Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts

Journal of Cell Biology

Volumn 171, Issue 5, 2005, Pages 883-892

  Schneider, Ian C ^a   Haugh, Jason M ^a  

^a North Carolina State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR;

ANIMAL CELL; ARTICLE; CELL MIGRATION; DICTYOSTELIUM DISCOIDEUM; FEEDBACK SYSTEM; FIBROBLAST; FLUORESCENCE MICROSCOPY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; WOUND HEALING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 3T3 CELLS; ALGORITHMS; ANIMALS; CHEMOTAXIS; DICTYOSTELIUM; FIBROBLASTS; MICE; MODELS, BIOLOGICAL; NEUTROPHILS; PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION;

ANIMALIA; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA;

EID: 28544448768     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200509028     Document Type: Article

References (50)

1. Arrieumerlou, C., and M. Meyer. 2005. A local coupling model and compass parameter for eukaryotic chemotaxis. Dev. Cell. 8:215-227.
2. Axelrod, D. 2001. Total internal reflection fluorescence microscopy in cell biology. Traffic. 2:764-774.
3. Bhalla, U.S., P.T. Ram, and R. Iyengar. 2002. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science. 297:1018-1023.
4. Bokoch, G.M., C.J. Vlahos, Y. Wang, U.G. Knaus, and A.E. Traynor-Kaplan. 1996. Rac GTPase interacts specifically with phosphatidylinositol 3-kinase. Biochem. J. 315:775-779.
5. Deuel, T.F., R.S. Kawahara, T.A. Mustoe, and G.F. Pierce. 1991. Growth factors and wound healing: platelet-derived growth factor as a model cytokine. Annu. Rev. Med. 42:567-584.
6. Devreotes, P., and C. Janetopoulos. 2003. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278:20445-20448.
7. Devreotes, P.N., and S.H. Zigmond. 1988. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4:649-686.
8. Haugh, J.M., and I.C. Schneider. 2004. Spatial analysis of 3′ phosphoinositide signaling in living fibroblasts: I. Uniform stimulation model and bounds on dimensionless groups. Biophys. J. 86:589-598.
9. Haugh, J.M., F. Codazzi, M. Teruel, and T. Meyer. 2000. Spatial sensing in fibroblasts mediated by 3′ phosphoinositides. J. Cell Biol. 151:1269-1279.
10. 2 3-OH kinase. Nature. 358:157-159.
11. Heldin, C.-H., and B. Westermark. 1999. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79:1283-1316.
12. Jackson, T.R., L.R. Stephens, and P.T. Hawkins. 1992. Receptor specificity of growth factor-stimulated synthesis of 3-phosphorylated inositol lipids in Swiss 3T3 cells. J. Biol. Chem. 267:16627-16636.
13. Janetopoulos, C., L. Ma, P.N. Devreotes, and P.A. Iglesias. 2004. Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc. Natl. Acad. Sci. USA. 101:8951-8956.
14. Kazlauskas, A., and J.A. Cooper. 1990. Phosphorylation of the PDGF receptor β-subunit creates a tight binding site for phosphatidylinositol-3 kinase. EMBO J. 9:3279-3286.
15. Kundra, V., J.A. Escobedo, A. Kazlauskas, H.K. Kim, S.G. Rhee, L.T. Williams, and B.R. Zetter. 1994. Regulation of chemotaxis by the platelet-derived growth factor receptor-β. Nature. 367:474-476.
16. Lanni, F., A.S. Waggoner, and D.L. Taylor. 1985. Structural organization of interphase 3T3 fibroblasts studied by total internal reflection fluorescence microscopy. J. Cell Biol. 100:1091-1102.
17. Lauffenburger, D.A., and A.F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
18. Levchenko, A., and P.A. Iglesias. 2002. Models of eukaryotic gradient sensing: application to chemotaxis of amoebae and neutrophils. Biophys. J. 82:50-63.
19. Ma, L., C. Janetopoulos, L. Yang, P.N. Devreotes, and P.A. Iglesias. 2004. Two complementary, local excitation, global inhibition mechanisms acting in parallel can explain the chemoattractant-induced regulation of PI(3,4,5)P3 response in Dictyostelium cells. Biophys. J. 87:3764-3774.
20. Meili, R., C. Ellsworth, S. Lee, T.B.K. Reddy, H. Ma, and R.A. Firtel. 1999. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 18:2092-2105.
21. Meinhardt, H. 1999. Orientation of chemotactic cells and growth cones: models and mechanisms. J. Cell Sci. 112:2867-2874.
22. Merlot, S., and R.A. Firtel. 2003. Leading the way: directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. J. Cell Sci. 116:3471-3478.
23. Narang, A., K.K. Subramanian, and D.A. Lauffenburger. 2001. A mathematical model for chemoattractant gradient sensing based on receptor-regulated membrane phospholipid signaling dynamics. Ann. Biomed. Eng. 29:677-691.
24. Parent, C.A., and P.N. Devreotes. 1999. A cell's sense of direction. Science. 284:765-770.
25. Parent, C.A., B.J. Blacklock, W.M. Froehlich, D.B. Murphy, and P.N. Devreotes. 1998. G protein signaling events are activated at the leading edge of chemotactic cells. Cell. 95:81-91.
26. Park, C.S., I.C. Schneider, and J.M. Haugh. 2003. Kinetic analysis of platelet-derived growth factor receptor/phosphoinositide 3-kinase/Akt signaling in fibroblasts. J. Biol. Chem. 278:37064-37072.
27. Postma, M., and P.J.M. Van Haastert. 2001. A diffusion-translocation model for gradient sensing by chemotactic cells. Biophys. J. 81:1314-1323.
28. Postma, M., J. Roelofs, J. Goedhart, H.M. Loovers, A.J. Visser, and P.J.M. Van Haastert. 2004. Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches. J. Cell Sci. 117:2925-2935.
29. Ridley, A.J. 2001. Rho GTPases and cell migration. J. Cell Sci. 114:2713-2722.
30. Schneider, I.C., and J.M. Haugh. 2004. Spatial analysis of 3′ phosphoinositide signaling in living fibroblasts: II. Parameter estimates for individual cells from experiments. Biophys. J. 86:599-608.
31. Schneider, I.C., E.M. Parrish, and J.M. Haugh. 2005. Spatial analysis of 3′ phosphoinositide signaling in living fibroblasts, III: Influence of cell morphology and morphological polarity. Biophys. J. 89:1420-1430.
32. Servant, G., O.D. Weiner, P. Herzmark, T. Balla, J.W. Sedat, and H.R. Bourne. 2000. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science. 287:1037-1040.
33. Singer, A.J., and R.A.F. Clark. 1999. Mechanisms of disease: cutaneous wound healing. N. Engl. J. Med. 341:738-746.
34. Skupsky, R., W. Losert, and R.J. Nossal. 2005. Distinguishing modes of eukaryotic gradient sensing. Biophys. J. 89:2806-2823.
35. 3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160:375-385.
36. Stephens, L.R., K.T. Hughes, and R.F. Irvine. 1991. Pathway of phosphatidylinositol( 3,4,5)-trisphosphate synthesis in activated neutrophils. Nature. 351:33-39.
37. Steyer, J.A., and W. Almers. 2001. A real-time view of life within 100 nm of the plasma membrane. Nat. Rev. Mol. Cell Biol. 2:268-275.
38. Subramanian, K.K., and A. Narang. 2004. A mechanistic model for eukaryotic gradient sensing: spontaneous and induced phosphoinositide polarization. J. Theor. Biol. 231:49-67.
39. Teruel, M.N., T.A. Blanpied, K. Shen, G.J. Augustine, and T. Meyer. 1999. A versatile microporation technique for the transfection of cultured CNS neurons. J. Neurosci. Methods. 93:37-48.
40. Tolias, K.F., L.C. Cantley, and C.L. Carpenter. 1995. Rho family GTPases bind to phosphoinositide kinases. J. Biol. Chem. 270:17656-17659.
41. Toomre, D., and D.J. Manstein. 2001. Lighting up the cell surface with evanescent wave microscopy. Trends Cell Biol. 11:298-303.
42. Vanhaesebroeck, B., S.J. Leevers, K. Ahmadi, J. Timms, R. Katso, P.C. Driscoll, R. Woscholski, P.J. Parker, and M.D. Waterfield. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70:535-602.
43. Wang, F., P. Herzmark, O.D. Weiner, S. Srinivasan, G. Servant, and H.R. Bourne. 2002. Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat. Cell Biol. 4:513-518.
44. Weiner, O.D. 2002. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14:196-202.
45. 3- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4:509-512.
46. Wennström, S., P. Hawkins, F. Cooke, K. Hara, K. Yonezawa, M. Kasuga, T. Jackson, L. Claesson-Welsh, and L. Stephens. 1994a. Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4:385-393.
47. Wennström, S., A. Siegbahn, K. Yokote, A. Arvidsson, C.-H. Heldin, S. Mori, and L. Claesson-Welsh. 1994b. Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene. 9:651-660.
48. Wymann, M., and A. Arcaro. 1994. Platelet-derived growth factor-induced phosphatidylinositol 3-kinase activation mediates actin rearrangements in fibroblasts. Biochem. J. 298:517-520.
49. Zigmond, S.H. 1977. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol. 75:606-616.
50. Zigmond, S.H., and S.J. Sullivan. 1979. Sensory adaptation of leukocytes to chemotactic peptides. J. Cell Biol. 82:517-527.