The crystal structure of the plant small GTPase OsRac1 reveals its mode of binding to NADPH oxidase

Journal of Biological Chemistry

Volumn 289, Issue 41, 2014, Pages 28569-28578

  Kosami, Ken Ichi ^a   Ohki, Izuru ^b,c   Nagano, Minoru ^b   Furuita, Kyoko ^a   Sugiki, Toshihiko ^a   Kawano, Yoji ^b   Kawasaki, Tsutomu ^b,d   Fujiwara, Toshimichi ^a   Nakagawa, Atsushi ^a   Shimamoto, Ko ^b   Kojima, Chojiro ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KINKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNE SYSTEM; PLANTS (BOTANY); PROTEINS;

CELLULAR RESPONSE; CONFORMATIONAL DIFFERENCES; INNATE IMMUNITY; MOLECULAR MECHANISM; MOLECULAR SWITCHES; POLLEN TUBE GROWTH; STRUCTURAL COMPARISON; STRUCTURAL INFORMATION;

CRYSTAL STRUCTURE;

GUANOSINE TRIPHOSPHATASE; GUANYLYLIMIDODIPHOSPHATE; MUTANT PROTEIN; OSRAC1; PROTEIN; RAC PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROP PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; POLYPHOSPHOINOSITIDE; PROTEIN BINDING; RAC1 PROTEIN; RECOMBINANT PROTEIN; ROP9 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME BINDING; ENZYME CONFORMATION; ENZYME STRUCTURE; IMMUNE RESPONSE; IN VITRO STUDY; MUTATION; NONHUMAN; PLANT CELL; PLANT IMMUNITY; RICE; AMINO ACID SEQUENCE; ARABIDOPSIS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, PLANT; GUANYLYL IMIDODIPHOSPHATE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; MUTATION; NADPH OXIDASE; ORYZA SATIVA; OXIDATION-REDUCTION; PHOSPHATIDYLINOSITOL PHOSPHATES; PLANT IMMUNITY; PLANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RAC1 GTP-BINDING PROTEIN; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84907652096     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.603282     Document Type: Article

References (49)

1. Yang, Z. (2002) Small GTPases: versatile signaling switches in plants. Plant Cell 14, suppl., S375-S388
2. Zheng, Z. L., and Yang, Z. (2000) The Rop GTPase: an emerging signaling switch in plants. Plant Mol. Biol. 44, 1-9
3. Nibau, C., Wu, H. M., and Cheung, A. Y. (2006) RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants. Trends Plant Sci. 11, 309-315
4. Yang, Z., and Fu, Y. (2007) ROP/RAC GTPase signaling. Curr. Opin. Plant Biol. 10, 490-494
5. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J. G., Wu, M. J., Perrot-Rechenmann, C., Friml, J., Jones, A. M., and Yang, Z. (2010) Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110
6. Oda, Y., and Fukuda, H. (2012) Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337, 1333-1336
7. Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H., and Shimamoto, K. (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. U.S.A. 96, 10922-10926
8. Ono, E., Wong, H. L., Kawasaki, T., Hasegawa, M., Kodama, O., and Shimamoto, K. (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc. Natl. Acad. Sci. U.S.A. 98, 759-764
9. Suharsono, U., Fujisawa, Y., Kawasaki, T., Iwasaki, Y., Satoh, H., and Shimamoto, K. (2002) The heterotrimeric G protein α acts upstream of the small GTPase Rac in disease resistance of rice. Proc. Natl. Acad. Sci. U.S.A. 99, 13307-13312
10. Fujiwara, M., Umemura, K., Kawasaki, T., and Shimamoto, K. (2006) Proteomics of Rac GTPase signaling reveals its predominant role in elicitorinduced defense response of cultured rice cells. Plant Physiol. 140, 734-745
11. Wong, H. L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K., Kojima, C., Yoshioka, H., Iba, K., Kawasaki, T., and Shimamoto, K. (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022-4034
12. Kawano, Y., Akamatsu, A., Hayashi, K., Housen, Y., Okuda, J., Yao, A., Nakashima, A., Takahashi, H., Yoshida, H., Wong, H. L., Kawasaki, T., and Shimamoto, K. (2010) Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity. Cell Host Microbe 7, 362-375
13. Akamatsu, A., Wong, H. L., Fujiwara, M., Okuda, J., Nishide, K., Uno, K., Imai, K., Umemura, K., Kawasaki, T., Kawano, Y., and Shimamoto, K. (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13, 465-476
14. Kawano, Y., Chen, L., and Shimamoto, K. (2010) The function of Rac small GTPase and associated proteins in rice innate immunity. Rice 3, 112-121
15. Kawano, Y., and Shimamoto, K. (2013) Early signaling network in rice PRR-mediated and R-mediated immunity. Curr. Opin. Plant Biol. 16, 496-504
16. Potocký, M., Pejchar, P., Gutkowska, M., Jiménez-Quesada, M. J., Potocká, A., Alché Jde, D., Kost, B., and Žárský, V. (2012) NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J. Plant Physiol. 169, 1654-1663
17. Craddock, C., Lavagi, I., and Yang, Z. (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol. 22, 492-501
18. Chen, X., Naramoto, S., Robert, S., Tejos, R., Löfke, C., Lin, D., Yang, Z., and Friml, J. (2012) ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr. Biol. 22, 1326-1332
19. Lin, D., Nagawa, S., Chen, J., Cao, L., Chen, X., Xu, T., Li, H., Dhonukshe, P., Yamamuro, C., Friml, J., Scheres, B., Fu, Y., and Yang, Z. (2012) A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr. Biol. 22, 1319-1325
20. Nagawa, S., Xu, T., Lin, D., Dhonukshe, P., Zhang, X., Friml, J., Scheres, B., Fu, Y., and Yang, Z. (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 10, e1001299
21. Zheng, Z. L., Nafisi, M., Tam, A., Li, H., Crowell, D. N., Chary, S. N., Schroeder, J. I., Shen, J., and Yang, Z. (2002) Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 14, 2787-2797
22. Li, Z., Li, Z., Gao, X., Chinnusamy, V., Bressan, R., Wang, Z. X., Zhu, J. K., Wu, J. W., and Liu, D. (2012) ROP11 GTPase negatively regulates ABA signaling by protecting ABI1 phosphatase activity from inhibition by the ABA receptor RCAR1/PYL9 in Arabidopsis. J. Integr. Plant. Biol. 54, 180-188
23. Nibau, C., Tao, L., Levasseur, K., Wu, H. M., and Cheung, A. Y. (2013) The Arabidopsis small GTPase AtRAC7/ROP9 is a modulator of auxin and abscisic acid signaling. J. Exp. Bot. 64, 3425-3437
24. Sørmo, C. G., Leiros, I., Brembu, T., Winge, P., Os, V., and Bones, A. M. (2006) The crystal structure of Arabidopsis thaliana RAC7/ROP9: the first RAS superfamily GTPase from the plant kingdom. Phytochemistry 67, 2332-2340
25. Thomas, C., Fricke, I., Scrima, A., Berken, A., and Wittinghofer, A. (2007) Structural evidence for a common intermediate in small G protein-GEF reactions. Mol. Cell 25, 141-149
26. Thomas, C., Fricke, I., Weyand, M., and Berken, A. (2009) 3D structure of a binary ROP-PRONE complex: the final intermediate for a complete set of molecular snapshots of the RopGEF reaction. Biol. Chem. 390, 427-435
27. Al-Mulla, F., Milner-White, E. J., Going, J. J., and Birnie, G. D. (1999) Structural differences between valine-12 and aspartate-12 Ras proteins may modify carcinoma aggression. J. Pathol. 187, 433-438
28. Oda, T., Hashimoto, H., Kuwabara, N., Hayashi, K., Kojima, C., Kawasaki, T., Shimamoto, K., Sato, M., and Shimizu, T. (2008) Crystallographic characterization of the N-terminal domain of a plant NADPH oxidase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64, 867-869
29. Oda, T., Hashimoto, H., Kuwabara, N., Akashi, S., Hayashi, K., Kojima, C., Wong, H. L., Kawasaki, T., Shimamoto, K., Sato, M., and Shimizu, T. (2010) Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. J. Biol. Chem. 285, 1435-1445
30. Kosami, K., Ohki, I., Hayashi, K., Tabata, R., Usugi, S., Kawasaki, T., Fujiwara, T., Nakagawa, A., Shimamoto, K., and Kojima, C. (2014) Purification, crystallization and preliminary X-ray crystallographic analysis of a rice Rac/Rop GTPase, OsRac1. Acta Crystallogr. F Struct. Biol. Commun. 70, 113-115
31. Otwinowski, Z., and Minor, W. (1997) Methods Enzymol. 276, 307-326
32. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
34. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
35. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
36. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, de Bakker, P. I. W., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: Φ,Ψ and Cβ deviation. Proteins Struct. Funct. Genet. 50, 437-450
37. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
38. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282
39. Longenecker, K., Read, P., Lin, S. K., Somlyo, A. P., Nakamoto, R. K., and Derewenda, Z. S. (2003) Structure of a constitutively activated RhoA mutant (Q63L) at 1.55 A˚ resolution. Acta Crystallogr. D Biol. Crystallogr. 59, 876-880
40. Hirshberg, M., Stockley, R. W., Dodson, G., and Webb, M. R. (1997) The crystal structure of human rac1, a member of the rho-family complexed with a GTP analogue. Nat. Struct. Biol. 4, 147-152
41. Ihara, K., Muraguchi, S., Kato, M., Shimizu, T., Shirakawa, M., Kuroda, S., Kaibuchi, K., and Hakoshima, T. (1998) Crystal structure of human RhoA in a dominantly active form complexed with a GTP analogue. J. Biol. Chem. 273, 9656-9666
42. Yamaguchi, K., Imai, K., Akamatsu, A., Mihashi, M., Hayashi, N., Shimamoto, K., and Kawasaki, T. (2012) SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J. 70, 389-397
43. Xu, X., Barry, D. C., Settleman, J., Schwartz, M. A., and Bokoch, G. M. (1994) Differing structural requirements for GTPase-activating protein responsiveness and NADPH oxidase activation by Rac. J. Biol. Chem. 269, 23569-23574
44. phoxparticipate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase. J. Biol. Chem. 274, 25051-25060
45. Bedard, K., and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
46. Han, C. H., Freeman, J. L., Lee, T., Motalebi, S. A., and Lambeth, J. D. (1998) Regulation of the neutrophil respiratory burst oxidase. Identification of an activation domain in p67phox. J. Biol. Chem. 273, 16663-16668
47. Diekmann, D., Abo, A., Johnston, C., Segal, A. W., and Hall, A. (1994) Interaction of Rac with p67phox and regulation of phagocytic NADPH oxidase activity. Science 265, 531-533
48. Lapouge, K., Smith, S. J., Walker, P. A., Gamblin, S. J., Smerdon, S. J., and Rittinger, K. (2000) Structure of the TPR domain of p67phox in complex with Rac-GTP. Mol. Cell 6, 899-907
49. Jones, M. A., Raymond, M. J., Yang, Z., and Smirnoff, N. (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot. 58, 1261-1270