Cost-benefit analysis of the mechanisms that enable migrating cells to sustain motility upon changes in matrix environments

Journal of the Royal Society Interface

Volumn 12, Issue 106, 2015, Pages

  Tozluoglu, Melda ^a,b   Mao, Yanlan ^a   Bates, Paul A ^b   Sahai, Erik ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Adaptation to extracellular matrix; Cancer cell motility; Cell extracellular matrix adhesion feedback; Plasma membrane blebbing; Plasticity of motility

Indexed keywords

ADHESION; CELL MEMBRANES; COST BENEFIT ANALYSIS; COST EFFECTIVENESS; CYTOLOGY; FEEDBACK; GEOMETRY; PROTEINS;

BIOCHEMICAL PROPERTIES; CANCER CELLS; COMPUTATIONAL MODEL; CONFINED ENVIRONMENT; EXTRACELLULAR ENVIRONMENTS; EXTRACELLULAR MATRICES; FEEDBACK MECHANISMS; MEMBRANE BLEBBING;

CELLS;

ACTIN;

ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CELL STRUCTURE; COST BENEFIT ANALYSIS; EXTRACELLULAR MATRIX; FOCAL ADHESION; PLASTICITY; POSITIVE FEEDBACK; REGULATORY MECHANISM; ADAPTATION; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; CELL PLASTICITY; COMPUTER SIMULATION; ECOSYSTEM; HUMAN; MECHANOTRANSDUCTION; PHYSIOLOGY; RADIATION RESPONSE;

ADAPTATION, PHYSIOLOGICAL; ALGORITHMS; ANIMALS; CELL ADHESION; CELL MOVEMENT; CELL PLASTICITY; COMPUTER SIMULATION; ECOSYSTEM; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL;

EID: 84929493059     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.1355     Document Type: Article

References (43)

1. Charras G, Sahai E. 2014 Physical influences of the extracellular environment on cell migration. Nat. Rev. Mol. Cell Biol. 15, 813-824. (doi:10.1038/nrm3897)
2. Tozluoglu M, Tournier AL, Jenkins RP, Hooper S, Bates PA, Sahai E. 2013 Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions. Nat. Cell Biol. 15, 751-762. (doi:10.1038/ncb2775)
3. Friedl P, Wolf K. 2010 Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188, 11-19. (doi:10.1083/jcb.200909003)
4. Lämmermann T, Germain R. 2014 The multiple faces of leukocyte interstitial migration. Semin. Immunopathol. 36, 227-251. (doi:10.1007/s00281-014-0418-8)
5. Madsen CD, Sahai E. 2010 Cancer dissemination: lessons from leukocytes. Dev. Cell 19, 13-26. (doi:10.1016/j.devcel.2010.06.013)
6. Otto A, Collins-Hooper H, Patel A, Dash PR, Patel K. 2011 Adult skeletal muscle stem cell migration is mediated by a blebbing/amoeboid mechanism. Rejuvenation Res. 14, 249-260. (doi:10.1089/rej. 2010.1151)
7. Choquet D, Felsenfeld DP, Sheetz MP. 1997 Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48. (doi:10.1016/S0092-8674(00)81856-5)
8. Galbraith C, Yamada K, Sheetz M. 2002 The relationship between force and focal complex development. J. Cell Biol. 159, 695-705. (doi:10. 1083/jcb.200204153)
9. Lorentzen A, Bamber J, Sadok A, Elson-Schwab I, Marshall CJ. 2011 An ezrin-rich, rigid uropod-like structure directs movement of amoeboid blebbing cells. J. Cell Sci. 124, 1256-1267. (doi:10.1242/jcs.074849)
10. del Pozo MA, Nieto M, Serrador JM, Sancho D, Vicente-Manzanares M, Martínez-A C, Sànchez-Madrid F. 1998 The two poles of the lymphocyte: specialized cell compartments for migration and recruitment. Cell Adhes. Commun. 6, 125-133. (doi:10.3109/15419069809004468)
11. Soriano S, Hons M, Schumann K, Kumar V, Dennier TJ, Lyck R, Sixt M, Stein JV. 2011 In vivo analysis of uropod function during physiological T cell trafficking. J. Immunol. 187, 2356-2364. (doi:10.4049/jimmunol.1100935)
12. Asokan S, Johnson HE, Rahman A, King SJ, Rotty JD, Lebedeva IP, Haugh JM, Bear JE. 2015 Mesenchymal chemotaxis requires selective inactivation of myosin II at the leading edge via a noncanonical PLCγ/PKCα pathway. Dev. Cell 31, 747-760. (doi:10.1016/j.devcel.2014.10.024)
13. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, Sahai E, Marshall CJ. 2008 Rac activation and inactivation control plasticity of tumor cell movement. Cell 135, 510-523. (doi:10.1016/j.cell.2008.09.043)
14. Croft DR et al. 2004 Conditional ROCK activation in vivo induces tumor cell dissemination and angiogenesis. Cancer Res. 64, 8994-9001. (doi:10.1158/0008-5472.CAN-04-2052)
15. Charras G et al. 2005 Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435, 365-369. (doi:10.1038/nature03550)
16. Bergert M, Chandradoss SD, Desai RA, Paluch E. 2012 Cell mechanics control rapid transitions between blebs and lamellipodia during migration. Proc. Natl Acad. Sci. USA 109, 14 434-14 439. (doi:10.1073/pnas.1207968109)
17. Oakes PW, Gardel ML. 2014 Stressing the limits of focal adhesion mechanosensitivity. Curr. Opin. Cell Biol. 30C, 68-73. (doi:10.1016/j.ceb.2014.06.003)
18. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, Sheetz MP. 2006 Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015-1026. (doi:10.1016/j.cell.2006.09.044)
19. Yao M et al. 2014 Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci. Rep. 4, 4610. (doi:10.1038/srep04610)
20. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009 Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641. (doi:10.1126/science.1162912)
21. Fouchard J, Bimbard C, Bufi N, Durand-Smet P, Proag A, Richert A, Cardoso O, Asnacios A. 2014 Three-dimensional cell body shape dictates the onset of traction force generation and growth of focal adhesions. Proc. Natl Acad. Sci. 111, 13 075-13 080. (doi:10.1073/pnas.1411785111)
22. Lämmermann T, Sixt M. 2009 Mechanical modes of 'amoeboid' cell migration. Curr. Opin. Cell Biol. 21, 636-644. (doi:10.1016/j.ceb.2009.05.003)
23. Starborg T et al. 2008 Extracellular matrix and cell junctions: electron microscopy of collagen fibril structure in vitro and in vivo including threedimensional reconstruction. In Introduction to electron microscopy for biologists (ed. T Allen), pp. 319-345. New York, NY: Elsevier.
24. Tyson RA, Zatulovskiy E, Kay RR, Bretschneider T. 2014 How blebs and pseudopods cooperate during chemotaxis. Proc. Natl Acad. Sci. USA 111, 11 703-11 708. (doi:10.1073/pnas.1322291111)
25. Zatulovskiy E, Tyson R, Bretschneider T, Kay RR. 2014 Bleb-driven chemotaxis of Dictyostelium cells. J. Cell Biol. 204, 1027-1044. (doi:10.1083/jcb.201306147)
26. Madsen C et al. 2015 STRIPAK components determine mode of cancer cell migration and metastasis. Nat. Cell Biol. 17, 68-80. (doi:10.1038/ncb3083)
27. Deakin N, Turner C. 2011 Distinct roles for paxillin and Hic-5 in regulating breast cancer cell morphology, invasion, and metastasis. Mol. Biol. Cell 22, 327-341. (doi:10.1091/mbc.E10-09-0790)
28. Strychalski W, Guy R. 2013 A computational model of bleb formation. Math. Med. Biol. 30, 115-130. (doi:10.1093/imammb/dqr030)
29. Woolley T, Gaffney EA, Oliver JM, Baker RE, Waters SL, Goriely A. 2014 Cellular blebs: pressure-driven, axisymmetric, membrane protrusions. Biomech. Model. Mechanobiol. 13, 463-476. (doi:10.1007/s10237-013-0509-9)
30. Woolley T, Gaffney EA, Waters SL, Oliver JM, Baker RE, Goriely A. 2014 Three mechanical models for blebbing and multi-blebbing. IMA J. Appl. Math. 79, 636-660. (doi:10.1093/imamat/hxu028)
31. Charras G, Coughlin M, Mitchison TJ, Mahadevan L. 2008 Life and times of a cellular bleb. Biophys. J. 94, 1836-1853. (doi:10.1529/biophysj.107.113605)
32. Tinevez J-Y, Schulze U, Salbreux G, Roensch J, Joanny J-F, Paluch E. 2009 Role of cortical tension in bleb growth. Proc. Natl Acad. Sci. USA 106, 18 581-18 586. (doi:10.1073/pnas.0903353106)
33. Mogilner A, Rubinstein B. 2005 The physics of filopodial protrusion. Biophys. J. 89, 782-795. (doi:10.1529/biophysj.104.056515)
34. Schaus T, Borisy G. 2008 Performance of a population of independent filaments in lamellipodial protrusion. Biophys. J. 95, 1393-1411. (doi:10.1529/biophysj.107.125005)
35. Novak I, Slepchenko B, Mogilner A. 2008 Quantitative analysis of G-actin transport in motile cells. Biophys. J. 95, 1627-1638. (doi:10.1529/biophysj.108.130096)
36. Schlüter D, Ramis-Conde I, Chaplain M. 2012 Computational modeling of single-cell migration: the leading role of extracellular matrix fibers. Biophys. J. 103, 1141-1151. (doi:10.1016/j.bpj.2012.07.048)
37. Zaman M, Kamm RD, Matsudaira P, Lauffenburger DA. 2005 Computational model for cell migration in three-dimensional matrices. Biophys. J. 89, 1389-1397. (doi:10.1529/biophysj.105.060723)
38. McDougall S, Dallon J, Sherratt J, Maini P. 2006 Fibroblast migration and collagen deposition during dermal wound healing: mathematical modelling and clinical implications. Phil. Trans. R. Soc. A 364, 1385-1405. (doi:10.1098/rsta.2006.1773)
39. Hawkins RJ, Piel M, Faure-Andre G, Lennon-Dumenil A, Joanny J, Prost J, Voituriez R. 2009 Pushing off the walls: a mechanism of cell motility in confinement. Phys. Rev. Lett. 102, 058103. (doi:10. 1103/PhysRevLett.102.058103)
40. Danuser G, Allard J, Mogilner A. 2013 Mathematical modeling of eukaryotic cell migration: insights beyond experiments. Annu. Rev. Cell Dev. Biol. 29, 501-528. (doi:10.1146/annurev-cellbio-101512-122308)
41. Neilson M, Veltman DM, van Haastert PJM, Webb SD, Mackenzie JA, Insall RH. 2011 Chemotaxis: a feedback-based computational model robustly predicts multiple aspects of real cell behaviour. PLoS Biol. 9, e1000618. (doi:10.1371/journal.pbio.1000618)
42. Marée A, Jilkine A, Dawes A, Grieneisen VA, Edelstein-Keshet L. 2006 Polarization and movement of keratocytes: a multiscale modelling approach. Bull. Math. Biol. 68, 1169-1211. (doi:10.1007/s11538-006-9131-7)
43. Painter KJ. 2009 Modelling cell migration strategies in the extracellular matrix. J. Math. Biol. 58, 511-543. (doi:10.1007/s00285-008-0217-8)