Chemotaxis: signalling the way forward (original) (raw)
Baggiolini, M. Chemokines and leukocyte traffic. Nature392, 565–568 (1998). CASPubMed Google Scholar
Campbell, J. J. & Butcher, E. C. Chemokines in tissue-specific and microenvironment-specific lymphocyte homing. Curr. Opin. Immunol.12, 336–341 (2000). CASPubMed Google Scholar
Crone, S. A. & Lee, K. F. The bound leading the bound: target-derived receptors act as guidance cues. Neuron36, 333–335 (2002). CASPubMed Google Scholar
Iijima, M., Huang, Y. E. & Devreotes, P. Temporal and spatial regulation of chemotaxis. Dev. Cell3, 469–478 (2002). CASPubMed Google Scholar
Berg, H. C. A physicist looks at bacterial chemotaxis. Cold Spring Harb. Symp. Quant. Biol.53, 1–9 (1988). CASPubMed Google Scholar
Bourret, R. B. & Stock, A. M. Molecular information processing: lessons from bacterial chemotaxis. J. Biol. Chem.277, 9625–9628 (2002). CASPubMed Google Scholar
Zigmond, S. H. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol.75, 606–616 (1977). ArticleCASPubMed Google Scholar
Devreotes, P. N. & Zigmond, S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol.4, 649–686 (1988). CASPubMed Google Scholar
Weiner, O. D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol.14, 196–202 (2002). CASPubMedPubMed Central Google Scholar
Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc. Natl Acad. Sci. USA101, 8951–8956 (2004).
Mato, J. M., Losada, A., Nanjundiah, V. & Konijn, T. M. Signal input for a chemotactic response in the cellular slime mold Dictyostelium discoideum. Proc. Natl Acad. Sci. USA72, 4991–4993 (1975). CASPubMedPubMed Central Google Scholar
Stock, J. Sensitivity, cooperativity and gain in chemotaxis signal transduction. Trends Microbiol.7, 1–4 (1999). CASPubMed Google Scholar
Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science302, 1704–1709 (2003). CASPubMed Google Scholar
Postma, M., Bosgraaf, L., Loovers, H. M. & Van Haastert, P. J. M. Chemotaxis: signalling modules join hands at front and tail. EMBO Rep.5, 35–40 (2004). The authors present a concept for chemotaxis based on the diffusion properties of signalling molecules, and their organization in several modules that regulate actin and myosin. CASPubMedPubMed Central Google Scholar
Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell112, 453–465 (2003). An excellent review on the regulation of actin filaments in motile cells by the Arp2/3 complex, profilin, capping proteins, WASP and WAVE/SCAR. CASPubMed Google Scholar
Swanson, J. A. & Taylor, D. L. Local and spatially coordinated movements in Dictyostelium discoideum amoebae during chemotaxis. Cell28, 225–232 (1982). CASPubMed Google Scholar
Varnum-Finney, B., Edwards, K. B., Voss, E. & Soll, D. R. Amebae of Dictyostelium discoideum respond to an increasing temporal gradient of the chemoattractant cAMP with a reduced frequency of turning: evidence for a temporal mechanism in ameboid chemotaxis. Cell Motil. Cytoskeleton8, 7–17 (1987). CASPubMed Google Scholar
Baldauf, S. L., Roger, A. J., Wenk-Siefert, I. & Doolittle, W. F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science290, 972–977 (2000). CASPubMed Google Scholar
Wessels, D., Vawter-Hugart, H., Murray, J. & Soll, D. R. Three-dimensional dynamics of pseudopod formation and the regulation of turning during the motility cycle of Dictyostelium. Cell Motil. Cytoskeleton27, 1–12 (1994). CASPubMed Google Scholar
Postma, M. et al. Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia. Mol. Biol. Cell14, 5019–5027 (2003). CASPubMedPubMed Central Google Scholar
Wu, L., Valkema, R., Van Haastert, P. J. & Devreotes, P. N. The G protein β subunit is essential for multiple responses to chemoattractants in Dictyostelium. J. Cell Biol.129, 1667–1675 (1995). CASPubMed Google Scholar
Insall, R. H., Soede, R. D., Schaap, P. & Devreotes, P. N. Two cAMP receptors activate common signaling pathways in Dictyostelium. Mol. Biol. Cell5, 703–711 (1994). CASPubMedPubMed Central Google Scholar
Kriebel, P. W., Barr, V. A. & Parent, C. A. Adenylyl cyclase localization regulates streaming during chemotaxis. Cell112, 549–560 (2003). CASPubMed Google Scholar
Soll, D. R., Wessels, D., Heid, P. J. & Zhang, H. A contextual framework for characterizing motility and chemotaxis mutants in Dictyostelium discoideum. J. Muscle Res. Cell Motil.23, 659–672 (2002). CASPubMed Google Scholar
Soll, D. R. The use of computers in understanding how animal cells crawl. Int. Rev. Cytol.163, 43–104 (1995). CASPubMed Google Scholar
Postma, M. et al. Sensitization of Dictyostelium chemotaxis by PI3-kinase mediated self-organizing signalling patches. J. Cell Sci.117, 2925–2935 (2004). CASPubMed Google Scholar
Varnum, B. & Soll, D. R. Effects of cAMP on single cell motility in Dictyostelium. J. Cell Biol.99, 1151–1155 (1984). CASPubMed Google Scholar
Verkhovsky, A. B., Svitkina, T. M. & Borisy, G. G. Self-polarization and directional motility of cytoplasm. Curr. Biol.9, 11–20 (1999). CASPubMed Google Scholar
Bretschneider, T. et al. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr. Biol.14, 1–10 (2004). CASPubMed Google Scholar
Nicolis, G. & Prigogine, I. Self-organization in nonequilibrium systems: from dissipative structures to order through fluctuations. (John Wiley & Sons, New York, 1977). Google Scholar
Devreotes, P. & Janetopoulos, C. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem.278, 20445–20448 (2003). The authors define directional sensing as the ability of a cell to detect an asymmetric extracellular cue and generate an internal amplified response, whereas polarization is defined as the propensity of the cell to assume an asymmetric shape with a defined anterior and posterior. With these definitions many models for chemotaxis are evaluated. ArticleCASPubMed Google Scholar
Chen, L. et al. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol. Biol. Cell14, 5028–5037 (2003). CASPubMedPubMed Central Google Scholar
Van Duijn, B. & Van Haastert, P. J. Independent control of locomotion and orientation during Dictyostelium discoideum chemotaxis. J. Cell Sci.102, 763–768 (1992). CASPubMed Google Scholar
Parent, C. A., Blacklock, B. J., Froehlich, W. M., Murphy, D. B. & Devreotes, P. N. G protein signaling events are activated at the leading edge of chemotactic cells. Cell95, 81–91 (1998). CASPubMed Google Scholar
Klein, P. S. et al. A chemoattractant receptor controls development in Dictyostelium discoideum. Science241, 1467–1472 (1988). CASPubMed Google Scholar
Saxe, C. L. 3rd, Johnson, R., Devreotes, P. N. & Kimmel, A. R. Multiple genes for cell surface cAMP receptors in Dictyostelium discoideum. Dev. Genet.12, 6–13 (1991). CASPubMed Google Scholar
Youn, B. S., Mantel, C. & Broxmeyer, H. E. Chemokines, chemokine receptors and hematopoiesis. Immunol. Rev.177, 150–174 (2000). CASPubMed Google Scholar
Le, Y., Murphy, P. M. & Wang, J. M. Formyl-peptide receptors revisited. Trends Immunol.23, 541–548 (2002). CASPubMed Google Scholar
Maghazachi, A. A. G protein-coupled receptors in natural killer cells. J. Leukoc. Biol.74, 16–24 (2003). CASPubMed Google Scholar
Kim, J. Y., Borleis, J. A. & Devreotes, P. N. Switching of chemoattractant receptors programs development and morphogenesis in Dictyostelium: receptor subtypes activate common responses at different agonist concentrations. Dev. Biol.197, 117–128 (1998). CASPubMed Google Scholar
Dormann, D., Kim, J. Y., Devreotes, P. N. & Weijer, C. J. cAMP receptor affinity controls wave dynamics, geometry and morphogenesis in Dictyostelium. J. Cell Sci.114, 2513–2523 (2001). CASPubMed Google Scholar
Kim, J. Y. et al. Phosphorylation of chemoattractant receptors is not essential for chemotaxis or termination of G-protein-mediated responses. J. Biol. Chem.272, 27313–27318 (1997). CASPubMed Google Scholar
Richardson, R. M., Marjoram, R. J., Barak, L. S. & Snyderman, R. Role of the cytoplasmic tails of CXCR1 and CXCR2 in mediating leukocyte migration, activation, and regulation. J. Immunol.170, 2904–2911 (2003). CASPubMed Google Scholar
Zhang, N., Long, Y. & Devreotes, P. N. Gγ in Dictyostelium: its role in localization of Gβγ to the membrane is required for chemotaxis in shallow gradients. Mol. Biol. Cell12, 3204–3213 (2001). CASPubMedPubMed Central Google Scholar
Janetopoulos, C., Jin, T. & Devreotes, P. Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science291, 2408–2411 (2001). CASPubMed Google Scholar
Xu, J. et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell114, 201–214 (2003). Expression of constitutively active and dominant-negative versions of various G proteins and GTPases in neutrophils indicate that chemoattractant-mediated signals segregate into two mutually exclusive pathways: Gi–PtdIns(3,4,5)P3–Rac-dependent formation of F-actin at the front of cells and G12/13–RhoA-dependent formation of myosin-II filaments at the back. CASPubMed Google Scholar
Araki, T. et al. Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor. Embo J.17, 4018–4028 (1998). CASPubMedPubMed Central Google Scholar
Milne, J. L., Wu, L., Caterina, M. J. & Devreotes, P. N. Seven helix cAMP receptors stimulate Ca2+ entry in the absence of functional G proteins in Dictyostelium. J. Biol. Chem.270, 5926–5931 (1995). CASPubMed Google Scholar
Maeda, M. & Firtel, R. A. Activation of the mitogen-activated protein kinase ERK2 by the chemoattractant folic acid in Dictyostelium. J. Biol. Chem.272, 23690–23695 (1997). CASPubMed Google Scholar
Meili, R. et al. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. Embo J.18, 2092–2105 (1999). CASPubMedPubMed Central Google Scholar
Servant, G. et al. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science287, 1037–1040 (2000). CASPubMedPubMed Central Google Scholar
Zhou, K., Takegawa, K., Emr, S. D. & Firtel, R. A. 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.15, 5645–5656 (1995). CASPubMedPubMed Central Google Scholar
Hirsch, E. et al. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science287, 1049–1053 (2000). CASPubMed Google Scholar
Huang, Y. E. et al. Receptor mediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. Mol. Biol. Cell14, 1913–1922 (2003). CASPubMedPubMed Central Google Scholar
Iijima, M. & Devreotes, P. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell109, 599–610 (2002). This paper and reference 60 characterize in detail the function and cellular localization of PI3K and Pten inD. discoideumcells. During chemotaxis PI3K is enriched at the leading edge and Pten accumulates at the posterior membrane of the cell. CASPubMed Google Scholar
Kalesnikoff, J. et al. The role of SHIP in cytokine-induced signaling. Rev. Physiol. Biochem. Pharmacol.149, 87–103 (2003). CASPubMed Google Scholar
Loovers, H. et al. A diverse family of inositol 5-phosphatases playing a role in growth and development in Dictyostelium discoideum. J. Biol. Chem.278, 5652–5658 (2002). PubMed Google Scholar
Funamoto, S., Meili, R., Lee, S., Parry, L. & Firtel, R. A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell109, 611–623 (2002). CASPubMed Google Scholar
Iijima, M., Huang, Y. E., Luo, H. R., Vazquez, F. & Devreotes, P. N. Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J. Biol. Chem.279, 16606–16613 (2004). CASPubMed Google Scholar
Wang, F. et al. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nature Cell Biol.4, 513–518 (2002). CASPubMed Google Scholar
Millard, T. H., Sharp, S. J. & Machesky, L. M. Signalling to actin assembly via the WASP (Wiskott–Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem. J.380, 1–17 (2004). CASPubMedPubMed Central Google Scholar
Machesky, L. M. & Insall, R. H. Scar1 and the related Wiskott–Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol.8, 1347–1356 (1998). CASPubMed Google Scholar
Blagg, S. L., Stewart, M., Sambles, C. & Insall, R. H. PIR121 regulates pseudopod dynamics and SCAR activity in Dictyostelium. Curr. Biol.13, 1480–1487 (2003). CASPubMed Google Scholar
Bear, J. E., Rawls, J. F. & Saxe, C. L. 3rd. SCAR, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J. Cell Biol.142, 1325–1335 (1998). CASPubMedPubMed Central Google Scholar
Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature420, 629–635 (2002). CASPubMed Google Scholar
Gardiner, E. M. et al. Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr. Biol.12, 2029–2034 (2002). CASPubMed Google Scholar
Itoh, R. E. et al. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell Biol.22, 6582–6591 (2002). CASPubMedPubMed Central Google Scholar
Wedlich-Soldner, R., Altschuler, S., Wu, L. & Li, R. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science299, 1231–1235 (2003). CASPubMed Google Scholar
Chubb, J. R. & Insall, R. H. Dictyostelium: an ideal organism for genetic dissection of Ras signalling networks. Biochim. Biophys. Acta1525, 262–271 (2001). CASPubMed Google Scholar
Lim, C. J., Spiegelman, G. B. & Weeks, G. Cytoskeletal regulation by Dictyostelium Ras subfamily proteins. J. Muscle Res. Cell Motil.23, 729–736 (2002). CASPubMed Google Scholar
Li, Z. et al. Directional sensing requires Gβγ-mediated PAK1 and PIXα-dependent activation of Cdc42. Cell114, 215–227 (2003). CASPubMed Google Scholar
Welch, H. C., Coadwell, W. J., Stephens, L. R. & Hawkins, P. T. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett.546, 93–97 (2003). CASPubMed Google Scholar
Welch, H. C. et al. P-Rex1, a PtdIns(3,4,5)P3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell108, 809–821 (2002). CASPubMed Google Scholar
Park, H. S. et al. Sequential activation of phosphatidylinositol 3-kinase, βPix, Rac1, and Nox1 in growth factor-induced production of H2O2 . Mol. Cell Biol.24, 4384–4394 (2004). CASPubMedPubMed Central Google Scholar
Srinivasan, S. et al. Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. J. Cell Biol.160, 375–385 (2003). CASPubMedPubMed Central Google Scholar
Levi, S., Polyakov, M. V. & Egelhoff, T. T. Myosin II dynamics in Dictyostelium: determinants for filament assembly and translocation to the cell cortex during chemoattractant responses. Cell Motil. Cytoskeleton53, 177–188 (2002). CASPubMed Google Scholar
Moores, S. L., Sabry, J. H. & Spudich, J. A. Myosin dynamics in live Dictyostelium cells. Proc. Natl Acad. Sci. USA93, 443–446 (1996). CASPubMedPubMed Central Google Scholar
Eddy, R. J., Pierini, L. M., Matsumura, F. & Maxfield, F. R. Ca2+-dependent myosin II activation is required for uropod retraction during neutrophil migration. J. Cell Sci.113, 1287–1298 (2000). CASPubMed Google Scholar
Bosgraaf, L. et al. A novel cGMP signalling pathway mediating myosin phosphorylation and chemotaxis in Dictyostelium. Embo J.21, 4560–4570 (2002). Using mutants with deletions of guanylyl cyclases, cGMP-phosphodiesterases or cGMP-binding targets, the authors characterize the function of cGMP inD. discoideumas an inducer of myosin-II filaments in the cortex at the back of the cell, leading to suppression of lateral pseudopodia. CASPubMedPubMed Central Google Scholar
Liu, G. & Newell, P. C. Role of cyclic GMP in signal transduction to cytoskeletal myosin. Symp. Soc. Exp. Biol.47, 283–295 (1993). CASPubMed Google Scholar
Goldberg, J. M., Bosgraaf, L., Van Haastert, P. J. M. & Smith, L. Identification of four candidate cGMP targets in Dictyostelium. Proc. Natl Acad. Sci. USA99, 6749–6754 (2002). CASPubMedPubMed Central Google Scholar
Roelofs, J., Smith, J. L. & Van Haastert, P. J. M. cGMP signalling: different ways to create a pathway. Trends Genet.19, 132–134 (2002). Google Scholar
Chung, C. Y., Potikyan, G. & Firtel, R. A. Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol. Cell7, 937–947 (2001). CASPubMed Google Scholar
De La Roche, M. A., Smith, J. L., Betapudi, V., Egelhoff, T. T. & Cote, G. P. Signaling pathways regulating Dictyostelium myosin II. J. Muscle Res. Cell Motil.23, 703–718 (2002). CASPubMed Google Scholar
Steimle, P. A. et al. Recruitment of a myosin heavy chain kinase to actin-rich protrusions in Dictyostelium. Curr. Biol.11, 708–713 (2001). CASPubMed Google Scholar
Riento, K. & Ridley, A. J. ROCKs: multifunctional kinases in cell behaviour. Nature Rev. Mol. Cell Biol.4, 446–456 (2003). CAS Google Scholar
Van Haastert, P. J. M. & Van der Heijden, P. R. Excitation, adaptation, and deadaptation of the cAMP-mediated cGMP response in Dictyostelium discoideum. J. Cell Biol.96, 347–353 (1983). CASPubMed Google Scholar
Berlot, C. H., Spudich, J. A. & Devreotes, P. N. Chemoattractant-elicited increases in myosin phosphorylation in Dictyostelium. Cell43, 307–314 (1985). CASPubMed Google Scholar
Zhang, H. et al. Phosphorylation of the myosin regulatory light chain plays a role in motility and polarity during Dictyostelium chemotaxis. J. Cell Sci.115, 1733–1747 (2002). CASPubMed Google Scholar
Stock, A. M. & Mowbray, S. L. Bacterial chemotaxis: a field in motion. Curr. Opin. Struct. Biol.5, 744–751 (1995). CASPubMed Google Scholar
Caterina, M. J., Devreotes, P. N., 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.270, 8667–8672 (1995). CASPubMed Google Scholar
Valkema, R. & Van Haastert, P. J. Inhibition of receptor-stimulated guanylyl cyclase by intracellular calcium ions in Dictyostelium cells. Biochem. Biophys. Res. Commun.186, 263–268 (1992). CASPubMed Google Scholar
Kuwayama, H. & Van Haastert, P. J. Regulation of guanylyl cyclase by a cGMP-binding protein during chemotaxis in Dictyostelium discoideum. J. Biol. Chem.271, 23718–23724 (1996). CASPubMed Google Scholar
Bosgraaf, L. et al. Identification and characterization of two unusual cGMP-stimulated phoshodiesterases in Dictyostelium. Mol. Biol. Cell13, 3878–3889 (2002). CASPubMedPubMed Central Google Scholar
Valkema, R. & Van Haastert, P. J. M. A model for cAMP-mediated cGMP response in Dictyostelium discoideum. Mol. Biol. Cell5, 575–585 (1994). CASPubMedPubMed Central Google Scholar
Jin, T., Zhang, N., Long, Y., Parent, C. A. & Devreotes, P. N. Localization of the G protein βγ complex in living cells during chemotaxis. Science287, 1034–1036 (2000). CASPubMed Google Scholar
Sadhu, C., Masinovsky, B., Dick, K., Sowell, C. G. & Staunton, D. E. Essential role of phosphoinositide 3-kinase δ in neutrophil directional movement. J. Immunol.170, 2647–2654 (2003). CASPubMed Google Scholar
Sulis, M. L. & Parsons, R. PTEN: from pathology to biology. Trends Cell Biol.13, 478–483 (2003). CASPubMed Google Scholar
Traynor-Kaplan, A. E. et al. Transient increase in phosphatidylinositol 3,4-bisphosphate and phosphatidylinositol trisphosphate during activation of human neutrophils. J. Biol. Chem.264, 15668–15673 (1989). CASPubMed Google Scholar
Roos, W., Scheidegger, C. & Gerish, G. Adenylate cyclase activity oscillations as signals for cell aggregation in Dictyostelium discoideum. Nature266, 259–261 (1977). CASPubMed Google Scholar
Jackowski, S. & Sha'afi, R. I. Response of adenosine cyclic 3′,5′-monophosphate level in rabbit neutrophils to the chemotactic peptide formyl-methionyl-leucyl-phenylalanine. Mol. Pharmacol.16, 473–481 (1979). CASPubMed Google Scholar
van Haastert, P. J. & van Dijken, P. Biochemistry and genetics of inositol phosphate metabolism in Dictyostelium. FEBS Lett.410, 39–43 (1997). CASPubMed Google Scholar
Berridge, M. J. & Irvine, R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature312, 315–321 (1984). CASPubMed Google Scholar
Bumann, J., Wurster, B. & Malchow, D. Attractant-induced changes and oscillations of the extracellular Ca++ concentration in suspensions of differentiating Dictyostelium cells. J. Cell Biol.98, 173–178 (1984). CASPubMed Google Scholar
Klein, P., Vaughan, R., Borleis, J. & Devreotes, P. The surface cyclic AMP receptor in Dictyostelium Levels of ligand-induced phosphorylation, solubilization, identification of primary transcript, and developmental regulation of expression. J. Biol. Chem.262, 358–364 (1987). CASPubMed Google Scholar
Xiao, Z., Zhang, N., Murphy, D. B. & Devreotes, P. N. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J. Cell Biol.139, 365–374 (1997). CASPubMedPubMed Central Google Scholar
Servant, G., Weiner, O. D., Neptune, E. R., Sedat, J. W. & Bourne, H. R. Dynamics of a chemoattractant receptor in living neutrophils during chemotaxis. Mol. Biol. Cell10, 1163–1178 (1999). CASPubMedPubMed Central Google Scholar
Chen, L. et al. 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 (2003). CASPubMedPubMed Central Google Scholar