Crystal structure of the lasA virulence factor from Pseudomonas aeruginosa: Substrate specificity and mechanism of M23 metallopeptidases

Journal of Molecular Biology

Volumn 396, Issue 4, 2010, Pages 908-923

  Spencer, James ^a,b   Murphy, Loretta M ^c   Conners, Rebecca ^a   Sessions, Richard B ^a   Gamblin, Steven J ^d  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF VIRGINIA   (United States)

^c BANGOR UNIVERSITY   (United Kingdom)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

M23 metallopeptidase; Pseudomonas aeruginosa; Structure mechanism; Zinc hydrolase

Indexed keywords

METALLOPROTEINASE; STAPHYLOLYSIN; TARTARIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

EID: 77649275546     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.12.021     Document Type: Article

References (94)

1. Quinn J.P. Clinical problems posed by multiresistant nonfermenting gram-negative pathogens. Clin. Infect. Dis. 1998, 27:S117-S124.
2. Bodey G.P., Bolivar R., Fainstein V., Jadeja L. Infections caused by Pseudomonas aeruginosa. Rev. Infect. Dis. 1983, 5:279-313.
3. Driscoll J.A., Brody S.L., Kollef M.H. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 2007, 67:351-368.
4. Pruitt B.A., McManus A.T., Kim S.H., Goodwin C.W. Burn wound infections: current status. World J. Surg. 1998, 22:135-145.
5. Fleiszig S.M., Evans D.J. The pathogenesis of bacterial keratitis: studies with Pseudomonas aeruginosa. Clin. Exp. Optom. 2002, 85:271-278.
6. Lyczak J.B., Cannon C.L., Pier G.B. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 2002, 15:194-222.
7. Hancock R.E., Speert D.P. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist. Updat. 2000, 3:247-255.
8. Clark N.M., Patterson J., Lynch J.P. Antimicrobial resistance among gram-negative organisms in the intensive care unit. Curr. Opin. Crit. Care 2003, 9:413-423.
9. Lyczak J.B., Cannon C.L., Pier G.B. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2000, 2:1051-1060.
10. Lau G.W., Hassett D.J., Britigan B.E. Modulation of lung epithelial functions by Pseudomonas aeruginosa. Trends Microbiol. 2005, 13:389-397.
11. Matsumoto K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol. Chem. 2004, 385:1007-1016.
12. Ohman D.E., Cryz S.J., Iglewski B.H. Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J. Bacteriol. 1980, 142:836-842.
13. Kessler E., Safrin M., Gustin J.K., Ohman D.E. Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J. Biol. Chem. 1998, 273:30225-30231.
14. Thayer M.M., Flaherty K.M., McKay D.B. Three-dimensional structure of the elastase of Pseudomonas aeruginosa at 1.5-Å resolution. J. Biol. Chem. 1991, 266:2864-2871.
15. Kessler E., Safrin M., Abrams W.R., Rosenbloom J., Ohman D.E. Inhibitors and specificity of Pseudomonas aeruginosa LasA. J. Biol. Chem. 1997, 272:9884-9889.
16. Vessillier S., Delolme F., Bernillon J., Saulnier J., Wallach J. Hydrolysis of glycine-containing elastin pentapeptides by LasA, a metalloelastase from Pseudomonas aeruginosa. Eur. J. Biochem. 2001, 268:1049-1057.
17. Peters J.E., Galloway D.R. Purification and characterization of an active fragment of the LasA protein from Pseudomonas aeruginosa: enhancement of elastase activity. J. Bacteriol. 1990, 172:2236-2240.
18. Park P.W., Pier G.B., Preston M.J., Goldberger O., Fitzgerald M.L., Bernfield M. Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J. Biol. Chem. 2000, 275:3057-3064.
19. Park P.W., Pier G.B., Hinkes M.T., Bernfield M. Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 2001, 411:98-102.
20. Li Q., Park P.W., Wilson C.L., Parks W.C. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002, 111:635-646.
21. Cowell B.A., Twining S.S., Hobden J.A., Kwong M.S., Fleiszig S.M. Mutation of lasA and lasB reduces Pseudomonas aeruginosa invasion of epithelial cells. Microbiology 2003, 149:2291-2299.
22. Schad P.A., Iglewski B.H. Nucleotide sequence and expression in Escherichia coli of the Pseudomonas aeruginosa lasA gene. J. Bacteriol. 1988, 170:2784-2789.
23. Rawlings N.D., Morton F.R., Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Res. 2006, 34:D270-D272.
24. Rawlings N.D., Barrett A.J. Evolutionary families of metallopeptidases. Methods Enzymol. 1995, 248:183-228.
25. Hooper N.M. Families of zinc metalloproteases. FEBS Lett. 1994, 354:1-6.
26. Park P.W., Mecham R.P. Lysostaphin. Handbook of Proteolytic Enzymes 2004, 1004-1005. Elsevier, London. 2nd edit. A.J. Barrett, N.D. Rawlings, J.F. Woessner (Eds.).
27. Barequet I.S., Ben Simon G.J., Safrin M., Ohman D.E., Kessler E. Pseudomonas aeruginosa LasA protease in treatment of experimental staphylococcal keratitis. Antimicrob. Agents Chemother. 2004, 48:1681-1687.
28. Barequet I.S., Habot-Wilner Z., Mann O., Safrin M., Ohman D.E., Kessler E., Rosner M. Evaluation of Pseudomonas aeruginosa staphylolysin (LasA protease) in the treatment of methicillin-resistant Staphylococcus aureus endophthalmitis in a rat model. Graefes Arch. Clin. Exp. Ophthalmol. 2009, 247:913-917.
29. Shah A., Mond J., Walsh S. Lysostaphin-coated catheters eradicate Staphylococccus aureus challenge and block surface colonization. Antimicrob. Agents Chemother. 2004, 48:2704-2707.
30. Wall R.J., Powell A.M., Paape M.J., Kerr D.E., Bannerman D.D., Pursel V.G., et al. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat. Biotechnol. 2005, 23:445-451.
31. Kokai-Kun J.F., Walsh S.M., Chanturiya T., Mond J.J. Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob. Agents Chemother. 2003, 47:1589-1597.
32. Smith T.J., Blackman S.A., Foster S.J. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 2000, 146:249-262.
33. Bernhardt T.G., de Boer P.A. Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol. 2004, 52:1255-1269.
34. Kessler E. β-Lytic endopeptidases. Methods Enzymol. 1995, 248:740-756.
35. Kessler E., Safrin M., Blumberg S., Ohman D.E. A continuous spectrophotometric assay for Pseudomonas aeruginosa LasA protease (staphylolysin) using a two-stage enzymatic reaction. Anal. Biochem. 2004, 328:225-232.
36. Xiang Y., Morais M.C., Cohen D.N., Bowman V.D., Anderson D.L., Rossmann M.G. Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage phi29 tail. Proc. Natl Acad. Sci. USA 2008, 105:9552-9557.
37. Bussiere D.E., Pratt S.D., Katz L., Severin J.M., Holzman T., Park C.H. The structure of VanX reveals a novel amino-dipeptidase involved in mediating transposon-based vancomycin resistance. Mol. Cell 1998, 2:75-84.
38. Charlier P., Wery J.-P., Dideberg O., Frere J.-M. Streptomyces albus G D-Ala-D-Ala carboxypeptidase. Handbook of Metalloproteins 2004, vol. 3:164-175. John Wiley & Sons, Chichester, NY. A. Messerschmidt, W. Bode, M. Cygler (Eds.).
39. Bochtler M., Odintsov S.G., Marcyjaniak M., Sabala I. Similar active sites in lysostaphins and D-Ala-D-Ala metallopeptidases. Protein Sci. 2004, 13:854-861.
40. Nilsen T., Nes I.F., Holo H. Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl. Environ. Microbiol. 2003, 69:2975-2984.
41. Fujiwara T., Aoki S., Komatsuzawa H., Nishida T., Ohara M., Suginaka H., Sugai M. Mutation analysis of the histidine residues in the glycylglycine endopeptidase ALE-1. J. Bacteriol. 2005, 187:480-487.
42. Ichimura T., Yamazoe M., Maeda M., Wada C., Hiraga S. Proteolytic activity of YibP protein in Escherichia coli. J. Bacteriol. 2002, 184:2595-2602.
43. Gargis S.R., Heath H.E., Heath L.S., Leblanc P.A., Simmonds R.S., Abbott B.D., et al. Use of 4-sulfophenyl isothiocyanate labeling and mass spectrometry to determine the site of action of the streptococcolytic peptidoglycan hydrolase zoocin A. Appl. Environ. Microbiol. 2009, 75:72-77.
44. Odintsov S.G., Sabala I., Marcyjaniak M., Bochtler M. Latent LytM at 1.3 Å resolution. J. Mol. Biol. 2004, 335:775-785.
45. Firczuk M., Mucha A., Bochtler M. Crystal structures of active LytM. J. Mol. Biol. 2005, 354:578-590.
46. Ragumani S., Kumaran D., Burley S.K., Swaminathan S. Crystal structure of a putative lysostaphin peptidase from Vibrio cholerae. Proteins: Struct. Funct. Genet. 2008, 72:1096-1103.
47. Gustin J.K., Kessler E., Ohman D.E. A substitution at His-120 in the LasA protease of Pseudomonas aeruginosa blocks enzymatic activity without affecting propeptide processing or extracellular secretion. J. Bacteriol. 1996, 178:6608-6617.
48. Pande A., Pande J., Asherie N., Lomakin A., Ogun O., King J., Benedek G.B. Crystal cataracts: human genetic cataract caused by protein crystallization. Proc. Natl Acad. Sci. USA 2001, 98:6116-6120.
49. Terwilliger T.C. Maximum likelihood density modification. Acta Crystallogr. D 2000, 56:965-972.
50. Terwilliger T.C. Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr. D 2003, 59:38-44.
51. Terwilliger T.C. Automated side-chain model building and sequence assignment by template matching. Acta Crystallogr. D 2003, 59:45-49.
52. Holm L., Sander C. DALI: a network tool for protein structure comparison. Trends Biochem. Sci. 1995, 20:478-480.
53. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucleic Acids Res 2000, 28:235-242.
54. Liao D.I., Kapadia G., Reddy P., Saier M.H., Reizer J., Herzberg O. Structure of the IIA domain of the glucose permease of Bacillus subtilis at 2.2-Å resolution. Biochemistry 1991, 30:9583-9594.
55. Ahmed K., Chohnan S., Ohashi H., Hirata T., Masaki T., Sakiyama F. Purification, bacteriolytic activity, and specificity of beta-lytic protease from Lysobacter sp. IB-9374. J. Biosci. Bioeng. 2003, 95:27-34.
56. Li S., Norioka S., Sakiyama F. Bacteriolytic activity and specificity of Achromobacter beta-lytic protease. J. Biochem. 1998, 124:332-339.
57. Li S.L., Norioka S., Sakiyama F. Molecular cloning and nucleotide sequence of the beta-lytic protease gene from Achromobacter lyticus. J. Bacteriol. 1990, 172:6506-6511.
58. Loewy A.G., Santer U.V., Wieczorek M., Blodgett J.K., Jones S.W., Cheronis J.C. Purification and characterization of a novel zinc-proteinase from cultures of Aeromonas hydrophila. J. Biol. Chem. 1993, 268:9071-9078.
59. Korndorfer I.P., Kanitz A., Danzer J., Zimmer M., Loessner M.J., Skerra A. Structural analysis of the L-alanoyl-D-glutamate endopeptidase domain of Listeria bacteriophage endolysin Ply500 reveals a new member of the LAS peptidase family. Acta Crystallogr. D 2008, 64:644-650.
60. Marcyjaniak M., Odintsov S.G., Sabala I., Bochtler M. Peptidoglycan amidase MepA is a LAS metallopeptidase. J. Biol. Chem. 2004, 279:43982-43989.
61. Breece R.M., Costello A., Bennett B., Sigdel T.K., Matthews M.L., Tierney D.L., Crowder M.W. A five-coordinate metal center in Co(II)-substituted VanX. J. Biol. Chem. 2005, 280:11074-11081.
62. Ehlert K., Tschierske M., Mori C., Schroder W., Berger-Bachi B. Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the Staphylococcal peptidoglycan interpeptide bridge. J. Bacteriol. 2000, 182:2635-2638.
63. Dehart H.P., Heath H.E., Heath L.S., Leblanc P.A., Sloan G.L. The lysostaphin endopeptidase resistance gene (epr) specifies modification of peptidoglycan cross bridges in Staphylococcus simulans and Staphylococcus aureus. Appl. Environ. Microbiol. 1995, 61:2811.
64. Kessler E., Safrin M., Olson J.C., Ohman D.E. Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J. Biol. Chem. 1993, 268:7503-7508.
65. Cohen D.N., Sham Y.Y., Haugstad G.D., Xiang Y., Rossmann M.G., Anderson D.L., Popham D.L. Shared catalysis in virus entry and bacterial cell wall depolymerization. J. Mol. Biol. 2009, 387:607-618.
66. Firczuk M., Bochtler M. Mutational analysis of peptidoglycan amidase MepA. Biochemistry 2007, 46:120-128.
67. Lipscomb W.N., Strater N. Recent advances in zinc enzymology. Chem. Rev. 1996, 96:2375-2433.
68. Gennadios H.A., Whittington D.A., Li X.C., Fierke C.A., Christianson D.W. Mechanistic inferences from the binding of ligands to LpxC, a metal-dependent deacetylase. Biochemistry 2006, 45:7940-7948.
69. Elston C., Wallach J., Saulnier J. New continuous and specific fluorometric assays for Pseudomonas aeruginosa elastase and LasA protease. Anal. Biochem. 2007, 368:87-94.
70. Hall T.M., Porter J.A., Beachy P.A., Leahy D.J. A potential catalytic site revealed by the 1.7-A crystal structure of the amino-terminal signalling domain of Sonic hedgehog. Nature 1995, 378:212-216.
71. Lessard I.A., Walsh C.T. Mutational analysis of active-site residues of the enterococcal D-Ala-D-Ala dipeptidase VanX and comparison with Escherichia coli D-Ala-D-Ala ligase and D-Ala-D-Ala carboxypeptidase VanY. Chem. Biol. 1999, 6:177-187.
72. Matthews M.L., Periyannan G., Hajdin C., Sidgel T.K., Bennett B., Crowder M.W. Probing the reaction mechanism of the D-Ala-D-Ala dipeptidase, VanX, by using stopped-flow kinetic and rapid-freeze quench EPR studies on the Co(II)-substituted enzyme. J. Am. Chem. Soc. 2006, 128:13050-13051.
73. Christianson D.W., Lipscomb W.N. Carboxypeptidase-A. Accts Chem. Res. 1989, 22:62-69.
74. Matthews B.W. Structural basis of the action of thermolysin and related zinc peptidases. Accts. Chem. Res. 1988, 21:333-340.
75. Hausrath A.C., Matthews B.W. Thermolysin in the absence of substrate has an open conformation. Acta Crystallogr. D 2002, 58:1002-1007.
76. Kilshtain-Vardi A., Glick M., Greenblatt H.M., Goldblum A., Shoham G. Refined structure of bovine carboxypeptidase A at 1.25 angstrom resolution. Acta Crystallogr. D 2003, 59:323-333.
77. Maynes J.T., Garen C., Cherney M.M., Newton G., Arad D., Av-Gay Y., et al. The crystal structure of 1-D-myo-inosityl-2-acetamido-2-deoxy-alpha-D-glucopyranoside deacetylase (MshB) from Mycobacterium tuberculosis reveals a zinc hydrolase with a lactate dehydrogenase fold. J. Biol. Chem. 2003, 278:47166-47170.
78. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
79. Jancarik J., Kim S.H. Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr. 1991, 24:409-411.
80. Cudney B., Patel S., Weisgraber K., Newhouse Y., McPherson A. Screening and optimization strategies for macromolecular crystal growth. Acta Crystallogr. D 1994, 50:414-423.
81. Murphy T.A., Catto L.E., Halford S.E., Hadfield A.T., Minor W., Walsh T.R., Spencer J. Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-beta-lactamases. J. Mol. Biol. 2006, 357:890-903.
82. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
83. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D 1999, 55:849-861.
84. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
85. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 2004, 60:2126-2132.
86. Lamzin V.S., Wilson K.S. Automated refinement for protein crystallography. Methods Enzymol 1997, 277:269-305.
87. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 1994, 50:760-763. Collaborative Computational Project, Number 4.
88. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 1997, 53:240-255.
89. Navaza, J. (2001). Implementation of molecular replacement in AMoRe. 57, 1367-1372.
90. Winn M.D., Isupov M.N., Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D 2001, 57:122-133.
91. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
92. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
93. Bond C.S., Schuttelkopf A.W. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D 2009, 65:510-512.
94. Potterton L., McNicholas S., Krissinel E., Gruber J., Cowtan K., Emsley P., et al. Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D 2004, 60:2288-2294.