tsunami, the Dictyostelium homolog of the Fused kinase, is required for polarization and chemotaxis

Genes and Development

Volumn 22, Issue 16, 2008, Pages 2278-2290

  Tang, Linnan ^a   Franca Koh, Jonathan ^a   Xiong, Yuan ^b   Chen, Mei Yu ^c   Long, Yu ^a   Bickford, Ross M ^d   Knecht, David A ^d   Iglesias, Pablo A ^b   Devreotes, Peter N ^a  

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

^b Johns Hopkins University   (United States)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Chemotaxis; Dictyostelium; Fused; Polarization

Indexed keywords

F ACTIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHOTRANSFERASE; PROTOZOAL PROTEIN; TSUA PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMOTAXIS; DICTYOSTELIUM; ENZYME ACTIVITY; GENE IDENTIFICATION; GENE MUTATION; GENETIC ANALYSIS; GENETIC SCREENING; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL POLARITY; CHEMOTAXIS; CYCLIC AMP; DICTYOSTELIUM; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; MICROTUBULES; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHOSPHATIDYLINOSITOLS; PROTEIN TRANSPORT; SEQUENCE DELETION; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; PSEUDOPODA;

EID: 50049103371     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1694508     Document Type: Article

References (51)

1. Bagorda, A., Mihaylov, V.A., and Parent, C.A. 2006. Chemotaxis: Moving forward and holding on to the past. Thromb. Haemost. 95: 12-21.
2. Basu, R. and Chang, F. 2007. Shaping the actin cytoskeleton using microtubule tips. Curr. Opin. Cell Biol. 19: 88-94.
3. Booth, E.O., Van Driessche, N., Zhuchenko, O., Kuspa, A., and Shaulsky, G. 2005. Microarray phenotyping in Dictyostelium reveals a regulon of chemotaxis genes. Bioinformatics 21: 4371-4377.
4. Bretschneider, T., Diez, S., Anderson, K., Heuser, J., Clarke, M., Muller-Taubenberger, A., Kohler, J., and Gerisch, G. 2004. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr. Biol. 14: 1-10.
5. Brito, D.A., Strauss, J., Magidson, V., Tikhonenko, I., Khodjakov, A., and Koonce, M.P. 2005. Pushing forces drive the comet-like motility of microtubule arrays in Dictyostelium. Mol. Biol. Cell 16: 3334-3340.
6. Chen, L., Janetopoulos, C., Huang, Y.E., Iijima, M., Borleis, J., and Devreotes, P.N. 2003. 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: 5028-5037.
7. Chen, M.H., Gao, N., Kawakami, T., and Chuang, P.T. 2005. Mice deficient in the fused homolog do not exhibit phenotypes indicative of perturbed hedgehog signaling during embryonic development. Mol. Cell. Biol. 25: 7042-7053.
8. Devreotes, P. and Janetopoulos, C. 2003. Eukaryotic chemotaxis: Distinctions between directional sensing and polarization. J. Biol. Chem. 278: 20445-20448.
9. Dharmawardhane, S., Warren, V., Hall, A.L., and Condeelis, J. 1989. Changes in the association of actin-binding proteins with the actin cytoskeleton during chemotactic stimulation of Dictyostelium discoideum. Cell Motil. Cytoskeleton 13: 57-63.
10. Etienne-Manneville, S. and Hall, A. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell 106: 489-498.
11. Feierbach, B., Verde, F., and Chang, F. 2004. Regulation of a formin complex by the microtubule plus end protein tea1p. J. Cell Biol. 165: 697-707.
12. Franca-Koh, J., Kamimura, Y., and Devreotes, P. 2006. Navigating signaling networks: Chemotaxis in Dictyostelium discoideum. Curr. Opin. Genet. Dev. 16: 333-338.
13. Futrelle, R.P., Traut, J., and McKee, W.G. 1982. Cell behavior in Dictyostelium discoideum: Preaggregation response to localized cyclic AMP pulses. J. Cell Biol. 92: 807-821.
14. Goldbeter, A. and Segel, L.A. 1980. Control of developmental transitions in the cyclic AMP signalling system of Dictyostelium discoideum. Differentiation 17: 127-135.
15. Gomes, E.R., Jani, S., and Gundersen, G.G. 2005. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121: 451-463.
16. Hall, A.L., Schlein, A., and Condeelis, J. 1988. Relationship of pseudopod extension to chemotactic hormone-induced actin polymerization in amoeboid cells. J. Cell. Biochem. 37: 285-299.
17. Hestermann, A. and Graf, R. 2004. The XMAP215-family protein DdCP224 is required for cortical interactions of microtubules. BMC Cell Biol. 5: 24. doi: 10.1186/1471-2121-5-24.
18. Iglesias, P.A. and Devreotes, P.N. 2008. Navigating through models of chemotaxis. Curr. Opin. Cell Biol. 20: 35-40.
19. Iijima, M. and Devreotes, P. 2002. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109: 599-610.
20. Kabacoff, C., Xiong, Y., Musib, R., Reichl, E.M., Kim, J., Iglesias, P.A., and Robinson, D.N. 2007. Dynacortin facilitates polarization of chemotaxing cells. BMC Biol. 5: 53. doi: 10.1186/1741-7007-5-53.
21. Krendel, M., Zenke, F.T., and Bokoch, G.M. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4: 294-301.
22. Kuspa, A. 2006. Restriction enzyme-mediated integration (REMI) mutagenesis. Methods Mol. Biol. 346: 201-209.
23. Martin, S.G., McDonald, W.H., Yates 3rd, J.R., and Chang, F. 2005. Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev. Cell 8: 479-491.
24. McRobbie, S.J. and Newell, P.C. 1983. Changes in actin associated with the cytoskeleton following chemotactic stimulation of Dictyostelium discoideum. Biochem. Biophys. Res. Commun. 115: 351-359.
25. Merchant, M., Evangelista, M., Luoh, S.M., Frantz, G.D., Chalasani, S., Carano, R.A., van Hoy, M., Ramirez, J., Ogasawara, A.K., McFarland, L.M., et al. 2005. Loss of the serine/ threonine kinase fused results in postnatal growth defects and lethality due to progressive hydrocephalus. Mol. Cell. Biol. 25: 7054-7068.
26. Niggli, V. 2003. Microtubule-disruption-induced and chemotactic-peptide- induced migration of human neutrophils: Implications for differential sets of signalling pathways. J. Cell Sci. 116: 813-822.
27. Oh, S.A., Johnson, A., Smertenko, A., Rahman, D., Park, S.K., Hussey, P.J., and Twell, D. 2005. A divergent cellular role for the FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr. Biol. 15: 2107-2111.
28. Parent, C.A., Blacklock, B.J., Froehlich, W.M., Murphy, D.B., and Devreotes, P.N. 1998. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95: 81-91.
29. Pegtel, D.M., Ellenbroek, S.I., Mertens, A.E., van der Kammen, R.A., de Rooij, J., and Collard, J.G. 2007. The Par-Tiam1 complex controls persistent migration by stabilizing microtubule-dependent front-rear polarity. Curr. Biol. 17: 1623-1634.
30. Preat, T., Therond, P., Lamour-Isnard, C., Limbourg-Bouchon, B., Tricoire, H., Erk, I., Mariol, M.C., and Busson, D. 1990. A putative serine/threonine protein kinase encoded by the segment-polarity fused gene of Drosophila. Nature 347: 87-89.
31. Rehberg, M., Kleylein-Sohn, J., Faix, J., Ho, T.H., Schulz, I., and Graf, R. 2005. Dictyostelium LIS1 is a centrosomal protein required for microtubule/cell cortex interactions, nucleus/ centrosome linkage, and actin dynamics. Mol. Biol. Cell 16: 2759-2771.
32. Ridley, A.J., Schwartz, M.A., Burridge, K., Firtel, R.A., Ginsberg, M.H., Borisy, G., Parsons, J.T., and Horwitz, A.R. 2003. Cell migration: Integrating signals from front to back. Science 302: 1704-1709.
33. Robbins, D.J., Nybakken, K.E., Kobayashi, R., Sisson, J.C., Bishop, J.M., and Therond, P.P. 1997. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90: 225-234.
34. Rodriguez, O.C., Schaefer, A.W., Mandato, C.A., Forscher, P., Bement, W.M., and Waterman-Storer, C.M. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5: 599-609.
35. Sasaki, A.T., Chun, C., Takeda, K., and Firtel, R.A. 2004. Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement. J. Cell Biol. 167: 505-518.
36. Satulovsky, J., Lui, R., and Wang, Y.L. 2008. Exploring the control circuit of cell migration by mathematical modeling. Biophys. J. 94: 3671-3683.
37. Soll, D.R., Wessels, D., Heid, P.J., and Zhang, H. 2002. A contextual framework for characterizing motility and chemotaxis mutants in Dictyostelium discoideum. J. Muscle Res. Cell Motil. 23: 659-672.
38. Sroka, J., Madeja, Z., Galanty, A., Michalik, M., Przestalski, S., Rakoczy, L., and Korohoda, W. 2001. Trimethyltin inhibits the chemotaxis of Dictyostelium discoideum amoebae. Eur. J. Protistol. 37: 313-326.
39. Tillinghast, H.S. and Newell, P.C. 1987. Chemotaxis towards pteridines during development of Dictyostelium. J. Cell Sci. 87: 45-53.
40. Ueda, M., Graf, R., MacWilliams, H.K., Schliwa, M., and Euteneuer, U. 1997. Centrosome positioning and directionality of cell movements. Proc. Natl. Acad. Sci. 94: 9674-9678.
41. Varjosalo, M. and Taipale, J. 2007. Hedgehog signaling. J. Cell Sci. 120: 3-6.
42. Varjosalo, M., Li, S.P., and Taipale, J. 2006. Divergence of hedgehog signal transduction mechanism between Drosophila and mammals. Dev. Cell 10: 177-186.
43. Vasiliev, J.M., Gelfand, I.M., Domnina, L.V., Ivanova, O.Y., Komm, S.G., and Olshevskaja, L.V. 1970. Effect of colcemid on the locomotory behaviour of fibroblasts. J. Embryol. Exp. Morphol. 24: 625-640.
44. Weiner, O.D., Neilsen, P.O., Prestwich, G.D., Kirschner, M.W., Cantley, L.C., and Bourne, H.R. 2002. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4: 509-513.
45. Willard, S.S. and Devreotes, P.N. 2006. Signaling pathways mediating chemotaxis in the social amoeba, Dictyostelium discoideum. Eur. J. Cell Biol. 85: 897-904.
46. Wittmann, T. and Waterman-Storer, C.M. 2001. Cell motility: Can Rho GTPases and microtubules point the way? J. Cell Sci. 114: 3795-3803.
47. Wittmann, T., Bokoch, G.M., and Waterman-Storer, C.M. 2003. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell Biol. 161: 845-851.
48. Wolff, C., Roy, S., and Ingham, P.W. 2003. Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 13: 1169-1181.
49. Wu, L.J. and Devreotes, P.N. 1991. Dictyostelium transiently expresses eight distinct G-protein α-subunits during its developmental program. Biochem. Biophys. Res. Commun. 179: 1141-1147.
50. Xu, J., Wang, F., Van Keymeulen, A., Rentel, M., and Bourne, H.R. 2005. Neutrophil microtubules suppress polarity and enhance directional migration. Proc. Natl. Acad. Sci. 102: 6884-6889.
51. Xu, J., Van Keymeulen, A., Wakida, N.M., Carlton, P., Berns, M.W., and Bourne, H.R. 2007. Polarity reveals intrinsic cell chirality. Proc. Natl. Acad. Sci. 104: 9296-9300.