Activated membrane patches guide chemotactic cell motility

PLoS Computational Biology

Volumn 7, Issue 6, 2011, Pages

  Hecht, Inbal ^a,b   Skoge, Monica L ^c   Charest, Pascale G ^c   Ben Jacob, Eshel ^b   Firtel, Richard A ^c   Loomis, William F ^c   Levine, Herbert ^a,d   Rappel, Wouter Jan ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; CELLS; CYTOLOGY;

CELL MOTILITY; CELL MOTION; CELL-BE; CELL/B.E; CELL/BE; ENVIRONMENTAL CUES; EUKARYOTIC CELLS; LOCALISED; MEMBRANE PATCH; SIGNALING SYSTEMS;

MEMBRANES;

RAS PROTEIN; GUANOSINE TRIPHOSPHATE;

ARTICLE; CELL MEMBRANE; CELL MOTILITY; CELL POLARITY; CELL SHAPE; CHEMOTAXIS; DICTYOSTELIUM DISCOIDEUM; MATHEMATICAL MODEL; MEMBRANE BIOLOGY; MEMBRANE COMPONENT; MEMBRANE PATCH; MICROFLUIDICS; NONHUMAN; PATCH DYNAMICS; PROTEIN LOCALIZATION; PSEUDOPODIUM; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; CELL MOTION; COMPUTER SIMULATION; CYTOLOGY; DICTYOSTELIUM; MICROFLUIDIC ANALYSIS; PHYSIOLOGY; SINGLE CELL ANALYSIS;

DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; PSEUDOPODA;

CELL MOVEMENT; CHEMOTAXIS; COMPUTER SIMULATION; DICTYOSTELIUM; GUANOSINE TRIPHOSPHATE; MICROFLUIDIC ANALYTICAL TECHNIQUES; MODELS, BIOLOGICAL; PSEUDOPODIA; RAS PROTEINS; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS;

EID: 79959836579     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002044     Document Type: Article

References (56)

1. Melchers F, Rolink AG, Schaniel C, (1999) The Role of Chemokines in Regulating Cell Migration during Humoral Immune Responses. Cell 99: 351-354.
2. Wadhams GH, Armitage JP, (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
3. Ben-Jacob E, Cohen I, Levine H, (2000) Cooperative self-organization of microorganisms. Advances in Physics 49: 395-554.
4. Shaffer BM, (1953) Aggregation in cellular slime moulds: in vitro isolation of acrasin. Nature 171: 975.
5. Newell PC, (1975) Cellular communication during aggregation of the slime mold Dictyostelium. In: Dworkin M, Shapiro L, editors. Microbiology 75 Washington, D.C. Am. Soc. Microbiol pp. 426-433.
6. Devreotes PN, Zigmond SH, (1988) Chemotaxis in eukaryotic cells: A focus on leukocytes and Dictyostelium. Annu Rev Cell Biol 4: 649-686.
7. Franca-Koh J, Kamimura Y, Devreotes P, (2006) Navigating signaling networks: chemotaxis in Dictyostelium discoideum. Curr Opin Genet Devel 16: 333-338.
8. Meier-Schellersheim M, Xu X, Angermann B, Kunkel EJ, Jin T, et al. (2006) Key role of local regulation in chemosensing revealed by a new molecular interaction-based modeling method. PLoS Comput Biol 2: e82.
9. Janetopoulos C, Ma L, Devreotes PN, Iglesias PA, (2004) Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc Natl Acad Sci USA 101: 8951-8956.
10. Rubinstein B, Jacobson K, Mogilner A, (2005) Multiscale Two-Dimensional Modeling of a Motile Simple-Shaped Cell. Multiscale Model Simul 3: 413-439.
11. Mogilner A, (2009) Mathematics of cell motility: have we got its number? J Math Biol 58: 105-134.
12. Satulovsky J, Lui R, Wang YL, (2008) Exploring the control circuit of cell migration by mathematical modeling. Biophys J 94: 3671-3683.
13. Nishimura SI, Ueda M, Sasai M, (2009) Cortical factor feedback model for cellular locomotion and cytofission. PLoS Comput Biol 5: e1000310.
14. Kruse K, Joanny JF, Julicher F, Prost J, (2006) Contractility and retrograde flow in lamellipodium motion. Phys Biol 3: 130-137.
15. Yang L, Effler JC, Kutscher BL, Sullivan SE, Robinson DN, et al. (2008) Modeling cellular deformations using the level set formalism. BMC Syst Biol 2: 68.
16. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.
17. Rappel W-J, Loomis WF, (2009) Eukaryotic chemotaxis. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 1: 141-149.
18. Bagorda A, Parent CA, (2008) Eukaryotic chemotaxis at a glance. J Cell Sci 121: 2621-2624.
19. Janetopoulos C, Firtel RA, (2008) Directional sensing during chemotaxis. FEBS Lett 582: 2075-2085.
20. Small JV, Resch GP, (2005) The comings and goings of actin: coupling protrusion and retraction in cell motility. Curr Opin Cell Biol 17: 517-523.
21. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
22. Sasaki AT, Chun C, Takeda K, Firtel RA, (2004) Localized Ras signaling at the leading edge regulates P13K, cell polarity, and directional cell movement. J Cell Biol 167: 505-518.
23. Charest PG, Firtel RA, (2006) Feedback signaling controls leading-edge formation during chemotaxis. Curr Opin Genet Dev 16: 339-347.
24. Postma M, Roelofs J, Goedhart J, Gadella TWJ, Visser AJWG, et al. (2003) Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia. Mol Biol Cell 14: 5019-5027.
25. Postma M, Roelofs J, Goedhart J, Loovers HM, Visser AJWG, et al. (2004) Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches. J Cell Sci 117: 2925-2935.
26. Sasaki AT, Janetopoulos C, Lee S, Charest PG, Takeda K, et al. (2007) G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility. J Cell Biol 178: 185-191.
27. Zhang S, Charest PG, Firtel RA, (2008) Spatiotemporal regulation of Ras activity provides directional sensing. Curr Biol 18: 1587-1593.
28. Bosgraaf L, Van Haastert PJ, (2009) The ordered extension of pseudopodia by amoeboid cells in the absence of external cues. PLoS One 4: e5253.
29. Bosgraaf L, Van Haastert PJ, (2009) Navigation of chemotactic cells by parallel signaling to pseudopod persistence and orientation. PLoS One 4: e6842.
30. Andrew N, Insall RH, (2007) Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nature Cell Biol 9: 193-200.
31. Arrieumerlou C, Meyer T, (2005) A local coupling model and compass parameter for eukaryotic chemotaxis. Dev Cell 8: 215-227.
32. Meili R, Firtel RA, (2003) Two poles and a compass. Cell 114: 153-156.
33. Buenemann M, Levine H, Rappel WJ, Sander LM, (2010) The role of cell contraction and adhesion in dictyostelium motility. Biophys J 99: 50-58.
34. Laevsky G, Knecht DA, (2001) Under-agarose folate chemotaxis of Dictyostelium discoideum amoebae in permissive and mechanically inhibited conditions. BioTechniques 31: 1140-1149.
35. Skoge M, Adler M, Groisman A, Levine H, Loomis WF, et al. (2010) Gradient sensing in defined chemotactic fields. Integr Biol (Camb) 2: 659-668.
36. Kessler DA, Koplik J, H. L, (1988) Pattern selection in fingered growth phenomena. Advances in Physics 37: 255-339.
37. Insall R, Andrew N, (2007) Chemotaxis in Dictyostelium: how to walk straight using parallel pathways. Curr Opin Microbiol 10: 578-581.
38. Kae H, Lim CJ, Spiegelman GB, Weeks G, (2004) Chemoattractant-induced Ras activation during Dictyostelium aggregation. EMBO Rep 5: 602-606.
39. Hecht I, Kessler DA, Levine H, (2010) Transient localized patterns in noise-driven reaction-diffusion systems. Phys Rev Lett 104: 158301.
40. Suel GM, Kulkarni RP, Dworkin J, Garcia-Ojalvo J, Elowitz MB, (2007) Tunability and noise dependence in differentiation dynamics. Science 315: 1716-1719.
41. Suel GM, Garcia-Ojalvo J, Liberman LM, Elowitz MB, (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440: 545-550.
42. Iglesias PA, Devreotes PN, (2008) Navigating through models of chemotaxis. Curr Op Cell Biol 20: 35-40.
43. Levine H, Kessler DA, Rappel WJ, (2006) Directional sensing in eukaryotic chemotaxis: A balanced inactivation model. Proc Natl Acad Sci USA 103: 9761-9766.
44. Fuller D, Chen W, Adler M, Groisman A, Levine H, et al. (2010) External and internal constraints on eukaryotic chemotaxis. Proc Natl Acad Sci U S A 107: 9656-9659.
45. Xiong Y, Huang CH, Iglesias PA, Devreotes PN, (2010) Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc Natl Acad Sci U S A 107: 17079-17086.
46. Swaney KF, Huang CH, Devreotes PN, (2010) Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys 39: 265-289.
47. Merkel R, Simson R, Simson DA, Hohenadl M, Boulbitch A, et al. (2000) A micromechanic study of cell polarity and plasma membrane cell body coupling in Dictyostelium. Biophys J 79: 707-719.
48. Meili R, Alonso-Latorre B, del Alamo JC, Firtel RA, Lasheras JC, (2010) Myosin II Is essential for the spatiotemporal organization of traction forces during cell motility. Mol Biol Cell 21: 405-417.
49. Bosgraaf L, Van Haastert PJ, (2009) Quimp3, an automated pseudopod-tracking algorithm. Cell Adh Migr 4: 46-55.
50. van Haastert PJ, Postma M, (2007) Biased random walk by stochastic fluctuations of chemoattractant-receptor interactions at the lower limit of detection. Biophys J 93: 1787-1796.
51. Song L, Nadkarni SM, Bodeker HU, Beta C, Bae A, et al. (2006) Dictyostelium discoideum chemotaxis: threshold for directed motion. Eur J Cell Biol 85: 981-989.
52. Wessels D, Soll DR, Knecht D, Loomis WF, De Lozanne A, et al. (1988) Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev Biol 128: 164-177.
53. Elson EL, Felder SF, Jay PY, Kolodny MS, Pasternak C, (1998) Forces and mechanical properties in cell locomotion. In: Soll DR, Wessels D, editors. Motion analysis of living cells New York Wiley-Liss pp. 67-84.
54. Parent CA, Devreotes PN, (1999) A cell's sense of direction. Science 284: 765-770.
55. Paliwal S, Iglesias PA, Campbell K, Hilioti Z, Groisman A, et al. (2007) MAPK-mediated bimodal gene expression and adaptive gradient sensing in yeast. Nature 446: 46-51.
56. Chou Y-l, (1975) Statistical analysis, with business and economic applications New York Holt, Rinehart and Winston.