Structure of recombinant Haemophilus influenzae e (P4) acid phosphatase reveals a new member of the haloacid dehalogenase superfamily

Biochemistry

Volumn 46, Issue 39, 2007, Pages 11110-11119

  Felts, Richard L ^a   Ou, Zhonghui ^b   Reilly, Thomas J ^a,c   Tanner, John J ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLINE RECOMBINANT ENZYMES; HALOACID DEHALOGENASE; LIPOPROTEINS; METALLOENZYMES; RECOMBINANT HAEMOPHILUS INFLUENZAE;

DIMERIZATION; LIGANDS; NUCLEOPHILES; PROTEINS; VACCINES;

ENZYME ACTIVITY;

ACID PHOSPHATASE; AMINO ACID; ASPARTIC ACID; CARBOXYL GROUP; DIMER; EPITOPE; HALOACID DEHALOGENASE; LIGAND; LIPOPROTEIN E; MAGNESIUM; RECOMBINANT ENZYME; TUNGSTEN; UNCLASSIFIED DRUG; WATER;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CATALYSIS; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; HAEMOPHILUS INFLUENZAE; HAEMOPHILUS INFLUENZAE E; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

ACID PHOSPHATASE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HAEMOPHILUS INFLUENZAE; HYDROLASES; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

HAEMOPHILUS INFLUENZAE;

EID: 34848923767     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701016m     Document Type: Article

References (40)

1. Foxwell, A. R., Kyd, J. M., and Cripps, A. W. (1998) Nontypeable Haemophilus influenzae: pathogenesis and prevention, Microbiol. Mol. Biol. Rev. 62, 294-308.
2. Loeb, M. R., and Smith, D. H. (1980) Outer membrane protein composition in disease isolates of Haemophilus influenzae: pathogenic and epidemiological implications, Infect. Immun. 30, 709-717.
3. Green, B. A., Baranyi, E., Reilly, T. J., Smith, A. L., and Zlotnick, G. W. (2005) Certain site-directed, nonenzymatically active mutants of the Haemophilus influenzae P4 lipoprotein are able to elicit bactericidal antibodies, Infect. Immun. 73, 4454-4457.
4. Hotomi, M., Ikeda, Y., Suzumoto, M., Yamauchi, K., Green, B. A., Zlotnick, G., Billal, D. S., Shimada, J., Fujihara, K., and Yamanaka, N. (2005) A recombinant P4 protein of Haemophilus influenzae induces specific immune responses biologically active against nasopharyngeal colonization in mice after intranasal immunization, Vaccine 23, 1294-1300.
5. Mason, K. W., Zhu, D., Scheuer, C. A., McMichael, J. C., Zlotnick, G. W., and Green, B. A. (2004) Reduction of nasal colonization of nontypeable Haemophilus influenzae following intranasal immunization with rLP4/rLP6/UspA2 proteins combined with aqueous formulation of RC529, Vaccine 22, 3449-3456.
6. Oropeza, V. C., Page, M. E., and Van Bockstaele, E. J. (2005) Systemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex, Brain Res. 1046, 45-54.
7. Kemmer, G., Reilly, T. J., Schmidt-Brauns, J., Zlotnik, G. W., Green, B. A., Fiske, M. J., Herbert, M., Kraiss, A., Schlor, S., Smith, A., and Reidl, J. (2001) NadN and e (P4) are essential for utilization of NAD and nicotinamide mononucleotide but not nicotinamide riboside in Haemophilus influenzae, J. Bacteriol. 183, 3974-3981.
8. Reidl, J., Schlor, S., Kraiss, A., Schmidt-Brauns, J., Kemmer, G., and Soleva, E. (2000) NADP and NAD utilization in Haemophilus influenzae, Mol. Microbiol. 35, 1573-1581.
9. Thaller, M. C., Schippa, S., and Rossolini, G. M. (1998) Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily, Protein Sci. 7, 1647-1652.
10. Passariello, C., Schippa, S., Iori, P., Berlutti, F., Thaller, M. C., and Rossolini, G. M. (2003) The molecular class C acid phosphatase of Chryseobacterium meningosepticum (OlpA) is a broad-spectrum nucleotidase with preferential activity on 5′-nucleotides, Biochim. Biophys. Acta 1648, 203-209.
11. Malke, H. (1998) Cytoplasmic membrane lipoprotein LppC of Streptococcus equisimilis functions as an acid phosphatase, Appl. Environ. Microbiol. 64, 2439-2442.
12. Green, B. A., Farley, J. E., Quinn-Dey, T., Deich, R. A., and Zlotnick, G. W. (1991) The e (P4) outer membrane protein of Haemophilus influenzae: biologic activity of anti-e serum and cloning and sequencing of the structural gene, Infect Immun. 59, 3191-3198.
13. Godlewska, R., Bujnicki, J. M., Ostrowski, J., and Jagusztyn-Krynicka, E. K. (2002) The hppA gene of Helicobacter pylori encodes the class C acid phosphatase precursor, FEBS Lett. 525, 39-42.
14. du Plessis, E. M., Theron, J., Joubert, L., Lotter, T., and Watson, T. G. (2002) Characterization of a phosphatase secreted by Staphylococcus aureus strain 154, a new member of the bacterial class C family of nonspecific acid phosphatases, Syst. Appl. Microbiol. 25, 21-30.
15. May, B. J., Zhang, Q., Li, L. L., Paustian, M. L., Whittam, T. S., and Kapur, V. (2001) Complete genomic sequence of Pasteurella multocida, Pm70, Proc. Natl. Acad. Sci. U.S.A. 98, 3460-3465.
16. Read, T. D., Peterson, S. N., Tourasse, N., Baillie, L. W., Paulsen, I. T., Nelson, K. E., Tettelin, H., Fouts, D. E., Eisen, J. A., Gill, S. R., Holtzapple, E. K., Okstad, O. A., Helgason, E., Rilstone, J., Wu, M., Kolonay, J. F., Beanan, M. J., Dodson, R. J., Brinkac, L. M., Gwinn, M., DeBoy, R. T., Madpu, R., Daugherty, S. C., Durkin, A. S., Haft, D. H., Nelson, W. C., Peterson, J. D., Pop, M., Khouri, H. M., Radune, D., Benton, J. L., Mahamoud, Y., Jiang, L., Hance, I. R., Weidman, J. F., Berry, K. J., Plaut, R. D., Wolf, A. M., Watkins, K. L., Nierman, W. C., Hazen, A., Cline, R., Redmond, C., Thwaite, J. E., White, O., Salzberg, S. L., Thomason, B., Friedlander, A. M., Koehler, T. M., Hanna, P. C., Kolsto, A. B., and Fraser, C. M. (2003) The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria, Nature 423, 81-86.
17. Reilly, T. J., and Smith, A. L. (1999) Purification and characterization of a recombinant Haemophilus influenzae outer membrane Phosphomonoesterase e (P4), Protein Expression Purif. 17, 401-409.
18. Reilly, T. J., Chance, D. L., and Smith, A. L. (1999) Outer membrane lipoprotein e (P4) of Haemophilus influenzae is a novel Phosphomonoesterase, J. Bacterial. 181, 6797-6805.
19. Ou, Z., Felts, R. L., Reilly, T. J., Nix, J. C., and Tanner, J. J. (2006) Crystallization of recombinant Haemophilus influenzae e (P4) acid phosphatase, Acta Crystallogr. F62, 464-466.
20. Pflugrath, J. W. (1999) The finer things in X-ray diffraction data collection, Acta Crystallogr. D55, 1718-1725.
21. Terwilliger, T. C. (2003) SOLVE and RESOLVE: automated structure solution and density modification, Methods Enzymol. 374, 22-37.
22. Morris, R. J., Perrakis, A., and Lamzin, V. S. (2002) ARP/wARP's model-building algorithms. I. The main chain, Acta Crystallogr. D58, 968-975.
23. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics, Acta Crystallogr. D60, 2126-2132.
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. F53, 240-255.
25. DeLano, W. L. (2002) The PyMOL Molecular Graphics System (http://www.pymol.org).
26. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank, Nucleic Acids Res. 28, 235-242.
27. Dietmann, S., Park, J., Notredame, C., Heger, A., Lappe, M., and Holm, L. (2001) A fully automatic evolutionary classification of protein folds: Dali Domain Dictionary version 3, Nucleic Acids Res. 29, 55-57.
28. Calderone, V., Forleo, C., Benvenuti, M., Thaller, M. C., Rossolini, G. M., and Mangani, S. (2006) A structure-based proposal for the catalytic mechanism of the bacterial acid phosphatase AphA belonging to the DDDD superfamily of phosphohydrolases, J. Mol. Biol. 355, 708-721.
29. Galburt, E. A., Pelletier, J., Wilson, G., and Stoddard, B. L. (2002) Structure of a tRNA repair enzyme and molecular biology workhorse: T4 polynucleotide kinase, Structure 10, 1249-1260.
30. Wallden, K., Ruzzenente, B., Rinaldo-Matthis, A., Bianchi, V., and Nordlund, P. (2005) Structural basis for substrate specificity of the human mitochondrial deoxyribonucleotidase, Structure 13, 1081-1088.
31. Peisach, E., Selengut, J. D., Dunaway-Mariano, D., and Allen, K. N. (2004) X-ray crystal structure of the hypothetical phosphotyrosine phosphatase MDP-1 of the haloacid dehalogenase superfamily, Biochemistry 43, 12770-12779.
32. Morais, M. C., Zhang, W., Baker, A. S., Zhang, G., Dunaway-Mariano, D., and Allen, K. N. (2000) The crystal structure of Bacillus cereus phosphonoacetaldehyde hydrolase: insight into catalysis of phosphorus bond cleavage and catalytic diversification within the HAD enzyme superfamily, Biochemistry 39, 10385-10396.
33. Allen, K. N., and Dunaway-Mariano, D. (2004) Phosphoryl group transfer: evolution of a catalytic scaffold, Trends Biochem. Sci. 29, 495-503.
34. Harding, M. M. (2004) The architecture of metal coordination groups in proteins, Acta Crystallogr. D60, 849-859.
35. Calderone, V., Forleo, C., Benvenuti, M., Cristina, Thaller, M., Maria, Rossolini, G., and Mangani, S. (2004) The first structure of a bacterial class B Acid phosphatase reveals further structural heterogeneity among phosphatases of the haloacid dehalogenase fold, J. Mol. Biol. 335, 761-773.
36. Krissinel, E., and Henick, K. (2005) Protein interfaces, surfaces and assemblies service PISA at European Bioinformatica Institute (http://www.ebi.ac.uk/msd-srv/prot_int/pistart.html), Comp. Life, 163-174.
37. Reidl, J., and Mekalanos, J. J. (1996) Lipoprotein e(P4) is essential for hemin uptake by Haemophilus influenzae, J. Exp. Med. 183, 621-629.
38. Reilly, T. J., Green, B. A., Zlotnick, G. W., and Smith, A. L. (2001) Contribution of the DDDD motif of H. influenzae e (P4) to Phosphomonoesterase activity and heme transport, FEBS Lett. 494, 19-23.
39. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for x-ray protein structure refinement, Acta Crystallogr. A47, 392-400.
40. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation, Proteins 50, 437-450.