Two Tails of Motility in Cells. Andrea J. Liu Department of Physics & Astronomy University of Pennsylvania
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1 Two Tails of Motility in Cells Andrea J. Liu Department of Physics & Astronomy University of Pennsylvania Kun-Chun Lee Edward Banigan Gareth Alexander Zemer Gitai Ned Wingreen Biophysics, UC Davis Physics, UPenn Physics, UPenn Biology, Princeton Biology, Princeton
2 Self-Assembly-Driven Motility Neutrophil chasing Staphylococcus aurea David Rogers, Vanderbilt Univ, research/cell_migration/ neutrophil.html Courtesy of T. M. Svitkina, G.G. Borisy Xenopus keratocytes How does self-assembly of actin into branched networks lead to motion? Kun-Chun Lee, Ed Banigan
3 Disassembly-Driven Motility Courtesy of C. W. Shebelut, J. M. Guberman, Z. Gitai Caulobacter crescentus How does the chromosome move across the cell during chromosomal segregation in certain asymmetric bacteria? Ed Banigan, Zemer Gitai, Ned Wingreen
4 Actin Polymerization and Depolymerization G-actin F-actin Molecular Cell Biology, Lodish et al Chen, Bernstein, Bamberg, Trends Biochem. Sci, 25, 19 (2000). A 3µm long filament turns over in 1 min in vivo ATP hydrolysis provides polarity to filament growth
5 How are Growing Ends Localized at Leading Edge? T. M. Svitkina, G. G. Borisy, J. Cell Biol. 145, 1009 (1999). Arp2/3 complex binds to F-actin and nucleates new branches
6 Dendritic Nucleation Model: Participating Proteins T. D. Pollard, L. Blanchoin, R. D. Mullins, Ann. Rev. Biophys. Biomol. Struct. 29, (2000)
7 Actin and Listeria Motility CDC Life cycle of Listeria monocytogenes Uses actin polymerization to move! Same physics as cell crawling
8 How Listeria Spreads from Cell to Cell Speeded up x900 Speeded up x150 Courtesy of Julie Theriot, Without proteins that generate comet tail, Listeria can
9 In vitro Realizations Courtesy of J. Theriot, cmgm.stanford.edu/ theriot/ x60 sphere Schwartz, Ehrenberg, Bindschadler, McGrath, Curr. Biol. 14, 1094 (2004) x1800 disk L. A. Cameron, T. M. Svitkina, D. Vignjevic, J. A. Theriot, G. G. Borisy, Current Biology, 11, 130 (2001). Actin comet tail has branchy structure similar to that of lamellipodium
10 Minimal Ingredients for Motility All you need is Actin and buffer w/atp Arp2/3 makes new growing ends Capping protein kills them off ADF/cofilin severs filaments Profilin converts ADP-G-actin to ATP-G-actin Bead coated with ActA,VCA, activates arp2/3 How does self-assembly into a branched structure lead to motility? Loisel, Boujemaa, Pantaloni, Carlier, Nature, 401, 613 (1999).
11 Brownian Dynamics Simulations Polymerization at + end (k + ) Depolymerization at - end (k - ) K. C. Lee and A. J. Liu, Biophys. J. 95, 4529 (2008). Branching (k a ) Debranching (k d ) Capping
12 We See Motility! 2D projection of 3D simulation Motion allowed in ±z direction, only K. C. Lee and A. J. Liu, Biophys. J. 95, 4529 (2008).
13 Newton s Third Law F = F tail disk ς tail vtail = ς disk vdisk v disk = ς tail ς disk vtail >1 Center of drag is stationary Center of mass can move
14 Problem with Accepted Mechanism Courtesy of S. Kuo A. Mogilner and G. Oster, Biophys J., 84, 1591 (2003). Stiff/flexible: 60+%/ 5% of force from tips At low viscosity, speed is independent of filament stiffness! Mechanism cannot depend on whether force comes from tips
15 Disk activates Arp2/3, which recruits F-actin Origin of Motility Concentration of F-actin high behind the disk compared to average disk If disk repels actin, then disk will move forwards to avoid F-actin Courtesy of J. Theriot In real system, concentration gradient is K. C. Lee and A. J. Liu, Biophys. J. 95, 4529 (2008).
16 BUT: Tail is Attached to Disk N-WASP/ActA contain binding sites for actin Same protein that activates Arp2/3 also binds actin to surface H. Boukellal, O. Campas, J.-F. Joanny, J. Prost, C. Sykes, PRE 69, (2004).
17 Include Filament Binding to Disk Some sites on disk have attraction ε to filament tips V(r,ψ ) = ε σ σ 14 r r 12 cos4 ψ Specific binding of filaments to the disk does not destroy motility E. Banigan
18 New Proposed Mechanism for Actin Motility Why do bagpipe players always walk while they play? To get away from the noise. K. C. Lee and A. J. Liu, Biophys. J. 95, 4529 (2008), Biophys. J. 97, 1295 (2009).
19 Chromosomal Segregation in Caulobacter Courtesy of C. W. Shebelut, J. M. Guberman, Z. Gitai Caulobacter crescentus
20 Asymmetric Cell Division Most cells divide symmetrically Caulobacter crescentus and Vibrio cholerae divide asymmetrically What is the mechanism for chromosomal motility?
21 Chromosomal Segregation in C. crescentus and V. Courtesy of C. W. Shebelut, J. M. Guberman, Z. Gitai Caulobacter crescentus We are interested in 4th stage How does the chromosome (ori) scoot across the cell?
22 Vibrio cholerae Courtesy of Popular Logistics
23 A Closer Look at Process replication ParB on origin attaches to ParA origin 2 origin 1 terminus origin 1 ori2/parb ParA ParA disassembles and ori moves origin and terminus switch places Origin is decorated with ParB which binds to and hydrolyzes ParA ParA filament structure depolymerizes and drags ParB along
24 Simulation Model
25 We See Translocation
26 How Robust is This Mechanism? v = ak d eff Speed given by where a is size of ParA monomer eff and k d is net depolymerization rate But if k d eff is too high, chromosome falls off For robust motility, need k d eff < τ relax -1 (relaxation time of chromosome)
27 Concentration Gradient Drives Motion System uses depolymerization to create steady-state
28 PARTICLE MOTION IN A CONCENTRATION GRADIENT Diffusiophoresis Actin-polymerization-driven motility arises from repulsions between particle (Listeria bacterium) and A (actin) ParA/ParB-driven-chromosomal segregation arises from attraction between particle (ParB) and A (ParA)
29 Self-Diffusiophoresis But there is no externally-imposed gradient of actin or ParA! In Listeria, bacterium activates actin polymerization to create its own actin concentration gradient In ParA case, ParB-decorated chromosome in Caulobacter uses ParA depolymerization to create its own ParA gradient
30 Self-Diffusiophoresis is Very General Golestanian, Liverpool, Ajdari, PRL 94, (2005). Coat Janus colloids with Pt and put in H 2 O 2 solution H 2 O 2 H 2 O O 2 Howse, et al. PRL 99, (2007). D eff = D V 2 τ R Diffusion enhanced by propulsion velocity V
31 PARTICLE MOTION IN A CONCENTRATION GRADIENT Self-diffusiophoresis occurs in a fluid Motion involves a balance between diffusion and advection G. Alexander
32 Simple Model spherical particle, radius a single solute species, concentration c reaction occurs in a patch surface interaction V, range δ<<a assume steady state motion
33 Boundary Layer Solute is pushed away from surface by interaction It carries fluid with it More fluid is pushes away where there is more solute This gives rise to flow at the boundary layer --> slip velocity This slip velocity propels particle
34 COMPARISON Self-diffusiophoresis at high and low Peclet number
35 Summary Physical mechanism underlying actin-polymerization-driven motility and chromosomal translocation in Caulobacter is self-diffusiophoresis But since branched actin network and ParA bundle do not diffuse; this is a new regime of self-diffusiophoresis, dominated by advection, not diffusion This affects the resulting motion profoundly Only two steady-state scenarios repulsive producer (actin-driven motility) attractive consumer (ParAB-driven motility)
36 Final Remarks Self-diffusiophoresis is the simplest form of chemotaxis Maybe it isn t surprising that it is exploited in cells Physicists tend to think mostly about systems in equilibrium Most many-body phenomena in the world occur far from equilibrium Simple, undiscovered, far-from-equilibrium mechanisms still abound! Kun-Chun Lee, Ed Banigan, Gareth Alexander, Zemer Gitai, Ned Wingreen
37 Curie Model F. Gerbal, P. Chaikin, Y. Rabin and J. Prost, Biophys. J. 79, 2259 (2000) Main ingredient is competition between compressive (forwards) stresses and tensile (backwards) stresses Compressive stresses put in by hand Actin comet tail is assumed to be elastic medium F-v relation from dep. of polymerization rate on stress BUT Motility is observed even in absence of crosslinkers
38 Comparison with Previous Simulations e.g. Alberts & Odell, PLOS Biology, 2, 2054 (2004). Realistic rates Realistic numbers of filaments BUT Monomers only exist when they are in filaments; artificial mass transfer gives rise to motility as an artifact Artificial forces used to avoid Our work Physically-consistent model Don t violate important physical principles BUT Depolymerization rate is too high [G-actin] is too high Filament stiffness is too low
39 Simulation Model
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