Excitable signal transduction induces both spontaneous and directional cell asymmetries in the phosphatidylinositol lipid signaling system for eukaryotic chemotaxis

Biophysical Journal

Volumn 106, Issue 3, 2014, Pages 723-734

  Nishikawa, Masatoshi ^a,b   Hörning, Marcel ^a   Ueda, Masahiro ^b,c,d   Shibata, Tatsuo ^a,b  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c RIKEN   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5-TRIPHOSPHATE; POLYPHOSPHOINOSITIDE;

ARTICLE; CHEMOTAXIS; DICTYOSTELIUM; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CHEMOTAXIS; DICTYOSTELIUM; PHOSPHATIDYLINOSITOL PHOSPHATES; SIGNAL TRANSDUCTION;

EID: 84893435383     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.12.023     Document Type: Article

References (48)

1. P.R. Fisher, R. Merkl, and G. Gerisch Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum by using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients J. Cell Biol. 108 1989 973 984
2. M. Ueda, and T. Shibata Stochastic signal processing and transduction in chemotactic response of eukaryotic cells Biophys. J. 93 2007 11 20
3. L. Song, and S.M. Nadkarni E. Bodenschatz Dictyostelium discoideum chemotaxis: threshold for directed motion Eur. J. Cell Biol. 85 2006 981 989
4. D. Fuller, and W. Chen W.F. Loomis External and internal constraints on eukaryotic chemotaxis Proc. Natl. Acad. Sci. USA 107 2010 9656 9659
5. F. Wang The signaling mechanisms underlying cell polarity and chemotaxis Cold Spring Harb. Perspect. Biol. 1 2009 a002980
6. L. Stephens, L. Milne, and P. Hawkins Moving towards a better understanding of chemotaxis Curr. Biol. 18 2008 R485 R494
7. A. Kortholt, and R. Kataria P.J. Van Haastert Dictyostelium chemotaxis: essential Ras activation and accessory signalling pathways for amplification EMBO Rep. 12 2011 1273 1279
8. L. Bosgraaf, I. Keizer-Gunnink, and P.J. Van Haastert PI3-kinase signaling contributes to orientation in shallow gradients and enhances speed in steep chemoattractant gradients J. Cell Sci. 121 2008 3589 3597
9. P.J. van Haastert, I. Keizer-Gunnink, and A. Kortholt Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis J. Cell Biol. 177 2007 809 816
10. O. Hoeller, and R.R. Kay Chemotaxis in the absence of PIP3 gradients Curr. Biol. 17 2007 813 817
11. C. Janetopoulos, and L. Ma P.A. Iglesias Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton Proc. Natl. Acad. Sci. USA 101 2004 8951 8956
12. Y. Arai, and T. Shibata M. Ueda Self-organization of the phosphatidylinositol lipids signaling system for random cell migration Proc. Natl. Acad. Sci. USA 107 2010 12399 12404
13. M. Postma, and J. Roelofs P.J. Van Haastert Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia Mol. Biol. Cell 14 2003 5019 5027
14. M. Postma, and J. Roelofs P.J. Van Haastert Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches J. Cell Sci. 117 2004 2925 2935
15. A.T. Sasaki, and C. Janetopoulos R.A. Firtel G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility J. Cell Biol. 178 2007 185 191
16. C. Arrieumerlou, and T. Meyer A local coupling model and compass parameter for eukaryotic chemotaxis Dev. Cell 8 2005 215 227
17. M.C. Weiger, and C.C. Wang J.M. Haugh Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts J. Cell Sci. 122 2009 313 323
18. G. Gerisch, and M. Ecke B. Schroth-Diez Different modes of state transitions determine pattern in the phosphatidylinositide-actin system BMC Cell Biol. 12 2011 42
19. O.D. Weiner, and W.A. Marganski M.W. Kirschner An actin-based wave generator organizes cell motility PLoS Biol. 5 2007 e221
20. H. Meinhardt Orientation of chemotactic cells and growth cones: models and mechanisms J. Cell Sci. 112 1999 2867 2874
21. M.G. Vicker Reaction-diffusion waves of actin filament polymerization/depolymerization in Dictyostelium pseudopodium extension and cell locomotion Biophys. Chem. 84 2000 87 98
22. Y. Xiong, and C.-H. Huang P.N. Devreotes Cells navigate with a local-excitation, global-inhibition-biased excitable network Proc. Natl. Acad. Sci. USA 107 2010 17079 17086
23. T. Shibata, and M. Nishikawa M. Ueda Modeling the self-organized phosphatidylinositol lipid signaling system in chemotactic cells using quantitative image analysis J. Cell Sci. 125 2012 5138 5150
24. I. Hecht, D.A. Kessler, and H. Levine Transient localized patterns in noise-driven reaction-diffusion systems Phys. Rev. Lett. 104 2010 158301
25. C.J. Wang, and A. Bergmann A. Levchenko Diverse sensitivity thresholds in dynamic signaling responses by social amoebae Sci. Signal. 5 2012 ra17
26. H.R. Bourne, and O. Weiner A chemical compass Nature 419 2002 21
27. D.J. Watts, and J.M. Ashworth Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture Biochem. J. 119 1970 171 174
28. M.J. Sato, and M. Ueda M. Ueda Input-output relationship in galvanotactic response of Dictyostelium cells Biosystems 88 2007 261 272
29. C. Beta, and D. Wyatt E. Bodenschatz Flow photolysis for spatiotemporal stimulation of single cells Anal. Chem. 79 2007 3940 3944
30. X. Xu, and M. Meier-Schellersheim T. Jin Quantitative imaging of single live cells reveals spatiotemporal dynamics of multistep signaling events of chemoattractant gradient sensing in Dictyostelium Mol. Biol. Cell 16 2005 676 688
31. X. Xu, and M. Meier-Schellersheim T. Jin Locally controlled inhibitory mechanisms are involved in eukaryotic GPCR-mediated chemosensing J. Cell Biol. 178 2007 141 153
32. A. Samadani, J. Mettetal, and A. van Oudenaarden Cellular asymmetry and individuality in directional sensing Proc. Natl. Acad. Sci. USA 103 2006 11549 11554
33. A.L. Hodgkin, and A.F. Huxley A quantitative description of membrane current and its application to conduction and excitation in nerve J. Physiol. 117 1952 500 544
34. E.M. Izhikevich Dynamical Systems in Neuroscience 2010 MIT Press Cambridge, MA
35. A. Loewer, and E. Batchelor G. Lahav Basal dynamics of p53 reveal transcriptionally attenuated pulses in cycling cells Cell 142 2010 89 100
36. C.A. Parent, and B.J. Blacklock P.N. Devreotes G protein signaling events are activated at the leading edge of chemotactic cells Cell 95 1998 81 91
37. K.F. Swaney, C.H. Huang, and P.N. Devreotes Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity Annu. Rev. Biophys. 39 2010 265 289
38. D. Taniguchi, and S. Ishihara S. Sawai Phase geometries of two-dimensional excitable waves govern self-organized morphodynamics of amoeboid cells Proc. Natl. Acad. Sci. USA 110 2013 5016 5021
39. K. Takeda, and D. Shao R.A. Firtel Incoherent feedforward control governs adaptation of activated ras in a eukaryotic chemotaxis pathway Sci. Signal. 5 2012 ra2
40. R. Kataria, and X. Xu A. Kortholt Dictyostelium Ric8 is a nonreceptor guanine exchange factor for heterotrimeric G proteins and is important for development and chemotaxis Proc. Natl. Acad. Sci. USA 110 2013 6424 6429
41. C. Janetopoulos, and R.A. Firtel Directional sensing during chemotaxis FEBS Lett. 582 2008 2075 2085
42. C. Shi, and C.-H. Huang P.A. Iglesias Interaction of motility, directional sensing, and polarity modules recreates the behaviors of chemotaxing cells PLOS Comput. Biol. 9 2013 e1003122
43. T. Killich, and P.J. Plath M.G. Vicker The locomotion, shape and pseudopodial dynamics of unstimulated Dictyostelium cells are not random J. Cell Sci. 106 1993 1005 1013
44. R. Krahe, and F. Gabbiani Burst firing in sensory systems Nat. Rev. Neurosci. 5 2004 13 23
45. P. Tiesinga, J.-M. Fellous, and T.J. Sejnowski Regulation of spike timing in visual cortical circuits Nat. Rev. Neurosci. 9 2008 97 107
46. G.M. Süel, and J. Garcia-Ojalvo M.B. Elowitz An excitable gene regulatory circuit induces transient cellular differentiation Nature 440 2006 545 550
47. T. Kalmar, and C. Lim A. Martinez Arias Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells PLoS Biol. 7 2009 e1000149
48. L. Cai, C.K. Dalal, and M.B. Elowitz Frequency-modulated nuclear localization bursts coordinate gene regulation Nature 455 2008 485 490