Chemotactic cell movement during Dictyostelium development and gastrulation

Current Opinion in Genetics and Development

Volumn 16, Issue 4, 2006, Pages 367-373

  Dormann, Dirk ^a   Weijer, Cornelis J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYCLIC AMP; FIBROBLAST GROWTH FACTOR; MYOSIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; CELL ADHESION; CELL MATURATION; CELL MIGRATION; CELL MOTION; CHEMOTAXIS; DEVELOPMENTAL STAGE; DICTYOSTELIUM; FILOPODIUM; GASTRULATION; LAMELLIPODIUM; MESODERM; MOLECULAR MECHANICS; MORPHOGENESIS; MUSCLE FIBER CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CHEMOTAXIS; CYCLIC AMP; DICTYOSTELIUM; GASTRULA; GROWTH SUBSTANCES; SIGNAL TRANSDUCTION; VERTEBRATES;

ANURA; DICTYOSTELIUM;

EID: 33745600126     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.06.003     Document Type: Review

References (75)

1. Weijer C.J. Dictyostelium morphogenesis. Curr Opin Genet Dev 14 (2004) 392-398
2. Kimmel A.R., and Firtel R.A. Breaking symmetries: regulation of Dictyostelium development through chemoattractant and morphogen signal-response. Curr Opin Genet Dev 14 (2004) 540-549
3. Brzostowski J.A., Parent C.A., and Kimmel A.R. A Gα-dependent pathway that antagonizes multiple chemoattractant responses that regulate directional cell movement. Genes Dev 18 (2004) 805-815
4. Comer F.I., and Parent C.A. Phosphoinositide 3-Kinase activity controls the chemoattractant-mediated activation and adaptation of adenylyl cyclase. Mol Biol Cell 17 (2006) 357-366. This study shows that both activation and adaptation of adenylyl cyclase require PIP3-dependent processes and that the activation pathway is more sensitive to PIP3 than is the adaptation pathway.
5. Sawai S., Thomason P.A., and Cox E.C. An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations. Nature 433 (2005) 323-326. This study provides an in-depth analysis of the wave propagation dynamics in several signalling mutants and shows that proper tuning of intracellular and extracellular cAMP is crucial for the centre formation and self-organization of aggregation territories.
6. 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
7. 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. This study conclusively shows that there is an amplification step between sensing of the graded extracellular cAMP signal by the cAMP receptors and the production of intracellular PIP3 as a part of the polarization process.
8. 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. This study shows that RasC is required for PI3K activation in the leading edge and that this results in PIP3 production and polymerization of actin, which then feeds back on the further recruitment of PI3K to the leading edge.
9. Wessels D., Brincks R., Kuhl S., Stepanovic V., Daniels K.J., Weeks G., Lim C.J., Spiegelman G., Fuller D., Iranfar N., et al. RasC plays a role in transduction of temporal gradient information in the cyclic-AMP wave of Dictyostelium discoideum. Eukaryot Cell 3 (2004) 646-662
10. 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
11. Ibarra N., Pollitt A., and Insall R.H. Regulation of actin assembly by SCAR/WAVE proteins. Biochem Soc Trans 33 (2005) 1243-1246
12. 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
13. 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
14. 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 10.1073/pnas. 0510570103. Proc Natl Acad Sci USA 103 (2006) 3633-3638. This study shows through single molecule analysis that PTEN molecules have a short residence time at the membrane and that Dictyostelium PTEN has a higher affinity for membrane binding sites than mammalian PTEN does, thus explaining the observation that mammalian PTEN is mostly cytosolic. It is further shown that membrane binding is strictly dependent on an N-terminal lipid-binding motif and that phosphorylation in the C-terminal tail affects binding affinity.
15. 3 response in Dictyostelium cells. Biophys J 87 (2004) 3764-3774
16. 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. This study shows the existence of nonlinear PIP3 production dynamics and corroborates the local-activation global-inhibition model.
17. 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
18. Postma M., Roelofs J., Goedhart J., Loovers H.M., Visser A.J., and Van Haastert P.J. Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches. J Cell Sci 117 (2004) 2925-2935
19. 3 accumulation and have unique roles during chemotaxis. Mol Biol Cell 14 (2003) 5028-5037
20. + exchanger in cell polarization, actin polymerization and efficient cell movement. The molecular mechanism by which this exchanger affects the above-named process remains unresolved, although evidence points to the fact that local pH must be an important determinant.
21. 3 during chemoattractant signaling in Dictyostelium: a quantitative in vivo analysis by inhibition of PI3-kinase. Mol Biol Cell 17 (2006) 1503-1513. This study shows that there exist alternative pathways for chemotactic signalling, because cells can still orient and move in the presence of inhibition of localised PIP3 formation.
22. Diez S., Gerisch G., Anderson K., Muller-Taubenberger A., and Bretschneider T. Subsecond reorganization of the actin network in cell motility and chemotaxis. Proc Natl Acad Sci USA 102 (2005) 7601-7606
23. 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
24. Schirenbeck A., Bretschneider T., Arasada R., Schleicher M., and Faix J. The diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat Cell Biol 7 (2005) 619-625
25. Schirenbeck A., Arasada R., Bretschneider T., Schleicher M., and Faix J. Formins and VASPs may co-operate in the formation of filopodia. Biochem Soc Trans 33 (2005) 1256-1259
26. Han Y.H., Chung C.Y., Wessels D., Stephens S., Titus M.A., Soll D.R., and Firtel R.A. Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in Dictyostelium. J Biol Chem 277 (2002) 49877-49887
27. Egelhoff T.T., Croft D., and Steimle P.A. Actin activation of myosin heavy chain kinase A in Dictyostelium: a biochemical mechanism for the spatial regulation of myosin II filament disassembly. J Biol Chem 280 (2005) 2879-2887
28. Yumura S., Yoshida M., Betapudi V., Licate L.S., Iwadate Y., Nagasaki A., Uyeda T.Q., and Egelhoff T.T. Multiple myosin II heavy chain kinases: roles in filament assembly control and proper cytokinesis in Dictyostelium. Mol Biol Cell 16 (2005) 4256-4266
29. Chung C.Y., Potikyan G., and Firtel R.A. Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol Cell 7 (2001) 937-947
30. de la Roche M., Mahasneh A., Lee S.F., Rivero F., and Cote G.P. Cellular distribution and functions of wild-type and constitutively activated Dictyostelium PakB. Mol Biol Cell 16 (2005) 238-247
31. Lee S., Rivero F., Park K.C., Huang E., Funamoto S., and Firtel R.A. Dictyostelium PAKc is required for proper chemotaxis. Mol Biol Cell 15 (2004) 5456-5469
32. Bosgraaf L., Waijer A., Engel R., Visser A.J., Wessels D., Soll D., and van Haastert P.J. RasGEF-containing proteins GbpC and GbpD have differential effects on cell polarity and chemotaxis in Dictyostelium. J Cell Sci 118 (2005) 1899-1910. This study conclusively shows that cGMP signal transduction is important in chemotaxis.
33. 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
34. Veltman D.M., Roelofs J., Engel R., Visser A.J., and Van Haastert P.J. Activation of soluble guanylyl cyclase at the leading edge during Dictyostelium chemotaxis. Mol Biol Cell 16 (2005) 976-983
35. 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
36. Zhang H., Heid P.J., Wessels D., Daniels K.J., Pham T., Loomis W.F., and Soll D.R. Constitutively active protein kinase A disrupts motility and chemotaxis in Dictyostelium discoideum. Eukaryot Cell 2 (2003) 62-75
37. Asano Y., Mizuno T., Kon T., Nagasaki A., Sutoh K., and Uyeda T.Q. Keratocyte-like locomotion in amiB-null Dictyostelium cells. Cell Motil Cytoskeleton 59 (2004) 17-27. The authors describe a mutant that shows keratinocyte-like cell movement behaviour and thus provides a genetically tractable model for the study of this mode of behaviour.
38. 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
39. Noegel A.A., Blau-Wasser R., Sultana H., Muller R., Israel L., Schleicher M., Patel H., and Weijer C.J. The cyclase-associated protein CAP as regulator of cell polarity and cAMP signaling in Dictyostelium. Mol Biol Cell 15 (2004) 934-945
40. Dormann D., and Weijer C.J. Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. Development 128 (2001) 4535-4543
41. Alvarez-Curto E., Rozen D.E., Ritchie A.V., Fouquet C., Baldauf S.L., and Schaap P. Evolutionary origin of cAMP-based chemoattraction in the social amoebae. Proc Natl Acad Sci USA 102 (2005) 6385-6390. By following the phylogeny of cAMP receptors, the authors are able to describe the evolutionary conservation of cAMP signalling. The data argue strongly that cAMP signalling was first used to control multicellular development and fruiting body formation.
42. 2 is the major metabolite during internalization of phagocytic membranes.
43. Tsujioka M., Yoshida K., and Inouye K. Talin B is required for force transmission in morphogenesis of Dictyostelium. EMBO J 23 (2004) 2216-2225
44. Bukharova T., Weijer G., Bosgraaf L., Dormann D., van Haastert P.J., and Weijer C.J. Paxillin is required for cell-substrate adhesion, cell sorting and slug migration during Dictyostelium development. J Cell Sci 118 (2005) 4295-4310. This study shows that Dictyostelium cells make focal adhesion plaques and that they play an important role in multicellular development, showing strong similarities to multicellular development in higher.
45. Iranfar N., Fuller D., and Loomis W.F. Transcriptional regulation of post-aggregation genes in Dictyostelium by a feed-forward loop involving GBF and LagC. Dev Biol 290 (2006) 460-469
46. Kibler K., Svetz J., Nguyen T.L., Shaw C., and Shaulsky G. A cell-adhesion pathway regulates intercellular communication during Dictyostelium development. Dev Biol 264 (2003) 506-521
47. Rieu J.P., Barentin C., Maeda Y., and Sawada Y. Direct mechanical force measurements during the migration of Dictyostelium slugs using flexible substrata. Biophys J 89 (2005) 3563-3576
48. Follstaedt S.C., Kirsten J.H., and Singleton C.K. Temporal and spatial expression of ammonium transporter genes during growth and development of Dictyostelium discoideum. Differentiation 71 (2003) 557-566
49. Kirsten J.H., Xiong Y., Dunbar A.J., Rai M., and Singleton C.K. Ammonium transporter C of Dictyostelium discoideum is required for correct prestalk gene expression and for regulating the choice between slug migration and culmination. Dev Biol 287 (2005) 146-156
50. Min J., Traynor D., Stegner A.L., Zhang L., Hanigan M.H., Alexander H., and Alexander S. Sphingosine kinase regulates the sensitivity of Dictyostelium discoideum cells to the anticancer drug cisplatin. Eukaryot Cell 4 (2005) 178-189
51. 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
52. Min J., Stegner A.L., Alexander H., and Alexander S. Overexpression of sphingosine-1-phosphate lyase or inhibition of sphingosine kinase in Dictyostelium discoideum results in a selective increase in sensitivity to platinum-based chemotherapy drugs. Eukaryot Cell 3 (2004) 795-805
53. Solnica-Krezel L. Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15 (2005) R213-R228
54. Keller R. Cell migration during gastrulation. Curr Opin Cell Biol 17 (2005) 533-541
55. Affolter M., and Weijer C.J. Signaling to cytoskeletal dynamics during chemotaxis. Dev Cell 9 (2005) 19-34
56. Yang X., Dormann D., Munsterberg A., and Weijer C. Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3 (2002) 425-437
57. Sun X., Meyers E.N., Lewandoski M., and Martin G.R. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev 13 (1999) 1834-1846
58. Ciruna B., and Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell 1 (2001) 37-49
59. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 103 (2000) 211-225
60. Thisse B., and Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287 (2005) 390-402
61. Nutt S.L., Dingwell K.S., Holt C.E., and Amaya E. Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev 15 (2001) 1152-1166
62. Bottcher R.T., and Niehrs C. Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26 (2005) 63-77
63. Sivak J.M., Petersen L.F., and Amaya E. FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev Cell 8 (2005) 689-701. This study dissects signalling pathways downstream of the FGF receptor and suggests that they are controlled both by Spred proteins that regulate the Map kinase activation and cell type-specific gene expression and by Sprouty2, which regulates a PLC- and PkCδ-dependent pathway to convergent extension.
64. Chung H.A., Hyodo-Miura J., Kitayama A., Terasaka C., Nagamune T., and Ueno N. Screening of FGF target genes in Xenopus by microarray: temporal dissection of the signalling pathway using a chemical inhibitor. Genes Cells 9 (2004) 749-761. This study identifies a novel FGF target and shows that this receptor can rescue convergent extension in the presence of the FGF receptor inhibitor SU5402.
65. Chung H.A., Hyodo-Miura J., Nagamune T., and Ueno N. FGF signal regulates gastrulation cell movements and morphology through its target NRH. Dev Biol 282 (2005) 95-110
66. Sasai N., Nakazawa Y., Haraguchi T., and Sasai Y. The neurotrophin-receptor-related protein NRH1 is essential for convergent extension movements. Nat Cell Biol 6 (2004) 741-748
67. Partanen J., Schwartz L., and Rossant J. Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev 12 (1998) 2332-2344
68. Gotoh N., Manova K., Tanaka S., Murohashi M., Hadari Y., Lee A., Hamada Y., Hiroe T., Ito M., Kurihara T., et al. The docking protein FRS2α is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol Cell Biol 25 (2005) 4105-4116. This study shows that Frs2α plays an essential role in early mouse development. Null mutants show severe defects in gastrulation, and the phenotypes are reminiscent of FGF receptor knockout mutants.
69. Hoch R.V., and Soriano P. Context-specific requirements for Fgfr1 signaling through Frs2 and Frs3 during mouse development. Development 133 (2006) 663-673
70. Huber T.L., Kouskoff V., Fehling H.J., Palis J., and Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432 (2004) 625-630
71. Hiratsuka S., Kataoka Y., Nakao K., Nakamura K., Morikawa S., Tanaka S., Katsuki M., Maru Y., and Shibuya M. Vascular endothelial growth factor A (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol Cell Biol 25 (2005) 355-363. This study provides evidence for an important role of VegfA in the anterior migration of haematopoietic precursor cells during early mouse development.
72. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.F., Breitman M.L., and Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 (1995) 62-66
73. Shalaby F., Ho J., Stanford W.L., Fischer K.D., Schuh A.C., Schwartz L., Bernstein A., and Rossant J. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89 (1997) 981-990
74. Nagel M., Tahinci E., Symes K., and Winklbauer R. Guidance of mesoderm cell migration in the Xenopus gastrula requires PDGF signaling. Development 131 (2004) 2727-2736. This study shows that PDGF is a major determinant in the anterior migration of prechordal plate cells.
75. Montero J.A., Kilian B., Chan J., Bayliss P.E., and Heisenberg C.P. Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr Biol 13 (2003) 1279-1289