Characterization of the self-cleaving effector protein NopE1 of Bradyrhizobium japonicum

Journal of Bacteriology

Volumn 193, Issue 15, 2011, Pages 3733-3739

  Schirrmeister, Jana ^a   Friedrich, Lars ^a,b   Wenzel, Mandy ^a   Hoppe, Markus ^a   Wolf, Christine ^a   Göttfert, Michael ^a   Zehner, Susanne ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARAGINE; ASPARTIC ACID; BACTERIAL PROTEIN; EDETIC ACID; GLUTAMIC ACID; MAGNESIUM; MANGANESE; NOPE1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BRADYRHIZOBIUM JAPONICUM; CALCIUM BINDING; DIMERIZATION; GEL ELECTROPHORESIS; NONHUMAN; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN MOTIF; TEMPERATURE; VIBRIO; VIBRIO CORALLIILYTICUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BRADYRHIZOBIUM; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY;

BRADYRHIZOBIUM JAPONICUM; BURKHOLDERIA PHYTOFIRMANS; PROTEOBACTERIA; VIBRIO CORALLIILYTICUS;

EID: 79960413207     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00437-11     Document Type: Article

References (33)

1. Ben-Haim, Y., et al. 2003. Vibrio coralliilyticus sp. nov., a temperature-de- pendent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 53:309-315.
2. Bi, M., J. R. Hickox, V. P. Winfrey, G. E. Olson, and D. M. Hardy. 2003. Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem. J. 375:477-488.
3. Catak, S., G. Monard, V. Aviyente, and M. F. Ruiz-López. 2008. Computa- tional study on nonenzymatic peptide bond cleavage at asparagine and as- partic acid. J. Phys. Chem. A 112:8752-8761.
4. Compant, S., et al. 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71:1685-1693.
5. Deakin, W. J., and W. J. Broughton. 2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:312-320.
6. Gifford, J. L., M. P. Walsh, and H. J. Vogel. 2007. Structures and metal-ion- binding properties of the Ca2Universal-GreekwithMathPi.-1.H11001-binding helix-loop-helix EF-hand motifs. Biochem. J. 405:199-221.
7. Hempel, J., S. Zehner, M. Göttfert, and T. Patschkowski. 2009. Analysis of the secretome of the soybean symbiont Bradyrhizobium japonicum. J. Bio- technol. 140:51-58.
8. Hennecke, H. 1990. Nitrogen fixation genes involved in the Bradyrhizobium japonicum-soybean symbiosis. FEBS Lett. 268:422-426.
9. Hogenhout, S. A., R. A. Van der Hoorn, R. Terauchi, and S. Kamoun. 2009. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22:115-122.
10. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
11. Krause, A., A. Doerfel, and M. Göttfert. 2002. Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 15:1228-1235.
12. Krishnan, H. B., et al. 2003. Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii USDA257. Mol. Plant Microbe Interact. 16:617-625.
13. Larkin, M. A., et al. 2007. ClustalW and ClustalX version 2. Bioinformatics 23:2947-2948.
14. Lidell, M. E., M. E. Johansson, and G. C. Hansson. 2003. An autocatalytic cleavage in the C-terminus of the human MUC2 mucin occurs at the low pH of the late secretory pathway. J. Biol. Chem. 278:13944-13951.
15. Lidell, M. E., and G. C. Hansson. 2006. Cleavage in the GDPH sequence of the C-terminal cysteine-rich part of the human MUC5AC mucin. Biochem. J. 399:121-129.
16. Monnier, P. P., et al. 2002. RGM is a repulsive guidance molecule for retinal axons. Nature 419:392-395.
17. Oldroyd, G. E., and J. A. Downie. 2004. Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol. 5:566-576.
18. Osička, R., K. Procházková, M. Šulc, I. Linhartová, V. Havlicek, and P. Šebo. 2004. A novel "clip-and-link" activity of repeat in toxin (RTX) proteins from gram-negative pathogens. Covalent protein cross-linking by an Asp-Lys isopeptide bond upon calcium-dependent processing at an Asp-Pro bond. J. Biol. Chem. 279:24944-24956.
19. Piszkiewicz, D., M. Landon, and E. L. Smith. 1970. Anomalous cleavage of aspartyl-proline peptide bonds during amino acid sequence determinations. Biochem. Biophys. Res. Commun. 40:1173-1178.
20. Puig, S., and L. Peñarrubia. 2009. Placing metal micronutrients in context: transport and distribution in plants. Curr. Opin. Plant Biol. 12:299-306.
21. Quiquampoix, H., B. C. Loughman, and R. G. Ratcliffe. 1993. A 31P-NMR study of the uptake and compartmentation of manganese by maize roots. J. Exp. Bot. 44:1819-1827.
22. Schägger, H., and G. Jagow. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199:223-231.
23. Sessitsch, A., et al. 2005. Burkholderia phytofirmans sp. nov., a novel plant- associated bacterium with plant-beneficial properties. Int. J. Syst. Evol. Mi- crobiol. 55:1187-1192.
24. Shaul, O. 2002. Magnesium transport and function in plants: the tip of the iceberg. BioMetals 15:307-321.
25. Sheng, Z. Q., S. R. Hull, and K. L. Carraway. 1990. Biosynthesis of the cell surface sialomucin complex of ascites 13762 rat mammary adenocarcinoma cells from a high molecular weight precursor. J. Biol. Chem. 265:8505-8510.
26. Stephenson, R. C., and S. Clarke. 1989. Succinimide formation from aspartyl and asparaginyl peptides as a model for the spontaneous degradation of proteins. J. Biol. Chem. 264:6164-6170.
27. Süß, C., et al. 2006. Identification of genistein-inducible and type III-se- creted proteins of Bradyrhizobium japonicum. J. Biotechnol. 126:69-77.
28. Thuveson, M., and E. Fries. 2000. The low pH in trans-Golgi triggers auto- catalytic cleavage of pre-alpha-inhibitor heavy chain precursor. J. Biol. Chem. 275:30996-31000.
29. Viprey, V., A. Del Greco, W. Golinowski, W. J. Broughton, and X. Perret. 1998. Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28:1381-1389.
30. Voorter, C. E., W. A. de Haard-Hoekman, P. J. van den Oetelaar, H. Bloemendal, and W. W. de Jong. 1988. Spontaneous peptide bond cleavage in aging alpha-crystallin through a succinimide intermediate. J. Biol. Chem. 263:19020-19023.
31. Wenzel, M., L. Friedrich, M. Göttfert, and S. Zehner. 2010. The type III- secreted protein NopE1 affects symbiosis and exhibits a calcium-dependent autocleavage activity. Mol. Plant Microbe Interact. 23:124-129.
32. Zehner, S., G. Schober, M. Wenzel, K. Lang, and M. Göttfert. 2008. Expres- sion of the Bradyrhizobium japonicum type III secretion system in legume nodules and analysis of the associated tts box promoter. Mol. Plant Microbe Interact. 21:1087-1093.
33. Zhang, A. S., A. P. West, Jr., A. E. Wyman, P. J. Bjorkman, and C. A. Enns. 2005. Interaction of hemojuvelin with neogenin results in iron accumulation in human embryonic kidney 293 cells. J. Biol. Chem. 280:33885-33894.