The Extended Conformation of the 2.9-Å Crystal Structure of the Three-PASTA Domain of a Ser/Thr Kinase from the Human Pathogen Staphylococcus aureus

Journal of Molecular Biology

Volumn 404, Issue 5, 2010, Pages 847-858

  Paracuellos, Patricia ^a   Ballandras, Allison ^a   Robert, Xavier ^a   Kahn, Richard ^b   Hervé, Mireille ^c   Mengin Lecreulx, Dominique ^c   Cozzone, Alain J ^a   Duclos, Bertrand ^a   Gouet, Patrice ^a  

^a INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Crystal structure; PASTA domain; Serine threonine kinase 1; Staphylococcus aureus

Indexed keywords

BACTERIAL ENZYME; DIMER; PENICILLIN BINDING PROTEIN 2X; PEPTIDOGLYCAN; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME LOCALIZATION; ENZYME SUBUNIT; HUMAN; MOLECULAR DOCKING; MOLECULAR INTERACTION; MOLECULAR MODEL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PENICILLIN BINDING PROTEIN AND SERINE THREONINE KINASE ASSOCIATED PROTEIN DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STAPHYLOCOCCUS AUREUS; STRUCTURAL HOMOLOGY;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); EUKARYOTA; FIRMICUTES; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 78649529310     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.10.012     Document Type: Article

References (52)

1. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 1995, 80:225-236.
2. Umeyama T., Lee P.C., Horinouchi S. Protein serine/threonine kinases in signal transduction for secondary metabolism and morphogenesis in Streptomyces. Appl. Microbiol. Biotechnol. 2002, 59:419-425.
3. Madec E., Laszkiewicz A., Iwanicki A., Obuchowski M., Seror S. Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol. Microbiol. 2002, 46:571-586.
4. Neu J.M., MacMillan S.V., Nodwell J.R., Wright G.D. StoPK-1, a serine/threonine protein kinase from the glycopeptide antibiotic producer Streptomyces toyocaensis NRRL 15009, affects oxidative stress response. Mol. Microbiol. 2002, 44:417-430.
5. Grangeasse C., Cozzone A.J., Deutscher J., Mijakovic I. Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem. Sci. 2007, 32:86-94.
6. Kristich C.J., Wells C.L., Dunny G.M. A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc. Natl Acad. Sci. USA 2007, 104:3508-3513.
7. Cozzone A.J. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J. Mol. Microbiol. Biotechnol. 2005, 9:198-213.
8. McGahee W., Lowy F.D. Staphylococcal infections in the intensive care unit. Semin. Respir. Infect. 2000, 15:308-313.
9. Lomas-Lopez R., Paracuellos P., Riberty M., Cozzone A.J., Duclos B. Several enzymes of the central metabolism are phosphorylated in Staphylococcus aureus. FEMS Microbiol. Lett. 2007, 272:35-42.
10. Debarbouillé M., Dramsi S., Dussurget O., Nahori M.A., Vaganay E., Jouvion G., et al. Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. J. Bacteriol. 2009, 191:4070-4081.
11. Ortiz-Lombardia M., Pompeo F., Boitel B., Alzari P.M. Crystal structure of the catalytic domain of the PknB serine/threonine kinase from Mycobacterium tuberculosis. J. Biol. Chem. 2003, 278:13094-13100.
12. Young T.A., Delagoutte B., Endrizzi J.A., Falick A.M., Alber T. Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat. Struct. Biol. 2003, 10:168-174.
13. Gay L.M., Ng H.L., Alber T. A conserved dimer and global conformational changes in the structure of apo-PknE Ser/Thr protein kinase from Mycobacterium tuberculosis. J. Mol. Biol. 2006, 360:409-420.
14. Scherr N., Honnappa S., Kunz G., Mueller P., Jayachandran R., Winkler F., et al. Structural basis for the specific inhibition of protein kinase G, a virulence factor of Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 2007, 104:12151-12156.
15. Yeats C., Finn R.D., Bateman A. The PASTA domain: a beta-lactam-binding domain. Trends Biochem. Sci 2002, 27:438.
16. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., et al. The Pfam protein families database. Nucleic Acids Res 2010, 38:D211-222.
17. Shah I.M., Laaberki M.H., Popham D.L., Dworkin J. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 2008, 135:486-496.
18. Barthe P., Mukamolova G.V., Roumestand C., Cohen-Gonsaud M. The structure of PknB extracellular PASTA domain from Mycobacterium tuberculosis suggests a ligand-dependent kinase activation. Structure 2010, 18:606-615.
19. Gordon E., Mouz N., Duee E., Dideberg O. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 2000, 299:477-485.
20. Wehenkel A., Bellinzoni M., Grana M., Duran R., Villarino A., Fernandez P., et al. Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim. Biophys. Acta 2008, 1784:193-202.
21. Paracuellos P., Ballandras A., Robert X., Cozzone A.J., Duclos B., Gouet P. Crystallization and initial X-ray diffraction study of the three PASTA domains of the Ser/Thr kinase Stk1 from the human pathogen Staphylococcus aureus. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2009, 65:1187-1189.
22. Litvinovich S.V., Ingham K.C. Interactions between type III domains in the 110 kDa cell-binding fragment of fibronectin. J. Mol. Biol. 1995, 248:611-626.
23. Pallova P., Hercik K., Saskova L., Novakova L., Branny P. A eukaryotic-type serine/threonine protein kinase StkP of Streptococcus pneumoniae acts as a dimer in vivo. Biochem. Biophys. Res. Commun. 2007, 355:526-530.
24. Greenstein A.E., Echols N., Lombana T.N., King D.S., Alber T. Allosteric activation by dimerization of the PknD receptor Ser/Thr protein kinase from Mycobacterium tuberculosis. J. Biol. Chem. 2007, 282:11427-11435.
25. Alber T. Signaling mechanisms of the Mycobacterium tuberculosis receptor Ser/Thr protein kinases. Curr. Opin. Struct. Biol. 2009, 19:650-657.
26. Holm L., Kaariainen S., Rosenstrom P., Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 2008, 24:2780-2781.
27. Ryan, K. J. & Ray, C. G. (2010). Sherris Medical Microbiology 5th edition, pp. 351-352. McGraw Hill Professional.
28. Schleifer K.H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 1972, 36:407-477.
29. Guan R., Mariuzza R.A. Peptidoglycan recognition proteins of the innate immune system. Trends Microbiol. 2007, 15:127-134.
30. Panneerselvam S., Marx A., Mandelkow E.M., Mandelkow E. Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 2006, 14:173-183.
31. Duran R., Villarino A., Bellinzoni M., Wehenkel A., Fernandez P., Boitel B., et al. Conserved autophosphorylation pattern in activation loops and juxtamembrane regions of Mycobacterium tuberculosis Ser/Thr protein kinases. Biochem. Biophys. Res. Commun. 2005, 333:858-867.
32. Wilson K.P., Fitzgibbon M.J., Caron P.R., Griffith J.P., Chen W., McCaffrey P.G., et al. Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 1996, 271:27696-27700.
33. Canagarajah B.J., Khokhlatchev A., Cobb M.H., Goldsmith E.J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 1997, 90:859-869.
34. D'Alise A.M., Amabile G., Iovino M., Di Giorgio F.P., Bartiromo M., Sessa F., et al. Reversine, a novel Aurora kinases inhibitor, inhibits colony formation of human acute myeloid leukemia cells. Mol. Cancer Ther. 2008, 7:1140-1149.
35. Grove T.Z., Cortajarena A.L., Regan L. Ligand binding by repeat proteins: natural and designed. Curr. Opin. Struct. Biol. 2008, 18:507-515.
36. Jones G., Dyson P. Evolution of transmembrane protein kinases implicated in coordinating remodeling of Gram-positive peptidoglycan: inside versus outside. J. Bacteriol. 2006, 188:7470-7476.
37. Collaborative Computational Project number 4. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50:760-763. CCP4.
38. Langer G., Cohen S.X., Lamzin V.S., Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 2008, 3:1171-1179.
39. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:2126-2132.
40. Navaza J. Implementation of molecular replacement in AMoRe. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2001, 57:1367-1372.
41. Moustakas D.T., Lang P.T., Pegg S., Pettersen E., Kuntz I.D., Brooijmans N., et al. Development and validation of a modular, extensible docking program: DOCK 5. J. Comput. Aided Mol. Des. 2006, 20:601-619.
42. Cho S., Wang Q., Swaminathan C.P., Hesek D., Lee M., Boons G.J., et al. Structural insights into the bactericidal mechanism of human peptidoglycan recognition proteins. Proc. Natl Acad. Sci. USA 2007, 104:8761-8766.
43. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
44. Herve M., Boniface A., Gobec S., Blanot D., Mengin-Lecreulx D. Biochemical characterization and physiological properties of Escherichia coli UDP-N-acetylmuramate:l-alanyl-γ-d-glutamyl-meso-diaminopimelate ligase. J. Bacteriol. 2007, 189:3987-3995.
45. Babic, A., Patin, D., Boniface, A., Hervé, M., Mengin-Lecreulx, D., Pecar, S. et al. (2007). 5Th Joint Meeting on Medicinal Chemistry, Portorož, Slovenia.
46. Blanot D., Kretsovali A., Abo-Ghalia M., Mengin-Lecreulx D., van Heijenoort J. Synthesis of analogues of precursors of bacterial peptidoglycan. Peptides 1983, 311-314. Walter de Gruyter, Berlin, Germany. K. Bláha, P. Malon (Eds.).
47. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y. et al. (2007). Comparative protein structure modeling using MODELLER. Curr. Protoc. Protein Sci. Chapter 2, Unit 2 9.
48. Hooft R.W., Vriend G., Sander C., Abola E.E. Errors in protein structures. Nature 1996, 381:272.
49. Humphrey W., Dalke A., Schulten K VMD-visual molecular dynamics. J. Mol. Graph. 1996, 1:33-38.
50. DeLano W.L. The PyMOL Molecular Graphics System 2008, DeLano Scientific LLC, Palo Alto, CA.
51. Gouet P., Robert X., Courcelle E. ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 2003, 31:3320-3323.
52. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 1991, 11:281-296.