Structure/function studies of Ser/Thr and Tyr protein phosphorylation in Mycobacterium tuberculosis

Journal of Molecular Microbiology and Biotechnology

Volumn 9, Issue 3-4, 2006, Pages 167-181

  Greenstein, Andrew E ^a   Grundner, Christoph ^a   Echols, Nathaniel ^a   Gay, Laurie M ^a   Lombana, T Noelle ^a   Miecskowski, Carl A ^a   Pullen, Kristi E ^a   Sung, Pei Yi ^a   Alber, Tom ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Protein kinase substrates; Protein tyrosine phosphatase; Ser Thr protein kinase

Indexed keywords

BACTERIAL ENZYME; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE PHOSPHATASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RECEPTOR PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; CELL DIVISION; CHEMICAL ANALYSIS; DIMERIZATION; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENETIC ANALYSIS; HOST PARASITE INTERACTION; METAL BINDING; MOLECULAR RECOGNITION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; TRANSPORT KINETICS;

BACTERIAL PROTEINS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES;

BACTERIA (MICROORGANISMS); EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA;

EID: 30744467404     PISSN: 14641801     EISSN: None     Source Type: Journal    
DOI: 10.1159/000089645     Document Type: Review

References (74)

1. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J., and Mustelin, T. 2004. Protein tyrosine phosphatases in the human genome. Cell 117:699-711.
2. Archambaud, C., Gouin, E., Pizarro-Cerda, J., Cossart, P., Dussurget, O. 2005. Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Mol Microbiol 56:383-396.
3. Av-Gay, Y., Jamil, S., Drews, S.J. 1999.Expression and characterization of the Mycobacterium tuberculosis serine/threonine protein kinase PknB. Infect Immun 67:5676-5682.
4. Av-Gay, Y., Everett M. 2000. The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol 8:238-244.
5. Bendt, A.K., Burkovski, A., Schaffer, S., Bott, M., Farwick, M., Hermann, T. 2003. Towards a phosphoproteome map of Corynebacterium glutamicum. Proteomics 3:1637-1646.
6. Boitel, B., Ortiz-Lombardia, M., Duran, R., Pompeo, F., Cole, S.T., Cervenansky, C., Alzari, P.M. 2003. PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol Microbiol 49:1493-1508.
7. Castandet, J., Prost, J.F., Peyron, P., Astarie-Dequeker, C., Anes, E., Cozzone, A.J., Griffiths, G., Maridonneau-Parini, I. 2005. Tyrosine phosphatase MptpA of Mycobacterium tuberculosis inhibits phagocytosis and increases actin polymerization in macrophages. Res Microbiol, in press.
8. Chaba, R., Raje, M., Chakraborti, P.K. 2002. Evidence that a eukaryotic-type serine/threonine protein kinase from Mycobacterium tuberculosis regulates morphological changes associated with cell division. Eur J Biochem 269:1078-1085.
9. Chopra, P., Singh, B., Singh, R., Vohra, R., Koul, A., Meena, L.S., Koduri, H., Ghildiyal, M., Deol, P., Das, T.K., Tyagi, A.K., Singh, Y. 2003. Phosphoprotein phosphatase of Mycobacterium tuberculosis dephosphorylates serine-threonine kinases PknA and PknB. Biochem Biophys Res Commun 311:112-120.
10. Cole, S.T. et al., 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
11. Cornells, G. R. 2002. The Yersinia Ysc-Yop 'type III' weaponry. Nat Rev Mol Cell Biol 3:742-752.
12. Cowley, S.C., Babakaiff, R., Av-Gay, Y. 2002. Expression and localization of the Mycobacterium tuberculosis protein tyrosine phosphatase PtpA. Res Microbiol 153:233-241.
13. Cowley, S., Ko, M., Pick, N., Chow, R., Downing, K.J., Gordhan, B.G., Betts JC, Mizrahi, V., Smith, D.A., Stokes, R.W., Av-Gay, Y. 2004. The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52:1691-1702.
14. Cozzone, A.J. 2005. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J Mol Microbiol Biotechnol 9:198-213.
15. Curry, J.M., Whalan, R., Hunt, D.M., Gohil, K., Strom, M., Rickman, L., Colston, M.J., Smerdon S.J., Buxton, R.S. 2005. An ABC transporter containing a forkhead-associated domain interacts with a serine-threonine protein kinase and is required for growth of Mycobacterium tuberculosis in mice. Infect Immun 73:4471-4477.
16. Das, A.K., Helps, N.R., Cohen, P.T., Barford, D. 1996. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J 15:6798-6809.
17. Deol, P., Vohra, R., Saini, A.K., Singh, A., Chandra, H., Chopra, P., Das, T.K., Tyagi, A.K., Singh, Y. 2005. Role of Mycobacterium tuberculosis Ser/Thr kinase PknF: implications in glucose transport and cell division. J Bacteriol 187:3415-3420.
18. Duran, R., Villarino, A., Bellinzoni, M., Wehenkel, A., Fernandez, P., Boitel, B., Cole, S.T., Alzari, P.M., Cervenansky C. 2005. Conserved autophosphorylation pattern in activation loops and juxtamembrane regions of Mycobacterium tuberculosis Ser/Thr protein kinases. Biochem Biophys Res Commun 333:858-867.
19. Durocher, D., Jackson, S.P. 2002. The FHA domain. FEBS Lett 513:58-66.
20. Fu, Y., Galan, J. E. 1999. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401:293-297.
21. Gaidenko, T.A., Kim, T.J., Price, C.W. 2002. The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J Bacteriol 184:6109-6114.
22. Galperin, M.Y., Nikolskaya, A.N., Koonin, E.V. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11-21.
23. Goldberg, J., Nairn, A.C., Kuriyan, J. 1996. Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I. Cell 84:875-887.
24. Good, M.C., Greenstein, A.E., Young, T.A., Ng, H.-L., Alber, T. 2004. Sensor domain of the Mycobacterium tuberculosis receptor Ser/Thr protein kinase, PknD, forms a highly symmetric β propeller. J Mol Biol 339:459-469.
25. Gopalaswamy, R., Narayanan, P.R., Narayanan, S. 2004. Cloning, overexpression, and characterization of a serine/threonine protein kinase pknI from Mycobacterium tuberculosis H37Rv. Protein Expr Purif 36:82-89.
26. Groen, A., Lemeer, S., van der Wijk, T., Overvoorde, J., Heck, A.J., Ostman, A., Barford, D., Slijper. M,, den Hertog, J. 2005. Differential oxidation of protein-tyrosine phosphatases. J Biol Chem 280:10298-10304.
27. Grundner, C., Gay, L.M., Alber, T. 2005a. Mycobacterium tuberculosis serine/threonine kinases PknB, PknD, PknE, and PknF phosphorylate multiple FHA domains. Protein Sci 14:1918-1921.
28. Grundner, C., Ng, H.-L., Alber, T. 2005b. Mycobacterium tuberculosis protein tyrosine phosphatase PtpB structure reveals a diverged fold with a buried active site. Structure 13:1625-1634.
29. Hoch, J.A. 2000. Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165-170.
30. Hughes, K.T., Mathee, K. 1998. The anti-sigma factors. Annu Rev Microbiol 52:231-286.
31. Huse, M., Kuriyan, J. 2002. The conformational plasticity of protein kinases. Cell 109:275-282.
32. Jackson, M.D., Denu, J.M. 2001. Molecular reactions of protein phosphatases - insights from structure and chemistry. Chem Rev 101:2313-2340.
33. Jackson, M.D., Fjeld, C.C., Denu, J.M. 2003. Probing the function of conserved residues in the serine/threonine phosphatase PP2Cα. Biochemistry 42:8513-8521.
34. Kang, C.M., Abbott, D.W., Park, S.T., Dascher, C.C., Cantley, L.C., Husson, R.N. 2005. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 19:1692-1704.
35. Kennelly, P.J. 2002. Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol Lett 206:1-8.
36. Kennelly, P.J. 2003. Archaeal protein kinases and protein phosphatases: insights from genomics and biochemistry. Biochem J 370:373-389.
37. Koul, A., Choidas, A., Treder, M., Tyagi, A.K., Drlica, K., Singh, Y., Ullrich, A. 2000. Cloning and characterization of secretory tyrosine phosphatases of Mycobacterium tuberculosis. J Bacteriol 182:5425-5432.
38. Koul, A., Choidas, A., Tyagi, A.K., Drlica, K., Singh, Y., Ullrich, A. 2001. Serine/threonine protein kinases PknF and PknG of Mycobacterium tuberculosis: characterization and localization. Microbiology 147:2307-2314.
39. Koul, A., Herget, T., Klebl, B., Ullrich, A. 2004. Interplay between mycobacteria and host signalling pathways. Nat Rev Microbiol 2:189-202.
40. Leonard, C.J., Aravind, L., Koonin, E.V. 1998. Novel families of putative protein kinases in bacteria and archaea: evolution of the 'eukaryotic' protein kinase superfamily. Genome Res 8:1038-1047.
41. Madec, E., Laszkiewicz, A., Iwanicki, A., Obuchowski, M., Seror, S. 2002. Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol Microbiol 46:571-586.
42. Madec, E., Stensballe, A., Kjellstrom, S., Cladiere, L., Obuchowski, M., Jensen, O.N., Seror, S.J. 2003. Mass spectrometry and site-directed mutagenesis identify several autophosphorylated residues required for the activity of PrkC, a Ser/Thr kinase from Bacillus subtilis. J Mol Biol 330:459-472.
43. Madhurantakam, C., Rajakumara, E., Mazumdar, P.A., Saha, B., Mitra, D., Wiker H.G., Sankaranarayanan, R., Das, A.K. 2005. Crystal structure of low-molecular-weight protein tyrosine phosphatase from Mycobacterium tuberculosis at 1.9-A resolution. J Bacteriol 187:2175-2181.
44. Madhusudan, Akamine, P., Xuong, N.H., Taylor, S.S. 2002. Crystal structure of a transition state mimic of the catalytic subunit of cAMP-dependent protein kinase. Nat Struct Biol 9:273-277.
45. Manning, G., Whyte, D.B, Martinez, R., Hunter, T., Sudarsanam, S. 2002. The protein kinase complement of the human genome. Science 298:1912-1934.
46. Matsumoto, A., Hong, S.K., Ishizuka, H., Horinouchi, S., Beppu, T. 1994. Phosphorylation of the AfsR protein involved in secondary metabolism in Streptomyces species by a eukaryotic-type protein kinase. Gene 146:47-56.
47. McCarty, D.R., Chory, J. 2000. Conservation and innovation in plant signaling pathways. Cell 103:201-209.
48. Meggio, F., Pinna, L.A. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368.
49. Molle, V., Girard-Blanc, C., Kremer, L., Doublet, P., Cozzone, A.J., Prost, J.F. 2003a. Protein PknE, a novel transmembrane eukaryotic-like serine/threonine kinase from Mycobacterium tuberculosis. Biochem Biophys Res Commun 308:820-825.
50. Molle, V., Kremer, L., Girard-Blanc, C., Besra, G.S., Cozzone, A.J. ,Prost, J.F. 2003b. An FHA phosphoprotein recognition domain mediates protein EmbR phosphorylation by PknH, a Ser/Thr protein kinase from Mycobacterium tuberculosis. Biochemistry 42:15300-15309.
51. Molle, V., Soulat, D., Jault, J.M., Grangeasse, C., Cozzone, A.J., Prost, J.F. 2004. Two FHA domains on an ABC transporter, Rv1747, mediate its phosphorylation by PknF, a Ser/Thr protein kinase from Mycobacterium tuberculosis. FEMS Microbiol Lett 234:215-223.
52. Ortiz-Lombardia, M., Pompeo, F., Boitel, B., Alzari, P.M. 2003. Crystal structure of the catalytic domain of the PknB Serine/Threonine kinase from Mycobacterium tuberculosis. J Biol Chem 278:13094-13100.
53. Papavinasasundaram, K.G., Chan, B., Chung, J.H., Colston, M.J., Davis, E.O., Av-Gay, Y. 2005. Deletion of the Mycobacterium tuberculosis pknH gene confers a higher bacillary load during the chronic phase of infection in BALB/c mice. J Bacteriol 187:5751-5760.
54. Parish. T., Smith, D.A., Kendall, S., Casali, N., Bancroft, G.J., Stoker, N.G. 2003. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect Immun 71:1134-1140.
55. Peirs, P., De Wit, L., Braibant, M., Huygen, K., Content, J. 1997. A serine/threonine protein kinase from Mycobacterium tuberculosis. Eur J Biochem 244:604-612.
56. Peirs, P., Lefevre, P., Boarbi, S., Wang, X.M., Denis, O., Braibant, M., Pethe, K., Locht, C., Huygen, K., Content, J. 2005. Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun 73:1898-1902.
57. Rajagopal, L., Clancy, A., Rubens, C.E. 2003. A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J Biol Chem 278:14429-14441.
58. Rajagopal, L., Vo, A., Silvestroni, A., Rubens, C.E. 2005. Regulation of purine biosynthesis by a eukaryotic-type kinase in Streptococcus agalactiae. Mol Microbiol 56:1329-1346.
59. Russell, D.G. 2001. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2:569-577.
60. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C., Hinks, J. A., Tonks, N. K., Barford, D. 2003. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769-773.
61. Sassetti, C.M., Boyd, D.H., Rubin, E.J. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48:77-84.
62. Sassetti, C.M., Rubin, E.J. 2003. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100:12989-12994.
63. Sawai, R., Suzuki, A., Takano, Y., Lee, P.C., Horinouchi, S. 2004. Phosphorylation of AfsR by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). Gene 334:53-61.
64. Sharma, K., Chandra, H., Gupta, P.K., Pathak, M., Narayan, A., Meena, L.S., D'Souza, R.C., Chopra, P., Ramachandran, S., Singh, Y. 2004. PknH, a transmembrane Hank's type serine/threonine kinase from Mycobacterium tuberculosis is differentially expressed under stress conditions. FEMS Microbiol Lett 233:107-113.
65. Sickmann, A., Meyer, H.E. 2001. Phosphoamino acid analysis. Proteomics 1:200-206.
66. Singh, R., Rao, V., Shakila, H., Gupta, R., Khera, A., Dhar, N., Singh, A., Koul, A., Singh, Y., Naseema, M., Narayanan, P.R., Paramasivan, C.N., Ramanathan, V.D., Tyagi, A.K. 2003. Disruption of mptpB impairs the ability of Mycobacterium tuberculosis to survive in guinea pigs. Mol Microbiol 50:751-762.
67. Umeyama, T., Lee, P.C., Horinouchi, S. 2002. Protein serine/threonine kinases in signal transduction for secondary metabolism and morphogenesis in Streptomyces. Appl Microbiol Biotechnol 59:419-425.
68. van Montfort, R. L., Congreve, M., Tisi, D., Carr, R., Jhoti, H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773-777.
69. Villarino, A., Duran, R., Wehenkel, A., Fernandez, P., England, P., Brodin, P., Cole, S.T., Zimny-Arndt, U., Jungblut, P.R., Cervenansky, C., Alzari P.M. 2005. Proteomic identification of M. tuberculosis protein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions. J Mol Biol 350:953-963.
70. Walburger, A., Koul, A., Ferrari, G., Nguyen, L., Prescianotto-Baschong, C., Huygen, K., Klebl, B., Thompson, C., Bacher, G., Pieters, J. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304:1800-1804.
71. Xu, W., Doshi, A., Lei, M., Eck, M.J., Harrison, S.C. 1999. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol Cell 3:629-638.
72. Young, M.A., Gonfloni, S., Superti-Furga, G., Roux, B., Kuriyan, J. 2001. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105:115-126.
73. Young, T.A., Delagoutte, B., Endrizzi, J.A., Falick, A.M., Alber, T. 2003. Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat Struct Biol 10:168-174.
74. Zhang, W., Munoz-Dorado, J., Inouye, M., Inouye, S. 1992. Identification of a putative eukaryotic-like protein kinase family in the developmental bacterium Myxococcus xanthus. J Bacteriol 174:5450-5453.