Navigating signaling networks: chemotaxis in Dictyostelium discoideum

Current Opinion in Genetics and Development

Volumn 16, Issue 4, 2006, Pages 333-338

  Franca Koh, Jonathan ^a   Kamimura, Yoichiro ^a   Devreotes, Peter ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT;

AMOEBA; CELL ACTIVITY; CELL MIGRATION; CELL POLARITY; CHEMOTAXIS; DICTYOSTELIUM DISCOIDEUM; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

ANIMALS; CELL POLARITY; CHEMOTAXIS; DICTYOSTELIUM; PSEUDOPODIA; SIGNAL TRANSDUCTION;

DICTYOSTELIUM DISCOIDEUM; PSEUDOPODA;

EID: 33745632621     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.06.001     Document Type: Review

References (30)

1. Manahan C.L., Iglesias P.A., Long Y., and Devreotes P.N. Chemoattractant signaling in Dictyostelium discoideum. Annu Rev Cell Dev Biol 20 (2004) 223-253
2. Funamoto S., Meili R., Lee S., Parry L., and Firtel R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109 (2002) 611-623
3. Huang Y.E., Iijima M., Parent C.A., Funamoto S., Firtel R.A., and Devreotes P. Receptor-mediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. Mol Biol Cell 14 (2003) 1913-1922
4. Iijima M., Huang Y.E., and Devreotes P. Temporal and spatial regulation of chemotaxis. Dev Cell 3 (2002) 469-478
5. Sasaki A.T., Chun C., Takeda K., and Firtel R.A. Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement. J Cell Biol 167 (2004) 505-518. The authors analyze Ras and PI3K activation at the leading edge and suggest the possibility of an actin polymerization-dependent positive feedback loop.
6. Janetopoulos C., Ma L., Devreotes P.N., and Iglesias P.A. 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
7. Schneider I.C., and Haugh J.M. Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts. J Cell Biol 171 (2005) 883-892. Through careful quantification of PH domain localization in living cells, this study demonstrates that, in contrast to D. discoideum and neutrophils, fibroblasts are unable to amplify the steepness of the extracellular gradient. Consistent with the local excitation-global inhibition model, the lack of amplification can be explained by the observation that fibroblasts do not adapt to constant, uniformly distributed stimulation.
8. Xu X., Meier-Schellersheim M., Jiao X., Nelson L.E., and Jin T. 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
9. Devreotes P., and Janetopoulos C. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J Biol Chem 278 (2003) 20445-20448. A detailed discussion of models that have been proposed to account for chemotaxis was beyond the scope of this current review. Readers are directed to this review of the field.
10. Iijima M., Huang Y.E., Luo H.R., Vazquez F., and Devreotes P.N. Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J Biol Chem 279 (2004) 16606-16613
11. Vazquez F., Matsuoka S., Sellers W.R., Yanagida T., Ueda M., and Devreotes P.N. Tumor suppressor PTEN acts through dynamic interaction with the plasma membrane. Proc Natl Acad Sci USA 103 (2006) 3633-3638
12. Chen L., Janetopoulos C., Huang Y.E., Iijima M., Borleis J., and Devreotes P.N. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol Biol Cell 14 (2003) 5028-5037
13. Wessels D., Srikantha T., Yi S., Kuhl S., Aravind L., and Soll D.R. The Shwachman-Bodian-Diamond syndrome gene encodes an RNA-binding protein that localizes to the pseudopod of Dictyostelium amoebae during chemotaxis. J Cell Sci 119 (2006) 370-379
14. Myers S.A., Han J.W., Lee Y., Firtel R.A., and Chung C.Y. A Dictyostelium homologue of WASP is required for polarized F-actin assembly during chemotaxis. Mol Biol Cell 16 (2005) 2191-2206
15. Ibarra N., Blagg S.L., Vazquez F., and Insall R.H. Nap1 regulates Dictyostelium cell motility and adhesion through SCAR-dependent and -independent pathways. Curr Biol 16 (2006) 717-722
16. Blagg S.L., Stewart M., Sambles C., and Insall R.H. PIR121 regulates pseudopod dynamics and SCAR activity in Dictyostelium. Curr Biol 13 (2003) 1480-1487
17. Park K.C., Rivero F., Meili R., Lee S., Apone F., and Firtel R.A. Rac regulation of chemotaxis and morphogenesis in Dictyostelium. EMBO J 23 (2004) 4177-4189
18. Meili R., Ellsworth C., Lee S., Reddy T.B., Ma H., and Firtel R.A. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J 18 (1999) 2092-2105
19. Lee S., Comer F.I., Sasaki A., McLeod I.X., Duong Y., Okumura K., Yates III J.R., Parent C.A., and Firtel R.A. TOR complex 2 integrates cell movement during chemotaxis and signal relay in Dictyostelium. Mol Biol Cell 16 (2005) 4572-4583. This study demonstrates that the Tor2 complex is conserved in D. discoideum and that the constituent proteins play roles in regulating chemotaxis and in PKB activity.
20. Comer F.I., Lippincott C.K., Masbad J.J., and Parent C.A. The PI3K-mediated activation of CRAC independently regulates adenylyl cyclase activation and chemotaxis. Curr Biol 15 (2005) 134-139
21. Heid P.J., Geiger J., Wessels D., Voss E., and Soll D.R. Computer-assisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium. J Cell Sci 118 (2005) 2225-2237
22. Bosgraaf L., Russcher H., Smith J.L., Wessels D., Soll D.R., and Van Haastert P.J. A novel cGMP signalling pathway mediating myosin phosphorylation and chemotaxis in Dictyostelium. EMBO J 21 (2002) 4560-4570
23. Chung C.Y., and Firtel R.A. PAKa, a putative PAK family member, is required for cytokinesis and the regulation of the cytoskeleton in Dictyostelium discoideum cells during chemotaxis. J Cell Biol 147 (1999) 559-576
24. Rubin H., and Ravid S. Polarization of myosin II heavy chain-protein kinase C in chemotaxing Dictyostelium cells. J Biol Chem 277 (2002) 36005-36008
25. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., Takuwa Y., Sugimoto N., Mitchison T., and Bourne H.R. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114 (2003) 201-214
26. Kumar A., Wessels D., Daniels K.J., Alexander H., Alexander S., and Soll D.R. Sphingosine-1-phosphate plays a role in the suppression of lateral pseudopod formation during Dictyostelium discoideum cell migration and chemotaxis. Cell Motil Cytoskeleton 59 (2004) 227-241
27. Patel H., and Barber D.L. A developmentally regulated Na-H exchanger in Dictyostelium discoideum is necessary for cell polarity during chemotaxis. J Cell Biol 169 (2005) 321-329
28. Stepanovic V., Wessels D., Daniels K., Loomis W.F., and Soll D.R. Intracellular role of adenylyl cyclase in regulation of lateral pseudopod formation during Dictyostelium chemotaxis. Eukaryot Cell 4 (2005) 775-786
29. •].
30. •] highlight the importance of PIP3 as a marker for polarity and asymmetry in contexts other than chemotaxis.