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MAP kinase function in amoeboid chemotaxis
Y. Wang, J. Liu, J.E. Segall
Journal of Cell Science 1998 111: 373-383;

Summary

Mutants lacking the MAP kinase DdERK2 show reduced chemotactic responses to folate and cAMP. Analysis of cAMP chemotaxis shows that Dderk2- cells are defective in chemotaxis to high concentrations of cAMP. This defect is due to an inability to repolarize in the continued presence of high concentrations of cAMP. Under these conditions, the speed of movement of mutant cells remains low. Instead of generating a leading pseudopod, mutant cells generate transient crown-like structures over multiple regions of the cell surface. These structures differ from pseudopods in that they contain myosin II as well as F actin and coronin. These studies identify a role for MAP kinases in coordinating the formation of cell projections generated in response to chemoattractants.

REFERENCES

    1. Aubry L.,
    2. Maeda M.,
    3. Insall R.,
    4. Devreotes P. N. and
    5. Firtel R. A.
    (1997). The Dictyostelium mitogen-activated protein kinase ERK2 is regulated by Ras and cAMP-dependent protein kinase (PKA) and mediates PKA function. J. Biol. Chem 272, 3883–3886
    OpenUrlAbstract/FREE Full Text
    1. Bornfeldt K. E.,
    2. Raines E. W.,
    3. Nakano T.,
    4. Graves L. M.,
    5. Krebs E. G. and
    6. Ross R.
    (1994). Insulin-like growth factor-I and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signaling pathways that are distinct from those of proliferation. J. Clin. Invest 93, 1266–1274
    OpenUrlCrossRefPubMedWeb of Science
    1. Bornfeldt K. E.,
    2. Graves L. M.,
    3. Raines E. W.,
    4. Igarashi Y.,
    5. Wayman G.,
    6. Yamamura S.,
    7. Yatomi Y.,
    8. Sidhu J. S.,
    9. Krebs E. G.,
    10. Hakomori S. and
    11. et al.
    (1995). Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis ofhuman arterial smooth muscle cells: spatial and temporal modulation of PDGF chemotactic signal transduction. J. Cell Biol 130, 193–206
    OpenUrlAbstract/FREE Full Text
    1. Bornfeldt K. E.,
    2. Raines E. W.,
    3. Graves L. M.,
    4. Skinner M. P.,
    5. Krebs E. G. and
    6. Ross R.
    (1995). Platelet-derived growth factor. Distinct signal transduction pathways associated with migration versus proliferation. Ann. NY Acad. Sci 766, 416–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Burns C. G.,
    2. Larochelle D. A.,
    3. Erickson H.,
    4. Reedy M. and
    5. De Lozanne A.
    (1995). Single-headed myosin II acts as a dominant negative mutation in Dictyostelium. Proc. Nat. Acad. Sci. USA 92, 8244–8248
    OpenUrlAbstract/FREE Full Text
    1. Burridge K. and
    2. Chrzanowska-Wodnicka M.
    (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol 12, 463–518
    OpenUrlCrossRefPubMedWeb of Science
    1. Campbell J. S.,
    2. Seger R.,
    3. Graves J. D.,
    4. Graves L. M.,
    5. Jensen A. M. and
    6. Krebs E. G.
    (1995). The MAP kinase cascade. Rec. Prog. Hor. Res 50, 131–159
    OpenUrl
    1. Cano E. and
    2. Mahadevan L. C.
    (1995). Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci 20, 117–122
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen P.,
    2. Xie H.,
    3. Sekar M. C.,
    4. Gupta K. and
    5. Wells A.
    (1994). Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J. Cell Biol 127, 847–857
    OpenUrlAbstract/FREE Full Text
    1. Chrzanowska-Wodnicka M. and
    2. Burridge K.
    (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol 133, 1403–1415
    OpenUrlAbstract/FREE Full Text
    1. Condeelis J.
    (1993). Life at the leading edge: the formation of cell protrusions. Annu. Rev. Cell Biol 9, 411–444
    OpenUrlCrossRefWeb of Science
    1. Cox D.,
    2. Condeelis J.,
    3. Wessels D.,
    4. Soll D.,
    5. Kern H. and
    6. Knecht D. A.
    (1992). Targeted disruption of the ABP-120 gene leads to cells with altered motility. J. Cell Biol 116, 943–955
    OpenUrlAbstract/FREE Full Text
    1. de Hostos E. L.,
    2. Bradtke B.,
    3. Lottspeich F.,
    4. Guggenheim R. and
    5. Gerisch G.
    (1991). Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein beta subunits. EMBO J 10, 4097–4104
    OpenUrlPubMedWeb of Science
    1. Devreotes P. N.
    (1994). G protein-linked signaling pathways control the developmental program of Dictyostelium. Neuron 12, 235–241
    OpenUrlCrossRefPubMedWeb of Science
    1. Dharmawardhane S.,
    2. Warren V.,
    3. Hall A. L. and
    4. Condeelis J.
    (1989). Changes in the association of actin-binding proteins with the actin cytoskeleton during chemotactic stimulation of Dictyostelium discoideum. Cell Motil. Cytoskel 13, 57–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Gaskins C.,
    2. Maeda M. and
    3. Firtel R. A.
    (1994). Identification and functional analysis of a developmentally regulated extracellular signal-regulated kinase gene in Dictyostelium discoideum. Mol. Cell Biol 14, 6996–7012
    OpenUrlAbstract/FREE Full Text
    1. Gaskins C.,
    2. Clark A. M.,
    3. Aubry L.,
    4. Segall J. E. and
    5. Firtel R. A.
    (1996). The Dictyostelium MAP kinase ERK2 regulates multiple, independent developmental pathways. Genes Dev 10, 118–128
    OpenUrlAbstract/FREE Full Text
    1. Hall A. L.,
    2. Schlein A. and
    3. Condeelis J.
    (1988). Relationship of pseudopod extension to chemotactic hormone-induced actin polymerization in amoeboid cells. J. Cell. Biochem 37, 285–299
    OpenUrlCrossRefPubMedWeb of Science
    1. Hall A.,
    2. Warren V. and
    3. Condeelis J.
    (1989). Transduction of the chemotactic signal to the actin cytoskeleton of Dictyostelium discoideum. Dev. Biol 136, 517–525
    OpenUrlCrossRefPubMedWeb of Science
    1. Hall A. L.,
    2. Warren V.,
    3. Dharmawardhane S. and
    4. Condeelis J.
    (1989). Identification of actin nucleation activity and polymerization inhibitor in ameboid cells: their regulation by chemotactic stimulation. J. Cell Biol 109, 2207–2213
    OpenUrlAbstract/FREE Full Text
    1. Insall R.,
    2. Kuspa A.,
    3. Lilly P. J.,
    4. Shaulsky G.,
    5. Levin L. R.,
    6. Loomis W. F. and
    7. Devreotes P.
    (1994). CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein-mediated activation of adenylyl cyclase in Dictyostelium. J. Cell Biol 126, 1537–1545
    OpenUrlAbstract/FREE Full Text
    1. Insall R. H.,
    2. Soede R. D.,
    3. Schaap P. and
    4. Devreotes P. N.
    (1994). Two cAMP receptors activate common signaling pathways in Dictyostelium. Mol. Biol. Cell 5, 703–711
    OpenUrlAbstract/FREE Full Text
    1. Janmey P. A.
    (1994). Phosphoinositide and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol 56, 169–191
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnson G. L. and
    2. Vaillancourt R. R.
    (1994). Sequential protein kinase reactions controlling cell growth and differentiation. Curr. Opin. Cell Biol 6, 230–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Jung G.,
    2. Wu X. and
    3. Hammer J. A.
    (1996). Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J. Cell Biol 133, 305–323
    OpenUrlAbstract/FREE Full Text
    1. Kim J. H.,
    2. Soede R. D.,
    3. Schaap P.,
    4. Valkema R.,
    5. Borleis J. A.,
    6. van Haastert P. J. M.,
    7. Devreotes P. N. and
    8. Hereld D.
    (1997). Phosphorylation of chemoattractant receptors is not essential for chemotaxisor termination of G-protein-coupled responses. J. Biol. Chem 272, 27313–27318
    OpenUrlAbstract/FREE Full Text
    1. Klemke R. L.,
    2. Cai S.,
    3. Giannini A. L.,
    4. Gallagher P. J.,
    5. De Lanerolle P. and
    6. Cheresh D. A.
    (1997). Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol 137, 481–492
    OpenUrlAbstract/FREE Full Text
    1. Knetsch M. L.,
    2. Epskamp J. P.,
    3. Schenk P. W.,
    4. Wang Y.,
    5. Segall J. E. and
    6. Snaar-Jagalska B. E.
    (1996). Dual role of cAMP and involvement of both G-proteins and ras in regulation of ERK2 in Dictyostelium discoideum. EMBO J 15, 3361–3368
    OpenUrlPubMedWeb of Science
    1. Kuroki M. and
    2. O'Flaherty J. T.
    (1997). Differential effects of a mitogen-activated protein kinase kinase inhibitor on human neutrophil responses to chemotactic factors. Biochem. Biophys. Res. Commun 232, 474–477
    OpenUrlCrossRefPubMedWeb of Science
    1. Kuspa A. and
    2. Loomis W. F.
    (1992). Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc. Nat. Acad. Sci. USA 89, 8803–8807
    OpenUrlAbstract/FREE Full Text
    1. Maeda M.,
    2. Aubry L.,
    3. Insall R.,
    4. Gaskins C.,
    5. Devreotes P. N. and
    6. Firtel R. A.
    (1996). Seven helix chemoattractant receptors transiently stimulate mitogen-activated protein kinase in Dictyostelium. Role of heterotrimeric G proteins. J. Biol. Chem 271, 3351–3354
    OpenUrlAbstract/FREE Full Text
    1. Maniak M.,
    2. Rauchenberger R.,
    3. Albrecht R.,
    4. Murphy J. and
    5. Gerisch G.
    (1995). Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 83, 915–924
    OpenUrlCrossRefPubMedWeb of Science
    1. Manstein D. J.
    (1993). Myosin function in the motile behaviour of cells. Symp. Soc. Exp. Biol 47, 375–381
    OpenUrlPubMed
    1. McRobbie S. J. and
    2. Newell P. C.
    (1983). Changes in actin associated with the cytoskeleton following chemotactic stimulation of Dictyostelium discoideum. Biochem. Biophys. Res. Commun 115, 351–359
    OpenUrlCrossRefPubMedWeb of Science
    1. Moores S. L.,
    2. Sabry J. H. and
    3. Spudich J. A.
    (1996). Myosin dynamics in live Dictyostelium cells. Proc. Nat. Acad. Sci. USA 93, 443–446
    OpenUrlAbstract/FREE Full Text
    1. Morrison D. L.,
    2. Slanghera J. S.,
    3. Stewart J.,
    4. Sutherland C.,
    5. Walsh M. P. and
    6. Pelech S. L.
    (1996). Phosphorylation and activation of smooth muscle myosin light chain kinase by MAP kinase and cyclin-dependent kinase-1. Biochem. Cell Biol 74, 549–557
    OpenUrlPubMedWeb of Science
    1. Noegel A. A. and
    2. Luna J. E.
    (1995). The Dictyostelium cytoskeleton. Experientia 51, 1135–1143
    OpenUrlCrossRefPubMedWeb of Science
    1. Ostrow B. D.,
    2. Chen P. and
    3. Chisholm R. L.
    (1994). Expression of a myosin regulatory light chain phosphorylation site mutant complements the cytokinesis and developmental defects of Dictyostelium RMLC null cells. J. Cell Biol 127, 1945–1955
    OpenUrlAbstract/FREE Full Text
    1. Pitt G. S.,
    2. Milona N.,
    3. Borleis J.,
    4. Lin K. C.,
    5. Reed R. R. and
    6. Devreotes P. N.
    (1992). Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell 69, 305–315
    OpenUrlCrossRefPubMedWeb of Science
    1. Robbins D. J.,
    2. Zhen E.,
    3. Cheng M.,
    4. Xu S.,
    5. Ebert D. and
    6. Cobb M. H.
    (1994). MAP kinases ERK1 and ERK2: Pleiotropic enzymes in a ubiquitous signaling network. Int. Rev. Cytol 150, 95–117
    OpenUrlPubMed
    1. Ruppel K. M. and
    2. Spudich J. A.
    (1995). Myosin motor function: structural and mutagenic approaches. Curr. Opin. Cell Biol 7, 89–93
    OpenUrlCrossRefPubMed
    1. Schleicher M.,
    2. Andre B.,
    3. Andreoli C.,
    4. Eichinger L.,
    5. Haugwitz M.,
    6. Hofmann A.,
    7. Karakesisoglou J.,
    8. Stockelhuber M. and
    9. Noegel A. A.
    (1995). Structure/function studies on cytoskeletal proteins in Dictyostelium amoebae as a paradigm. FEBS Lett 369, 38–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Segall J. E.,
    2. Fisher P. R. and
    3. Gerisch G.
    (1987). Selection of chemotaxis mutants of Dictyostelium discoideum. J. Cell Biol 104, 151–161
    OpenUrlAbstract/FREE Full Text
    1. Segall J. E.
    (1992). Behavioral responses of streamer F mutants of Dictyostelium discoideum: effects of cyclic GMP on cell motility. J. Cell Sci 101, 589–597
    OpenUrlAbstract/FREE Full Text
    1. Segall J. E.,
    2. Kuspa A.,
    3. Shaulsky G.,
    4. Ecke M.,
    5. Maeda M.,
    6. Gaskins C.,
    7. Firtel R. A. and
    8. Loomis W. F.
    (1995). A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J. Cell Biol 128, 405–413
    OpenUrlAbstract/FREE Full Text
    1. Seger R.,
    2. Ahn N. G.,
    3. Boulton T. G.,
    4. Yancopoulos G. D.,
    5. Panayotatos N.,
    6. Radziejewska E.,
    7. Ericsson L.,
    8. Bratlien R. L.,
    9. Cobb M. H. and
    10. Krebs E. G.
    (1991). Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: implications for their mechanism of activation. Proc. Nat. Acad. Sci. USA 88, 6142–6146
    OpenUrlAbstract/FREE Full Text
    1. Soede R. D.,
    2. Insall R. H.,
    3. Devreotes P. N. and
    4. Schaap P.
    (1994). Extracellular cAMP can restore development in Dictyostelium cells lacking one, but not two subtypes of early cAMP receptors (cARs). Evidence for involvement of cAR1 in aggregative gene expression. Development 120, 1997–2002
    OpenUrlAbstract
    1. Theibert A. and
    2. Devreotes P. N.
    (1986). Surface receptor-mediated activation of adenylate cyclase in Dictyostelium. Regulation by guanine nucleotides in wild-type cells and aggregation deficient mutants. J. Biol. Chem 261, 15121–15125
    OpenUrlAbstract/FREE Full Text
    1. Theriot J. A.
    (1994). Regulation of the actin cytoskeleton in living cells. Semin. Cell Biol 5, 193–199
    OpenUrlCrossRefPubMed
    1. Titus M. A.,
    2. Wessels D.,
    3. Spudich J. A. and
    4. Soll D.
    (1993). The unconventional myosin encoded by the myoA gene plays a role in Dictyostelium motility. Mol. Biol. Cell 4, 233–246
    OpenUrlAbstract/FREE Full Text
    1. Tomchik K. J. and
    2. Devreotes P. N.
    (1981). Adenosine 3,5 -monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution-fluorography. Science 212, 443–446
    OpenUrlAbstract/FREE Full Text
    1. Treisman R.
    (1996). Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol 8, 205–215
    OpenUrlCrossRefPubMedWeb of Science
    1. Van Haastert P. J.
    (1995). Transduction of the chemotactic cAMP signal across the plasma membrane of Dictyostelium cells. Experientia 51, 1144–1154
    OpenUrlCrossRefPubMedWeb of Science
    1. Varnum B. and
    2. Soll D. R.
    (1984). Effects of cAMP on single cell motility in Dictyostelium. J. Cell Biol 99, 1151–1155
    OpenUrlAbstract/FREE Full Text
    1. Vaughan R. A. and
    2. Devreotes P. N.
    (1988). Ligand-induced phosphorylation of the cAMP receptor from Dictyostelium discoideum. J. Biol. Chem 263, 14538–14543
    OpenUrlAbstract/FREE Full Text
    1. Yumura S. and
    2. Fukui Y.
    (1985). Reversible cyclic AMP-dependent change in distribution of myosin thick filaments in Dictyostelium. Nature 314, 194–196
    OpenUrlCrossRefPubMed
    1. Zigmond S. H.
    (1977). The ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol 75, 606–616
    OpenUrlAbstract/FREE Full Text
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Journal Articles
MAP kinase function in amoeboid chemotaxis
Y. Wang, J. Liu, J.E. Segall
Journal of Cell Science 1998 111: 373-383;
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