Signaling requirements for translocation of P-Rex1, a key Rac2 exchange factor involved in chemoattractant-stimulated human neutrophil function

Journal of Leukocyte Biology

Volumn 81, Issue 4, 2007, Pages 1127-1136

  Zhao, Tieming ^a   Nalbant, Perihan ^a   Hoshino, Mikio ^b   Dong, Xuemei ^c   Wu, Dianqing ^c   Bokoch, Gary M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chemoattractant receptors; Chemotaxis; GTPases; NADPH oxidase; Signal transduction

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN PREX 1; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; RAC2 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL MEMBRANE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL ADHESION; CELL MEMBRANE; CELLS, CULTURED; CHEMOTACTIC FACTORS; GTP-BINDING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; NEUTROPHILS; PROTEIN KINASES; PROTEIN TRANSPORT; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 33947684328     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0406251     Document Type: Article

References (44)

1. Greaves, D. R., Schall, T. J. (2000) Chemokines and myeloid cell recruitment. Microbes Infect. 2, 331-336.
2. Schall, T. J., Bacon, K. B. (1994) Chemokines, leukocyte trafficking, and inflammation. Curr. Opin. Immunol. 6, 865-873.
3. Bokoch, G. M. (2005) Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15, 163-171.
4. Diebold, B. A., Bokoch, G. M. (2005) Rho GTPases and the control of the oxidative burst in polymorphonuclear leukocytes. Curr. Top. Microbiol. Immunol. 291, 91-111.
5. Clark, R. A. (1990) The human neutrophil respiratory burst oxidase. J. Infect. Dis. 161, 1140-1147.
6. Benard, V., Bohl, B. P., Bokoch, G. M. (1999) Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13198-13204.
7. Zheng, Y. (2001) Dbl family guanine nucleotide exchange factors. Trends Biochem. Sci. 26, 724-732.
8. Rossman, K. L., Der, C. J., Sondek, J. (2005) GEF means go: turning on Rho GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180.
9. Welch, H. C., Coadwell, W. J., Ellson, C. D., Ferguson, G. J., Andrews, S. R., Erdjument-Bromage, H., Tempst, P., Hawkins, P. T., Stephens, L. R. (2002) P-Rex1, a PtdIns(3,4,5)P3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809-821.
10. Dong, X., Mo, Z., Bokoch, G., Guo, C., Li, Z., Wu, D. (2005) P-Rex1 is a primary Rac2 guanine nucleotide exchange factor in mouse neutrophils. Curr. Biol. 15, 1874-1879.
11. Welch, H. C., Condliffe, A. M., Milne, L. J., Ferguson, G. J., Hill, K., Webb, L. M., Okkenhaug, K., Coadwell, W. J., Andrews, S. R., Thelen, M., Jones, G. E., Hawkins, P. T., Stephens, L. R. (2005) P-Rex1 regulates neutrophil function. Curr. Biol. 15, 1867-1873.
12. Yoshizawa, M., Kawauchi, T., Sone, M., Nishimura, Y. V., Terao, M., Chihama, K., Nabeshima, Y., Hoshino, M. (2005) Involvement of a Rac activator, P-Rex1, in neurotrophin-derived signaling and neuronal migration. J. Neurosci. 25, 4406-4419.
13. Hill, K., Krugmann, S., Andrews, S. R., Coadwell, W. J., Finan, P., Welch, H. C., Hawkins, P. T., Stephens, L. R. (2005) Regulation of P-Rex1 by phosphatidylinositol (3,4,5)-trisphosphate and Gβγ subunits. J. Biol. Chem. 280, 4166-4173.
14. Mayeenuddin, L. H., McIntire, W. E., Garrison, J. C. (2006) Differential sensitivity of P-Rex1 to isoforms of G protein βγ dimers. J. Biol. Chem. 281, 1913-1920.
15. Heyworth, P. G., Bohl, B. P., Bokoch, G. M., Curnutte, J. T. (1994) Rac translocates independently of the neutrophil NADPH oxidase components p47-phox and p67-phox. Evidence for its interaction with flavocytochrome b558. J. Biol. Chem. 269, 30749-30752.
16. Quinn, M. T., Evans, T., Loetterle, L. R., Jesaitis, A. J., Bokoch, G. M. (1993) Translocation of Rac correlates with NADPH oxidase activation. Evidence for equimolar translocation of oxidase components. J. Biol. Chem. 268, 20983-20987.
17. Knaus, U. G., Heyworth, P. G., Kinsella, B. T., Curnutte, J. T., Bokoch, G. M. (1992) Purification and characterization of Rac 2. A cytosolic GTP-binding protein that regulates human neutrophil NADPH oxidase. J. Biol. Chem. 267, 23575-23582.
18. Jesaitis, A. J., Naemura, J. R., Painter, R. G., Sklar, L. A., Cochrane, C. G. (1982) Intracellular localization of N-formyl chemotactic receptor and Mg2+ dependent ATPase in human granulocytes. Biochim. Biophys. Acta 719, 556-568.
19. Bokoch, G. M., Bickford, K., Bohl, B. P. (1988) Subcellular localization and quantitation of the major neutrophil pertussis toxin substrate, Gn. J. Cell Biol. 106, 1927-1936.
20. Bokoch, G. M. (1987) The presence of free G protein β/γ subunits in human neutrophils results in suppression of adenylate cyclase activity. J. Biol. Chem. 262, 589-594.
21. Parkos, C. A., Cochrane, C. G., Schmitt, M., Jesaitis, A. J. (1985) Regulation of the oxidative response of human granulocytes to chemoattractants. No evidence for stimulated traffic of redox enzymes between endo and plasma membranes. J. Biol. Chem. 260, 6541-6547.
22. Bonacci, T. M., Mathews, J. L., Yuan, C., Lehmann, D. M., Malik, S., Wu, D., Font, J. L., Bidlack, J. M., Smrcka, A. V. (2006) Differential targeting of Gβα-subunit signaling with small molecules. Science 312, 443-446.
23. Zhao, T., Benard, V., Bohl, B. P., Bokoch, G. M. (2003) The molecular basis for adhesion-mediated suppression of reactive oxygen species generation by human neutrophils. J. Clin. Invest. 112, 1732-1740.
24. Bokoch, G. M., Bohl, B. P., Chuang, T. H. (1994) Guanine nucleotide exchange regulates membrane translocation of Rac/Rho GTP-binding proteins. J. Biol. Chem. 269, 31674-31679.
25. Coue, M., Brenner, S. L., Spector, I., Korn, E. D. (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett. 213, 316-318.
26. Gardiner, E. M., Pestonjamasp, K. N., Bohl, B. P., Chamberlain, C., Hahn, K. M., Bokoch, G. M. (2002) Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr. Biol. 12, 2029-2034.
27. Bokoch, G. M., Gilman, A. G. (1984) Inhibition of receptor-mediated release of arachidonic acid by pertussis toxin. Cell 39, 301-308.
28. Mayeenuddin, L. H., Garrison, J. C. (2006) Phosphorylation of P-Rex1 by the cyclic AMP-dependent protein kinase inhibits the phosphatidylinositiol (3,4,5)-trisphosphate and Gβγ-mediated regulation of its activity. J. Biol. Chem. 281, 1921-1928.
29. Christensen, A. E., Selheim, F., de Rooij, J., Dremier, S., Schwede, F., Dao, K. K., Martinez, A., Maenhaut, C., Bos, J. L., Genieser, H. G., Doskeland, S. O. (2003) cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J. Biol. Chem. 278, 35394-35402.
30. Srinivasan, S., Wang, F., Glavas, S., Ott, A., Hofmann, F., Aktories, K., Kalman, D., Bourne, H. R. (2003) Rac and Cdc42 play distinct roles in regulating PI (3,4,5)P3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160, 375-385.
31. Jin, T., Zhang, N., Long, Y., Parent, C. A., Devreotes, P. N. (2000) Localization of the G protein βγ complex in living cells during chemotaxis. Science 287, 1034-1036.
32. Zhao, T., Bokoch, G. M. (2005) Critical role of proline-rich tyrosine kinase 2 in reversion of the adhesion-mediated suppression of reactive oxygen species generation by human neutrophils. J. Immunol. 174, 8049-8055.
33. Kim, C., Marchal, C. C., Penninger, J., Dinauer, M. C. (2003) The hemopoietic Rho/Rac guanine nucleotide exchange factor Vav1 regulates N-formyl-methionyl-leucyl-phenylalanine-activated neutrophil functions. J. Immunol. 171, 4425-4430.
34. Van Aelst, L., D'Souza-Schorey, C. (1997) Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
35. Michiels, F., Stam, J. C., Hordijk, P. L., van der Kammen, R. A., Ruuls-Van Stalle, L., Feltkamp, C. A., Collard, J. G. (1997) Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation. J. Cell Biol. 137, 387-398.
36. Buchanan, F. G., Elliot, C. M., Gibbs, M., Exton, J. H. (2000) Translocation of the Rac1 guanine nucleotide exchange factor Tiam1 induced by platelet-derived growth factor and lysophosphatidic acid. J. Biol. Chem. 275, 9742-9748.
37. Han, J., Luby-Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R. D., Krishna, U. M., Falck, J. R., White, M. A., Broek, D. (1998) Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279, 558-560.
38. Vedham, V., Phee, H., Coggeshall, K. M. (2005) Vav activation and function as a Rac guanine nucleotide exchange factor in macrophage colony-stimulating factor-induced macrophage chemotaxis. Mol. Cell. Biol. 25, 4211-4220.
39. Krendel, M., Zenke, F. T., Bokoch, G. M. (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4, 294-301.
40. Rivkin, I., Rosenblatt, J., Becker, E. L. (1975) The role of cyclic AMP in the chemotactic responsiveness and spontaneous motility of rabbit peritoneal neutrophils. The inhibition of neutrophil movement and the elevation of cyclic AMP levels by catecholamines, prostaglandins, theophylline and cholera toxin. J. Immunol. 115, 1126-1134.
41. Harvath, L., Robbins, J. D., Russell, A. A., Seamon, K. B. (1991) cAMP and human neutrophil chemotaxis. Elevation of cAMP differentially affects chemotactic responsiveness. J. Immunol. 146, 224-232.
42. Zalavary, S., Bengtsson, T. (1998) Adenosine inhibits actin dynamics in human neutrophils: evidence for the involvement of cAMP. Eur. J. Cell Biol. 75, 128-139.
43. Jones, S. L., Sharief, Y. (2005) Asymmetrical protein kinase A activity establishes neutrophil cytoskeletal polarity and enables chemotaxis. J. Leukoc. Biol. 78, 248-258.
44. Howe, A. K., Baldor, L. C., Hogan, B. P. (2005) Spatial regulation of the cAMP-dependent protein kinase during chemotactic cell migration. Proc. Natl. Acad. Sci. USA 102, 14320-14325.