Steady state distributions of moving particles in one dimension: with an eye towards axonal transport.
Intracellular cargo transport
Mitochondrial transport
Neurofilaments
Particle motion
Renewal theory
Stochastic process
Journal
Journal of mathematical biology
ISSN: 1432-1416
Titre abrégé: J Math Biol
Pays: Germany
ID NLM: 7502105
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
31
12
2023
accepted:
20
10
2024
revised:
03
07
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Axonal transport, propelled by motor proteins, plays a crucial role in maintaining the homeostasis of functional and structural components over time. To establish a steady-state distribution of moving particles, what conditions are necessary for axonal transport? This question is pertinent, for instance, to both neurofilaments and mitochondria, which are structural and functional cargoes of axonal transport. In this paper we prove four theorems regarding steady state distributions of moving particles in one dimension on a finite domain. Three of the theorems consider cases where particles approach a uniform distribution at large time. Two consider periodic boundary conditions and one considers reflecting boundary conditions. The other theorem considers reflecting boundary conditions where the velocity is space dependent. If the theoretical results hold in the complex setting of the cell, they would imply that the uniform distribution of neurofilaments observed under healthy conditions appears to require a continuous distribution of neurofilament velocities. Similarly, the spatial distribution of axonal mitochondria may be linked to spatially dependent transport velocities that remain invariant over time.
Identifiants
pubmed: 39476169
doi: 10.1007/s00285-024-02157-x
pii: 10.1007/s00285-024-02157-x
doi:
Substances chimiques
Molecular Motor Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
56Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Akhmanova A, Kapitein L (2022) Mechanisms of microtubule organization in differentiated animal cells. Nat Rev Mol Cell Biol 23(8):541–558. https://doi.org/10.1038/s41580-022-00473-y
doi: 10.1038/s41580-022-00473-y
Bomont P (2021) The dazzling rise of neurofilaments: physiological functions and roles as biomarkers. Curr Opinion Cell Biol 68:181–191. https://doi.org/10.1016/j.ceb.2020.10.011
doi: 10.1016/j.ceb.2020.10.011
Borovkov AA (2013) Probability theory, fifth edn. Universitext. Springer, London. https://doi.org/10.1007/978-1-4471-5201-9
Boyer NP, Julien JP, Jung P, Brown A (2022) Neurofilament transport is bidirectional in vivo. eNeuro. https://doi.org/10.1523/ENEURO.0138-22.2022
doi: 10.1523/ENEURO.0138-22.2022
Cason SE, Holzbaur EL (2022) Selective motor activation in organelle transport along axons. Nat Rev Mol Cell Biol 23(11):699–714. https://doi.org/10.1038/s41580-022-00491-w
doi: 10.1038/s41580-022-00491-w
Chevalier-Larsen E, Holzbaur E (2006) Axonal transport and neurodegenerative disease. Biochim Biophys Acta 1762(11–12):1094–1108. https://doi.org/10.1016/j.bbadis.2006.04.002
doi: 10.1016/j.bbadis.2006.04.002
Dallon J, Leduc C, Etienne-Manneville S, Portet S (2019) Stochastic modeling reveals how motor protein and filament properties affect intermediate filament transport. J Theor Biol 464:132–148. https://doi.org/10.1016/j.jtbi.2018.12.022
doi: 10.1016/j.jtbi.2018.12.022
Dallon JC, Leduc C, Grant CP, Evans EJ, Etienne-Manneville S, Portet S (2022) Using fluorescence recovery after photobleaching data to uncover filament dynamics. PLoS Comput Biol 18(9):1–24. https://doi.org/10.1371/journal.pcbi.1010573
doi: 10.1371/journal.pcbi.1010573
Etienne-Manneville S (2018) Cytoplasmic intermediate filaments in cell biology. Annu Rev Cell Dev Biol 34:1–28. https://doi.org/10.1146/annurev-cellbio-100617-062534
doi: 10.1146/annurev-cellbio-100617-062534
Fenn JD, Johnson CM, Peng J, Jung P, Brown A (2018) Kymograph analysis with high temporal resolution reveals new features of neurofilament transport kinetics. Cytoskeleton 75(1):22–41. https://doi.org/10.1002/cm.21411
doi: 10.1002/cm.21411
Fenn JD, Li Y, Julien JP, Jung P, Brown A (2023) The mobility of neurofilaments in mature myelinated axons of adult mice. eNeuro. https://doi.org/10.1523/ENEURO.0029-23.2023
doi: 10.1523/ENEURO.0029-23.2023
Hancock WO (2014) Bidirectional cargo transport: moving beyond tug of war. Nat Rev Mol Cell Biol 15(9):615. https://doi.org/10.1038/nrm3853
doi: 10.1038/nrm3853
Helfand BT, Chang L, Goldman RD (2003) The dynamic and motile properties of intermediate filaments. Annu Rev Cell Dev Biol 19(1):445–467. https://doi.org/10.1146/annurev.cellbio.19.111401.092306
doi: 10.1146/annurev.cellbio.19.111401.092306
Helfand BT, Chang L, Goldman RD (2004) Intermediate filaments are dynamic and motile elements of cellular architecture. J Cell Sci 117(2):133–141. https://doi.org/10.1146/annurev.cellbio.19.111401.092306
doi: 10.1146/annurev.cellbio.19.111401.092306
Helfand BT, Loomis P, Yoon M, Goldman RD (2003) Rapid transport of neural intermediate filament protein. J Cell Sci 116(11):2345–2359. https://doi.org/10.1242/jcs.00526
doi: 10.1242/jcs.00526
Hoffman PN (1995) Review: the synthesis, axonal transport, and phosphorylation of neurofilaments determine axonal caliber in myelinated nerve fibers. Neuroscientist 1(2):76–83. https://doi.org/10.1177/107385849500100204
doi: 10.1177/107385849500100204
Koppers M, Farías GG (2021) Organelle distribution in neurons: logistics behind polarized transport. Curr Opinion Cell Biol 71:46–54. https://doi.org/10.1016/j.ceb.2021.02.004
doi: 10.1016/j.ceb.2021.02.004
Leduc C, Etienne-Manneville S (2017) Regulation of microtubule-associated motors drives intermediate filament network polarization. J Cell Biol 216(6):1689–1703. https://doi.org/10.1083/jcb.201607045
doi: 10.1083/jcb.201607045
Mogre SS, Brown AI, Koslover EF (2020) Getting around the cell: physical transport in the intracellular world. Phys Biol 17(6):061003. https://doi.org/10.1088/1478-3975/aba5e5
doi: 10.1088/1478-3975/aba5e5
Nowier RM, Friedman A, Brown A, Jung P (2023) The role of neurofilament transport in the radial growth of myelinated axons. Mol Biol Cell 34(6):ar58. https://doi.org/10.1091/mbc.E22-12-0565
doi: 10.1091/mbc.E22-12-0565
Portet S, Etienne-Manneville S, Leduc C, Dallon J (2022) Impact of noise on the regulation of intracellular transport of intermediate filaments. J Theor Biol 547:111183. https://doi.org/10.1016/j.jtbi.2022.111183
doi: 10.1016/j.jtbi.2022.111183
Portet S, Leduc C, Etienne-Manneville S, Dallon J (2019) Deciphering the transport of elastic filaments by antagonistic motor proteins. Phys Rev E 99(4):042414. https://doi.org/10.1103/PhysRevE.99.042414
doi: 10.1103/PhysRevE.99.042414
Robert A, Hookway C, Gelfand VI (2016) Intermediate filament dynamics: what we can see now and why it matters. BioEssays 38(3):232–243. https://doi.org/10.1002/bies.201500142
doi: 10.1002/bies.201500142
Saxton WM, Hollenbeck PJ (2012) The axonal transport of mitochondria. J Cell Sci 125(9):2095–2104. https://doi.org/10.1242/jcs.053850
doi: 10.1242/jcs.053850
Sleigh JN, Rossor AM, Fellows AD, Tosolini A, Schiavo G (2019) Axonal transport and neurological disease. Nat Rev Neurol 15(12):691–703. https://doi.org/10.1038/s41582-019-0257-2
doi: 10.1038/s41582-019-0257-2
Smith WL (1953) II. asymptotic renewal theorems. In: Proceedings of the royal society of Edinburgh section a: mathematics 64(1):9–48. https://doi.org/10.1017/S0080454100007305
Uchida A, Peng J, Brown A (2023) Regulation of neurofilament length and transport by a dynamic cycle of phospho-dependent polymer severing and annealing. Mol Biol Cell 34(7):ar68. https://doi.org/10.1091/mbc.E23-01-0024
doi: 10.1091/mbc.E23-01-0024
Walker CL, Uchida A, Li Y, Trivedi N, Fenn JD, Monsma PC, Lariviére RC, Julien JP, Jung P, Brown A (2019) Local acceleration of neurofilament transport at nodes of Ranvier. J Neurosci 39(4):663–677. https://doi.org/10.1523/JNEUROSCI.2272-18.2018
doi: 10.1523/JNEUROSCI.2272-18.2018
Williams D (1991) Probability with martingales. Cambridge Mathematical Textbooks. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511813658
Wu C, Yin H, Fu S, Yoo H, Zhang M, Park H (2024) Altered anterograde axonal transport of mitochondria in cultured striatal neurons of a knock-in mouse model of Huntington’s disease. Biochem Biophys Res Commun 691:149246. https://doi.org/10.1016/j.bbrc.2023.149246
doi: 10.1016/j.bbrc.2023.149246