Memoryless self-reinforcing directionality in endosomal active transport within living cells

Chen, Kejia; Wang, Bo; Granick, Steve

doi:10.1038/nmat4239

Memoryless self-reinforcing directionality in endosomal active transport within living cells

Journal Article · Mon Mar 30 00:00:00 EDT 2015 · Nature Materials

DOI:https://doi.org/10.1038/nmat4239· OSTI ID:1252187

Chen, Kejia ^[1]; Wang, Bo ^[2]; Granick, Steve ^[3]

Univ. of Illinois, Urbana, IL (United States); University of Illinois
Univ. of Illinois, Urbana, IL (United States)
Univ. of Illinois, Urbana, IL (United States); IBS Center for Soft and Living Matter, UNIST, Ulsan (South Korea)

In contrast to Brownian transport, the active motility of microbes, cells, animals and even humans often follows another random process known as truncated Levy walk^1,2. These stochastic motions are characterized by clustered small steps and intermittent longer jumps that often extend towards the size of the entire system. As there are repeated suggestions, although disagreement, that Levy walks have functional advantages over Brownian motion in random searching and transport kinetics^3-8, their intentional engineering into active materials could be useful. Here, we show experimentally in the classic active matter system of intracellular trafficking^9-15 that Brownian-like steps self-organize into truncated Levy walks through an apparent time-independent positive feedback such that directional persistence increases with the distance traveled persistently. A molecular model that allows the maximum output of the active propelling forces to fluctuate slowly fits the experiments quantitatively. Furthermore, our findings offer design principles for programming efficient transport in active materials.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Illinois, Urbana, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-02ER46019

OSTI ID:: 1252187

Journal Information:: Nature Materials, Journal Name: Nature Materials Journal Issue: 6 Vol. 14; ISSN 1476-1122

Publisher:: Springer Nature - Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (34)

Long-Range Transport of Giant Vesicles along Microtubule Networks Herold, Christoph; Leduc, Cécile; Stock, Robert ChemPhysChem, Vol. 13, Issue 4 https://doi.org/10.1002/cphc.201100669	journal	December 2011
Anomalous diffusion in disordered media: Statistical mechanisms, models and physical applications Bouchaud, Jean-Philippe; Georges, Antoine Physics Reports, Vol. 195, Issue 4-5 https://doi.org/10.1016/0370-1573(90)90099-N	journal	November 1990
Cargo transport: molecular motors navigate a complex cytoskeleton Ross, Jennifer L.; Ali, M. Yusuf; Warshaw, David M. Current Opinion in Cell Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.ceb.2007.11.006	journal	February 2008
Intracellular transport by active diffusion Brangwynne, Clifford P.; Koenderink, Gijsje H.; MacKintosh, Frederick C. Trends in Cell Biology, Vol. 19, Issue 9 https://doi.org/10.1016/j.tcb.2009.04.004	journal	September 2009
Diagnosing Heterogeneous Dynamics in Single-Molecule/Particle Trajectories with Multiscale Wavelets Chen, Kejia; Wang, Bo; Guan, Juan ACS Nano, Vol. 7, Issue 10 https://doi.org/10.1021/nn402787a	journal	August 2013
Strange kinetics Shlesinger, Michael F.; Zaslavsky, George M.; Klafter, Joseph Nature, Vol. 363, Issue 6424 https://doi.org/10.1038/363031a0	journal	May 1993
Optimizing the success of random searches Viswanathan, G. M.; Buldyrev, Sergey V.; Havlin, Shlomo Nature, Vol. 401, Issue 6756 https://doi.org/10.1038/44831	journal	October 1999
‘Infotaxis’ as a strategy for searching without gradients Vergassola, Massimo; Villermaux, Emmanuel; Shraiman, Boris I. Nature, Vol. 445, Issue 7126 https://doi.org/10.1038/nature05464	journal	January 2007
Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer Edwards, Andrew M.; Phillips, Richard A.; Watkins, Nicholas W. Nature, Vol. 449, Issue 7165 https://doi.org/10.1038/nature06199	journal	October 2007
A Lévy flight for light Barthelemy, Pierre; Bertolotti, Jacopo; Wiersma, Diederik S. Nature, Vol. 453, Issue 7194 https://doi.org/10.1038/nature06948	journal	May 2008
Generalized Lévy walks and the role of chemokines in migration of effector CD8+ T cells Harris, Tajie H.; Banigan, Edward J.; Christian, David A. Nature, Vol. 486, Issue 7404 https://doi.org/10.1038/nature11098	journal	May 2012
Cell and molecular mechanics of biological materials Bao, G.; Suresh, S. Nature Materials, Vol. 2, Issue 11 https://doi.org/10.1038/nmat1001	journal	November 2003
Enhanced reaction kinetics in biological cells Loverdo, C.; Bénichou, O.; Moreau, M. Nature Physics, Vol. 4, Issue 2 https://doi.org/10.1038/nphys830	journal	January 2008
Cooperative cargo transport by several molecular motors Klumpp, S.; Lipowsky, R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 48 https://doi.org/10.1073/pnas.0507363102	journal	November 2005
Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors Muller, M. J. I.; Klumpp, S.; Lipowsky, R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 12 https://doi.org/10.1073/pnas.0706825105	journal	March 2008
Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections Bálint, Štefan; Verdeny Vilanova, Ione; Sandoval Álvarez, Ángel Proceedings of the National Academy of Sciences, Vol. 110, Issue 9 https://doi.org/10.1073/pnas.1219206110	journal	February 2013
Intracellular transport of insulin granules is a subordinated random walk Tabei, S. M. A.; Burov, S.; Kim, H. Y. Proceedings of the National Academy of Sciences, Vol. 110, Issue 13 https://doi.org/10.1073/pnas.1221962110	journal	March 2013
Levy flights do not always optimize random blind search for sparse targets Palyulin, V. V.; Chechkin, A. V.; Metzler, R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 8 https://doi.org/10.1073/pnas.1320424111	journal	February 2014
A maximum entropy framework for nonexponential distributions Peterson, J.; Dixit, P. D.; Dill, K. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 51 https://doi.org/10.1073/pnas.1320578110	journal	December 2013
Helical Levy walks: Adjusting searching statistics to resource availability in microzooplankton Bartumeus, F.; Peters, F.; Pueyo, S. Proceedings of the National Academy of Sciences, Vol. 100, Issue 22 https://doi.org/10.1073/pnas.2137243100	journal	October 2003
Self-organization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells Reilein, Amy; Yamada, Soichiro; Nelson, W. James The Journal of Cell Biology, Vol. 171, Issue 5 https://doi.org/10.1083/jcb.200505071	journal	November 2005
Temporal Analysis of Active and Passive Transport in Living Cells Arcizet, Delphine; Meier, Börn; Sackmann, Erich Physical Review Letters, Vol. 101, Issue 24 https://doi.org/10.1103/PhysRevLett.101.248103	journal	December 2008
Coupling of Active Motion and Advection Shapes Intracellular Cargo Transport Khuc Trong, Philipp; Guck, Jochen; Goldstein, Raymond E. Physical Review Letters, Vol. 109, Issue 2 https://doi.org/10.1103/PhysRevLett.109.028104	journal	July 2012
Bursts of Active Transport in Living Cells Wang, Bo; Kuo, James; Granick, Steve Physical Review Letters, Vol. 111, Issue 20 https://doi.org/10.1103/PhysRevLett.111.208102	journal	November 2013
Stochastic Process with Ultraslow Convergence to a Gaussian: The Truncated Lévy Flight Mantegna, Rosario N.; Stanley, H. Eugene Physical Review Letters, Vol. 73, Issue 22 https://doi.org/10.1103/PhysRevLett.73.2946	journal	November 1994
Stochastic models of intracellular transport Bressloff, Paul C.; Newby, Jay M. Reviews of Modern Physics, Vol. 85, Issue 1 https://doi.org/10.1103/RevModPhys.85.135	journal	January 2013
Levy Walks Evolve Through Interaction Between Movement and Environmental Complexity de Jager, M.; Weissing, F. J.; Herman, P. M. J. Science, Vol. 332, Issue 6037 https://doi.org/10.1126/science.1201187	journal	June 2011
High-resolution mapping of intracellular fluctuations using carbon nanotubes Fakhri, N.; Wessel, A. D.; Willms, C. Science, Vol. 344, Issue 6187 https://doi.org/10.1126/science.1250170	journal	May 2014
Mechanical Signaling in Networks of Motor and Cytoskeletal Proteins Howard, Jonathon Annual Review of Biophysics, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.biophys.050708.133732	journal	June 2009
Analysis of Transient Behavior in Complex Trajectories: Application to Secretory Vesicle Dynamics Huet, Sébastien; Karatekin, Erdem; Tran, Viet Samuel Biophysical Journal, Vol. 91, Issue 9 https://doi.org/10.1529/biophysj.105.080622	journal	November 2006
Enhanced reaction kinetics in biological cells Loverdo, C.; Benichou, O.; Moreau, M. arXiv https://doi.org/10.48550/arxiv.0802.1493	text	January 2008
Coupling of Active Motion and Advection Shapes Intracellular Cargo Transport Trong, P. Khuc; Guck, J.; Goldstein, R. E. arXiv https://doi.org/10.48550/arxiv.1206.2842	text	January 2012
Bursts of Active Transport in Living Cells Wang, Bo; Kuo, James; Granick, Steve arXiv https://doi.org/10.48550/arxiv.1307.1898	text	January 2013
A maximum entropy framework for non-exponential distributions Peterson, Jack; Dixit, Purushottam D.; Dill, Ken A. arXiv https://doi.org/10.48550/arxiv.1501.01049	text	January 2015

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Neuronal messenger ribonucleoprotein transport follows an aging Lévy walk Song, Minho S.; Moon, Hyungseok C.; Jeon, Jae-Hyung Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02700-z	journal	January 2018
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Current status and future directions of Lévy walk research Reynolds, Andy M. Biology Open, Vol. 7, Issue 1 https://doi.org/10.1242/bio.030106	journal	January 2018
Navigation Strategies of Motor Proteins on Decorated Tracks Bertalan, Zsolt; Budrikis, Zoe; La Porta, Caterina A. M. PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0136945	journal	August 2015
Lévy foraging patterns of rural humans Reynolds, Andy; Ceccon, Eliane; Baldauf, Cristina PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0199099	journal	June 2018
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Swarm dynamics may give rise to Lévy flights Reynolds, Andrew M.; Ouellette, Nicholas T. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30515	journal	July 2016
Towards a full quantitative description of single-molecule reaction kinetics in biological cells Grebenkov, Denis S.; Metzler, Ralf; Oshanin, Gleb Physical Chemistry Chemical Physics, Vol. 20, Issue 24 https://doi.org/10.1039/c8cp02043d	journal	January 2018
Detection of ε -ergodicity breaking in experimental data—A study of the dynamical functional sensibility Loch-Olszewska, Hanna; Szwabiński, Janusz The Journal of Chemical Physics, Vol. 148, Issue 20 https://doi.org/10.1063/1.5025941	journal	May 2018
DNA molecules deviate from shortest trajectory when driven through hydrogel Guan, Juan; Chen, Kejia; Jee, Ah-Young The Journal of Chemical Physics, Vol. 149, Issue 16 https://doi.org/10.1063/1.5033990	journal	October 2018
Transient superdiffusion of polydisperse vacuoles in highly motile amoeboid cells Thapa, Samudrajit; Lukat, Nils; Selhuber-Unkel, Christine The Journal of Chemical Physics, Vol. 150, Issue 14 https://doi.org/10.1063/1.5086269	journal	April 2019
The topography of the environment alters the optimal search strategy for active particles Volpe, Giorgio; Volpe, Giovanni Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1711371114	journal	October 2017
Facilitation of polymer looping and giant polymer diffusivity in crowded solutions of active particles Shin, Jaeoh; Cherstvy, Andrey G.; Kim, Won Kyu New Journal of Physics, Vol. 17, Issue 11 https://doi.org/10.1088/1367-2630/17/11/113008	journal	October 2015
Crossover from anomalous to normal diffusion: truncated power-law noise correlations and applications to dynamics in lipid bilayers Molina-Garcia, Daniel; Sandev, Trifce; Safdari, Hadiseh New Journal of Physics, Vol. 20, Issue 10 https://doi.org/10.1088/1367-2630/aae4b2	journal	October 2018
Fractional Brownian motion in a finite interval: correlations effect depletion or accretion zones of particles near boundaries Guggenberger, T.; Pagnini, G.; Vojta, T. New Journal of Physics, Vol. 21, Issue 2 https://doi.org/10.1088/1367-2630/ab075f	journal	February 2019
Conservative random walks in confining potentials Dybiec, Bartłomiej; Capała, Karol; Chechkin, Aleksei V. Journal of Physics A: Mathematical and Theoretical, Vol. 52, Issue 1 https://doi.org/10.1088/1751-8121/aaefc2	journal	November 2018
Transport in exclusion processes with one-step memory: density dependence and optimal acceleration Teomy, Eial; Metzler, Ralf Journal of Physics A: Mathematical and Theoretical, Vol. 52, Issue 38 https://doi.org/10.1088/1751-8121/ab37e4	journal	August 2019
Deterministic and randomized motions in single-well potentials Mandrysz, Michał; Dybiec, Bartłomiej Journal of Physics A: Mathematical and Theoretical, Vol. 52, Issue 42 https://doi.org/10.1088/1751-8121/ab4350	journal	September 2019
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The Weierstrassian movement patterns of snails Reynolds, Andy; Santini, Giacomo; Chelazzi, Guido Royal Society Open Science, Vol. 4, Issue 6 https://doi.org/10.1098/rsos.160941	journal	June 2017
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Movement behavioral plasticity of benthic diatoms driven by optimal foraging Hu, Wen-Si; Huang, Mingji; Zhang, H. P. https://doi.org/10.1101/682153	preprint	January 2020
Langevin picture of Lévy walk in a constant force field Chen, Yao; Wang, Xudong; Deng, Weihua Physical Review E, Vol. 100, Issue 6 https://doi.org/10.1103/physreve.100.062141	journal	December 2019
Memory effects and Lévy walk dynamics in intracellular transport of cargoes Fedotov, Sergei; Korabel, Nickolay; Waigh, Thomas A. Physical Review E, Vol. 98, Issue 4 https://doi.org/10.1103/physreve.98.042136	journal	October 2018
Langevin dynamics for a Lévy walk with memory Chen, Yao; Wang, Xudong; Deng, Weihua Physical Review E, Vol. 99, Issue 1 https://doi.org/10.1103/physreve.99.012135	journal	January 2019
Universal Proximity Effect in Target Search Kinetics in the Few-Encounter Limit Godec, Aljaž; Metzler, Ralf Physical Review X, Vol. 6, Issue 4 https://doi.org/10.1103/physrevx.6.041037	journal	November 2016
Transport of a graphene nanosheet sandwiched inside cell membranes Chen, Pengyu; Yue, Hua; Zhai, Xiaobo Science Advances, Vol. 5, Issue 6 https://doi.org/10.1126/sciadv.aaw3192	journal	June 2019
Non-Markovian intracellular transport with sub-diffusion and run-length dependent detachment rate Korabel, Nickolay; Waigh, Thomas A.; Fedotov, Sergei PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0207436	journal	November 2018
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Universal proximity effect in target search kinetics in the few-encounter limit Godec, A.; Metzler, R. arXiv https://doi.org/10.48550/arxiv.1611.07788	text	January 2016
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