Structural and Biochemical Characterization Reveals LysGH15 as an Unprecedented "EF-Hand-Like" Calcium-Binding Phage Lysin

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Gu, Jingmin ^a   Feng, Yingang ^b   Feng, Xin ^a   Sun, Changjiang ^a   Lei, Liancheng ^a   Ding, Wei ^c   Niu, Fengfeng ^c   Jiao, Lianying ^c   Yang, Mei ^a   Li, Yue ^a   Liu, Xiaohe ^a   Song, Jun ^a   Cui, Ziyin ^a   Han, Dong ^a   Du, Chongtao ^a   Yang, Yongjun ^a   Ouyang, Songying ^c   Liu, Zhi Jie ^c   Han, Wenyu ^a  

^a JILIN UNIVERSITY   (China)

^b QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; ANTIINFECTIVE AGENT; CALCIUM; LYSIN; MUCOPROTEIN;

AMINO ACID SEQUENCE; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVE SITE; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST; MOLECULAR GENETICS; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS PHAGE; ULTRASTRUCTURE;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; CALCIUM; CATALYTIC DOMAIN; CELL WALL; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUCOPROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS PHAGES;

EID: 84901657828     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004109     Document Type: Article

References (67)

1. Zoll S, Patzold B, Schlag M, Gotz F, Kalbacher H, et al. (2010) Structural basis of cell wall cleavage by a staphylococcal autolysin. PLoS Pathog 6: e1000807.
2. Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, et al. (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42: 647-656.
3. DeLeo FR, Otto M, (2008) An antidote for Staphylococcus aureus pneumonia? J Exp Med 205: 271-274.
4. Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, et al. (2005) Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352: 1445-1453.
5. Brumfitt W, Hamilton-Miller J, (1989) Methicillin-resistant Staphylococcus aureus. N Engl J Med 320: 1188-1196.
6. Enright MC, (2003) The evolution of a resistant pathogen-the case of MRSA. Curr Opin Pharmacol 3: 474-479.
7. Hermoso JA, Garcia JL, Garcia P, (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol 10: 461-472.
8. Fischetti VA, (2011) Exploiting what phage have evolved to control gram-positive pathogens. Bacteriophage 1: 188-194.
9. Loeffler JM, Nelson D, Fischetti VA, (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294: 2170-2172.
10. Borysowski J, Weber-Dabrowska B, Gorski A, (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med (Maywood) 231: 366-377.
11. Gu J, Xu W, Lei L, Huang J, Feng X, et al. (2011) LysGH15, a novel bacteriophage lysin, protects a murine bacteremia model efficiently against lethal methicillin-resistant Staphylococcus aureus infection. J Clin Microbiol 49: 111-117.
12. Gu J, Zuo J, Lei L, Zhao H, Sun C, et al. (2011) LysGH15 reduces the inflammation caused by lethal methicillin-resistant Staphylococcus aureus infection in mice. Bioeng Bugs 2: 96-99.
13. Gu J, Liu X, Yang M, Li Y, Sun C, et al. (2013) Genomic characterization of lytic Staphylococcus aureus phage GH15: providing new clues to intron shift in phages. J Gen Virol 94: 906-915.
14. Gu J, Lu R, Liu X, Han W, Lei L, et al. (2011) LysGH15B, the SH3b domain of staphylococcal phage endolysin LysGH15, retains high affinity to staphylococci. Curr Microbiol 63: 538-542.
15. Sass P, Bierbaum G, (2007) Lytic activity of recombinant bacteriophage phi11 and phi12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl Environ Microbiol 73: 347-352.
16. O'Flaherty S, Coffey A, Meaney W, Fitzgerald GF, Ross RP, (2005) The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J Bacteriol 187: 7161-7164.
17. Cabanes D, Dehoux P, Dussurget O, Frangeul L, Cossart P, (2002) Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol 10: 238-245.
18. Rossi P, Aramini JM, Xiao R, Chen CX, Nwosu C, et al. (2009) Structural elucidation of the Cys-His-Glu-Asn proteolytic relay in the secreted CHAP domain enzyme from the human pathogen Staphylococcus saprophyticus. Proteins 74: 515-519.
19. McGuffin LJ, Bryson K, Jones DT, (2000) The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
20. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-549.
21. McGowan S, Buckle AM, Mitchell MS, Hoopes JT, Gallagher DT, et al. (2012) X-ray crystal structure of the streptococcal specific phage lysin PlyC. Proc Natl Acad Sci U S A 109: 12752-12757.
22. Goldenberg O, Erez E, Nimrod G, Ben-Tal N, (2009) The ConSurf-DB: pre-calculated evolutionary conservation profiles of protein structures. Nucleic Acids Res 37: D323-327.
23. Low LY, Yang C, Perego M, Osterman A, Liddington RC, (2005) Structure and lytic activity of a Bacillus anthracis prophage endolysin. J Biol Chem 280: 35433-35439.
24. Lu JZ, Fujiwara T, Komatsuzawa H, Sugai M, Sakon J, (2006) Cell wall-targeting domain of glycylglycine endopeptidase distinguishes among peptidoglycan cross-bridges. J Biol Chem 281: 549-558.
25. Hirakawa H, Akita H, Fujiwara T, Sugai M, Kuhara S, (2009) Structural insight into the binding mode between the targeting domain of ALE-1 (92AA) and pentaglycine of peptidoglycan. Protein Eng Des Sel 22: 385-391.
26. Zhou Y, Yang W, Kirberger M, Lee HW, Ayalasomayajula G, et al. (2006) Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins 65: 643-655.
27. Fenton M, Ross RP, McAuliffe O, O'Mahony J, Coffey A, (2011) Characterization of the staphylococcal bacteriophage lysin CHAP(K). J Appl Microbiol 111: 1025-1035.
28. Donovan DM, Lardeo M, Foster-Frey J, (2006) Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiol Lett 265: 133-139.
29. Pritchard DG, Dong S, Baker JR, Engler JA, (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 150: 2079-2087.
30. Celia LK, Nelson D, Kerr DE, (2008) Characterization of a bacteriophage lysin (Ply700) from Streptococcus uberis. Vet Microbiol 130: 107-117.
31. Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC, (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385: 833-838.
32. Lytle BL, Volkman BF, Westler WM, Heckman MP, Wu JHD, (2001) Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J Mol Biol 307: 745-753.
33. Eijsink VG, Matthews BW, Vriend G, (2011) The role of calcium ions in the stability and instability of a thermolysin-like protease. Protein Sci 20: 1346-1355.
34. Pai CH, Chiang BY, Ko TP, Chou CC, Chong CM, et al. (2006) Dual binding sites for translocation catalysis by Escherichia coli glutathionylspermidine synthetase. EMBO J 25: 5970-5982.
35. Donovan DM, Foster-Frey J, (2008) LambdaSa2 prophage endolysin requires Cpl-7-binding domains and amidase-5 domain for antimicrobial lysis of streptococci. FEMS Microbiol Lett 287: 22-33.
36. Pritchard DG, Dong S, Kirk MC, Cartee RT, Baker JR, (2007) LambdaSa1 and LambdaSa2 prophage lysins of Streptococcus agalactiae. Appl Environ Microbiol 73: 7150-7154.
37. Becker SC, Dong S, Baker JR, Foster-Frey J, Pritchard DG, et al. (2009) LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells. FEMS Microbiol Lett 294: 52-60.
38. Horgan M, O'Flynn G, Garry J, Cooney J, Coffey A, et al. (2009) Phage lysin LysK can be truncated to its CHAP domain and retain lytic activity against live antibiotic-resistant staphylococci. Appl Environ Microbiol 75: 872-874.
39. Kerff F, Petrella S, Mercier F, Sauvage E, Herman R, et al. (2010) Specific structural features of the N-acetylmuramoyl-L-alanine amidase AmiD from Escherichia coli and mechanistic implications for enzymes of this family. J Mol Biol 397: 249-259.
40. McLaughlin S, Wang J, Gambhir A, Murray D, (2002) PIP(2) and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31: 151-175.
41. Liang W, Ouyang S, Shaw N, Joachimiak A, Zhang R, et al. (2011) Conversion of D-ribulose 5-phosphate to D-xylulose 5-phosphate: new insights from structural and biochemical studies on human RPE. FASEB J 25: 497-504.
42. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276: 307-326.
43. Ru H, Zhao L, Ding W, Jiao L, Shaw N, et al. (2012) S-SAD phasing study of death receptor 6 and its solution conformation revealed by SAXS. Acta Crystallogr D Biol Crystallogr 68: 521-530.
44. Liu ZJ, Lin D, Tempel W, Praissman JL, Rose JP, et al. (2005) Parameter-space screening: a powerful tool for high-throughput crystal structure determination. Acta Crystallogr D Biol Crystallogr 61: 520-527.
45. Hendrickson WA, (1991) Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254: 51-58.
46. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
47. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
48. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
49. Gong W, Zhou T, Mo J, Perrett S, Wang J, et al. (2012) Structural insight into recognition of methylated histone tails by retinoblastoma-binding protein 1. J Biol Chem 287: 8531-8540.
50. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
51. Johnson BA, (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278: 313-352.
52. Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, et al. (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids- (IUPAC Recommendations 1998). Pure Appl Chem 70: 117-142.
53. Herrmann T, Guntert P, Wuthrich K, (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209-227.
54. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
55. Duggan BM, Legge GB, Dyson HJ, Wright PE, (2001) SANE (Structure Assisted NOE Evaluation): an automated model-based approach for NOE assignment. J Biomol NMR 19: 321-329.
56. Shen Y, Bax A, (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 56: 227-241.
57. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CA, et al. (2005) RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 59: 662-672.
58. Koradi R, Billeter M, Wuthrich K, (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32.
59. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM, (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
60. Ouyang S, Song X, Wang Y, Ru H, Shaw N, et al. (2012) Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36: 1073-1086.
61. Baytak S, Zereen F, Arslan Z, (2011) Preconcentration of trace elements from water samples on a minicolumn of yeast (Yamadazyma spartinae) immobilized TiO2 nanoparticles for determination by ICP-AES. Talanta 84: 319-323.
62. Wang L, Yang X, Li S, Wang Z, Liu Y, et al. (2014) Structural and mechanistic insights into MICU1 regulation of mitochondrial calcium uptake. EMBO J 33: 594-604 (DOI: 10.1002/embj.201386523).
63. Zhao L, Hua T, Crowley C, Ru H, Ni X, et al. (2014) Structural analysis of asparaginyl endopeptidase reveals the activation mechanism and a reversible intermediate maturation stage. Cell Res 24: 344-358.
64. Lavinder JJ, Hari SB, Sullivan BJ, Magliery TJ, (2009) High-throughput thermal scanning: a general, rapid dye-binding thermal shift screen for protein engineering. J Am Chem Soc 131: 3794-3795.
65. Fyfe PK, Oza SL, Fairlamb AH, Hunter WN, (2008) Leishmania trypanothione synthetase-amidase structure reveals a basis for regulation of conflicting synthetic and hydrolytic activities. J Biol Chem 283: 17672-17680.
66. Low LY, Yang C, Perego M, Osterman A, Liddington R, (2011) Role of net charge on catalytic domain and influence of cell wall binding domain on bactericidal activity, specificity, and host range of phage lysins. J Biol Chem 286: 34391-34403.
67. Delano W (2002) PyMOL. New York, NY: Schrodinger, Inc. Available: http://www.pymol.org.