NleH Defines a new family of bacterial effector kinases

Structure

Volumn 22, Issue 2, 2014, Pages 250-259

  Grishin, Andrey M ^a   Cherney, Maia ^a   Anderson, Deborah H ^a   Phanse, Sadhna ^b   Babu, Mohan ^b   Cygler, Miroslaw ^a,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF REGINA   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; PHOSPHOTRANSFERASE; PROTEIN NLEH; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; NLEH KINASE;

ARTICLE; AUTOPHOSPHORYLATION; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; PATHOGENIC ESCHERICHIA COLI; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; CATALYSIS; ENZYME ACTIVITY; NONHUMAN; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; APOPTOSIS; CATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84893803095     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.11.006     Document Type: Article

References (48)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, N. Echols, J.J. Headd, L.W. Hung, S. Jain, G.J. Kapral, and R.W. Grosse Kunstleve et al. The Phenix software for automated determination of macromolecular structures Methods 55 2011 94 106
2. J. Braman, C. Papworth, and A. Greener Site-Directed Mutagenesis Using Double-Stranded Plasmid DNA Templates M. Trower, In Vitro Mutagenesis Protocols 1996 Humana Press New York 31 44
3. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
4. C. Cole, J.D. Barber, and G.J. Barton The Jpred 3 secondary structure prediction server Nucleic Acids Res. 36 Web Server issue 2008 W197 W201
5. P. Dean Functional domains and motifs of bacterial type III effector proteins and their roles in infection FEMS Microbiol. Rev. 35 2011 1100 1125
6. S. Doublié Preparation of selenomethionyl proteins for phase determination Methods Enzymol. 276 1997 523 530
7. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
8. J.A. Endicott, M.E.M. Noble, and L.N. Johnson The structural basis for control of eukaryotic protein kinases Annu. Rev. Biochem. 81 2012 587 613
9. W.H. Eschenfeldt, S. Lucy, C.S. Millard, A. Joachimiak, and I.D. Mark A family of LIC vectors for high-throughput cloning and purification of proteins Methods Mol. Biol. 498 2009 105 115
10. S. Ferreira-Cerca, V. Sagar, T. Schäfer, M. Diop, A.M. Wesseling, H. Lu, E. Chai, E. Hurt, and N. LaRonde-LeBlanc ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit Nat. Struct. Mol. Biol. 19 2012 1316 1323
11. A. Filloux, A. Hachani, and S. Bleves The bacterial type VI secretion machine: yet another player for protein transport across membranes Microbiology 154 2008 1570 1583
12. M. Fookes, G.N. Schroeder, G.C. Langridge, C.J. Blondel, C. Mammina, T.R. Connor, H. Seth-Smith, G.S. Vernikos, K.S. Robinson, and M. Sanders et al. Salmonella bongori provides insights into the evolution of the Salmonellae PLoS Pathog. 7 2011 e1002191
13. J.E. Galán Common themes in the design and function of bacterial effectors Cell Host Microbe 5 2009 571 579
14. X. Gao, F. Wan, K. Mateo, E. Callegari, D. Wang, W. Deng, J. Puente, F. Li, M.S. Chaussee, and B.B. Finlay et al. Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function PLoS Pathog. 5 2009 e1000708
15. J. Ge, H. Xu, T. Li, Y. Zhou, Z. Zhang, S. Li, L. Liu, and F. Shao A Legionella type IV effector activates the NF-kappaB pathway by phosphorylating the IkappaB family of inhibitors Proc. Natl. Acad. Sci. USA 106 2009 13725 13730
16. R.G. Gerlach, and M. Hensel Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens Int. J. Med. Microbiol. 297 2007 401 415
17. C.S. Gibbs, and M.J. Zoller Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions J. Biol. Chem. 266 1991 8923 8931
18. S.K. Hanks, and T. Hunter Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification FASEB J. 9 1995 576 596
19. C. Hemrajani, C.N. Berger, K.S. Robinson, O. Marchès, A. Mousnier, and G. Frankel NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection Proc. Natl. Acad. Sci. USA 107 2010 3129 3134
20. W.A. Hendrickson, J.R. Horton, and D.M. LeMaster Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure EMBO J. 9 1990 1665 1672
21. E. Hervet, X. Charpentier, A. Vianney, J.C. Lazzaroni, C. Gilbert, D. Atlan, and P. Doublet Protein kinase LegK2 is a type IV secretion system effector involved in endoplasmic reticulum recruitment and intracellular replication of Legionella pneumophila Infect. Immun. 79 2011 1936 1950
22. M. Huse, and J. Kuriyan The conformational plasticity of protein kinases Cell 109 2002 275 282
23. N. Kannan, S.S. Taylor, Y. Zhai, J.C. Venter, and G. Manning Structural and functional diversity of the microbial kinome PLoS Biol. 5 2007 e17
24. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
25. D.W. Kim, G. Lenzen, A.L. Page, P. Legrain, P.J. Sansonetti, and C. Parsot The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes Proc. Natl. Acad. Sci. USA 102 2005 14046 14051
26. A.P. Kornev, N.M. Haste, S.S. Taylor, and L.F. Eyck Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Proc. Natl. Acad. Sci. USA 103 2006 17783 17788
27. A.P. Kornev, S.S. Taylor, and L.F. Ten Eyck A helix scaffold for the assembly of active protein kinases Proc. Natl. Acad. Sci. USA 105 2008 14377 14382
28. N. LaRonde-LeBlanc, and A. Wlodawer A family portrait of the RIO kinases J. Biol. Chem. 280 2005 37297 37300
29. E.D. Lowe, M.E. Noble, V.T. Skamnaki, N.G. Oikonomakos, D.J. Owen, and L.N. Johnson The crystal structure of a phosphorylase kinase peptide substrate complex: kinase substrate recognition EMBO J. 16 1997 6646 6658
30. M.N. Lurie-Weinberger, L. Gomez-Valero, N. Merault, G. Glöckner, C. Buchrieser, and U. Gophna The origins of eukaryotic-like proteins in Legionella pneumophila Int. J. Med. Microbiol. 300 2010 470 481
31. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
32. E. Martinez, G.N. Schroeder, C.N. Berger, S.F. Lee, K.S. Robinson, L. Badea, N. Simpson, R.A. Hall, E.L. Hartland, V.F. Crepin, and G. Frankel Binding to Na(+) /H(+) exchanger regulatory factor 2 (NHERF2) affects trafficking and function of the enteropathogenic Escherichia coli type III secretion system effectors Map, EspI and NleH Cell. Microbiol. 12 2010 1718 1731
33. H. Matsumoto, and G.M. Young Proteomic and functional analysis of the suite of Ysp proteins exported by the Ysa type III secretion system of Yersinia enterocolitica Biovar 1B Mol. Microbiol. 59 2006 689 706
34. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
35. W. Minor, M. Cymborowski, Z. Otwinowski, and M. Chruszcz HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. D Biol. Crystallogr. 62 2006 859 866
36. T.H. Pham, X. Gao, K. Tsai, R. Olsen, F. Wan, and P.R. Hardwidge Functional differences and interactions between the Escherichia coli type III secretion system effectors NleH1 and NleH2 Infect. Immun. 80 2012 2133 2140
37. J. Poh, C. Odendall, A. Spanos, C. Boyle, M. Liu, P. Freemont, and D.W. Holden SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling Cell. Microbiol. 10 2008 20 30
38. J. Prilusky, C.E. Felder, T. Zeev-Ben-Mordehai, E.H. Rydberg, O. Man, J.S. Beckmann, I. Silman, and J.L. Sussman FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded Bioinformatics 21 2005 3435 3438
39. E. Roberts, J. Eargle, D. Wright, and Z. Luthey-Schulten MultiSeq: unifying sequence and structure data for evolutionary analysis BMC Bioinformatics 7 2006 382
40. K.S. Robinson, A. Mousnier, C. Hemrajani, N. Fairweather, C.N. Berger, and G. Frankel The enteropathogenic Escherichia coli effector NleH inhibits apoptosis induced by Clostridium difficile toxin B Microbiology 156 2010 1815 1823
41. S.V. Royan, R.M. Jones, A. Koutsouris, J.L. Roxas, K. Falzari, A.W. Weflen, A. Kim, A. Bellmeyer, J.R. Turner, and A.S. Neish et al. Enteropathogenic E. coli non-LEE encoded effectors NleH1 and NleH2 attenuate NF-κB activation Mol. Microbiol. 78 2010 1232 1245
42. A. Sethi, P. O'Donoghue, and Z. Luthey-Schulten Evolutionary profiles from the QR factorization of multiple sequence alignments Proc. Natl. Acad. Sci. USA 102 2005 4045 4050
43. P.V. Troshin, J.B. Procter, and G.J. Barton Java bioinformatics analysis web services for multiple sequence alignment - JABAWS:MSA Bioinformatics 27 2011 2001 2002
44. F. Wan, D.E. Anderson, R.A. Barnitz, A. Snow, N. Bidere, L. Zheng, V. Hegde, L.T. Lam, L.M. Staudt, and D. Levens et al. Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation Cell 131 2007 927 939
45. F. Wan, A. Weaver, X. Gao, M. Bern, P.R. Hardwidge, and M.J. Lenardo IKKβ phosphorylation regulates RPS3 nuclear translocation and NF-κB function during infection with Escherichia coli strain O157:H7 Nat. Immunol. 12 2011 335 343
46. D.J. Wiley, N. Shrestha, J. Yang, N. Atis, K. Dayton, and K. Schesser The activities of the Yersinia protein kinase A (YpkA) and outer protein J (YopJ) virulence factors converge on an eIF2alpha kinase J. Biol. Chem. 284 2009 24744 24753
47. B. Xue, R.L. Dunbrack, R.W. Williams, A.K. Dunker, and V.N. Uversky PONDR-FIT: a meta-predictor of intrinsically disordered amino acids Biochim. Biophys. Acta 1804 2010 996 1010
48. J. Zheng, E.A. Trafny, D.R. Knighton, N.H. Xuong, S.S. Taylor, L.F. Ten Eyck, and J.M. Sowadski 2.2 A refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor Acta Crystallogr. D Biol. Crystallogr. 49 1993 362 365