Negative charges in the flexible N-terminal domain of Rho GDP-dissociation inhibitors (RhoGDIs) regulate the targeting of the RhoGDI-Rac1 complex to membranes

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2560-2569

  Ueyama, Takehiko ^a   Son, Jeonghyun ^a   Kobayashi, Takeshi ^b   Hamada, Takeshi ^a   Nakamura, Takashi ^a   Sakaguchi, Hirofumi ^c   Shirafuji, Toshihiko ^a   Saito, Naoaki ^a  

^a KOBE UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FC RECEPTOR; HETERODIMER; PHOSPHOLIPID; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CYTOPLASM; HUMAN; HUMAN CELL; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALS; CELL MEMBRANE; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MICROSCOPY, CONFOCAL; PHAGOSOMES; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RHO-SPECIFIC GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS;

EID: 84883348477     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300209     Document Type: Article

References (33)

1. Garcia-Mata, R., E. Boulter, and K. Burridge. 2011. The "invisible hand": regulation of RHO GTPases by RHOGDIs. Nat. Rev. Mol. Cell Biol. 12: 493-504.
2. Dovas, A., and J. R. Couchman. 2005. RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390: 1-9.
3. Takahashi, K., T. Sasaki, A. Mammoto, K. Takaishi, T. Kameyama, S. Tsukita, and Y. Takai. 1997. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272: 23371-23375.
4. Yamashita, T., and M. Tohyama. 2003. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6: 461-467.
5. DerMardirossian, C., A. Schnelzer, and G. M. Bokoch. 2004. Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol. Cell 15: 117-127.
6. DerMardirossian, C., G. Rocklin, J. Y. Seo, and G. M. Bokoch. 2006. Phosphorylation of RhoGDI by Src regulates Rho GTPase binding and cytosolmembrane cycling. Mol. Biol. Cell 17: 4760-4768.
7. Ugolev, Y., Y. Berdichevsky, C. Weinbaum, and E. Pick. 2008. Dissociation of Rac1(GDP)·RhoGDI complexes by the cooperative action of anionic liposomes containing phosphatidylinositol 3,4,5-trisphosphate, Rac guanine nucleotide exchange factor, and GTP. J. Biol. Chem. 283: 22257-22271.
8. Leto, T. L., S. Morand, D. Hurt, and T. Ueyama. 2009. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid. Redox Signal. 11: 2607-2619.
9. Nauseef, W. M. 2008. Biological roles for the NOX family NADPH oxidases. J. Biol. Chem. 283: 16961-16965.
10. Sumimoto, H. 2008. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275: 3249-3277.
11. Brunet, N., A. Morin, and B. Olofsson. 2002. RhoGDI-3 regulates RhoG and targets this protein to the Golgi complex through its unique N-terminal domain. Traffic 3: 342-357.
12. Keep, N. H., M. Barnes, I. Barsukov, R. Badii, L. Y. Lian, A. W. Segal, P. C. Moody, and G. C. Roberts. 1997. A modulator of rho family G proteins, rhoGDI, binds these G proteins via an immunoglobulin-like domain and a flexible N-terminal arm. Structure 5: 623-633.
13. Grizot, S., J. Fauré, F. Fieschi, P. V. Vignais, M. C. Dagher, and E. Pebay-Peyroula. 2001. Crystal structure of the Rac1-RhoGDI complex involved in NADPH oxidase activation. Biochemistry 40: 10007-10013.
14. Scheffzek, K., I. Stephan, O. N. Jensen, D. Illenberger, and P. Gierschik. 2000. The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nat. Struct. Biol. 7: 122-126.
15. Ueyama, T., M. Eto, K. Kami, T. Tatsuno, T. Kobayashi, Y. Shirai, M. R. Lennartz, R. Takeya, H. Sumimoto, and N. Saito. 2005. Isoform-specific membrane targeting mechanism of Rac during FcγR-mediated phagocytosis: positive charge-dependent and independent targeting mechanism of Rac to the phagosome. J. Immunol. 175: 2381-2390.
16. Yeung, T., B. Heit, J.-F. Dubuisson, G. D. Fairn, B. Chiu, R. Inman, A. Kapus, M. Swanson, and S. Grinstein. 2009. Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation. J. Cell Biol. 185: 917-928.
17. Garin, J., R. Diez, S. Kieffer, J. F. Dermine, S. Duclos, E. Gagnon, R. Sadoul, C. Rondeau, and M. Desjardins. 2001. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152: 165-180.
18. Robinson, J. M., and J. A. Badwey. 2002. Rapid association of cytoskeletal remodeling proteins with the developing phagosomes of human neutrophils. Histochem. Cell Biol. 118: 117-125.
19. Dovas, A., Y. Choi, A. Yoneda, H. A. Multhaupt, S. H. Kwon, D. Kang, E. S. Oh, and J. R. Couchman. 2010. Serine 34 phosphorylation of rho guanine dissociation inhibitor (RhoGDIα) links signaling from conventional protein kinase C to RhoGTPase in cell adhesion. J. Biol. Chem. 285: 23296-23308.
20. Ueyama, T., M. R. Lennartz, Y. Noda, T. Kobayashi, Y. Shirai, K. Rikitake, T. Yamasaki, S. Hayashi, N. Sakai, H. Seguchi, et al. 2004. Superoxide production at phagosomal cup/phagosome through βI protein kinase C during FcγR-mediated phagocytosis in microglia. J. Immunol. 173: 4582-4589.
21. phox. Mol. Biol. Cell 18: 441-454.
22. phox phosphatidylinositol 3-phosphate (PI(3)P) binding. J. Biol. Chem. 286: 40693-40705.
23. Ueyama, T., M. Geiszt, and T. L. Leto. 2006. Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases. Mol. Cell. Biol. 26: 2160-2174.
24. Karasawa, S., T. Araki, T. Nagai, H. Mizuno, and A. Miyawaki. 2004. Cyanemitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem. J. 381: 307-312.
25. Colley, W. C., T. C. Sung, R. Roll, J. Jenco, S. M. Hammond, Y. Altshuller, D. Bar-Sagi, A. J. Morris, and M. A. Frohman. 1997. Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr. Biol. 7: 191-201.
26. Cheeseman, K. L., T. Ueyama, T. M. Michaud, K. Kashiwagi, D. Wang, L. A. Flax, Y. Shirai, D. J. Loegering, N. Saito, and M. R. Lennartz. 2006. Targeting of protein kinase C-ε during Fcγ receptor-dependent phagocytosis requires the εC1B domain and phospholipase C-γ1. Mol. Biol. Cell 17: 799-813.
27. Dransart, E., A. Morin, J. Cherfils, and B. Olofsson. 2005. Uncoupling of inhibitory and shuttling functions of Rho GDP dissociation inhibitors. J. Biol. Chem. 280: 4674-4683.
28. Nomanbhoy, T. K., and R. Cerione. 1996. Characterization of the interaction between RhoGDI and Cdc42Hs using fluorescence spectroscopy. J. Biol. Chem. 271: 10004-10009.
29. Golovanov, A. P., T. H. Chuang, C. DerMardirossian, I. Barsukov, D. Hawkins, R. Badii, G. M. Bokoch, L. Y. Lian, and G. C. Roberts. 2001. Structure-activity relationships in flexible protein domains: regulation of rho GTPases by RhoGDI and D4 GDI. J. Mol. Biol. 305: 121-135.
30. Dransart, E., B. Olofsson, and J. Cherfils. 2005. RhoGDIs revisited: novel roles in Rho regulation. Traffic 6: 957-966.
31. Chianale, F., E. Rainero, C. Cianflone, V. Bettio, A. Pighini, P. E. Porporato, N. Filigheddu, G. Serini, F. Sinigaglia, G. Baldanzi, and A. Graziani. 2010. Diacylglycerol kinase a mediates HGF-induced Rac activation and membrane ruffling by regulating atypical PKC and RhoGDI. Proc. Natl. Acad. Sci. USA 107: 4182-4187.
32. Abramovici, H., P. Mojtabaie, R. J. Parks, X. P. Zhong, G. A. Koretzky, M. K. Topham, and S. H. Gee. 2009. Diacylglycerol kinase ζ regulates actin cytoskeleton reorganization through dissociation of Rac1 from RhoGDI. Mol. Biol. Cell 20: 2049-2059.
33. Wu, W., Y. M. Hsu, L. Bi, Z. Songyang, and X. Lin. 2009. CARD9 facilitates microbe-elicited production of reactive oxygen species by regulating the LyGDIRac1 complex. Nat. Immunol. 10: 1208-1214.