Sequential signaling in plasma-membrane domains during macropinosome formation in macrophages

Journal of Cell Science

Volumn 122, Issue 18, 2009, Pages 3250-3261

  Yoshida, Sei ^a   Hoppe, Adam D ^a,b   Araki, Nobukazu ^c   Swanson, Joel A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c KAGAWA UNIVERSITY   (Japan)

Author keywords

FRET; Macrophage; Macropinocytosis; PtdIns (3,4,5)P3; Rac1

Indexed keywords

PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; RAB PROTEIN; RAC1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL VACUOLE; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MACROPHAGE; MACROPINOSOME; MOUSE; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL MEMBRANE; FEMALE; MACROPHAGES; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PINOCYTOSIS; RAB5 GTP-BINDING PROTEINS; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 70350349921     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.053207     Document Type: Article

References (44)

1. Amyere, M., Payrastre, B., Krause, U., van der Smissen, P., Veithen, A. and Courtoy, P. J. (2000). Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation phosphoinositide 3-kinase and phospholipase C. Mol. Biol. Cell 11, 3453-3467.
2. Araki, N., Johnson, M. T. and Swanson, J. A. (1996). A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135, 1249-1260.
3. Araki, N., Hatae, T., Furukawa, A. and Swanson, J. A. (2003). Phosphoinositide-3-kinase-independent contractile activites associated with Fcγ-receptor-mediated phagocytosis and macropinocytosis in macrophages. J. Cell Sci. 116, 247-257.
4. Araki, N., Hamasaki, M., Egami, Y. and Hatae, T. (2006). Effect of 3-methylamide on the fusion process of macropinosomes in EGF-stimulated A431 cells. Cell Struct. Funct. 31, 145-157.
5. Araki, N., Egami, Y., Watanabe, Y. and Hatae, T. (2007). Phosphoinositide metabolism during membrane ruffling and macropinosome formation in EGF-stimulated A431 cells. Exp. Cell Res. 313, 1496-1507.
6. Bar-Sagi, D. and Feramisco, J. R. (1986). Induction of membrane ruffling and fluid-phase pinocytosis in quiscent fibroblasts by ras proteins. Science 233, 1061-1068.
7. Beemiller, P., Hoppe, A. D. and Swanson, J. A. (2006). A phosphatidylinositol-3-kinase-dependent signal transduction regulates ARF1 and ARF6 during Fcγ receptor-mediated phagocytosis. PLoS Biol. 4, 0987-0999.
8. Cox, D., Chang, P., Zhang, Q., Reddy, P. G., Bokoch, G. M. and Greenberg, S. (1997). Requirement for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J. Exp. Med. 186, 1487-1494.
9. Dharmawardhane, S., Schurmann, A., Sells, M. A., Chernoff, J., Schmid, S. L. and Bokoch, G. M. (2000). Regulation of macropinocytosis by p21-activated kinase-1. Mol. Biol. Cell 11, 3341-3352.
10. Garrett, W. S., Chen, L. M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., Galan, J. E. and Mellman, I. (2000). Developmental control of endocytosis in Dendritic cells by Cdc42. Cell 102, 325-334.
11. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G. and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
12. Henry, R., Hoppe, A. D., Joshi, N. and Swanson, J. A. (2004). The uniformity of phagosome maturation in macrophages. J. Cell Biol. 164, 185-194.
13. Hewlett, L. J., Prescott, A. R. and Watts, C. (1994). The coated pit and macropinocytic pathways serve distinct endosome populations. J. Cell Biol. 124, 689-703.
14. Hoppe, A. D. and Swanson, J. A. (2004). Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15, 3509-3519.
15. Hoppe, A. D., Christensen, K. A. and Swanson, J. A. (2002). Fluorescence resonance energy transfer-based stoichiometry in living cells. Biophys. J. 83, 3652-3664.
16. Hoppe, A. D., Shorte, S. L., Swanson, J. A. and Heintzmann, R. (2008). Three-dimensional FRET reconstruction microscopy for analysis of dynamic molecular interaction in live cells. Biophys. J. 95, 400-418.
17. Ihara, S., Oka, T. and Fukui, Y. (2006). Direct binding of SWAP-70 to non-muscle actin is required for membrane ruffling. J. Cell Sci. 119, 500-507.
18. Kamen, L. A., Levinsohn, J. and Swanson, J. A. (2007). Differential association of phosphatidylinositol 3-kinase, SHIP-1, and PTEN with forming phagosomes. Mol. Biol. Cell 18, 2463-2472.
19. Katoh, H. and Negishi, H. (2003). RhoG activates Rac1 by direct interaction with Dock180-binding protein Elmo. Nature 424, 461-464.
20. Kerr, M. C. and Teasdale, R. D. (2009). Defining macropinocytosis. Traffic 10, 364-371.
21. Kheir, W. A., Gevrey, J.-C., Yamaguchi, H., Issac, B. and Cox, D. (2005). A WAVE2-Abi1 complex mediates CSF-1induced F-actin-rich membrane protrusions and migration in macrophage. J. Cell Sci. 118, 5369-5379.
22. Kutateladze, T. G., Ogburn, K. D., Watson, W. T., de Beer, T., Emr, S. D., Burd, C. G. and Overduin, M. (1999). Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol. Cell 3, 805-811.
23. Lanzetti, L., Palamidessi, A., Areces, L., Scita, G. and DiFiore, P. P. (2004). Rab5 is a signaling GTPase involved in actin remodeling by receptor tyrosine kinases. Nature 429, 309-314.
24. Lawe, D. C., Chawla, A., Merithew, E., Dumas, J., Carrington, W., Fogarty, K., Lifshiz, L., Tuft, R., Lambright, D. and Corvera, S. (2002). Sequential roles for phosphatidylinositol 3-phosphate and Rab5 in tethering and fusion of early endosomes via their interaction with EEA1. J. Biol. Chem. 277, 8611-8617.
25. Li, G., D'Souza-Schorey, C., Barbieri, M. A., Cooper, J. A. and Stahl, P. D. (1997). Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J. Biol. Chem. 272, 10337-10340.
26. Liberali, P., Kakkonen, E., Turacchio, G., Valente, C., Spaar, A., Perinetti, G., Böckmann, R. A., Corda, D., Colanzi, A., Marjomaki, V. et al. (2008). The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J. 27, 970-981.
27. Mercanti, V., Charette, S. J., Bennett, N., Ryckewaert, J. J., Letourneur, F. and Cosson, P. (2006). Selective membrane exclusion in phagocytic and macropinocytic cups. J. Cell Sci. 119, 4079-4087.
28. Mercer, J. and Helenius, A. (2009). Virus entry by macropinocytosis. Nat. Cell Biol. 11, 510-520.
29. Norbury, C. C. (2006). Drinking a lot is good for dendritic cells. Immunology 117, 443-451.
30. Papaconstanti, E. A., Ridley, A. J. and Vanhaesebroeck, B. (2007). The p100 delta isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J. 26, 3050-3061.
31. Porat-Shliom, N., Kloog, Y. and Donaldson, J. G. (2008). A unique platform for H-Ras signaling involving clathrin-independent endocytosis. Mol. Biol. Cell 19, 765-775.
32. Racoosin, E. L. and Swanson, J. A. (1989). Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J. Exp. Med. 170, 1635-1648.
33. Schnatwinkel, C., Christoforidis, S., Lindsay, M. R., Uttenweiler-Joseph, S., Wilm, M., Parton, R. G. and Zerial, M. (2004). The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2, 1363-1380.
34. Simonsen, A., Lippe, R., Christoforidis, S., Graullier, J. M., Brech, A., Callahan, J., Toh, B. H., Murphy, C., Zerial, M. and Stenmark, H. (1998). EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498.
35. 3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160, 375-385.
36. Swanson, J. A. (1989). Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J. Cell Sci. 94, 135-142.
37. Swanson, J. A. (2008). shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649.
38. Topp, J. D., Gray, N. W., Gerard, R. D. and Horazdovsky, B. F. (2004). Alsin is a Rab5 and Rac1 guanine nucleotide exchange factor. J. Biol. Chem. 279, 24612-24623.
39. Topp, J. D., Carney, D. S. and Horazdovsky, B. F. (2005). Biochemical characterization of Alsin, a Rab5 and Rac1 Guanine nucleotide Exchange Factor. Methods Enzymol. 403, 261-276.
40. Varnai, P. and Balla, T. (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist0induced dynamics and relationship to myo-[3H]inositol -labeled phosphoinositides pools. J. Cell Biol. 143, 501-510.
41. Varnai, P., Rother, K. I. and Balla, T. (1999). Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274, 10983-10989.
42. Wells, C. M., Walmsley, M., Ooi, S., Tybulewicz, V. and Ridley, A. J. (2004). Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J. Cell Sci. 117, 1259-1268.
43. West, M. A., Prescott, A. R., Eskelinen, E. L., Ridley, A. J. and Watts, C. (2000). Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr. Biol. 10, 839-848.
44. Zhang, Q., Calafat, J., Janssen, K. and Greenberg, S. (1999). ARF6 is required for growth factor- and Rac-mediated membrane ruffling in macrophages at a stage distal to Rac membrane targeting. Mol. Cell. Biol. 19, 8158-8168.