1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 53, 2024
  5. Article

Annual Review of Biophysics

Volume 53, 2024

Emergent Spatiotemporal Organization in Stochastic Intracellular Transport Dynamics

Abstract

The interior of a living cell is an active, fluctuating, and crowded environment, yet it maintains a high level of coherent organization. This dichotomy is readily apparent in the intracellular transport system of the cell. Membrane-bound compartments called endosomes play a key role in carrying cargo, in conjunction with myriad components including cargo adaptor proteins, membrane sculptors, motor proteins, and the cytoskeleton. These components coordinate to effectively navigate the crowded cell interior and transport cargo to specific intracellular locations, even though the underlying protein interactions and enzymatic reactions exhibit stochastic behavior. A major challenge is to measure, analyze, and understand how, despite the inherent stochasticity of the constituent processes, the collective outcomes show an emergent spatiotemporal order that is precise and robust. This review focuses on this intriguing dichotomy, providing insights into the known mechanisms of noise suppression and noise utilization in intracellular transport processes, and also identifies opportunities for future inquiry.

Keyword(s): emergent order, endosomal trafficking, intracellular transport, noise, stochastic dynamics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-030422-044448
2024-07-16
2025-01-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/53/1/annurev-biophys-030422-044448.html?itemId=/content/journals/10.1146/annurev-biophys-030422-044448&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Allen LJ. 2010.. An Introduction to Stochastic Processes with Applications to Biology. Boca Raton, FL:: CRC Press
     [Google Scholar]
  2. 2.
    Amoruso C, Lagache T, Holcman D. 2011.. Modeling the early steps of cytoplasmic trafficking in viral infection and gene delivery. . SIAM J. Appl. Math. 71:(6):2334–58
     [Crossref] [Google Scholar]
  3. 3.
    Axelrod D. 1981.. Cell-substrate contacts illuminated by total internal reflection fluorescence. . J. Cell Biol. 89:(1):141–45
     [Crossref] [Google Scholar]
  4. 4.
    Axelrod D. 2001.. Total internal reflection fluorescence microscopy in cell biology. . Traffic 2:(11):764–74
     [Crossref] [Google Scholar]
  5. 5.
    Bakker J, Spits M, Neefjes J, Berlin I. 2017.. The EGFR odyssey—from activation to destruction in space and time. . J. Cell Sci. 130:(24):4087–96
     [Crossref] [Google Scholar]
  6. 6.
    Bartumeus F, da Luz MGE, Viswanathan GM, Catalan J. 2005.. Animal search strategies: a quantitative random-walk analysis. . Ecology 86:(11):3078–87
     [Crossref] [Google Scholar]
  7. 7.
    Bénichou O, Loverdo C, Moreau M, Voituriez R. 2011.. Intermittent search strategies. . Rev. Mod. Phys. 83:(1):81–129
     [Crossref] [Google Scholar]
  8. 8.
    Bertalan Z, Budrikis Z, La Porta CAM, Zapperi S. 2015.. Navigation strategies of motor proteins on decorated tracks. . PLOS ONE 10:(8):e0136945
     [Crossref] [Google Scholar]
  9. 9.
    Binder B, Holzhütter HG. 2012.. A hypothetical model of cargo-selective Rab recruitment during organelle maturation. . Cell Biochem. Biophys. 63:(1):59–71
     [Crossref] [Google Scholar]
  10. 10.
    Blue RE, Curry EG, Engels NM, Lee EY, Giudice J. 2018.. How alternative splicing affects membrane-trafficking dynamics. . J. Cell Sci. 131:(10):jcs216465
     [Crossref] [Google Scholar]
  11. 11.
    Blythe RA, Evans MR. 2007.. Nonequilibrium steady states of matrix-product form: a solver's guide. . J. Phys. A 40:(46):R333
     [Crossref] [Google Scholar]
  12. 12.
    Bonifacino JS, Rojas R. 2006.. Retrograde transport from endosomes to the trans-Golgi network. . Nat. Rev. Mol. Cell Biol. 7:(8):568–79
     [Crossref] [Google Scholar]
  13. 13.
    Bonucci M, Shu T, Holt LJ. 2023.. How it feels in a cell. . Trends Cell Biol. 33:(11):P92438
     [Crossref] [Google Scholar]
  14. 14.
    Bouchaud JP, Georges A. 1990.. Anomalous diffusion in disordered media: statistical mechanisms, models and physical applications. . Phys. Rep. 195:(4–5):127–293
     [Crossref] [Google Scholar]
  15. 15.
    Brandizzi F, Frangne N, Marc-Martin S, Hawes C, Neuhaus JM, Paris N. 2002.. The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. . Plant Cell 14:(5):1077–92
     [Crossref] [Google Scholar]
  16. 16.
    Brangwynne CP, Gijsje HK, MacKintosh FC, Weitz DA. 2009.. Intracellular transport by active diffusion. . Trends Cell Biol. 19:(9):423–27
     [Crossref] [Google Scholar]
  17. 17.
    Bressloff PC. 2014.. Stochastic Processes in. Cell Biology. Interdiscip. Appl. Math. 41:. Berlin:: Springer
     [Crossref] [Google Scholar]
  18. 18.
    Bressloff PC, Newby JM. 2012.. Filling of a Poisson trap by a population of random intermittent searchers. . Phys. Rev. E 85:(3):031909
     [Crossref] [Google Scholar]
  19. 19.
    Bressloff PC, Newby JM. 2013.. Stochastic models of intracellular transport. . Rev. Mod. Phys. 85:(1):135–96
     [Crossref] [Google Scholar]
  20. 20.
    Brown AI, Westrate LM, Koslover EF. 2020.. Impact of global structure on diffusive exploration of organelle networks. . Sci. Rep. 10::4984
     [Crossref] [Google Scholar]
  21. 21.
    Bruggeman FJ, Teusink B. 2018.. Living with noise: on the propagation of noise from molecules to phenotype and fitness. . Curr. Opin. Syst. Biol. 8::144–50
     [Crossref] [Google Scholar]
  22. 22.
    Burov S, Jeon JH, Metzler R, Barkai E. 2011.. Single particle tracking in systems showing anomalous diffusion: the role of weak ergodicity breaking. . Phys. Chem. Chem. Phys. 13:(5):1800–12
     [Crossref] [Google Scholar]
  23. 23.
    Campàs O, Leduc C, Bassereau P, Casademunt J, Joanny JF, Prost J. 2008.. Coordination of kinesin motors pulling on fluid membranes. . Biophys. J. 94:(12):5009–17
     [Crossref] [Google Scholar]
  24. 24.
    Cardelli L, Laurenti L, Csikasz-Nagy A. 2020.. Coupled membrane transporters reduce noise. . Phys. Rev. E 101::012414
     [Crossref] [Google Scholar]
  25. 25.
    Carlton JG, Cullen PJ. 2005.. Coincidence detection in phosphoinositide signaling. . Trends Cell Biol. 15:(10):540–47
     [Crossref] [Google Scholar]
  26. 26.
    Castro M, Lythe G, Smit J, Molina-París C. 2021.. Fusion and fission events regulate endosome maturation and viral escape. . Sci Rep. 11::7845
     [Crossref] [Google Scholar]
  27. 27.
    Charras GT, Coughlin M, Mitchison TJ, Mahadevan L. 2008.. Life and times of a cellular bleb. . Biophys. J. 94:(5):1836–53
     [Crossref] [Google Scholar]
  28. 28.
    Chen BC, Legant WR, Wang K, Shao L, Milkie DE, et al. 2014.. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. . Science 346:(6208):1257998
     [Crossref] [Google Scholar]
  29. 29.
    Chepyala SR, Chen YC, Yan CCS, Lu CYD, Wu YC, Hsu CP. 2016.. Noise propagation with interlinked feed-forward pathways. . Sci. Rep. 6::23607
     [Crossref] [Google Scholar]
  30. 30.
    Chou T, Mallick K, Zia RKP. 2011.. Non-equilibrium statistical mechanics: from a paradigmatic model to biological transport. . Rep. Prog. Phys. 74:(11):116601
     [Crossref] [Google Scholar]
  31. 31.
    Cullen PJ. 2008.. Endosomal sorting and signalling: an emerging role for sorting nexins. . Nat. Rev. Mol. Cell Biol. 9::574–82
     [Crossref] [Google Scholar]
  32. 32.
    Cullen PJ, Carlton JG. 2014.. Phosphoinositides in the mammalian endo-lysosomal network. . Subcell. Biochem. 59::65–110
     [Crossref] [Google Scholar]
  33. 33.
    Cullen PJ, Steinberg F. 2018.. To degrade or not to degrade: mechanisms and significance of endocytic recycling. . Nat. Rev. Mol. Cell Biol. 19:(11):679–96
     [Crossref] [Google Scholar]
  34. 34.
    Derivery E, Gautreau A. 2010.. Assaying WAVE and WASH complex constitutive activities toward the Arp2/3 complex. . Methods Enzymol. 484::677–95
     [Crossref] [Google Scholar]
  35. 35.
    Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A. 2009.. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. . Dev. Cell 17:(5):712–23
     [Crossref] [Google Scholar]
  36. 36.
    Dix JA, Verkman AS. 2008.. Crowding effects on diffusion in solutions and cells. . Annu. Rev. Biophys. 37::247–63
     [Crossref] [Google Scholar]
  37. 37.
    Drechsler M, Giavazzi F, Cerbino R, Primo L, Lichtenstein L, Ferrari A. 2017.. Active diffusion and advection in Drosophila oocytes result from the interplay of actin and microtubules. . Nat. Commun. 8::1520
     [Crossref] [Google Scholar]
  38. 38.
    Einstein A. 1905.. Investigations on the theory of the Brownian movement. . Ann. Phys. 17::549–60
     [Crossref] [Google Scholar]
  39. 39.
    Eling N, Morgan MD, Marioni JC. 2019.. Challenges in measuring and understanding biological noise. . Nat. Rev. Genet. 20:(9):536–48
     [Crossref] [Google Scholar]
  40. 40.
    Érdi P, Lente G. 2016.. Stochastic Chemical Kinetics. Berlin:: Springer
     [Google Scholar]
  41. 41.
    Everitt B. 1998.. The Cambridge Dictionary of Statistics. Cambridge, UK:: Cambridge Univ. Press
     [Google Scholar]
  42. 42.
    Ferro LS, Can S, Turner MA, ElShenawy MM, Yildiz A. 2019.. Kinesin and dynein use distinct mechanisms to bypass obstacles. . eLife 8::e48629
     [Crossref] [Google Scholar]
  43. 43.
    Foret L, Dawson JE, Villaseñor R, Collinet C, Deutsch A, et al. 2012.. A general theoretical framework to infer endosomal network dynamics from quantitative image analysis. . Curr. Biol. 22:(15):1381–90
     [Crossref] [Google Scholar]
  44. 44.
    Ganguly S, Williams LS, Palacios IM, Goldstein RE. 2012.. Cytoplasmic streaming in Drosophila oocytes varies with kinesin activity and correlates with the microtubule cytoskeleton architecture. . PNAS 109:(38):15109–14
     [Crossref] [Google Scholar]
  45. 45.
    Gardiner C. 2009.. Stochastic Methods: A Handbook for the Natural and Social Sciences. Berlin:: Springer
     [Google Scholar]
  46. 46.
    Gennerich A, Vale RD. 2009.. Walking the walk: how kinesin and dynein coordinate their steps. . Curr. Opin. Cell Biol. 21:(1):59–67
     [Crossref] [Google Scholar]
  47. 47.
    Gillespie DT. 1976.. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. . J. Comp. Phys. 22:(4):403–34
     [Crossref] [Google Scholar]
  48. 48.
    Golding I, Cox EC. 2006.. Physical nature of bacterial cytoplasm. . Phys. Rev. Lett. 96:(9): 098102.
     [Crossref] [Google Scholar]
  49. 49.
    Granger E, McNee G, Allan V, Woodman P. 2014.. The role of the cytoskeleton and molecular motors in endosomal dynamics. . Semin. Cell Dev. Biol. 31:(100):20–29
     [Crossref] [Google Scholar]
  50. 50.
    Guo M, Ehrlicher AJ, Jensen MH, Renz M, Moore JR, et al. 2014.. Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy. . Cell 158:(4):822–32
     [Crossref] [Google Scholar]
  51. 51.
    Gupta SK, Guo M. 2017.. Equilibrium and out-of-equilibrium mechanics of living mammalian cytoplasm. . J. Mech. Phys. Solids 107::284–93
     [Crossref] [Google Scholar]
  52. 52.
    Helenius J, Brouhard G, Kalaidzidis Y, Diez S, Howard J. 2006.. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. . Nature 441:(7089):115–19
     [Crossref] [Google Scholar]
  53. 53.
    Hirokawa N, Noda Y, Tanaka Y, Niwa S. 2009.. Kinesin superfamily motor proteins and intracellular transport. . Nat. Rev. Mol. Cell Biol. 10:(10):682–96
     [Crossref] [Google Scholar]
  54. 54.
    Howard J. 2001.. Mechanics of Motor Proteins and the Cytoskeleton. Sunderland, MA:: Sinauer Assoc.
     [Google Scholar]
  55. 55.
    Hu J, Iyer-Biswas S, Sealfon SC, Wetmur J, Jayaprakash C, Hayot F. 2009.. Power-laws in interferon-B mRNA distribution in virus-infected dendritic cells. . Biophys. J. 97:(7):1984–89
     [Crossref] [Google Scholar]
  56. 56.
    Iyer-Biswas S. 2009.. Applications of methods of non-equilibrium statistical physics to models of stochastic gene expression. PhD thesis , Ohio State Univ., Columbus:
     [Google Scholar]
  57. 57.
    Iyer-Biswas S, Crooks GE, Scherer NF, Dinner AR. 2014.. Universality in stochastic exponential growth. . Phys. Rev. Lett. 113:(2):028101
     [Crossref] [Google Scholar]
  58. 58.
    Iyer-Biswas S, Hayot F, Jayaprakash C. 2009.. Stochasticity of gene products from transcriptional pulsing. . Phys. Rev. E 79:(3):031911
     [Crossref] [Google Scholar]
  59. 59.
    Iyer-Biswas S, Jayaprakash C. 2014.. Mixed Poisson distributions in exact solutions of stochastic autoregulation models. . Phys. Rev. E 90:(5):052712
     [Crossref] [Google Scholar]
  60. 60.
    Iyer-Biswas S, Wright CS, Henry JT, Lo K, Burov S, et al. 2014.. Scaling laws governing stochastic growth and division of single bacterial cells. . PNAS 111:(45):15912–17
     [Crossref] [Google Scholar]
  61. 61.
    Iyer-Biswas S, Zilman A. 2016.. First-passage processes in cellular biology. . Adv. Chem. Phys. 160::261–306
     [Google Scholar]
  62. 62.
    Jafarpour F, Vennettilli M, Iyer-Biswas S. 2017.. Biological timekeeping in the presence of stochasticity. . arXiv:1703.10058 [q-bio.MN]
  63. 63.
    Jeon JH, Tejedor V, Burov S, Barkai E, Selhuber-Unkel C, et al. 2011.. In vivo anomalous diffusion and weak ergodicity breaking of lipid granules. . Phys. Rev. Lett. 106:(4):048103
     [Crossref] [Google Scholar]
  64. 64.
    Joshi K, Biswas RR, Iyer-Biswas S. 2023.. Intergenerational scaling law determines the precision kinematics of stochastic individual-cell-size homeostasis. . bioRxiv 2023.01.20.525000. https://doi.org/10.1101/2023.01.20.525000
  65. 65.
    Joshi K, Roy S, Biswas RR, Iyer-Biswas S. 2023.. Cellular dynamics under time-varying conditions. . bioRxiv 2023.03.07.531540. https://doi.org/10.1101/2023.03.07.531540
  66. 66.
    Joshi K, Wright CS, Ziegler KF, Spiers EM, Crosser JT, et al. 2023.. Emergent simplicities in stochastic intergenerational homeostasis. . bioRxiv 2023.01.18.524627. https://doi.org/10.1101/2023.01.18.524627
  67. 67.
    Joshi K, Ziegler KF, Roy S, Wright CS, Gandhi R, et al. 2023.. Non-Markovian memory and emergent simplicities in the stochastic and plastic adaptation of individual cells to dynamic environments. . bioRxiv 023.05.27.542601 . https://doi.org/10.1101/2023.05.27.542601
  68. 68.
    Jović M, Kean MJ, Dubankova A, Boura E, Gingras AC, et al. 2014.. Endosomal sorting of VAMP3 is regulated by PI4K2A. . J. Cell Sci. 127:(17):3745–56
     [Google Scholar]
  69. 69.
    Jülicher F, Ajdari A, Prost J. 1997.. Modeling molecular motors. . Rev. Mod. Phys. 69:(4):1269
     [Crossref] [Google Scholar]
  70. 70.
    Kar J, Kar S, Gupta A, Jana SS. 2023.. Assembly and disassembly dynamics of nonmuscle myosin II control endosomal fission. . Cell Rep. 42:(2):112108
     [Crossref] [Google Scholar]
  71. 71.
    Keim NC, Paulsen JD, Zeravcic Z, Sastry S, Nagel SR. 2019.. Memory formation in matter. . Rev. Mod. Phys. 91:(3):035002
     [Crossref] [Google Scholar]
  72. 72.
    Keller D, Bustamante C. 2000.. The mechanochemistry of molecular motors. . Biophys. J. 78:(2):541–56
     [Crossref] [Google Scholar]
  73. 73.
    Klumpp S, Nieuwenhuizen TM, Lipowsky R. 2005.. Movements of molecular motors: ratchets, random walks and traffic phenomena. . Phys. E 29:(1–2):380–89
     [Crossref] [Google Scholar]
  74. 74.
    Kolomeisky AB, Fisher ME. 2007.. Molecular motors: a theorist's perspective. . Annu. Rev. Phys. Chem. 58::675–95
     [Crossref] [Google Scholar]
  75. 75.
    Lagache T, Danos O, Holcman D. 2012.. Modeling the step of endosomal escape during cell infection by a nonenveloped virus. . Biophys. J. 102:(5):980–89
     [Crossref] [Google Scholar]
  76. 76.
    Lagache T, Sieben C, Meyer T, Herrmann A, Holcman D. 2017.. Stochastic model of acidification, activation of hemagglutinin and escape of influenza viruses from an endosome. . Front. Phys. 5::25
     [Crossref] [Google Scholar]
  77. 77.
    Lewis OL, Zhang S, Guy RD, Del Alamo JC. 2015.. Coordination of contractility, adhesion and flow in migrating Physarum amoebae. . J. R. Soc. Interface 12:(106):20141359
     [Crossref] [Google Scholar]
  78. 78.
    Liepelt S, Lipowsky R. 2007.. Kinesin's network of chemomechanical motor cycles. . Phys. Rev. Lett. 98:(25):258102
     [Crossref] [Google Scholar]
  79. 79.
    Lin C, Schuster M, Guimaraes SC, Ashwin P, Schrader M, et al. 2016.. Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells. . Nat. Commun. 7::11814
     [Crossref] [Google Scholar]
  80. 80.
    Lipowsky R, Klumpp S. 2005.. ``Life is motion'': multiscale motility of molecular motors. . Phys. A 352:(1):53–112
     [Crossref] [Google Scholar]
  81. 81.
    Lippincott-Schwartz J, Snapp EL, Phair RD. 2018.. The development and enhancement of FRAP as a key tool for investigating protein dynamics. . Biophys. J. 115:(7):1146–55
     [Crossref] [Google Scholar]
  82. 82.
    Luby-Phelps K. 2013.. The physical chemistry of cytoplasm and its influence on cell function: an update. . Mol. Biol. Cell 24:(17):2593–96
     [Crossref] [Google Scholar]
  83. 83.
    Mandelbrot BB, Van Ness JW. 1968.. Fractional Brownian motions, fractional noises and applications. . SIAM Rev. 10:(4):422–37
     [Crossref] [Google Scholar]
  84. 84.
    Margiotta A, Bucci C. 2016.. Role of intermediate filaments in vesicular traffic. . Cells 5:(2):20
     [Crossref] [Google Scholar]
  85. 85.
    Mayle KM, Le AM, Kamei DT. 2012.. The intracellular trafficking pathway of transferrin. . Biochim. Biophys. Acta 1820:(3):264–81
     [Crossref] [Google Scholar]
  86. 86.
    Mim C, Unger VM. 2012.. Membrane curvature and its generation by BAR proteins. . Trends Biochem. Sci. 37:(12):526–33
     [Crossref] [Google Scholar]
  87. 87.
    Mitchison TJ, Charras GT, Mahadevan L. 2008.. Implications of a poroelastic cytoplasm for the dynamics of animal cell shape. . Semin. Cell Dev. Biol. 19:(3):215–23
     [Crossref] [Google Scholar]
  88. 88.
    Moeendarbary E, Valon L, Fritzsche M, Harris AR, Moulding DA, et al. 2013.. The cytoplasm of living cells behaves as a poroelastic material. . Nat. Mater. 12:(3):253–61
     [Crossref] [Google Scholar]
  89. 89.
    Mogilner A, Manhart A. 2018.. Intracellular fluid mechanics: coupling cytoplasmic flow with active cytoskeletal gel. . Annu. Rev. Fluid Mech. 50::347–70
     [Crossref] [Google Scholar]
  90. 90.
    Mogre SS, Brown AI, Koslover EF. 2020.. Getting around the cell: physical transport in the intracellular world. . Phys. Biol. 17:(6):061003
     [Crossref] [Google Scholar]
  91. 91.
    Parmeggiani A, Jülicher F, Ajdari A, Prost J. 1999.. Energy transduction of isothermal ratchets: generic aspects and specific examples close to and far from equilibrium. . Phys. Rev. E 60:(2):2127
     [Crossref] [Google Scholar]
  92. 92.
    Peskin CS, Oster G. 1995.. Coordinated hydrolysis explains the mechanical behavior of kinesin. . Biophys. J. 68:(4 Suppl):202S–11S
     [Google Scholar]
  93. 93.
    Picas L, Viaud J, Schauer K, Vanni S, Hnia K, et al. 2014.. BIN1/M-Amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin. . Nat. Commun. 5::5647
     [Crossref] [Google Scholar]
  94. 94.
    Posor Y, Jang W, Haucke V. 2022.. Phosphoinositides as membrane organizers. . Nat. Rev. Mol. Cell Biol. 23:(12):797–816
     [Crossref] [Google Scholar]
  95. 95.
    Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J. 1997.. ER-to-Golgi transport visualized in living cells. . Nature 389:(6646):81–85
     [Crossref] [Google Scholar]
  96. 96.
    Prost J, Chauwin JF, Peliti L, Ajdari A. 1994.. Asymmetric pumping of particles. . Phys. Rev. Lett. 72:(16):2652
     [Crossref] [Google Scholar]
  97. 97.
    Radszuweit M, Alonso S, Engel H, Bär M. 2013.. Intracellular mechanochemical waves in an active poroelastic model. . Phys. Rev. Lett. 110:(13):138102
     [Crossref] [Google Scholar]
  98. 98.
    Rai A, Pathak D, Thakur S, Singh S, Dubey AK, Mallik R. 2016.. Dynein clusters into lipid microdomains on phagosomes to drive rapid transport toward lysosomes. . Cell 164:(4):722–34
     [Crossref] [Google Scholar]
  99. 99.
    Rajagopal V, Arumugam S, Hunter PJ, Khadangi A, Chung J, Pan M. 2022.. The cell physiome: What do we need in a computational physiology framework for predicting single-cell biology?. Annu. Rev. Biomed. Data Sci. 5::341–66
     [Crossref] [Google Scholar]
  100. 100.
    Reimann P. 2002.. Brownian motors: noisy transport far from equilibrium. . Phys. Rep. 361:(2–4):57–265
     [Crossref] [Google Scholar]
  101. 101.
    Rink J, Ghigo E, Kalaidzidis Y, Zerial M. 2005.. Rab conversion as a mechanism of progression from early to late endosomes. . Cell 122:(5):735–49
     [Crossref] [Google Scholar]
  102. 102.
    Roberts AJ, Kon T, Knight PJ, Sutoh K, Burgess SA. 2013.. Functions and mechanics of dynein motor proteins. . Nat. Rev. Mol. Cell Biol. 14:(11):713–26
     [Crossref] [Google Scholar]
  103. 103.
    Rodriguez-Boulan E, Kreitzer G, Müsch A. 2005.. Organization of vesicular trafficking in epithelia. . Nat. Rev. Mol. Cell Biol. 6::233–47
     [Crossref] [Google Scholar]
  104. 104.
    Rowland AA, Chitwood PJ, Phillips MJ, Voeltz GK. 2014.. ER contact sites define the position and timing of endosome fission. . Cell 159:(5):1027–41
     [Crossref] [Google Scholar]
  105. 105.
    Ryu J, Galan AK, Xin X, Dong F, Abdul-Ghani MA, et al. 2014.. APPL1 potentiates insulin sensitivity by facilitating the binding of IRS1/2 to the insulin receptor. . Cell Rep. 7:(4):1227–38
     [Crossref] [Google Scholar]
  106. 106.
    Sanders S, Joshi K, Levin PA, Iyer-Biswas S. 2023.. Beyond the average: an updated framework for understanding the relationship between cell growth, DNA replication, and division in a bacterial system. . PLOS Genet. 19:(1):e1010505
     [Crossref] [Google Scholar]
  107. 107.
    Sarfati R, Joshi K, Martin O, Hayes JC, Iyer-Biswas S, Peleg O. 2023.. Emergent periodicity in the collective synchronous flashing of fireflies. . eLife 12::e78908
     [Crossref] [Google Scholar]
  108. 108.
    Schadschneider A, Chowdhury D, Nishinari K. 2010.. Stochastic Transport in Complex Systems: From Molecules to Vehicles. Amsterdam:: Elsevier
     [Google Scholar]
  109. 109.
    Scher H, Montroll EW. 1975.. Anomalous transit-time dispersion in amorphous solids. . Phys. Rev. B 12:(6):2455
     [Crossref] [Google Scholar]
  110. 110.
    Schnitzer MJ, Visscher K, Block SM. 2000.. Force production by single kinesin motors. . Nat. Cell Biol. 2:(10):718–23
     [Crossref] [Google Scholar]
  111. 111.
    Schrödinger E. 1915.. Zur theorie der fall-und steigversuche an teilchen mit brownscher bewegung. . Phys. Z. 16::289–95
     [Google Scholar]
  112. 112.
    Seksek O, Biwersi J, Verkman A. 1997.. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. . J. Cell Biol. 138:(1):131–42
     [Crossref] [Google Scholar]
  113. 113.
    Shakiba N, Li C, Garcia-Ojalvo J, Cho KH, Patil K, et al. 2022.. How can Waddington-like landscapes facilitate insights beyond developmental biology?. Cell Syst. 13:(1):4–9
     [Crossref] [Google Scholar]
  114. 114.
    Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. 2008.. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. . Dev. Cell 15:(2):209–19
     [Crossref] [Google Scholar]
  115. 115.
    Simunovic M, Voth GA, Callan-Jones A, Bassereau P. 2015.. When physics takes over: BAR proteins and membrane curvature. . Rev. Trends Cell Biol. 25:(12):780–92
     [Crossref] [Google Scholar]
  116. 116.
    Smelser AM, Macosko JC, O'Dell AP, Smyre S, Bonin K, Holzwarth G. 2015.. Mechanical properties of normal versus cancerous breast cells. . Biomech. Model. Mechanobiol. 14::1335–47
     [Crossref] [Google Scholar]
  117. 117.
    Soldati T, Schliwa M. 2006.. Powering membrane traffic in endocytosis and recycling. . Nat. Rev. Mol. Cell Biol. 7::897–908
     [Crossref] [Google Scholar]
  118. 118.
    Stanoev A, Mhamane A, Schuermann KC, Grecco HE, Stallaert W, et al. 2018.. Interdependence between EGFR and phosphatases spatially established by vesicular dynamics generates a growth factor sensing and responding network. . Cell Syst. 7:(3):295–309.e11
     [Crossref] [Google Scholar]
  119. 119.
    Striepen JF, Voeltz GK. 2022.. Coronin 1C restricts endosomal branched actin to organize ER contact and endosome fission. . J. Cell Biol. 221:(8):e202110089
     [Crossref] [Google Scholar]
  120. 120.
    Thattai M, Van Oudenaarden A. 2002.. Attenuation of noise in ultrasensitive signaling cascades. . Biophys. J. 82:(6):2943–50
     [Crossref] [Google Scholar]
  121. 121.
    Tolić-Nørrelykke IM, Munteanu EL, Thon G, Oddershede L, Berg-Sørensen K. 2004.. Anomalous diffusion in living yeast cells. . Phys. Rev. Lett. 93:(7):078102
     [Crossref] [Google Scholar]
  122. 122.
    Tominaga M, Kimura A, Yokota E, Haraguchi T, Shimmen T, et al. 2013.. Cytoplasmic streaming velocity as a plant size determinant. . Dev. Cell 27:(3):345–52
     [Crossref] [Google Scholar]
  123. 123.
    Tsimring LS. 2014.. Noise in biology. . Rep. Prog. Phys. 77:(2):026601
     [Crossref] [Google Scholar]
  124. 124.
    Vagne Q, Sens P. 2018.. Stochastic model of maturation and vesicular exchange in cellular organelles. . Biophys. J. 114:(4):947–57
     [Crossref] [Google Scholar]
  125. 125.
    Villaseñor R, Kalaidzidis Y, Zerial M. 2016.. Signal processing by the endosomal system. . Curr. Opin. Cell Biol. 39::53–60
     [Crossref] [Google Scholar]
  126. 126.
    Villaseñor R, Nonaka H, Del Conte-Zerial P, Kalaidzidis Y, Zerial M. 2015.. Regulation of EGFR signal transduction by analogue-to-digital conversion in endosomes. . eLife 4::e06156
     [Crossref] [Google Scholar]
  127. 127.
    Visscher K, Schnitzer MJ, Block SM. 1999.. Single kinesin molecules studied with a molecular force clamp. . Nature 400:(6740):184–89
     [Crossref] [Google Scholar]
  128. 128.
    Wallroth A, Haucke V. 2018.. Phosphoinositide conversion in endocytosis and the endolysosomal system. . J. Biol. Chem. 293:(5):1526–35
     [Crossref] [Google Scholar]
  129. 129.
    Wandinger-Ness A, Zerial M. 2014.. Rab proteins and the compartmentalization of the endosomal system. . Cold Spring Harb. Perspect. Biol. 6:(6):a022616
     [Crossref] [Google Scholar]
  130. 130.
    Wang HY, Elston T, Mogilner A, Oster G. 1998.. Force generation in RNA polymerase. . Biophys. J. 74:(3):1186–202
     [Crossref] [Google Scholar]
  131. 131.
    Weber SC, Spakowitz AJ, Theriot JA. 2010.. Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm. . Phys. Rev. Lett. 104:(23):238102
     [Crossref] [Google Scholar]
  132. 132.
    Wehrens M, Büke F, Nghe P, Tans SJ. 2018.. Stochasticity in cellular metabolism and growth: approaches and consequences. . Curr. Opin. Syst. Biol. 8::131–36
     [Crossref] [Google Scholar]
  133. 133.
    Weigel AV, Simon B, Tamkun MM, Krapf D. 2011.. Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. . PNAS 108:(16):6438–43
     [Crossref] [Google Scholar]
  134. 134.
    Woodhouse FG, Goldstein RE. 2013.. Cytoplasmic streaming in plant cells emerges naturally by microfilament self-organization. . PNAS 110:(35):14132–37
     [Crossref] [Google Scholar]
  135. 135.
    Yang X, Heinemann M, Howard J, Huber G, Iyer-Biswas S, et al. 2021.. Physical bioenergetics: energy fluxes, budgets, and constraints in cells. . PNAS 118:(26):e2026786118
     [Crossref] [Google Scholar]
  136. 136.
    York HM, Coyle J, Arumugam S. 2020.. To be more precise: the role of intracellular trafficking in development and pattern formation. . Biochem. Soc. Trans. 48:(5):2051–66
     [Crossref] [Google Scholar]
  137. 137.
    York HM, Joshi K, Wright CS, Kreplin LZ, Rodgers S, et al. 2022.. Deterministic early endosomal maturations emerge from a stochastic trigger-and-convert mechanism. . Nat. Commun. 14::4652
     [Crossref] [Google Scholar]
  138. 138.
    York HM, Patil A, Moorthi UK, Kaur A, Bhowmik A, et al. 2021.. Rapid whole cell imaging reveals a calcium-APPL1-dynein nexus that regulates cohort trafficking of stimulated EGF receptors. . Commun. Biol. 4:(1):224
     [Crossref] [Google Scholar]
  139. 139.
    Yu L, Lei Y, Ma Y, Liu M, Zheng J, et al. 2021.. A comprehensive review of fluorescence correlation spectroscopy. . Front. Phys. 9::644450
     [Crossref] [Google Scholar]
  140. 140.
    Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, et al. 2012.. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. . Nature 485:(7399):465–70
     [Crossref] [Google Scholar]
  141. 141.
    Zerial M, McBride H. 2001.. Rab proteins as membrane organizers. . Nat. Rev. Mol. Cell Biol. 2:(2):107–17
     [Crossref] [Google Scholar]
  142. 142.
    Zhang ML, Ti HY, Wang PY, Li H. 2021.. Intracellular transport dynamics revealed by single-particle tracking. . Biophys. Rep. 7:(5):413–27
     [Crossref] [Google Scholar]
  143. 143.
    Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. 2009.. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. . Cell 136:(6):1110–21
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-biophys-030422-044448
Loading
Emergent Spatiotemporal Organization in Stochastic Intracellular Transport Dynamics
Annual Review of Biophysics 53, 193 (2024); https://doi.org/10.1146/annurev-biophys-030422-044448
/content/journals/10.1146/annurev-biophys-030422-044448
/content/journals/10.1146/annurev-biophys-030422-044448
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error