A serine/threonine phosphatase encoded by MG-207 of Mycoplasma genitalium is critical for its virulence

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Martinez, Mario A ^a,b   Das, Kishore ^a   Saikolappan, Sankaralingam ^a   Materon, Luis A ^b   Dhandayuthapani, Subramanian ^a  

^a University of Texas Health Science Center   (United States)

^b UNIVERSITY OF TEXAS PAN AMERICAN   (United States)

Author keywords

Mycoplasma; Pathogenesis; Phosphatase; Serine; Threonine kinase; Virulence

Indexed keywords

4 NITROPHENYL PHOSPHATE; ALKALINE PHOSPHATASE; CYTOSKELETON PROTEIN; HYDROGEN PEROXIDE; PHOSPHATASE; PYRUVATE DEHYDROGENASE; SERINE; SERINE THREONINE PHOSPHATASE; THREONINE; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOTOXICITY; ESCHERICHIA COLI; HELA CELL; MASS SPECTROMETRY; MYCOPLASMA GENITALIUM; NONHUMAN; PROTEIN PHOSPHORYLATION; TRANSPOSON;

BACTERIAL PROTEINS; CELL DEATH; CELL LINE; DNA TRANSPOSABLE ELEMENTS; EPITHELIAL CELLS; ESCHERICHIA COLI; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; HUMANS; HYDROLYSIS; MONOCYTES; MUTAGENESIS, INSERTIONAL; MYCOPLASMA GENITALIUM; NITROPHENOLS; ORGANOPHOSPHORUS COMPOUNDS; PHOSPHOPROTEIN PHOSPHATASES; RECOMBINANT PROTEINS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MYCOPLASMA; MYCOPLASMA GENITALIUM;

EID: 84874008790     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-44     Document Type: Article

References (59)

1. Hoch JA, Silhavy TJ, Two component singnal transduction Washington, D.C.: American Society of Microbiology 1995
2. Two-component and phosphorelay signal transduction. Hoch JA, Curr Opin Microbiol 2000 3 2 165 170 10.1016/S1369-5274(00)00070-9 10745001
3. Bacterial signalling involving eukaryotic-type protein kinases. Zhang CC, Mol Microbiol 1996 20 1 9 15 10.1111/j.1365-2958.1996.tb02483.x 8861199
4. Eukaryote-like serine/threonine kinases and phosphatases in bacteria. Pereira SF, Goss L, Dworkin J, Microbiol Mol Biol Rev 2011 75 1 192 212 10.1128/MMBR.00042-10 21372323
5. Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. Kennelly PJ, FEMS Microbiol Lett 2002 206 1 1 8 10.1111/j.1574-6968.2002.tb10978.x 11786249
6. Diversity in domain architectures of Ser/Thr kinases and their homologues in prokaryotes. Krupa A, Srinivasan N, BMC Genomics 2005 6 129 10.1186/1471-2164-6-129 16171520
7. Regulation of prokaryotic gene expression by eukaryotic-like enzymes. Burnside K, Rajagopal L, Curr Opin Microbiol 2012 15 2 125 131 10.1016/j.mib.2011.12.006 22221896
8. Two-component signal transduction as potential drug targets in pathogenic bacteria. Gotoh Y, Eguchi Y, Watanabe T, Okamoto S, Doi A, Utsumi R, Curr Opin Microbiol 2010 13 2 232 239 10.1016/j.mib.2010.01.008 20138000
9. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Galyov EE, Hakansson S, Forsberg A, Wolf-Watz H, Nature 1993 361 6414 730 732 10.1038/361730a0 8441468
10. A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Juris SJ, Rudolph AE, Huddler D, Orth K, Dixon JE, Proc Natl Acad Sci U S A 2000 97 17 9431 9436 10.1073/pnas. 170281997 10920208
11. The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Cowley S, Ko M, Pick N, Chow R, Downing KJ, Gordhan BG, Betts JC, Mizrahi V, Smith DA, Stokes RW, Mol Microbiol 2004 52 6 1691 1702 10.1111/j.1365-2958. 2004.04085.x 15186418
12. Deletion of the Mycobacterium tuberculosis pknH gene confers a higher bacillary load during the chronic phase of infection in BALB/c mice. Papavinasasundaram KG, Chan B, Chung JH, Colston MJ, Davis EO, Av-Gay Y, J Bacteriol 2005 187 16 5751 5760 10.1128/JB.187.16.5751-5760.2005 16077122
13. Staphylococcal PknB as the first prokaryotic representative of the proline-directed kinases. Miller M, Donat S, Rakette S, Stehle T, Kouwen TR, Diks SH, Dreisbach A, Reilman E, Gronau K, Becher D, PLoS One 2010 5 2 9057 10.1371/journal.pone.0009057 20140229
14. Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. Debarbouille M, Dramsi S, Dussurget O, Nahori MA, Vaganay E, Jouvion G, Cozzone A, Msadek T, Duclos B, J Bacteriol 2009 191 13 4070 4081 10.1128/JB.01813-08 19395491
15. Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Echenique J, Kadioglu A, Romao S, Andrew PW, Trombe MC, Infect Immun 2004 72 4 2434 2437 10.1128/IAI.72.4.2434-2437.2004 15039376
16. Streptococcus pyogenes Ser/Thr kinase-regulated cell wall hydrolase is a cell division plane-recognizing and chain-forming virulence factor. Pancholi V, Boel G, Jin H, J Biol Chem 2010 285 40 30861 30874 10.1074/jbc.M110.153825 20643653
17. A novel serine/threonine protein kinase homologue of Pseudomonas aeruginosa is specifically inducible within the host infection site and is required for full virulence in neutropenic mice. Wang J, Li C, Yang H, Mushegian A, Jin S, J Bacteriol 1998 180 24 6764 6768 9852028
18. A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. Rajagopal L, Clancy A, Rubens CE, J Biol Chem 2003 278 16 14429 14441 10.1074/jbc.M212747200 12562757
19. Regulation of cytotoxin expression by converging eukaryotic-type and two-component signalling mechanisms in Streptococcus agalactiae. Rajagopal L, Vo A, Silvestroni A, Rubens CE, Mol Microbiol 2006 62 4 941 957 10.1111/j.1365-2958.2006.05431.x 17005013
20. The stability of cytadherence proteins in Mycoplasma pneumoniae requires activity of the protein kinase PrkC. Schmidl SR, Gronau K, Hames C, Busse J, Becher D, Hecker M, Stulke J, Infect Immun 2009 78 1 184 192 19858294
21. The prpZ gene cluster encoding eukaryotic-type Ser/Thr protein kinases and phosphatases is repressed by oxidative stress and involved in Salmonella enterica serovar Typhi survival in human macrophages. Faucher SP, Viau C, Gros PP, Daigle F, Le Moual H, FEMS Microbiol Lett 2008 281 2 160 166 10.1111/j.1574-6968.2008.01094.x 18312574
22. Role of serine/threonine phosphatase (SP-STP) in Streptococcus pyogenes physiology and virulence. Agarwal S, Pancholi P, Pancholi V, J Biol Chem 2011 286 48 41368 41380 10.1074/jbc.M111.286690 21917918
23. Serine/threonine phosphatase (SP-STP), secreted from Streptococcus pyogenes, is a pro-apoptotic protein. Agarwal S, Jin H, Pancholi P, Pancholi V, J Biol Chem 2012 287 12 9147 9167 10.1074/jbc.M111.316554 22262847
24. Serine/threonine phosphatase Stp1 mediates post-transcriptional regulation of hemolysin, autolysis, and virulence of group B Streptococcus. Burnside K, Lembo A, Harrell MI, Gurney M, Xue L, BinhTran NT, Connelly JE, Jewell KA, Schmidt BZ, de los Reyes M, J Biol Chem 2011 286 51 44197 44210 10.1074/jbc.M111.313486 22081606
25. Strain-specific regulatory role of eukaryote-like serine/threonine phosphatase in pneumococcal adherence. Agarwal S, Pancholi P, Pancholi V, Infect Immun 2012 80 4 1361 1372 10.1128/IAI.06311-11 22311926
26. Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Archambaud C, Gouin E, Pizarro-Cerda J, Cossart P, Dussurget O, Mol Microbiol 2005 56 2 383 396 10.1111/j.1365-2958.2005.04551.x 15813732
27. The minimal gene complement of Mycoplasma genitalium. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Science 1995 270 5235 397 403 10.1126/science.270.5235.397 7569993
28. Mycoplasma genitalium: from Chrysalis to multicolored butterfly. Taylor-Robinson D, Jensen JS, Clin Microbiol Rev 2011 24 3 498 514 10.1128/CMR.00006-11 21734246
29. Mycoplasma genitalium: should we treat and how? Manhart LE, Broad JM, Golden MR, Clin Infect Dis 2011 53 3 129 142 10.1093/cid/cir702
30. The demographic, sexual health and behavioural correlates of Mycoplasma genitalium infection among women with clinically suspected pelvic inflammatory disease. Short VL, Totten PA, Ness RB, Astete SG, Kelsey SF, Murray P, Haggerty CL, Sex Transm Infect 2009 86 1 29 31 19703841
31. Clinical presentation of Mycoplasma genitalium Infection versus Neisseria gonorrhoeae infection among women with pelvic inflammatory disease. Short VL, Totten PA, Ness RB, Astete SG, Kelsey SF, Haggerty CL, Clin Infect Dis 2009 48 1 41 47 10.1086/594123 19025498
32. Association between Mycoplasma genitalium and acute endometritis. Cohen CR, Manhart LE, Bukusi EA, Astete S, Brunham RC, Holmes KK, Sinei SK, Bwayo JJ, Totten PA, Lancet 2002 359 9308 765 766 10.1016/S0140-6736(02)07848-0 11888591
33. Association of Mycoplasma genitalium and HIV infection: a systematic review and meta-analysis. Napierala Mavedzenge S, Weiss HA, AIDS 2009 23 5 611 620 10.1097/QAD.0b013e328323da3e 19194271
34. Intracellular DNA replication and long-term survival of pathogenic mycoplasmas. Dallo SF, Baseman JB, Microb Pathog 2000 29 5 301 309 10.1006/mpat.2000.0395 11031124
35. Interaction of Mycoplasma genitalium with host cells: evidence for nuclear localization. Ueno PM, Timenetsky J, Centonze VE, Wewer JJ, Cagle M, Stein MA, Krishnan M, Baseman JB, Microbiology 2008 154 Pt 10 3033 3041 18832309
36. Persistent Mycoplasma genitalium infection of human endocervical epithelial cells elicits chronic inflammatory cytokine secretion. McGowin CL, Annan RS, Quayle AJ, Greene SJ, Ma L, Mancuso MM, Adegboye D, Martin DH, Infect Immun 2012 80 11 3842 3849 10.1128/IAI.00819-12 22907815
37. Regulation of bacterial virulence by two-component systems. Beier D, Gross R, Curr Opin Microbiol 2006 9 2 143 152 10.1016/j.mib.2006.01.005 16481212
38. Signaling-mediated bacterial persister formation. Vega NM, Allison KR, Khalil AS, Collins JJ, Nat Chem Biol 2012 8 5 431 433 10.1038/nchembio.915 22426114
39. Mycobacterial persistence: adaptation to a changing environment. Honer Zu Bentrup K, Russell DG, Trends Microbiol 2001 9 12 597 605 10.1016/S0966- 842X(01)02238-7 11728873
40. Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li B, Herrmann R, Nucl Acids Res 1996 24 4420 4449 10.1093/nar/24.22.4420 8948633
41. Comparative analysis of the genomes of the bacteria Mycoplasma pneumoniae and Mycoplasma genitalium. Himmelreich R, Plagens H, Hilbert H, Reiner B, Herrmann R, Nucleic Acids Res 1997 25 4 701 712 10.1093/nar/25.4.701 9016618
42. Regulatory protein phosphorylation in Mycoplasma pneumoniae. A PP2C-type phosphatase serves to dephosphorylate HPr(Ser-P). Halbedel S, Busse J, Schmidl SR, Stulke J, J Biol Chem 2006 281 36 26253 26259 10.1074/jbc.M605010200 16857667
43. Essential genes of a minimal bacterium. Glass JI, Assad-Garcia N, Alperovich N, Yooseph S, Lewis MR, Maruf M, Hutchison CA 3rd, Smith HO, Venter JC, Proc Natl Acad Sci U S A 2006 103 2 425 430 10.1073/pnas.0510013103 16407165
44. Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. Novakova L, Saskova L, Pallova P, Janecek J, Novotna J, Ulrych A, Echenique J, Trombe MC, Branny P, FEBS J 2005 272 5 1243 1254 10.1111/j.1742-4658.2005.04560.x 15720398
45. Protein phosphatases. Barford D, Curr Opin Struct Biol 1995 5 6 728 734 10.1016/0959-440X(95)80004-2 8749359
46. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. Das AK, Helps NR, Cohen PT, Barford D, EMBO J 1996 15 24 6798 6809 9003755
47. Mapping phosphoproteins in Mycoplasma genitalium and Mycoplasma pneumoniae. Su HC, Hutchison CA, Giddings MC 3rd, BMC Microbiol 2007 7 63 10.1186/1471-2180-7-63 17605819
48. A Comprehensive Proteome of Mycoplasma genitalium. Parraga-Nino N, Colome-Calls N, Canals F, Querol E, Ferrer-Navarro M, J Proteome Res 2012 11 6 3305 3316 10.1021/pr300084c
49. The phosphoproteome of the minimal bacterium Mycoplasma pneumoniae: analysis of the complete known Ser/Thr kinome suggests the existence of novel kinases. Schmidl SR, Gronau K, Pietack N, Hecker M, Becher D, Stulke J, Mol Cell Proteomics 2010 9 6 1228 1242 10.1074/mcp.M900267-MCP200 20097688
50. Intracellular Mycoplasma genitalium infection of human vaginal and cervical epithelial cells elicits distinct patterns of inflammatory cytokine secretion and provides a possible survival niche against macrophage-mediated killing. McGowin CL, Popov VL, Pyles RB, BMC Microbiol 2009 9 139 10.1186/1471-2180-9-139 19602269
51. Disruption of gene mg218 of Mycoplasma genitalium through homologous recombination leads to an adherence-deficient phenotype. Dhandayuthapani S, Rasmussen WG, Baseman JB, Proc Natl Acad Sci USA 1999 96 5227 5232 10.1073/pnas.96.9.5227 10220448
52. Influence of cell shape and surface charge on attachment of Mycoplasma pneumoniae to glass surfaces. Feldner J, Bredt W, Kahane I, J Bacteriol 1983 153 1 1 5 6401275
53. Genetic and biochemical characterization of glycerol uptake in Mycoplasma mycoides subsp. mycoides SC: its impact on H(2)O(2) production and virulence. Vilei EM, Frey J, Clin Diagn Lab Immunol 2001 8 1 85 92 11139200
54. Methionine sulfoxide reductase A (MsrA) deficient Mycoplasma genitalium shows decreased interactions with host cells. Das K, De la Garza G, Maffi S, Saikolappan S, Dhandayuthapani S, PLoS One 2012 7 4 36247 10.1371/journal.pone. 0036247 22558404
55. Interactions of OxyR with the promoter region of the oxyR and ahpC genes from Mycobacterium leprae and Mycobacterium tuberculosis. Dhandayuthapani S, Mudd M, Deretic V, J Bacteriol 1997 179 7 2401 2409 9079928
56. Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium. Dhandayuthapani S, Blaylock MW, Bebear CM, Rasmussen WG, Baseman JB, J Bacteriol 2001 183 19 5645 5650 10.1128/JB.183.19.5645-5650. 2001 11544227
57. Mycoplasma genitalium as a contributor to the multiple etiologies of cervicitis in women attending sexually transmitted disease clinics. Gaydos C, Maldeis NE, Hardick A, Hardick J, Quinn TC, Sex Transm Dis 2009 36 10 598 606 10.1097/OLQ.0b013e3181b01948 19704398
58. Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine. Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolff SP, Anal Biochem 1994 220 2 403 409 10.1006/abio.1994.1357 7978285
59. OsmC proteins of Mycobacterium tuberculosis and Mycobacterium smegmatis protect against organic hydroperoxide stress. Saikolappan S, Das K, Sasindran SJ, Jagannath C, Dhandayuthapani S, Tuberculosis (Edinb) 2011 91 Suppl 1 119 127