Eukaryotic Chemotaxis: a Network of Signaling Pathways Controls Motility, Directional Sensing, and Polarity

Overview

Journal Annu Rev Biophys

Publisher Annual Reviews

Specialty Biophysics

Date 2010 Mar 3

PMID 20192768

Citations 266

Authors

Kristen F Swaney

Chuan-Hsiang Huang

Peter N Devreotes

Affiliations

Soon will be listed here.

Abstract

Chemotaxis, the directed migration of cells in chemical gradients, is a vital process in normal physiology and in the pathogenesis of many diseases. Chemotactic cells display motility, directional sensing, and polarity. Motility refers to the random extension of pseudopodia, which may be driven by spontaneous actin waves that propagate through the cytoskeleton. Directional sensing is mediated by a system that detects temporal and spatial stimuli and biases motility toward the gradient. Polarity gives cells morphologically and functionally distinct leading and lagging edges by relocating proteins or their activities selectively to the poles. By exploiting the genetic advantages of Dictyostelium, investigators are working out the complex network of interactions between the proteins that have been implicated in the chemotactic processes of motility, directional sensing, and polarity.

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References

Iijima M, Huang Y, Luo H, Vazquez F, Devreotes P . Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J Biol Chem. 2004; 279(16):16606-13. DOI: 10.1074/jbc.M312098200. View

van Haastert P . Guanine nucleotides modulate cell surface cAMP-binding sites in membranes from Dictyostelium discoideum. Biochem Biophys Res Commun. 1984; 124(2):597-604. DOI: 10.1016/0006-291x(84)91596-1. View

Marin I, van Egmond W, van Haastert P . The Roco protein family: a functional perspective. FASEB J. 2008; 22(9):3103-10. DOI: 10.1096/fj.08-111310. View

Levine H, Kessler D, Rappel W . Directional sensing in eukaryotic chemotaxis: a balanced inactivation model. Proc Natl Acad Sci U S A. 2006; 103(26):9761-6. PMC: 1502527. DOI: 10.1073/pnas.0601302103. View

Kay R, Langridge P, Traynor D, Hoeller O . Changing directions in the study of chemotaxis. Nat Rev Mol Cell Biol. 2008; 9(6):455-63. DOI: 10.1038/nrm2419. View

Park K, Rivero F, Meili R, Lee S, Apone F, Firtel R . Rac regulation of chemotaxis and morphogenesis in Dictyostelium. EMBO J. 2004; 23(21):4177-89. PMC: 524383. DOI: 10.1038/sj.emboj.7600368. View

Caterina M, Devreotes P, Borleis J, Hereld D . Agonist-induced loss of ligand binding is correlated with phosphorylation of cAR1, a G protein-coupled chemoattractant receptor from Dictyostelium. J Biol Chem. 1995; 270(15):8667-72. DOI: 10.1074/jbc.270.15.8667. View

Pitt G, Milona N, Borleis J, Lin K, Reed R, Devreotes P . Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell. 1992; 69(2):305-15. DOI: 10.1016/0092-8674(92)90411-5. View

Meinhardt H . Orientation of chemotactic cells and growth cones: models and mechanisms. J Cell Sci. 1999; 112 ( Pt 17):2867-74. DOI: 10.1242/jcs.112.17.2867. View

10.

Kedrin D, van Rheenen J, Hernandez L, Condeelis J, Segall J . Cell motility and cytoskeletal regulation in invasion and metastasis. J Mammary Gland Biol Neoplasia. 2007; 12(2-3):143-52. DOI: 10.1007/s10911-007-9046-4. View

11.

Milne J, Devreotes P . The surface cyclic AMP receptors, cAR1, cAR2, and cAR3, promote Ca2+ influx in Dictyostelium discoideum by a G alpha 2-independent mechanism. Mol Biol Cell. 1993; 4(3):283-92. PMC: 300926. DOI: 10.1091/mbc.4.3.283. View

12.

Jin T, Zhang N, Long Y, Parent C, Devreotes P . Localization of the G protein betagamma complex in living cells during chemotaxis. Science. 2000; 287(5455):1034-6. DOI: 10.1126/science.287.5455.1034. View

13.

Tang L, Franca-Koh J, Xiong Y, Chen M, Long Y, Bickford R . tsunami, the Dictyostelium homolog of the Fused kinase, is required for polarization and chemotaxis. Genes Dev. 2008; 22(16):2278-90. PMC: 2518819. DOI: 10.1101/gad.1694508. View

14.

Stephens L, Milne L, Hawkins P . Moving towards a better understanding of chemotaxis. Curr Biol. 2008; 18(11):R485-94. DOI: 10.1016/j.cub.2008.04.048. View

15.

Eichinger L, Pachebat J, Glockner G, Rajandream M, Sucgang R, Berriman M . The genome of the social amoeba Dictyostelium discoideum. Nature. 2005; 435(7038):43-57. PMC: 1352341. DOI: 10.1038/nature03481. View

16.

Zhang N, Long Y, Devreotes P . Ggamma in dictyostelium: its role in localization of gbetagamma to the membrane is required for chemotaxis in shallow gradients. Mol Biol Cell. 2001; 12(10):3204-13. PMC: 60167. DOI: 10.1091/mbc.12.10.3204. View

17.

Brzostowski J, Kimmel A . Nonadaptive regulation of ERK2 in Dictyostelium: implications for mechanisms of cAMP relay. Mol Biol Cell. 2006; 17(10):4220-7. PMC: 1635358. DOI: 10.1091/mbc.e06-05-0376. View

18.

Weiner O, Marganski W, Wu L, Altschuler S, Kirschner M . An actin-based wave generator organizes cell motility. PLoS Biol. 2007; 5(9):e221. PMC: 1945041. DOI: 10.1371/journal.pbio.0050221. View

19.

Hereld D, Vaughan R, Kim J, Borleis J, Devreotes P . Localization of ligand-induced phosphorylation sites to serine clusters in the C-terminal domain of the Dictyostelium cAMP receptor, cAR1. J Biol Chem. 1994; 269(9):7036-44. View

20.

Bolourani P, Spiegelman G, Weeks G . Delineation of the roles played by RasG and RasC in cAMP-dependent signal transduction during the early development of Dictyostelium discoideum. Mol Biol Cell. 2006; 17(10):4543-50. PMC: 1635367. DOI: 10.1091/mbc.e05-11-1019. View