking,” Adv. Drug Delivery Rev. 49(3), 237–250 (2001).
[Crossref]

M. Nishiyama, E. Muto, Y. Inoue, T. Yanagida, and H. Higuchi, “Substeps within the 8-nm step of the atpase cycle of single kinesin molecules,” Nat. Cell Biol. 3(4), 425–428 (2001).
[Crossref]

H. Hess and V. Vogel, “Molecular shuttles based on motor proteins: active transport in synthetic environments,” Rev. Mol. Biotechnol. 82(1), 67–85 (2001).
[Crossref]

R. J. Ellis, “Macromolecular crowding: an important but neglected aspect of the intracellular environment,” Curr. Opin. Struct. Biol. 11(1), 114–119 (2001).
[Crossref]

2000 (1)

S. J. King and T. A. Schroer, “Dynactin increases the processivity of the cytoplasmic dynein motor,” Nat. Cell Biol. 2(1), 20–24 (2000).
[Crossref]

1999 (2)

J. Kurebayashi, T. Otsuki, C. Tang, M. Kurosumi, S. Yamamoto, K. Tanaka, M. Mochizuki, H. Nakamura, and H. Soono, “Isolation and characterization of a new human breast cancer cell line, kpl-4, expressing the erb b family receptors and interleukin-6,” Br. J. Cancer 79(5-6), 707–717 (1999).
[Crossref]

J.-D. Huang, S. T. Brady, B. W. Richards, D. Stenoien, J. H. Resau, N. G. Copeland, and N. A. Jenkins, “Direct interaction of microtubule-and actin-based transport motors,” Nature 397(6716), 267–270 (1999).
[Crossref]

1998 (1)

N. Hirokawa, “Kinesin and dynein superfamily proteins and the mechanism of organelle transport,” Science 279(5350), 519–526 (1998).
[Crossref]

Allard, J. F.

J. P. Bergman, M. J. Bovyn, F. F. Doval, A. Sharma, M. V. Gudheti, S. P. Gross, J. F. Allard, and M. D. Vershinin, “Cargo navigation across 3d microtubule intersections,” Proc. Natl. Acad. Sci. 115(3), 537–542 (2018).
[Crossref]

Alvarez, A. S.

I. Verdeny-Vilanova, F. Wehnekamp, N. Mohan, A. S. Alvarez, J. S. Borbely, J. J. Otterstrom, D. C. Lamb, and M. Lakadamyali, “3d motion of vesicles along microtubules helps them to circumvent obstacles in cells,” J. Cell Sci. 130(11), 1904–1916 (2017).
[Crossref]

Álvarez, Á. S.

Š. Bálint, I. V. Vilanova, Á. S. Álvarez, and M. Lakadamyali, “Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections,” Proc. Natl. Acad. Sci. 110(9), 3375–3380 (2013).
[Crossref]

Anthony, S. M.

Y. Gao, S. M. Anthony, Y. Yi, W. Li, Y. Yu, and Y. Yu, “Single-janus rod tracking reveals the “rock-and-roll”, of endosomes in living cells,” Langmuir 34(3), 1151–1158 (2018).
[Crossref]

Y. Gao, S. M. Anthony, Y. Yu, Y. Yi, and Y. Yu, “Cargos rotate at microtubule intersections during intracellular trafficking,” Biophys. J. 114(12), 2900–2909 (2018).
[Crossref]

Arcizet, D.

A. Dupont, M. Gorelashvili, V. Schüller, F. Wehnekamp, D. Arcizet, Y. Katayama, D. Lamb, and D. Heinrich, “Three-dimensional single-particle tracking in live cells: news from the third dimension,” New J. Phys. 15(7), 075008 (2013).
[Crossref]

D. Arcizet, B. Meier, E. Sackmann, J. O. Rädler, and D. Heinrich, “Temporal analysis of active and passive transport in living cells,” Phys. Rev. Lett. 101(24), 248103 (2008).
[Crossref]

Ashdown, G.

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with imagej through super-resolution radial fluctuations,” Nat. Commun. 7(1), 12471 (2016).
[Crossref]

Bálint, Š.

Š. Bálint, I. V. Vilanova, Á. S. Álvarez, and M. Lakadamyali, “Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections,” Proc. Natl. Acad. Sci. 110(9), 3375–3380 (2013).
[Crossref]

Bergman, J.

O. Osunbayo, J. Butterfield, J. Bergman, L. Mershon, V. Rodionov, and M. Vershinin, “Cargo transport at microtubule crossings: evidence for prolonged tug-of-war between kinesin motors,” Biophys. J. 108(6), 1480–1483 (2015).
[Crossref]

Bergman, J. P.

J. P. Bergman, M. J. Bovyn, F. F. Doval, A. Sharma, M. V. Gudheti, S. P. Gross, J. F. Allard, and M. D. Vershinin, “Cargo navigation across 3d microtubule intersections,” Proc. Natl. Acad. Sci. 115(3), 537–542 (2018).
[Crossref]

Borbely, J. S.

I. Verdeny-Vilanova, F. Wehnekamp, N. Mohan, A. S. Alvarez, J. S. Borbely, J. J. Otterstrom, D. C. Lamb, and M. Lakadamyali, “3d motion of vesicles along microtubules helps them to circumvent obstacles in cells,” J. Cell Sci. 130(11), 1904–1916 (2017).
[Crossref]

Bovyn, M. J.

J. P. Bergman, M. J. Bovyn, F. F. Doval, A. Sharma, M. V. Gudheti, S. P. Gross, J. F. Allard, and M. D. Vershinin, “Cargo navigation across 3d microtubule intersections,” Proc. Natl. Acad. Sci. 115(3), 537–542 (2018).
[Crossref]

Brady, S. T.

J.-D. Huang, S. T. Brady, B. W. Richards, D. Stenoien, J. H. Resau, N. G. Copeland, and N. A. Jenkins, “Direct interaction of microtubule-and actin-based transport motors,” Nature 397(6716), 267–270 (1999).
[Crossref]

Butterfield, J.

O. Osunbayo, J. Butterfield, J. Bergman, L. Mershon, V. Rodionov, and M. Vershinin, “Cargo transport at microtubule crossings: evidence for prolonged tug-of-war between kinesin motors,” Biophys. J. 108(6), 1480–1483 (2015).
[Crossref]

Can, S.

S. Can, M. A. Dewitt, and A. Yildiz, “Bidirectional helical motility of cytoplasmic dynein around microtubules,” eLife 3, 03205 (2014).
[Crossref]

Chacón, M. R.

I. Kalinina, A. Nandi, P. Delivani, M. R. Chacón, A. H. Klemm, D. Ramunno-Johnson, A. Krull, B. Lindner, N. Pavin, and I. M. Tolić-Nørrelykke, “Pivoting of microtubules around the spindle pole accelerates kinetochore capture,” Nat. Cell Biol. 15(1), 82–87 (2013).
[Crossref]

Chen, N.

M. Liu, Q. Li, L. Liang, J. Li, K. Wang, J. Li, M. Lv, N. Chen, H. Song, J. Lee, J. Shi, L. Wang, R. Lal, and C. Fan, “Real-time visualization of clustering and intracellular transport of gold nanoparticles by correlative imaging,” Nat. Commun. 8:15646 (2017).
[Crossref] [PubMed]

Cho, K.

J. H. Seo, K. Cho, S. Y. Lee, and S.-W. Joo, “Concentration-dependent fluorescence live-cell imaging and tracking of intracellular nanoparticles,” Nanotechnology 22(23), 235101 (2011).
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Biochem. Biophys. Res. Commun. (1)

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Cell (1)

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J. Cell. Physiol. (1)

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Langmuir (1)

Y. Gao, S. M. Anthony, Y. Yi, W. Li, Y. Yu, and Y. Yu, “Single-janus rod tracking reveals the “rock-and-roll”, of endosomes in living cells,” Langmuir 34(3), 1151–1158 (2018).
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Nanotechnology (1)

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M. Nishiyama, E. Muto, Y. Inoue, T. Yanagida, and H. Higuchi, “Substeps within the 8-nm step of the atpase cycle of single kinesin molecules,” Nat. Cell Biol. 3(4), 425–428 (2001).
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Nat. Commun. (2)

N. Gustafsson, S. Culley, G. Ashdown, D. M. Owen, P. M. Pereira, and R. Henriques, “Fast live-cell conventional fluorophore nanoscopy with imagej through super-resolution radial fluctuations,” Nat. Commun. 7(1), 12471 (2016).
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Nat. Methods (1)

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “Nih image to imagej: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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Nat. Rev. Mol. Cell Biol. (2)

A. Sorkin and M. von Zastrow, “Signal transduction and endocytosis: close encounters of many kinds,” Nat. Rev. Mol. Cell Biol. 3(8), 600–614 (2002).
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Nature (2)

J.-D. Huang, S. T. Brady, B. W. Richards, D. Stenoien, J. H. Resau, N. G. Copeland, and N. A. Jenkins, “Direct interaction of microtubule-and actin-based transport motors,” Nature 397(6716), 267–270 (1999).
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New J. Phys. (1)

A. Dupont, M. Gorelashvili, V. Schüller, F. Wehnekamp, D. Arcizet, Y. Katayama, D. Lamb, and D. Heinrich, “Three-dimensional single-particle tracking in live cells: news from the third dimension,” New J. Phys. 15(7), 075008 (2013).
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Opt. Express (1)

Phys. Rev. E (1)

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Figures (7)

Fig. 1.
Fig. 1. Workflow of superpositioning microtubule network and vesicle trajectory images. An endocytic vesicle labeled by quantum dots was imaged and tracked in a living cell where the microtubules were labeled by GFP. For imaging microtubules-GFP, sixty images were taken at 1 fps. Immediately after the microtubule images were taken, vesicle-quantum dot images were taken for 10 s at 100 fps, under dual focus optics [12]. To acquire specific vesicle trajectories of vesicles that moved on microtubules, SRRF [25] was applied to microtubule images, the standard deviation (STD) of the intensity variance of the vesicle image stacks was projected, and the two images were combined (ImageJ) [26]. In this combined microtubule-vesicle image, a representative vesicle trajectory on microtubules is shown in the white box. Blue arrow indicates the initial position, and yellow arrow refers to the final position of the vesicle. Scale bar = 10 $\mu$m.
Fig. 2.
Fig. 2. A representative three-dimensional trajectory of the vesicle moved on microtubules, reconstructed by using dual focus optics [12]. $\phi _{2D}$ represents the angle that can be roughly estimated from 2D tracking data. In contrast, $\phi _{3D}$ indicates the angle between the red segments in three dimensions, which are the estimated positions of the microtubules in the linear sections detected by numerical analysis based on PCA for the detected linear sectionsed in pink) [21]. The random movements between linear sections areed in mint green.
Fig. 3.
Fig. 3. The 3D angles measured between the estimated locations of microtubules. (A) Vesicle-quantum dot trajectory (in red) and microtubule-GFP images (in green) were combined to detect the vesicle movement on the microtubule (scale bar = 1 $\mu$m), and the 3D trajectory of a vesicle moving in a microtubule network was reconstructed and divided into the linear sectionsed in pink) and pause or direction change sectionsed in mint green) based on the numerical position data analysis reported in our previous work [21]. The estimated location of a microtubule was calculated from the linear section via PCA [21]. The trajectory started at the point indicated by the blue arrow and finished at the point showed by yellow arrow. The angle $\phi$ was defined as the angle between the adjacent estimated microtubules. (B) The distribution of angle $\phi$ was acquired from 61 different trajectories. (C) The time taken for the respective case of abrupt direction changes or smooth transfers in a similar direction. (D) Distribution of the linear section lengths. (E) Distribution of the mean speeds of vesicles in the linear section.
Fig. 4.
Fig. 4. The rotational movement of a vesicle trajectory detected in the linear sections. (A) A representative trajectory that contains left-handed rotational movement of the vesicle in the linear section. The blue arrow indicates the position where the trajectory starts, while the yellow arrow represents the end point of the trajectory. The linear section showing the rotational movement along the estimated microtubule segment is indicated in the dashed-line box. (B) Left-handed rotation detected in the linear section, shown with a cross-sectional view, and the changes in angular and translational velocities. Cross-sectional view of the rotational movement after the noise is removed by a Gaussian noise filter (see Materials and Methods). The red dot in the center indicates the position of the estimated microtubule, which runs inward. The changes in the angle $\psi _{i}$ over time represents the angular velocity during the rotation. Monotonically decreasing $\psi _{i}$ represents the left-handed rotational movement of the vesicle around the axis of the estimated microtubule. The small red arrows indicate the inflection points in angular velocity. Note that the inflection points are 180° apart. The changes in the translational distance of the vesicle along the microtubuleed in yellow) was increased during the rotation, showing almost constant velocity. (C) A representative case of right-handed rotational movement of the vesicle, with increasing $\psi _{i}$ as the vesicle walks along the microtubule. (D) A representative case of the incomplete rotation which showed a turning-back motion. Note that the translational velocity is still constant for the above three cases.
Fig. 5.
Fig. 5. The physical properties of the rotational movement. (A) Comparison of length distribution between all linear sectionsed in red) and the pitch lengths of the detected rotationsed in pink). (B) Distribution of the mean radii of the rotational movements ($n$=$29$). (C) Distribution of mean translational velocities on the estimated microtubule. The grand mean value was close to 1 $\mu$m s$^{-1}$. The translational velocity refers to the mean of instantaneous speed of the vesicle while walking along the microtubule.
Fig. 6.
Fig. 6. MSD and MSAD for the detected rotational movement. (A) A representative case of $\alpha$ calculated from the linear section where rotational movement was observed (Left). The mean value of $\alpha$ was approximate 1.95 (Right). (B) A representative case of $\beta$ from the rotational movement (Left) and the histogram of $\beta$ which produced 2.14 of mean value (Right).
Fig. 7.
Fig. 7. Analysis on the type of motor proteins involved in the observed vesicle transport. (A) The movement direction of vesicle according to the estimated position of the centrosome. The angle $\theta$ represents the direction of movement, which is calculated using inner products of two vectors, $\overrightarrow {\textrm {CI}}$ and $\overrightarrow {\textrm {IF}}$: $\overrightarrow {\textrm {CI}}$ indicates the vector from the estimated centrosome to the initial position of the vesicle, and $\overrightarrow {\textrm {IF}}$ is the vector from the initial position to the final position of the vesicle trajectory. If the angle $\theta$ is close to $0\ ^\circ$, the vesicle is likely to be transported via kinesin, while the angle $\theta \sim 180\ ^\circ$ implies that dynein can be involved in the vesicle transport. Scale bar = 1 $\mu$m. (B) The distribution of $\theta$ for the detected rotational movement. The calculated $\theta$ showed broad distribution in both right and left handed rotational movement, which can be interpreted as the possibility that the rotational movement of vesicle is not caused by a specific type of motor protein, but can be shown with both types of motor proteins.

Equations (2)

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MSD ( τ ) = Δ r ( τ ) 2 = [ r ( t + τ ) r ( t ) ] 2 = 2 n D τ α
MSAD ( τ ) = Δ ψ ( τ ) 2 = 2 n D α τ β