Chemotaxis of a model organism: Progress with Dictyostelium

Current Opinion in Cell Biology

Volumn 36, Issue , 2015, Pages 7-12

  Nichols, John M E ^a,b   Veltman, Douwe ^a   Kay, Robert R ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITIDE; PIP3 PROTEIN; PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; PHOSPHATIDYLINOSITOL;

ACTIN FILAMENT; ADAPTATION; CELL ELONGATION; CELL FUNCTION; CELL MEMBRANE; CELL MOTILITY; CELL STIMULATION; CHEMOTAXIS; DICTYOSTELIUM; MUTATION; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEOMICS; PSEUDOPODIUM; REVIEW; SIGNAL PROCESSING; SIGNAL TRANSDUCTION; CYTOLOGY; METABOLISM;

DICTYOSTELIUM; MAMMALIA;

ACTIN CYTOSKELETON; ADAPTATION, PHYSIOLOGICAL; CHEMOTAXIS; DICTYOSTELIUM; PHOSPHATIDYLINOSITOLS; SIGNAL TRANSDUCTION;

EID: 84937026947     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.06.005     Document Type: Review

References (51)

1. Artemenko Y., Lampert T.J., Devreotes P.N. Moving towards a paradigm: common mechanisms of chemotactic signaling in Dictyostelium and mammalian leukocytes. Cell Mol Life Sci 2014, 71:3711-3747.
2. Kay R.R., Langridge P., Traynor D., Hoeller O. Changing directions in the study of chemotaxis. Nat Rev Mol Cell Biol 2008, 9:455-463.
3. Zatulovskiy E., Tyson R., Bretschneider T., Kay R.R. Bleb-driven chemotaxis of Dictyostelium cells. J Cell Biol 2014, 204:1027-1044.
4. Howe J.D., Barry N.P., Bretscher M.S. How do amoebae swim and crawl?. PLoS One 2013, 8:e74382.
5. Tyson R.A., Zatulovskiy E., Kay R.R., Bretschneider T. How blebs and pseudopods cooperate during chemotaxis. Proc Natl Acad Sci U S A 2014, 111:11703-11708.
6. Tweedy L., Meier B., Stephan J., Heinrich D., Endres R.G. Distinct cell shapes determine accurate chemotaxis. Sci Rep 2013, 3:2606.
7. Bastounis E., Meili R., Alvarez-Gonzalez B., Francois J., del Alamo J.C., Firtel R.A., Lasheras J.C. Both contractile axial and lateral traction force dynamics drive amoeboid cell motility. J Cell Biol 2014, 204:1045-1061.
8. Alvarez-Gonzalez B., Meili R., Bastounis E., Firtel R.A., Lasheras J.C., Del Alamo J.C. Three-dimensional balance of cortical tension and axial contractility enables fast amoeboid migration. Biophys J 2015, 108:821-832.
9. Dang I., Gorelik R., Sousa-Blin C., Derivery E., Guerin C., Linkner J., Nemethova M., Dumortier J.G., Giger F.A., Chipysheva T.A., et al. Inhibitory signalling to the Arp2/3 complex steers cell migration. Nature 2013, 503:281-284.
10. Veltman D.M., King J.S., Machesky L.M., Insall R.H. SCAR knockouts in Dictyostelium: WASP assumes SCAR's position and upstream regulators in pseudopods. J Cell Biol 2012, 198:501-508.
11. Ura S., Pollitt A.Y., Veltman D.M., Morrice N.A., Machesky L.M., Insall R.H. Pseudopod growth and evolution during cell movement is controlled through SCAR/WAVE dephosphorylation. Curr Biol 2012, 22:553-561.
12. Wang Y., Senoo H., Sesaki H., Iijima M. Rho GTPases orient directional sensing in chemotaxis. Proc Natl Acad Sci U S A 2013, 110:4723-4732.
13. Para A., Krischke M., Merlot S., Shen Z., Oberholzer M., Lee S., Briggs S., Firtel R.A. Dictyostelium Dock180-related RacGEFs regulate the actin cytoskeleton during cell motility. Mol Biol Cell 2009, 20:699-707.
14. Pakes N.K., Veltman D.M., Rivero F., Nasir J., Insall R., Williams R.S. The Rac GEF ZizB regulates development, cell motility and cytokinesis in Dictyostelium. J Cell Sci 2012, 125:2457-2465.
15. Westendorf C., Negrete J., Bae A.J., Sandmann R., Bodenschatz E., Beta C. Actin cytoskeleton of chemotactic amoebae operates close to the onset of oscillations. Proc Natl Acad Sci U S A 2013, 110:3853-3858.
16. Gerisch G. Self-organizing actin waves that simulate phagocytic cup structures. PMC Biophys 2010, 3:7.
17. Gerhardt M., Ecke M., Walz M., Stengl A., Beta C., Gerisch G. Actin and PIP3 waves in giant cells reveal the inherent length scale of an excited state. J Cell Sci 2014, 127:4507-4517.
18. Huang C.H., Tang M., Shi C., Iglesias P.A., Devreotes P.N. An excitable signal integrator couples to an idling cytoskeletal oscillator to drive cell migration. Nat Cell Biol 2013, 15:1307-1316.
19. McRobbie S.J., Newell P.C. Changes in actin associated with cytoskeleton following chemotactic stimulation of Dictyostelium discoideum. Biochem Biophys Res Commun 1983, 115:351-359.
20. Sobczyk G.J., Wang J., Weijer C.J. SILAC-based proteomic quantification of chemoattractant-induced cytoskeleton dynamics on a second to minute timescale. Nat Commun 2014, 5:3319.
21. Luo T., Mohan K., Iglesias P.A., Robinson D.N. Molecular mechanisms of cellular mechanosensing. Nat Mater 2013, 12:1064-1071.
22. Filic V., Marinovic M., Faix J., Weber I. A dual role for Rac1 GTPases in the regulation of cell motility. J Cell Sci 2012, 125:387-398.
23. Lemieux M.G., Janzen D., Hwang R., Roldan J., Jarchum I., Knecht D.A. Visualization of the actin cytoskeleton: different F-actin-binding probes tell different stories. Cytoskeleton 2014, 71:157-169.
24. Hoeller O., Gong D., Weiner O.D. How to understand and outwit adaptation. Dev Cell 2014, 28:607-616.
25. Shi C., Huang C.H., Devreotes P.N., Iglesias P.A. Interaction of motility, directional sensing, and polarity modules recreates the behaviors of chemotaxing cells. PLoS Comput Biol 2013, 9:e1003122.
26. Gerhardt M., Walz M., Beta C. Signaling in chemotactic amoebae remains spatially confined to stimulated membrane regions. J Cell Sci 2014, 127:5115-5125.
27. Nakajima A., Ishihara S., Imoto D., Sawai S. Rectified directional sensing in long-range cell migration. Nat Commun 2014, 5:5367.
28. Skoge M., Yue H., Erickstad M., Bae A., Levine H., Groisman A., Loomis W.F., Rappel W.J. Cellular memory in eukaryotic chemotaxis. Proc Natl Acad Sci U S A 2014, 111:14448-14453.
29. Tang M., Wang M., Shi C., Iglesias P.A., Devreotes P.N., Huang C.H. Evolutionarily conserved coupling of adaptive and excitable networks mediates eukaryotic chemotaxis. Nat Commun 2014, 5:5175.
30. Devreotes P.N., Sherring J.A. Kinetics and concentration dependence of reversible cAMP-induced modification of the surface cAMP receptor in Dictyostelium. J Biol Chem 1985, 260:6378-6384.
31. Kim J.Y., Soede R.D., Schaap P., Valkema R., Borleis J.A., Van H.P., Devreotes P.N., Hereld D. Phosphorylation of chemoattractant receptors is not essential for chemotaxis or termination of G-protein-mediated responses. J Biol Chem 1997, 272:27313-27318.
32. Brzostowski J.A., Sawai S., Rozov O., Liao X.H., Imoto D., Parent C.A., Kimmel A.R. Phosphorylation of chemoattractant receptors regulates chemotaxis, actin reorganization and signal relay. J Cell Sci 2013, 126:4614-4626.
33. Liao X.H., Buggey J., Lee Y.K., Kimmel A.R. Chemoattractant stimulation of TORC2 is regulated by receptor/G protein-targeted inhibitory mechanisms that function upstream and independently of an essential GEF/Ras activation pathway in Dictyostelium. Mol Biol Cell 2013, 24:2146-2155.
34. Cao X., Yan J., Shu S., Brzostowski J.A., Jin T. Arrestins function in cAR1 GPCR-mediated signaling and cAR1 internalization in the development of Dictyostelium discoideum. Mol Biol Cell 2014, 25:3210-3221.
35. Kataria R., Xu X., Fusetti F., Keizer-Gunnink I., Jin T., van Haastert P.J., Kortholt A. Dictyostelium Ric8 is a nonreceptor guanine exchange factor for heterotrimeric G proteins and is important for development and chemotaxis. Proc Natl Acad Sci U S A 2013, 110:6424-6429.
36. Yan J., Mihaylov V., Xu X., Brzostowski J.A., Li H., Liu L., Veenstra T.D., Parent C.A., Jin T. A Gbetagamma effector, ElmoE, transduces GPCR signaling to the actin network during chemotaxis. Dev Cell 2012, 22:92-103.
37. Clark J., Kay R.R., Kielkowska A., Niewczas I., Fets L., Oxley D., Stephens L.R., Hawkins P.T. Dictyostelium uses ether-linked inositol phospholipids for intracellular signalling. EMBO J 2014, 33:2188-2200.
38. Parent C.A., Blacklock B.J., Froelich W.M., Murphy D.B., Devreotes P.N. G Protein signaling events are activated at the leading edge of chemotactic cells. Cell 1998, 95:81-91.
39. Srinivasan K., Wright G.A., Hames N., Housman M., Roberts A., Aufderheide K.J., Janetopoulos C. Delineating the core regulatory elements crucial for directed cell migration by examining folic-acid-mediated responses. J Cell Sci 2013, 126:221-233.
40. Hoeller O., Bolourani P., Clark J., Stephens L.R., Hawkins P.T., Weiner O.D., Weeks G., Kay R.R. Two distinct functions for PI3-kinases in macropinocytosis. J Cell Sci 2013, 126:4296-4307.
41. Nishikawa M., Horning M., Ueda M., Shibata T. Excitable signal transduction induces both spontaneous and directional cell asymmetries in the phosphatidylinositol lipid signaling system for eukaryotic chemotaxis. Biophys J 2014, 106:723-734.
42. Chen C.L., Wang Y., Sesaki H., Iijima M. Myosin I links PIP3 signaling to remodeling of the actin cytoskeleton in chemotaxis. Sci Signal 2012, 5:ra10.
43. Fets L., Nichols J.M., Kay R.R. A PIP5 kinase essential for efficient chemotactic signaling. Curr Biol 2014, 24:415-421.
44. Kortholt A., Keizer-Gunnink I., Kataria R., Van Haastert P.J. Ras activation and symmetry breaking during Dictyostelium chemotaxis. J Cell Sci 2013, 126:4502-4513.
45. Chattwood A., Bolourani P., Weeks G. RasG signaling is important for optimal folate chemotaxis in Dictyostelium. BMC Cell Biol 2014, 15:13.
46. Kolsch V., Shen Z., Lee S., Plak K., Lotfi P., Chang J., Charest P.G., Romero J.L., Jeon T.J., Kortholt A., et al. Daydreamer, a Ras effector and GSK-3 substrate, is important for directional sensing and cell motility. Mol Biol Cell 2013, 24:100-114.
47. Bloomfield G., Traynor D., Sander S.P., Veltman D., Pachebat J.A., Kay R.R. Neurofibromin controls macropinocytosis and phagocytosis in Dictyostelium. eLife 2015, 4:e04940.
48. Veltman D.M., Lemieux M.G., Knecht D.A., Insall R.H. PIP3-dependent macropinocytosis is incompatible with chemotaxis. J Cell Biol 2014, 204:497-505.
49. Sugden C., Urbaniak M.D., Araki T., Williams J.G. The Dictyostelium prestalk inducer differentiation-inducing factor-1 (DIF-1) triggers unexpectedly complex global phosphorylation changes. Mol Biol Cell 2015, 26:805-820.
50. Cai H., Katoh-Kurasawa M., Muramoto T., Santhanam B., Long Y., Li L., Ueda M., Iglesias P.A., Shaulsky G., Devreotes P.N. Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. Science 2014, 343:1249531.
51. Corrigan A.M., Chubb J.R. Regulation of transcriptional bursting by a naturally oscillating signal. Curr Biol 2014, 24:205-211.