The role of membrane stiffness and actin turnover on the force exerted by DRG lamellipodia

Biophysical Journal

Volumn 102, Issue 11, 2012, Pages 2451-2460

  Amin, Ladan ^a   Ercolini, Erika ^a,b   Shahapure, Rajesh ^a   Migliorini, Elisa ^b,c   Torre, Vincent ^a,d  

^a SISSA   (Italy)

^b Cluster in Biomedicine   (Italy)

^c IOM CNR LABORATORIO TASC   (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYCLODEXTRIN; DEPSIPEPTIDE; JASPAMIDE;

ANIMAL; ARTICLE; BIOMECHANICS; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; METABOLISM; PHYSIOLOGY; PSEUDOPODIUM; RAT; SPINAL GANGLION; WISTAR RAT; YOUNG MODULUS;

ACTINS; ANIMALS; BIOMECHANICS; CELL MEMBRANE; CYCLODEXTRINS; DEPSIPEPTIDES; ELASTIC MODULUS; GANGLIA, SPINAL; PSEUDOPODIA; RATS; RATS, WISTAR;

EID: 84861850381     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.04.036     Document Type: Article

References (45)

1. D.J. Solecki, E.E. Govek, and M.E. Hatten mPar6 α controls neuronal migration J. Neurosci. 26 2006 10624 10625
2. H.T. Ghashghaei, C. Lai, and E.S. Anton Neuronal migration in the adult brain: are we there yet? Nat. Rev. Neurosci. 8 2007 141 151
3. C.S. Goodman Mechanisms and molecules that control growth cone guidance Annu. Rev. Neurosci. 19 1996 341 377
4. H.J. Song, and M.M. Poo The cell biology of neuronal navigation Nat. Cell Biol. 3 2001 E81 E88
5. A.K. Mongiu, E.L. Weitzke, O.Y. Chaga, and G.G. Borisy Kinetic-structural analysis of neuronal growth cone veil motility J. Cell. Sci. 120 2007 1113 1125
6. A. Mogilner, and G. Oster Cell motility driven by actin polymerization 25 Biophys. J. 71 1996 3030 3045
7. T.D. Pollard, and G.G. Borisy Cellular motility driven by assembly and disassembly of actin filaments Cell 112 2003 453 465
8. C.W. Pak, K.C. Flynn, and J.R. Bamburg Actin-binding proteins take the reins in growth cones Nat. Rev. Neurosci. 9 2008 136 147
9. J. Howard Mechanics of Motor Proteins and the Cytoskeleton 2001 Sinauer Associates Sunderland, MA
10. D. Raucher, and M.P. Sheetz Cell spreading and lamellipodial extension rate is regulated by membrane tension J. Cell Biol. 148 2000 127 136
11. D.A. Fletcher, and J.A. Theriot An introduction to cell motility for the physical scientist Phys. Biol. 1 2004 T1 T10
12. C.S. Peskin, G.M. Odell, and G.F. Oster Cellular motions and thermal fluctuations - the Brownian ratchet Biophys. J. 65 1993 316 324
13. A. Mogilner, and G. Oster Force generation by actin polymerization II: the elastic ratchet and tethered filaments 26 Biophys. J. 84 2003 1591 1605
14. A.E. Carlsson Growth velocities of branched actin networks Biophys. J. 84 2003 2907 2918
15. A. Mogilner On the edge: modeling protrusion Curr. Opin. Cell Biol. 18 2006 32 39
16. S. Ilangumaran, and D.C. Hoessli Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane Biochem. J. 335 1998 433 440
17. E.J. Westover, D.F. Covey, H.L. Brockman, R.E. Brown, and L.J. Pike Cholesterol depletion results in site-specific increases in epidermal growth factor receptor phosphorylation due to membrane level effects - studies with cholesterol enantiomers J. Biol. Chem. 278 2003 51125 51133
18. D.A. Brown, and E. London Structure and function of sphingolipid- and cholesterol-rich membrane rafts J. Biol. Chem. 275 2000 17221 17224
19. D.H. Jones, K.R. Barber, E.W. VanDerLoo, and C.W.M. Grant Epidermal growth factor receptor transmembrane domain: H-2 NMR implications for orientation and motion in a bilayer environment Biochemistry 37 1998 16780 16787
20. K. Simons, and E. Ikonen Cell biology - how cells handle cholesterol Science 290 2000 1721 1726
21. T.D. Pollard, L. Blanchoin, and R.D. Mullins Molecular mechanisms controlling actin filament dynamics in nonmuscle cells Annu. Rev. Biophys. Biomol. Struct. 29 2000 545 576
22. M.R. Bubb, I. Spector, B.B. Beyer, and K.M. Fosen Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations J. Biol. Chem. 275 2000 5163 5170
23. C.A. Wilson, and M.A. Tsuchida J.A. Theriot Myosin II contributes to cell-scale actin network treadmilling through network disassembly Nature 465 2010 373 377
24. D. Cojoc, and F. Difato V. Torre Properties of the force exerted by filopodia and lamellipodia and the involvement of cytoskeletal components PLoS ONE 2 2007 e1072
25. R. Shahapure, and F. Difato V. Torre Force generation in lamellipodia is a probabilistic process with fast growth and retraction events Biophys. J. 98 2010 979 988
26. L. Amin, E. Ercolini, R. Shahapure, G. Bisson, and V. Torre The elementary events underlying force generation in neuronal lamellipodia Sci. Rep. 1 2011 153
27. H. Hertz Ueber die Berührung fester elastischer Körper J. Reine. Angew. Math. 92 1881 156 171
28. C. Rotsch, K. Jacobson, and M. Radmacher Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy Proc. Natl. Acad. Sci. USA 96 1999 921 926
29. E.K. Dimitriadis, F. Horkay, J. Maresca, B. Kachar, and R.S. Chadwick Determination of elastic moduli of thin layers of soft material using the atomic force microscope Biophys. J. 82 2002 2798 2810
30. K.C. Neuman, and S.M. Block Optical trapping Rev. Sci. Instrum. 75 2004 2787 2809
31. S. Felder, and E.L. Elson Mechanics of fibroblast locomotion - quantitative-analysis of forces and motions at the leading lamellas of fibroblasts J. Cell Biol. 111 1990 2513 2526
32. B. Daily, E.L. Elson, and G.I. Zahalak Cell poking. Determination of the elastic area compressibility modulus of the erythrocyte membrane Biophys. J. 45 1984 671 682
33. C. Odaka, M.L. Sanders, and P. Crews Jasplakinolide induces apoptosis in various transformed cell lines by a caspase-3-like protease-dependent pathway Clin. Diagn. Lab. Immunol. 7 2000 947 952
34. C. Rotsch, and M. Radmacher Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study Biophys. J. 78 2000 520 535
35. M. Edidin The state of lipid rafts: from model membranes to cells Annu. Rev. Biophys. Biomol. Struct. 32 2003 257 283
36. S.J. Potocnik, N. Jenkins, T.V. Murphy, and M.A. Hill Membrane cholesterol depletion with beta-cyclodextrin impairs pressure-induced contraction and calcium signalling in isolated skeletal muscle arterioles J. Vasc. Res. 44 2007 292 302
37. F.J. Byfield, H. Aranda-Espinoza, V.G. Romanenko, G.H. Rothblat, and I. Levitan Cholesterol depletion increases membrane stiffness of aortic endothelial cells Biophys. J. 87 2004 3336 3343
38. E.L. Elson, and E. Fried G.M. Genin Phase separation in biological membranes: integration of theory and experiment Ann. Rev. Biophys. 39 2010 207 226
39. C. Roduit, and F.G. van der Goot S. Kasas Elastic membrane heterogeneity of living cells revealed by stiff nanoscale membrane domains Biophys. J. 94 2008 1521 1532
40. V.M. Laurent, and S. Kasas J.J. Meister Gradient of rigidity in the lamellipodia of migrating cells revealed by atomic force microscopy Biophys. J. 89 2005 667 675
41. L. Cardamone, and A. Laio A. DeSimone Cytoskeletal actin networks in motile cells are critically self-organized systems synchronized by mechanical interactions Proc. Natl. Acad. Sci. USA 108 2011 13978 13983
42. M. Prass, K. Jacobson, A. Mogilner, and M. Radmacher Direct measurement of the lamellipodial protrusive force in a migrating cell J. Cell Biol. 174 2006 767 772
43. S.H. Parekh, O. Chaudhuri, J.A. Theriot, and D.A. Fletcher Loading history determines the velocity of actin-network growth 28 Nat. Cell Biol. 7 2005 1219 1223
44. V.C. Abraham, V. Krishnamurthi, D.L. Taylor, and F. Lanni The actin-based nanomachine at the leading edge of migrating cells Biophys. J. 77 1999 1721 1732
45. V. Okreglak, and D.G. Drubin Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway J. Cell Biol. 188 2010 769 777