On the generation of force required for actin-based motility.
Actin-based motility
Chemo-transport-mechanics
Continuum mechanics
Finite elements
High performance computing
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
08 Aug 2024
08 Aug 2024
Historique:
received:
27
02
2024
accepted:
05
08
2024
medline:
9
8
2024
pubmed:
9
8
2024
entrez:
8
8
2024
Statut:
epublish
Résumé
The fundamental question of how forces are generated in a motile cell, a lamellipodium, and a comet tail is the subject of this note. It is now well established that cellular motility results from the polymerization of actin, the most abundant protein in eukaryotic cells, into an interconnected set of filaments. We portray this process in a continuum mechanics framework, claiming that polymerization promotes a mechanical swelling in a narrow zone around the nucleation loci, which ultimately results in cellular or bacterial motility. To this aim, a new paradigm in continuum multi-physics has been designed, departing from the well-known theory of Larché-Cahn chemo-transport-mechanics. In this note, we set up the theory of network growth and compare the outcomes of numerical simulations with experimental evidence.
Identifiants
pubmed: 39117762
doi: 10.1038/s41598-024-69422-3
pii: 10.1038/s41598-024-69422-3
doi:
Substances chimiques
Actins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18384Informations de copyright
© 2024. The Author(s).
Références
Borisy, G. G. & Svitkina, T. M. Actin machinery: Pushing the envelope. Curr. Opin. Cell Biol. 12(1), 104–112 (2000).
pubmed: 10679366
doi: 10.1016/S0955-0674(99)00063-0
Pantaloni, D., Le Clainche, C. & Carlier, M.-F. Mechanism of actin-based motility. Science 292(5521), 1502–1506 (2001).
pubmed: 11379633
doi: 10.1126/science.1059975
Blanchoin, L., Boujemaa-Paterski, R., Sykes, C. & Plastino, J. Actin dynamics, architecture, and mechanics in cell motility. Physiol. Rev. 94(1), 235–263 (2014).
pubmed: 24382887
doi: 10.1152/physrev.00018.2013
Marston, D. J. & Goldstein, B. Actin-based forces driving embryonic morphogenesis in caenorhabditis elegans. Curr. Opin. Genet. Dev. 16(4), 392–398 (2006).
pubmed: 16782324
doi: 10.1016/j.gde.2006.06.002
Barrasa-Ramos, S., Dessalles, C., Hautefeuille, M. & Barakat A. Mechanical regulation of the early stages of angiogenesis. J. R. Soc. Interface19(20220360) (2022).
Stuelten, C. H., Parent, C. A. & Montell, D. J. Cell motility in cancer invasion and metastasis: Insights from simple model organisms. Nat. Rev. Cancer 18(5), 296–312 (2018).
pubmed: 29546880
pmcid: 6790333
doi: 10.1038/nrc.2018.15
Acharya, D. et al. Actin cytoskeleton remodeling primes RIG-I-like receptor activation. Cell 185(19), 3588–360221 (2022).
pubmed: 36113429
pmcid: 9680832
doi: 10.1016/j.cell.2022.08.011
Dos Remedios, C. G. & Thomas, D. D. (eds) Molecular Interactions of Actin: Actin-Myosin Interaction and Actin-Based Regulation (Springer, Berlin, 2001).
Cameron, L. A., Giardini, P. A., Soo, F. S. & Theriot, J. A. Secrets of actin-based motility revealed by a bacterial pathogen. Nat. Rev. Mol. Cell Bio. 1(2), 110–119 (2000).
doi: 10.1038/35040061
Choe, J. E. & Welch, M. D. Actin-based motility of bacterial pathogens: Mechanistic diversity and its impact on virulence. Pathog. Dis. 74(8), ftw0919 (2016).
doi: 10.1093/femspd/ftw099
Kühn, S. & Enninga, J. The actin comet guides the way: How listeria actin subversion has impacted cell biology, infection biology and structural biology. Cell Microbiol. 22(4), e13190 (2020).
pubmed: 32185894
doi: 10.1111/cmi.13190
Svitkina, T. The actin cytoskeleton and actin-based motility. Csh. Perspect. Biol. 10(1), a018267 (2018).
Marchand, J. B. et al. Actin-based movement of Listeria monocytogenes: Actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J. Cell Biol. 130(2), 331–343 (1995).
pubmed: 7615635
doi: 10.1083/jcb.130.2.331
Hu, L. & Papoian, G. A. Mechano-chemical feedbacks regulate actin mesh growth in lamellipodial protrusions. Biophys. J. 98(8), 1375–1384 (2010).
pubmed: 20409456
pmcid: 2856144
doi: 10.1016/j.bpj.2009.11.054
Ni, H. & Papoian, G. A. Membrane-medyan: Simulating deformable vesicles containing complex cytoskeletal networks. J. Phys. Chem. B 125(38), 10710–10719 (2021).
pubmed: 34461720
doi: 10.1021/acs.jpcb.1c02336
Carlsson, A. E. Growth of branched actin networks against obstacles. Biophys. J . 81(4), 1907–1923 (2001).
pubmed: 11566765
pmcid: 1301666
doi: 10.1016/S0006-3495(01)75842-0
Carlsson, A. E. Growth velocities of branched actin networks. Biophys. J . 84(5), 2907–2918 (2003).
pubmed: 12719223
pmcid: 1302854
doi: 10.1016/S0006-3495(03)70018-6
Lin, Y., Shenoy, V. B., Hu, B. & Bai, L. A microscopic formulation for the actin-driven motion of listeria in curved paths. Biophys. J. 99(4), 1043–1052 (2010).
pubmed: 20712987
pmcid: 2920721
doi: 10.1016/j.bpj.2010.06.001
John, K., Caillerie, D. & Misbah, C. Spontaneous polarization in an interfacial growth model for actin filament networks with a rigorous mechanochemical coupling. Phys. Rev. E 90, 052706 (2014).
doi: 10.1103/PhysRevE.90.052706
John, K., Peyla, P., Kassner, K., Prost, J. & Misbah, C. Nonlinear study of symmetry breaking in actin gels: Implications for cellular motility. Phys. Rev. Lett. 100, 068101 (2008).
pubmed: 18352520
doi: 10.1103/PhysRevLett.100.068101
Mogilner, A. & Oster, G. Force generation by actin polymerization II: The elastic ratchet and tethered filaments. Biophys. J . 84(3), 1591–1605 (2003).
pubmed: 12609863
pmcid: 1302730
doi: 10.1016/S0006-3495(03)74969-8
Gerbal, F., Chaikin, P., Rabin, Y. & Prost, J. An elastic analysis of listeria monocytogenes propulsion. Biophys. J . 79(5), 2259–2275 (2000).
pubmed: 11053107
pmcid: 1301115
doi: 10.1016/S0006-3495(00)76473-3
Egan, P., Sinko, R., LeDuc, P. R. & Keten, S. The role of mechanics in biological and bio-inspired systems. Nat. Commun. 6(1), 7418 (2015).
pubmed: 26145480
doi: 10.1038/ncomms8418
Gong, B., Wei, X., Qian, J. & Lin, Y. Modeling and simulations of the dynamic behaviors of actin-based cytoskeletal networks. ACS Biomater. Sci. Eng. 5(8), 3720–3734 (2019).
pubmed: 33405887
doi: 10.1021/acsbiomaterials.8b01228
Gurtin, M. E., Fried, E. & Anand, L. The Mechanics and Thermodynamics of Continua (Cambridge University Press, Cambridge, 2010).
doi: 10.1017/CBO9780511762956
Humphrey, J. D. Constrained mixture models of soft tissue growth and remodeling—twenty years after. J. Elasticity 145(1–2), 49–75 (2021).
doi: 10.1007/s10659-020-09809-1
Humphrey, J. D. & Rajagopal, K. R. A constrained mixture model for growth and remodeling of soft tissues. Math. Mod. Meth. Appl. S 12, 407–430 (2002).
doi: 10.1142/S0218202502001714
Kimpton, L. S., Whiteley, J. P., Waters, S. L., King, J. R. & Oliver, J. M. Multiple travelling-wave solutions in a minimal model for cell motility. Math. Med. Bio. 30(3), 241–272 (2012).
doi: 10.1093/imammb/dqs023
Kimpton, L. S., Whiteley, J. P., Waters, S. L. & Oliver, J. M. On a poroviscoelastic model for cell crawling. J. Math. Biol. 70(1), 133–171 (2015).
pubmed: 24509816
doi: 10.1007/s00285-014-0755-1
Parekh, S. H., Chaudhuri, O., Theriot, J. A. & Fletcher, D. A. Loading history determines the velocity of actin-network growth. Nat. Cell Biol. 7(12), 1219–1223 (2005).
pubmed: 16299496
doi: 10.1038/ncb1336
Higgs, H. Getting down to basics with actin. Nat. Cell Biol. 3(8), E189–E189 (2001).
doi: 10.1038/35087135
Noireaux, V. et al. Growing an actin gel on spherical surfaces. Biophys. J . 278, 1643–1654 (2000).
doi: 10.1016/S0006-3495(00)76716-6
Kuo, S. C. & McGrath, J. L. Steps and fluctuations of listeria monocytogenes during actin-based motility. Nature 407, 1026–1029 (2000).
pubmed: 11069185
doi: 10.1038/35039544
Salvadori, A., McMeeking, R. M., Grazioli, D. & Magri, M. A coupled model of transport-reaction-mechanics with trapping. Part I-small strain analysis. J. Mech. Phys. Solids 114, 1–30 (2018).
doi: 10.1016/j.jmps.2018.02.006
Arricca, M. et al. A coupled model of transport-reaction-mechanics with trapping, Part II: large strain analysis. J. Mech. Phys. Solids 181, 105425 (2023).
doi: 10.1016/j.jmps.2023.105425
Bonanno, C., Serpelloni, M., Arricca, M., McMeeking, R. M. & Salvadori, A. Actin based motility unveiled: How chemical energy is converted into motion. J. Mech. Phys. Solids 175, 105273 (2023).
doi: 10.1016/j.jmps.2023.105273
Theriot, J. A. The polymerization motor. Traffic 1(1), 19–28 (2000).
pubmed: 11208055
doi: 10.1034/j.1600-0854.2000.010104.x
Deshpande, V. S., McMeeking, R. M. & Evans, A. G. A bio-chemo-mechanical model for cell contractility. PNAS 103(45), 17064–17065 (2006).
Serpelloni, M., Arricca, M., Bonanno, C. & Salvadori, A. Modeling cells spreading, motility, and receptors dynamics: A general framework. Acta Mech. Sin. 37(6), 1013–1030 (2021).
doi: 10.1007/s10409-021-01088-w
Anand, L. A Cahn–Hilliard-type theory for species diffusion coupled with large elastic-plastic deformations. J. Mech. Phys. Solids 60(12), 1983–2002 (2012).
doi: 10.1016/j.jmps.2012.08.001
McGrath, J. L. et al. The force-velocity relationship for the actin-based motility of listeria monocytogenes. Curr. Biol. 13(4), 329–332 (2003).
pubmed: 12593799
doi: 10.1016/S0960-9822(03)00051-4
Marcy, Y., Prost, J., Carlier, M. F. & Sykes, C. Forces generated during actin-based propulsion: A direct measurement by micromanipulation. PNAS 101(16), 5992–5997 (2004).
pubmed: 15079054
pmcid: 395911
doi: 10.1073/pnas.0307704101
Holzapfel, G. Nonlinear Solid Mechanics: A Continuum Approach for Engineering (Wiley, Hoboken, 2001).
Aroush, D.R.-B. et al. Actin turnover in lamellipodial fragments. Curr. Biol. 27(19), 2963-29731.e4 (2017).
pmcid: 5679493
doi: 10.1016/j.cub.2017.08.066
Kiuchi, T., Nagai, T., Ohashi, K. & Mizuno, K. Measurements of spatiotemporal changes in G-actin concentration reveal its effect on stimulus-induced actin assembly and lamellipodium extension. J. Cell Biol. 193(2), 365–380 (2011).
pubmed: 21502360
pmcid: 3080261
doi: 10.1083/jcb.201101035
Mogilner, A. & Oster, G. Cell motility driven by actin polymerization. Biophys. J . 71(6), 3030–3045 (1996).
pubmed: 8968574
pmcid: 1233792
doi: 10.1016/S0006-3495(96)79496-1
Quirion, F. & Gicquaud, C. Changes in molar volume and heat capacity of actin upon polymerization. Biochem. J. 295(3), 671–672 (1993).
pubmed: 8240275
pmcid: 1134611
doi: 10.1042/bj2950671
Damioli, V., Salvadori, A., Beretta, G. P., Ravelli, C. & Mitola, S. Multi-physics interactions drive VEGFR2 relocation on endothelial cells. Sci. Rep.-UK 7(1), 16700 (2017).
doi: 10.1038/s41598-017-16786-4
Kiana Naghibzadeh, S., Walkington, N. & Dayal, K. Surface growth in deformable solids using an Eulerian formulation. J. Mech. Phys. Solids 154, 104499 (2021).
doi: 10.1016/j.jmps.2021.104499
Abeyaratne, R., Puntel, E. & Tomassetti, G. Treadmilling stability of a one-dimensional actin growth model. Int. J. Solids Struct. 198, 87–98 (2020).
doi: 10.1016/j.ijsolstr.2020.04.009
Arndt, D. et al. The deal.II library, version 9.5. J. Numer. Math. 31(3), 231–246 (2023).
doi: 10.1515/jnma-2023-0089
Gerbal, F. et al. Measurement of the elasticity of the actin tail of listeria monocytogenes. Eur. Biophys. J. 29(2), 134–140 (2000).
pubmed: 10877022
doi: 10.1007/s002490050258
Kocks, C., Hellio, R., Gounon, P., Ohayon, H. & Cossart, P. Polarized distribution of Listeria monocytogenes surface protein Acta at the site of directional actin assembly. J. Cell Sci. 105(3), 699–710 (1993).
pubmed: 8408297
doi: 10.1242/jcs.105.3.699
Kawska, A. et al. How actin network dynamics control the onset of actin-based motility. PNAS 109, 14440–14445 (2012).
pubmed: 22908255
pmcid: 3437907
doi: 10.1073/pnas.1117096109
Svitkina, T. M. & Borisy, G. G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145(5), 1009–1026 (1999).
pubmed: 10352018
pmcid: 2133125
doi: 10.1083/jcb.145.5.1009
Hodge, N. & Papadopoulos, P. Continuum modeling and numerical simulation of cell motility. J. Math. Biol. 64(7), 1253–1279 (2012).
pubmed: 21710139
doi: 10.1007/s00285-011-0446-0
Serpelloni, M., Arricca, M., Bonanno, C. & Salvadori, A. Chemo-transport-mechanics in advecting membranes. Int. J. Eng. Sci. 181, 103746. https://doi.org/10.1016/j.ijengsci.2022.103746 (2022}.
Weichsel, J. & Schwarz, U. S. Two competing orientation patterns explain experimentally observed anomalies in growing actin networks. PNAS 107(14), 6304–6309 (2010).
pubmed: 20308581
pmcid: 2852010
doi: 10.1073/pnas.0913730107
Schreiber, C., Amiri, B., Heyn, J. C. J., Rädler, J. O. & Falcke, M. On the adhesion-velocity relation and length adaptation of motile cells on stepped fibronectin lanes. PNAS 118(4), e2009959118 (2021).
pubmed: 33483418
pmcid: 7869109
doi: 10.1073/pnas.2009959118
Doyle, A. D., Sykora, D. J., Pacheco, G. G., Kutys, M. L. & Yamada, K. M. 3D mesenchymal cell migration is driven by anterior cellular contraction that generates an extracellular matrix Prestrain. Dev. Cell 56(6), 826–841 (2021).
pubmed: 33705692
pmcid: 8082573
doi: 10.1016/j.devcel.2021.02.017
Shenoy, V. B., Tambe, D. T., Prasad, A. & Theriot, J. A. A kinematic description of the trajectories of listeria monocytogenes propelled by actin comet tails. PNAS 104(20), 8229–8234 (2007).
pubmed: 17485664
pmcid: 1895934
doi: 10.1073/pnas.0702454104