The molecular genetics of chemotaxis: Sensing and responding to chemoattractant gradients

BioEssays

Volumn 22, Issue 7, 2000, Pages 603-615

  Firtel, Richard A ^a   Chung, Chang Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICTYOSTELIUM;

EID: 0033948436     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-1878(200007)22:7<603::aid-bies3>3.0.co;2-%23     Document Type: Review

References (80)

1. Chung CY, Firtel RA. Dictyostelium: A model experimental system for elucidating the pathways and mechanisms controlling chemotaxis. In: Means A, Conn, PM, editor. Molecular Regulation. Totowa, NJ: The Humana Press; 2000: in press.
2. Devreotes PN, Zigmond SH. Chemotaxis in eukaryotic cells: a locus on leukocytes and Dictyostelium. Ann Rev Cell Biol 1988;4:649-686.
3. Downey GP. Mechanisms of leukocyte motility and chemotaxis. Curr Opin Immunol 1994;6(1):113-124.
4. Lahrtz F, Piali L, Spanaus KS, Seebach J. Fontana A. Chemokines and chemotaxis of leukocytes in infectious meningitis. J Neuroimmunol 1998; 85:33-43.
5. Parent C, Devreotes P. A cell's sense of direction. Science 1999;284: 765-770.
6. Aubry L, Firtel RA. Integration of signaling networks that regulate Dictyostelium differentiation. Ann Rev Cell Dev Biol 1999;15:469-517.
7. Verkhovsky A, Svitkina T, Borisy G. Self-polarization and directional motility of cytoplasm. Curr Biol 1999;9:11-20.
8. Parent CA, Devreotes PN. Molecular genetics of signal transduction in Dictyostelium. Ann Rev Biochem 1996;65:411-440.
9. Boulay F, Naik N, Giannini E, Tardif M, Brouchon L. Phagocyte chemoattractant receptors. Ann N Y Acad Sci 1997;832:69-84.
10. Cross AK, Richardson V, Ali SA, Palmer I, Taub DD, Rees RC. Migration responses of human monocytic cell lines to alpha-and beta-chemokines. Cytokine 1997;9:521-528.
11. Neptune ER, Bourne HR, Receptors induce chemotaxis by releasing the betagamma subunit of Gi, not by activating Gq or Gs. Proc Natl Acad Sci USA 1997;94 14489-14494.
12. Hadwiger JA Lee S, Firtel RA. The Gα subunit Gα4 couples to pterin receptors and identifies a signaling pathway that is essential for multicellular development in Dictyostelium. Proc Natl Acad Sci USA 1994;91: 10566-10570.
13. van Haastert PJ, Kuwayama H. cGMP as second messenger during Dictyostelium chemotaxis. FEBS Lett 1997;410:25-28.
14. Silveira LA, Smith JL, Tan JL, Spudich JA. MLCK-A, an unconventional myosin light chain kinase from Dictyostelium, is activated by a cGMP-dependent pathway. Proc Natl Acad Sci USA 1998;95: 13000-13005.
15. Newell PC, Liu G. Streamer F mutants and chemotaxis of Dictyostelium. Bioessays 1992;14:473-479.
16. Wessels D, Soll DR, Knecht D, Loomis WF, De Lozanne A, Spudich J. Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev Biol 1988;128:164-177.
17. Ma H, Gamper M, Parent C, Firtel RA. The Dictyostelium MAP kinase kinase DdMEK1 regulates chemotaxis and is essential for chemoattractant-mediated activation of guarylyl cyclase. EMBO J 1997;16: 4317-4332.
18. Zhou KM, Takegawa K, Emr SD, Firtel RA. A phosphatidylinositol (PI) kinase gene family in Dictyostelium discoideum: Biological roles of putative mammalian p110 and yeast Vps34p PI 3-kinase homologs during growth and development. Mol Cell Biol 1995;15:5645-5656.
19. Leevers SJ, Vanhaesebroeck B, Waterfield MD. Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr Opin Cell Biol 1999;11:219-225.
20. Buczynski G, Grove B, Nomura A, Kleve M, Bush J, Firtel RA, Cardelli J. Inactivation of two Dictyostelium discoideum genes, DdPIK1 and DdPIK2, encoding proteins related to mammalian phosphatidylinositide 3-kinases, results in defects in endocytosis, lysosome to postlysosome transport, and actin cytoskeleton organization. J Cell Biol 1997;136: 1271-1286.
21. Zhou K, Pandol S, Bokoch G, Traynor-Kaplan AE. Disruption of Dictyostelium PI3K genes reduces [32P]phosphatidylinositol 3, 4 bisphosphate and [32P]phosphatidylinositol trisphosphate levels, alters F-actin distribution and impairs pinocytosis. J Cell Sci 1998;111:283-294.
22. Dunzendorfer S, Meierholer C, Wiedermann CJ. Signalling in neuropeptide-induced migration of human eosinophils. J Leukoc Biol 1998;64: 828-834.
23. Vanhaesebroeck B, Jones GE, Allen WE, Zicha D, Hooshmand-Rad R, Sawyer C, Wells C, Waterfield MD, Ridley AJ. Distict PI(3)Ks mediate mitogenic signalling and cell migration in macrophages. Nature Cell Biol 1999;1:69-71.
24. Meili R, Ellsworth C, Lee S, Reddy TBK, Firtel RA, Chemoattractantmediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J 1999; in press.
25. Alessi D, James S, Downes C, Holmes A, Gaffney P, Reese C, Cohen P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 1997;7:261-269.
26. Andjelkovic M, Alessi D, Meier R, Fernandez A, Lamb N, Frech M, Cron P, Lucocq J, Hemmings B. Role of translocation in the activation and function of protein kinase B. J Biol Chem 1997;272:31515-31524.
27. Alessi D, Deak M, Casamayor A, Caudwell F, Morrice N, Norman D, Gaffney P, Reese C, MacDougall C, Harbison D et al. 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase Curr Biol 1997;7:776-789.
28. Wymann M, Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim Biophys Acta 1998;1436:127-150.
29. Rodriguez-Viciana P, Warne P, Khwaja A, Marte B, Pappin D, Das P, Waterfield M, Ridley A, Downward J. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 1997;89:457-467.
30. Tilton B, Andjelkovic M, Didichenko SA, Hemmings BA, Thelen M, G-Protein-coupled receptors and Fcgamma-receptors mediate activation of Akt/protein kinase B in human phagocytes. J Biol Chem 1997;272: 28096-28101.
31. Servant G, Weiner O, Herzmark P. Balla T, Sedat J, Bourne H. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 1999;in press.
32. Eichinger L, Lee SS, Schleicher M. Dictyostelium as model system for studies of the actin cytoskeleton by molecular genetics. Microsci Res Tech 1999;47:124-134.
33. Shariff A, Luna EJ. Diacylglycerol-stimulated formation of actin nucleation sites at plasma membranes. Science 1992;256:245-247.
34. Lee SF, Mahasneh A, de la Roche M, Côté GP. Regulation of the p21-activated kinase-related Dictyostelium myosin I heavy chain kinase by autophosphorylation, acidic phospnolipids, and Ca2 + calmodulin. J Biol Chem 1998;273:2791-27917.
35. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998; 279:509-514.
36. Chung CY, Lee S, Briscoe C, Ellsworth C, Firtel RA. Role of Rac in controlling the actin cytoskeleton and chemotaxis in motile cells. Proc Natl Acad Sci USA 2000;in press.
37. Zigmond SH, Joyce M, Borleis J, Bokoch GM, Devreotes PN. Regulation of actin polymerization in cell-free systems by GTPgammaS and Cdc42. J Cell Biol 1997;138:363-374.
38. Allen WE, Zicha D, Ridley AJ, Jones GE. A role for Cdc42 in macrophage chemotaxis. J Cell Biol 1998;141:1147-1157.
39. Nobes C, Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 1999;144:1235-1244.
40. Castellano F, Montcourrier P, Guillemot J, Gouin E, Machesky L, Cossart P, Chavrier P. Inducible recruitment of Cdc42 or WASP to a cell-surface receptor triggers actin polymerization and filopodium formation. Curr Biol 1999;9:351-360.
41. Cantrell D. Lymphocyte signalling: A coordinating role for Vav? Curr Biol 1998;8:R535-R538.
42. Gerisch G, Albrecht R, De Hostos E, Wallraff E, Heizer C, Kreitmeier M, Müller-Taubenberger A. Actin-associated proteins in motility and chemotaxis of Dictyostelium cells. Symp Soc Exper Bio 1993;47:297-315.
43. Yumura S, Uyeda TQ. Myosin II can be localized to the cleavage furrow and to the posterior region of Dictyostelium amoebae without control by phosphorylation of myosin heavy and light chains. Cell Motil Cytoskel 1997;36:313-322.
44. Svitkina TM, Borisy GG. Arp2/3 complex and actin depolymerization facot/Cofilin in dendritic organization and treadmilling of action filament arra in lamellipodia. J. Cell Biol. 1999;145:1009-1026.
45. Cramer LP, Siebert M, Mitchison TJ. Identification of novel graded polarity actin filament bundles in locomoting heart fibroblasts: Implications for the generation of motile force. J Cell Biol 1997;136:1287-1305.
46. Condeelis J. Life at the leading edge: the formation of cell protrusions. Ann Rev Cell Biol 1993 9:411-444.
47. Clow P, McNally JG. In vivo observations of myosin II dynam cs support a role in rear retraction. Mol Biol Cell 1999;10:1309-1323.
48. Stites J, Wessels D, Uhl A, Egelhoff T, Shutt D, Soll DR. Phosphorylation of the Dictyostelium myosin il heavy chain is necessary for maintaining cellular polarity and suppressing turning during chemotaxis. Cell Motil Cytoskel 1998;39:31 51.
49. Wessels D, Vawter-Hugart H, Murray J, Soll DR. Three-dimensional dynamics of pseudopod formation and the regulation of turning during the motility cycle of Dictyostelium. Cell Motil Cytoskel 1994;27:1-12.
50. Machesky L, Mullins R, Higgs H, Kaiser D, Blanchoin L, May R, Hall M, Pollard T. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 1999;96: 3739-3744.
51. Machesky LM, Insall RH. Scar1 and the related Wiskott-Aldrich syndrome prote n, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 1998;8:1347-1356.
52. Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T, Takenawa T, Kirschner M. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 1999;97:221-231.
53. O'Sullivan E, Kinnon C, Brickell P. Wiskott-Aldrich syndrome protein, WASP. Intl J Biochem Cell Biol 1999;31:383-387.
54. Chen TL, Kowalczyk PA, Ho G, Chisholm RL. Targeted disruption of the Dictyostelium myosin essential light chain gene produces cells defective in cytokinesis and morphogenesis. J Cell Sci 1995;108: 3207-3218.
55. Shelden E, Knecht DA. Dictyostelium cel shape generation requires myosin II Cell Motil Cytoskel 1996;35:59-67.
56. Egelhoff TT, Lee RJ, Spudich JA. Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo. Cell 1993;75:363-371.
57. van Leeuwen FN, van Delft S, Kain HE, van der Kammen RA, Colard JG. Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading. Nat Cell Biol 1999: 242-248.
58. Chung CY, Firtel RA, A p21-activated protein kinase, PAKa, is required for cytokinesis and the regulation of the cytoskeleton in Dictyostelium cells during chemotaxis. J Cell Biol 1999;147:559-575.
59. Abu-Elneel K, Karchi M, Ravid S. Dictyostelium myosin II is regulated during chemotaxis by a novel protein kinase C. J Biol Chem 1996;271: 977-984.
60. Clancy CE, Mendoza MG, Naismith TV, Kolman MF, Egelhoff TT. Identification of a protein kinase from Dictyostelium with homology to the novel catalytic domain of myosin heavy chain kinase A. J Biol Chem 1997;272:11812-11815.
61. Dembinsky A, Rubin H, Ravid S. Chemoattractant-mediated increases in cGMP induce changes in Dictyostelium myosin II heavy chain-specific protein kinase C activities. J Cell Biol 1996;134:911-921.
62. Kolman MF, Futey LM, Egelhoff TT. Dictyostelium myosin heavy chain kinase A regulates myosin localization during growth and development. J Cell Biol 1996;132:101-109.
63. Tu H, Wigler M. Genetic evidence for Pak1 autoinhibition and its release by Cdc42. Mol Cell Biol 1999;19:602-611.
64. Egelhoff TT, Naismith TV, Brozovich FV. Myosin-based cortical tension in Dictyostelium resolved into heavy and light chain-regulated components. J Muscle Res Cell Motil 1996;17:269-274.
65. Wessels D, Murray J, Jung G, Hammer JA, Soll DR. Myosin IB null mutants of Dictyostelium exhibit abnormalities in motility. Cell Motil Cytoskel 1991;20:301-315.
66. Wessels D, Titus M, Soll DR. A Dictyostelium myosin I plays a crucial role n regulating the frequency of pseudopods formed on the substratum. Cell Motil Cytoskel 1996;33:64-79.
67. Morita YS, Jung G, Hammer JA, 3rd, Fukui Y. Localization of Dictyostelium myoB and myoD to filopodia and cell-cell contact sites using isoform-specific antibodies. Eur J Cell Biol 1996;71:371-379.
68. Lee SF, Egelhoff TT, Mahasneh A, Côté GP. Cloning and characterization of a Dictyostelium myosin I heavy chain kinase activated by Cdc42 and Rac. J Biol Chem 1996;271:27044-82704.
69. Brzeska H, Young R, Knaus U, Korn ED. Myosin I heavy chain kinase: Cloning of the full-length gene and acidic lipid-dependent activation by Rac and Cdc42. Proc Natl Acad Sci USA 1999;96:394-399.
70. Parent CA, Blacklock BJ, Froehlich WM, Murphy DB, Devreotes PN. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 1998;95:81-91.
71. Weiner OD, Servant G, Welch MD, Mitchison TJ, Sedat JW, Bourne HR. Spatial control of actin polymerization during neutrophil chemotaxis. Nat Cell Biol 1999;1:75-81.
72. Xiao Z, Zhang N, Murphy DB, Devreotes PN. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J Cell Biol 1997;139 365-374.
73. Servant G, Weiner OD, Neptune ER John W, Sedat JW, Bourne HR. Dynamics of a chemoattractant receptor in living neutrophils during chemotaxis. Mol Biol Cell 1999;10:1163-1178.
74. Mato JM, Losada A, Nanjurdiah V, Konijn TM. Signal input for a chemotactic response in the cellular slime mold Dictylostelium discoideum. Proc Natl Acad Sci USA 1975;72:4991-4993.
75. Tranquillo RT, Lauffenburger DA. Zigmond SH. A stochastic model for leukocyte random motility and chemotaxis based on receptor binding fluctuations. J Cell Biol 1988;106:303-309.
76. Zigmond SH. Consequences of chemotactic peptide receptor modulation for leukocyte orientation. J Cell Biol 1981;88:644-647.
77. Mackay DA, Kuskel JR, Wilkinson PC. Studies of chemotactic factor-induced polarity in human neutrophils. Lipid mobility, receptor distribution and time-sequence of polarization. J Cell Sci 1991;100:473-479.
78. Nieto M, Frade JMR, Sancho D, Mellado M, Martinez AC, Sanchez-Madrid F. Polarization of chemokine receptors to the leading edge during lymphocyte chemotaxis. J Exp Med 1997;186:153-158.
79. Insall RH, Borleis J, Devreotes PN. The Aimless Ras GEF is required for processing of chemotactic signals through G-protein-coupled receptors in Dictyostelium Curr Biol 1996;6:719-729.
80. Lee S, Parent CA, R. I, Firtel RA. A novel Ras interacting proteir required for chemotaxis and cyclic adenosine monophosphate signal relay in Dictyostelium. Mol Biol Cell 1999;10:2829-2845.