Analyzing the catalytic mechanism of MPtpA: A low molecular weight protein tyrosine phosphatase from Mycobacterium tuberculosis through site-directed mutagenesis

Proteins: Structure, Function and Genetics

Volumn 71, Issue 2, 2008, Pages 706-714

  Madhurantakam, Chaithanya ^a   Chavali, Venkata Ramana Murthy ^a,b   Das, Amit Kumar ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY   (India)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Inhibition kinetics; Low molecular weight protein tyrosine phosphatase; MPtpA; Mycobacterium tuberculosis; pNPP; PTP loop; Site directed mutagenesis; Sodium molybdate; Sodium orthovanadate; Sodium tungstate

Indexed keywords

4 NITROPHENYL PHOSPHATE; ACID; MOLYBDATE SODIUM; PHOSPHATE; PROTEIN TYROSINE PHOSPHATASE; SODIUM DERIVATIVE; TUNGSTATE SODIUM; UNCLASSIFIED DRUG; VANADATE SODIUM;

ARTICLE; BACTERIAL VIRULENCE; CATALYSIS; CHEMICAL ENVIRONMENT; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; MOLECULAR WEIGHT; MUTATIONAL ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; WILD TYPE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYSIS; HYDROGEN-ION CONCENTRATION; INHIBITORY CONCENTRATION 50; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM TUBERCULOSIS; NITROPHENOLS; ORGANOPHOSPHORUS COMPOUNDS; PROTEIN TYROSINE PHOSPHATASES; SEQUENCE ALIGNMENT;

MYCOBACTERIUM TUBERCULOSIS;

EID: 41149155493     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21816     Document Type: Article

References (38)

1. WHO Report 2002: Global Tuberculosis Control - Surveillance, Planning, Financing. Geneva, Switzerland: World Health Organization; 2002.
2. Armstrong JA, Hart PD. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 1975;142:1-16.
3. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG. Lack of acidification in mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994;263:678-681.
4. Guan KL, Dixon JE. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 1990;249:553-556.
5. Fallman M, Andersson K, Hakansson S, Magnusson KE, Stendahl O, Wolf-Watz H. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 1995;63:3117-3124.
6. Kaniga K, Uralil J, Bliska JB, Galán JE. A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol Microbiol 1996;21:633-641.
7. Fu Y, Galan JE. The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 1998;27:359-368.
8. Selbach M, Moese S, Hurwitz R, Hauck CR, Meyer TF, Backert S. The Helicobacter pylori CagA protein induces cortactin dephosphorylation and actin rearrangement by c-Src inactivation. EMBO J 2003;22:515-528.
9. DeVinney R, Steele-Mortimer O, Finlay BB. Phosphatases and kinases delivered to the host cell by bacterial pathogens. Trends Microbiol 2000;8:29-33.
10. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry 3rd CE, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998;393:537-544.
11. Koul A, Choidas A, Treder M, Tyagi AK, Drlica K, Singh Y, Ullrich A. Cloning and characterization of secretory tyrosine phosphatases of Mycobacterium tuberculosis. J Bacteriol 2000;182:5425-5432.
12. Cowley SC, Babakaiff R, Av-Gay Y. Expression and localization of the Mycobacterium tuberculosis protein tyrosine phosphatase PtpA. Res Microbiol 2002;153:233-241.
13. Castandet J, Prost J-F, Peyron P, Dequeker CA, Anes E, Cozzone AJ, Griffiths G, Parini IM. Tyrosine phosphatase MptpA of Mycobacterium tuberculosis inhibits phagocytosis and increases actin polymerization in macrophages. Res in Microbiol 2005;156:1005-1013.
14. Evans B, Tishmack PA, Pokalsky C, Zhang M, Van Etten RL. Site-directed mutagenesis, kinetic, and spectroscopic studies of the P-loop residues in a low molecular weight protein tyrosine phosphatase. Biochemistry 1996;35:13609-13617.
15. Madhurantakam C, Rajakumara E, Mazumdar PA, Saha B, Mitra D, Wiker HG, Sankaranarayanan R, Das AK. Crystal structure of low-molecular-weight protein tyrosine phosphatase from Mycobacterium tuberculosis at 1.9-Å resolution. J Bacteriol 2005;187:2175-2181.
16. Fischer EH, Charbonneau H, Tonks NK. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science 1991;253:401-406.
17. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 1995;80:225-236.
18. Neel BG, Tonks NK. Protein tyrosine phosphatases in signal transduction. Curr Opin Cell Biol 1997;9:193-204.
19. Zhang ZY. Protein-tyrsoine phosphatases: biological function, structural characteristics, and mechanism of catalysis. Crit Rev Biochem Mol Biol 1998;33:1-52.
20. Zhang ZY, Dixon JE. Protein tyrsoine phosphatases: mechanism of catalysis and substrate specificity. Adv Enzymol Relat Areas Mol Biol 1994;68:1-36.
21. Su X.-D, Taddei N, Stefani M, Ramponi G, Nordlund P. The crystal structure of a low-molecular-weight phosphotyrosine phosphatase. Nature 1994;370:575-578.
22. Hoff RH, Hengge AC, Wu L, Keng Y-F, Zhang Z-Y. Effects on general acid catalysis from mutations of the invariant tryptophan and arginine residues in the protein tyrosine phosphatase from Yersinia. Biochemistry 2000;39:46-54.
23. Huyer G, Liu S, Kelly J, Moffat J, Payette P, Kennedy B, Tsaprailis G, Gresser MJ, Ramachandran C. Mechanism of inhibition of protein-tyrsoine phosphatases by vanadate and pervanadate. J Biol Chem 1997;272:843-851.
24. Heo Y-S, Ryu JM, Park SM, Park JH, Lee H-C, Hwang KY, Kim J. Structural basis of inhibition of protein tyrosine phosphatases by keggin compounds phosphomolybdate and phosphotungstate. Exp Mol Med 2002;34:211-223.
25. Barford D, Flint AJ, Tonks NK. Crystal structure of human protein tyrosine phosphatase 1B. Science 1994;263:1397-1404.
26. Pannifer AD, Flint AJ, Tonks NK, Barford D. Visualization of the cysteinyl-phosphate intermediate of a protein tyrosine phosphatase by x-ray crystallography. J Biol Chem 1998;273:10454-10462.
27. Cirri P, Fiaschi T, Chiarugi P, Camici G, Manao G, Raugei G, Ramponi G. The molecular basis of the differing kinetic behavior of the two low molecular mass phosphotyrosine protein phosphatase isoforms. J Biol Chem 1996;271:2604-2607.
28. Wang S, Tabernero L, Zhang M, Harms E, Van Etten RL, Stauffacher CV. Crystal structure of a low-molecular weight protein tyrosine phosphatase from Saccharomyces cerevisiae and its complex with the substrate p-nitrophenyl phosphate. Biochemistry 2000;39:1903-1914.
29. Kolmodin K, Aî qvist J. The catalytic mechanism of protein tyrosine phosphatases revisited. FEBS Letts 2001;498:208-213.
30. Ho SN, Henry DH, Horton RM, Pullen JK, Peasea LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989;77:51-59.
31. GraphPad Prism version 4.00 for Windows, 2004; San Diego, CA: GraphPad Software. Available at www.graphpad.com.
32. Chen L, Wu L, Otaka A, Smyth MS, Roller PP, Burke TR, Jr, den Hertog J, Zhang ZY. Why is phosphono-difuoromethyl phenylalanine a more potent inhibitory moiety than phosphonomethyl phenylalanine toward protein tyrosine phosphatases? Biochem Biophys Res Commun 1995;216:976-978.
33. DeLano ,W.L. The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific LLC; 2002. Available at http://www.pymol.org.
34. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive-multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
35. Clamp M, Cuff J, Searle SM, Barton GJ. The Jalview Java alignment editor. Bioinformatics 2004;20:426-427.
36. Kim J-H, Shin DY, Han M-H, Choi M-U. Mutational and kinetic evaluation of conserved His-123 in dual specificity protein-tyrosine phosphatase Vaccinia H1-related phosphatase. J Biol Chem 2001;276:27568-27574.
37. Zhang ZY. Kinetic and mechanistic characterization of a mammalian protein-tyrsoine phosphatase. J Biol Chem 1995;270:11199-11204.
38. Denu JM, Lohse DL, Vijayalakshmi J, Saper MA, Dixon JE. Visualization of intermediate and transition-state structures in protein-tyrosine phosphatase catalysis. Proc Natl Acad Sci USA 1996;93:2493-2498.