Serine/threonine protein kinase PrkA of the human pathogen Listeria monocytogenes: Biochemical characterization and identification of interacting partners through proteomic approaches

Journal of Proteomics

Volumn 74, Issue 9, 2011, Pages 1720-1734

  Lima, Analía ^a   Durán, Rosario ^a   Schujman, Gustavo Enrique ^b   Marchissio, María Julia ^b   Portela, María Magdalena ^a   Obal, Gonzalo ^c   Pritsch, Otto ^c,d   de Mendoza, Diego ^b   Cerveñansky, Carlos ^a  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^c INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^d UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Interactome; Listeria monocytogenes; Phosphopeptide identification; Phosphoresidues identification; Ser Thr protein kinase

Indexed keywords

BINDING PROTEIN; CARRIER PROTEIN; DNA; HISTIDINE; LIPOPROTEIN; MYELIN BASIC PROTEIN; PROTEIN PRKA; PROTEIN SERINE THREONINE KINASE; RNA; THREONINE; UNCLASSIFIED DRUG;

ADAPTATION; AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; BACTERIAL GENOME; CARBOHYDRATE METABOLISM; CARBOXY TERMINAL SEQUENCE; CELL METABOLISM; CELL WALL; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; LISTERIA MONOCYTOGENES; MOLECULAR INTERACTION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEOMICS; RNA SYNTHESIS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; HUMANS; LISTERIA MONOCYTOGENES; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); EUKARYOTA; LISTERIA MONOCYTOGENES; PROKARYOTA;

EID: 79961047261     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.03.005     Document Type: Article

References (70)

1. Vazquez-Boland J.A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., Gonzalez-Zorn B., Wehland J., Kreft J. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001, 14:584-640.
2. Gandhi M., Chikindas M.L. Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 2007, 113:1-15.
3. Hamon M., Bierne H., Cossart P. Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 2006, 4:423-434.
4. Buchrieser C., Rusniok C., Kunst F., Cossart P., Glaser P. Listeria Consortium. Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: clues for evolution and pathogenicity. FEMS Immunol Med Microbiol 2003, 35:207-213.
5. Hunter T. Signaling-2000 and beyond. Cell 2000, 100:113-127.
6. Cohen P. The origins of protein phosphorylation. Nat Cell Biol 2002, 4:E127-E130.
7. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Annu Rev Biochem 2000, 69:183-215.
8. Hanks S.K., Hunter T. Protein kinases 6. The eukarytic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 1995, 9:576-596.
9. Bakal C.J., Davies J.E. No longer an exclusive club: eukaryotic signaling domains in bacteria. Trends Cell Biol 2000, 10:32-38.
10. Av-Gay Y., Everett M. The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol 2000, 8:238-244.
11. Cozzone A.J. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J Mol Microbiol Biotechnol 2005, 9:198-213.
12. Kristich C.J., Wells C.L., Dunny G.M. A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc Natl Acad Sci 2007, 104:3508-3513.
13. Molle V., Kremer L. Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Mol Microbiol 2010, 75:1064-1077.
14. Ohlsen K., Donat S. The impact of serine/threonine phosphorylation in Staphylococcus aureus. Int J Med Microbiol 2010, 300:137-141.
15. Wehenkel A., Bellinzoni M., Grana M., Duran R., Villarino A., Fernandez P., Andre-Leroux G., England P., Takiff H., Cerveñansky C., Cole S.T., Alzari P.M. Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim Biophys Acta 2008, 1784:193-202.
16. Archambaud C., Gouin E., Pizarro-Cerda J., Cossart P., Dussurget O. Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Mol Microbiol 2005, 56:383-396.
17. Sambrook J.E., Fritsch F., Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
18. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
19. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
20. Mann M., Ong S.E., Gronborg M., Steen H., Jensen O.N., Pandey A. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 2002, 20:261-268.
21. Hellman U. Sample preparation by SDS-PAGE and in-gel digestion. Proteomics in functional genomics. Protein structure analysis 2000, 43-54. Birkhäuser Verlag, Basel, Switzerland. P. Jollès, H. Jörnvall (Eds.).
22. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996, 68:850-858.
23. Boitel B., Ortiz-Lombardía M., Durán R., Pompeo F., Cole S.T., Cerveñansky C., Alzari P.M. PknB kinase activity is regulated by phosphorylation in two Thr residues and de-phosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol Microbiol 2003, 49:1493-1508.
24. Débarbouillé M., Dramsi S., Dussurget O., Nahori M.A., Vaganay E., Jouvion G., Cozzone A., Msadek T., Duclos B. Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. J Bacteriol 2009, 191:4070-4081.
25. Madec E., Laszkiewicz A., Iwanicki A., Obuchowski M., Séror S. Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol Microbiol 2002, 46:571-586.
26. Mukhopadhyay S., Kapatral V., Xu W., Chakrabarty A.M. Characterization of a Hank's type serine/threonine kinase and serine/threonine phosphoprotein phosphatase in Pseudomonas aeruginosa. J Bacteriol 1999, 181:6615-6622.
27. Rajagopal L., Clancy A., Rubens C.E. 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 2003, 278:14429-14441.
28. Beltramini A.M., Mukhopadhyay C.D., Pancholi V. Modulation of cell wall structure and antimicrobial susceptibility by a Staphylococcus aureus eukaryote-like serine/threonine kinase and phosphatase. Infect Immun 2009, 77:1406-1416.
29. Gaidenko T.A., Kim T.J., Price C.W. The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J Bacteriol 2002, 184:6109-6114.
30. von Heijne G. Membrane protein structure prediction, hydrophobicity analysis and the positive-inside rule. J Mol Biol 1992, 225:487-494.
31. Shah I.M., Laaberki M.H., Popham D.L., Dworkin J. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 2008, 135:486-496.
32. Yeats C., Finn R.D., Bateman A. The PASTA domain: a beta-lactam-binding domain. Trends Biochem Sci 2002, 27:438-440.
33. Echenique J., Kadioglu A., Romao S., Andrew P.W., Trombe M.C. Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect Immun 2004, 72:2434-2437.
34. Fiuza M., Canova M.J., Zanella-Cléon I., Becchi M., Cozzone A.J., Mateos L.M., Kremer L., Gil J.A., Molle V. From the characterization of the four serine/threonine protein kinases (PknA/B/G/L) of Corynebacterium glutamicum toward the role of PknA and PknB in cell division. J Biol Chem 2008, 283:18099-18112.
35. Madec E., Stensballe A., Kjellström S., Cladière L., Obuchowski M., Jensen O.N., Séror S.J. 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 2003, 330:459-472.
36. Durán R., Villarino A., Bellinzoni M., Wehenkel A., Fernandez P., Boitel B., Cole S.T., Alzari P.M., Cerveñansky C. Conserved autophosphorylation pattern in activation loops and juxtamembrane regions of Mycobacterium tuberculosis Ser/Thr protein kinases. Biochem Biophys Res Commun 2005, 333:858-867.
37. D'Ambrosio C., Salzano A.M., Arena S., Renzone G., Scaloni A. Analytical methodologies for the detection and structural characterization of phosphorylated proteins. J Chromatogr B Analyt Technol Biomed Life Sci 2007, 849:163-180.
38. Canova M.J., Veyron-Churlet R., Zanella-Cleon I., Cohen-Gonsaud M., Cozzone A.J., Becchi M., Kremer L., Molle V. The Mycobacterium tuberculosis serine/threonine kinase PknL phosphorylates Rv2175c: mass spectrometric profiling of the activation loop phosphorylation sites and their role in the recruitment of Rv2175c. Proteomics 2008, 8:5215-5233.
39. Johnson D.L., Mahony J.B. Chlamydophila pneumoniae PknD exhibits dual acid specificity and phosphorylates Cpn0712, a putative type III secretion YscD homolog. J Bacteriol 2007, 189:7549-7555.
40. Kumar P., Kumar D., Parikh A., Rananaware D., Gupta M., Singh Y., Nandicoori V.K. The Mycobacterium tuberculosis protein kinase K modulates activation of transcription from the promoter of mycobacterial monooxygenase operon through phosphorylation of the transcriptional regulator VirS. J Biol Chem 2009, 284:11090-11099.
41. Meyer H.E., Hoffmann-Posorske E., Korte H., Heilmeyer L.M. Sequence analysis of phosphoserine-containing peptides. Modif picomolar sensitivity FEBS Lett 1986, 204:61-66.
42. Huse M., Kuriyan J. The conformational plasticity of protein kinases. Cell 2002, 109:275-282.
43. Villarino A., Duran R., Wehenkel A., Fernandez P., England P., Brodin P., Cole S.T., Zimny-Arndt U., Jungblut P.R., Cerveñansky C., Alzari P.M. Proteomic identification of M. tuberculosis protein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions. J Mol Biol 2005, 29:953-963.
44. Bendt A.K., Burkovski A., Schaffer S., Bott M., Farwick M., Hermann T. Towards a phosphoproteome map of Corynebacterium glutamicum. Proteomics 2003, 3:1637-1646.
45. Eymann C., Becher D., Bernhardt J., Gronau K., Klutzny A., Hecker M. Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. Proteomics 2007, 7:3509-3526.
46. Lévine A., Vannier F., Absalon C., Kuhn L., Jackson P., Scrivener E., Labas V., Vinh J., Courtney P., Garin J., Séror S.J. Analysis of the dynamic Bacillus subtilis Ser/Thr/Tyr phosphoproteome implicated in a wide variety of cellular processes. Proteomics 2006, 6:2157-2173.
47. Macek B., Mijakovic I., Olsen J.V., Gnad F., Kumar C., Jensen P.R., Mann M. The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 2007, 6:697-707.
48. Macek B., Gnad F., Soufi B., Kumar C., Olsen J.V., Mijakovic I., Mann M. Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 2008, 7:299-307.
49. Prisic S., Dankwa S., Schwartz D., Chou M.F., Locasale J.W., Kang C.M., Bemis G., Church G.M., Steen H., Husson R.N. Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc Natl Acad Sci 2010, 20(107):7521-7526.
50. Ravichandran A., Sugiyama N., Tomita M., Swarup S., Ishihama Y. Ser/Thr/Tyr phosphoproteome analysis of pathogenic and non-pathogenic Pseudomonas species. Proteomics 2009, 9:2764-2775.
51. Soufi B., Gnad F., Jensen P.R., Petranovic D., Mann M., Mijakovic I., Macek B. The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics 2008, 8:3486-3493.
52. Sun X., Ge F., Xiao C.L., Yin X.F., Ge R., Zhang L.H., He Q.Y. Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J Proteome Res 2010, 9:275-282.
53. Voisin S., Watson D.C., Tessier L., Ding W., Foote S., Bhatia S., Kelly J.F., Young N.M. The cytoplasmic phosphoproteome of the Gram-negative bacterium Campylobacter jejuni: evidence for modification by unidentified protein kinases. Proteomics 2007, 7:4338-4348.
54. Petrak J., Ivanek R., Toman O., Cmejla R., Cmejlova J., Vyoral D., Zivny J., Vulpe C.D. Déjà vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 2008, 8:1744-1749.
55. Wang P., Bouwman F.G., Mariman E.C. Generally detected proteins in comparative proteomics-a matter of cellular stress response?. Proteomics 2009, 9:2955-2966.
56. Donat S., Streker K., Schirmeister T., Rakette S., Stehle T., Liebeke M., Lalk M., Ohlsen K. Transcriptome and functional analysis of the eukaryotic-type serine/threonine kinase PknB in Staphylococcus aureus. J Bacteriol 2009, 191:4056-4069.
57. Bott M. Offering surprises: TCA cycle regulation in Corynebacterium glutamicum. Trends Microbiol 2007, 15:417-425.
58. O'Hare H.M., Durán R., Cerveñansky C., Bellinzoni M., Wehenkel A.M., Pritsch O., Obal G., Baumgartner J., Vialaret J., Johnsson K., Alzari P.M. Regulation of glutamate metabolism by protein kinases in mycobacteria. Mol Microbiol 2008, 70:1408-1423.
59. Durocher D., Jackson S.P. The FHA domain. FEBS Lett 2002, 513:58-66.
60. Absalon C., Obuchowski M., Madec E., Delattre D., Holland I.B., Séror S.J. CpgA, EF-Tu and the stressosome protein YezB are substrates of the Ser/Thr kinase/phosphatase couple, PrkC/PrpC, in Bacillus subtilis. Microbiology 2009, 155:932-943.
61. Dasgupta A., Datta P., Kundu M., Basu J. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 2006, 152:493-504.
62. Molle V., Kremer L., Girard-Blanc C., Besra G.S., Cozzone A.J., Prost J.F. An FHA phosphoprotein recognition domain mediates protein EmbR phosphorylation by PknH, a Ser/Thr protein kinase from Mycobacterium tuberculosis. Biochemistry 2003, 42:15300-15309.
63. Molle V., Soulat D., Jault J.M., Grangeasse C., Cozzone A.J., Prost J.F. Two FHA domains on an ABC transporter, Rv1747, mediate its phosphorylation by PknF, a Ser/Thr protein kinase from Mycobacterium tuberculosis. FEMS Microbiol Lett 2004, 15:215-223.
64. Gaidenko T.A., Kim T.J., Price C.W. The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J Bacteriol 2002, 184:6109-6114.
65. Nováková L., Sasková L., Pallová P., Janecek J., Novotná J., Ulrych A., Echenique J., Trombe M.C., Branny P. Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. FEBS J 2005, 272:1243-1254.
66. Nováková L., Bezousková S., Pompach P., Spidlová P., Sasková L., Weiser J., Branny P. Identification of multiple substrates of the StkP Ser/Thr protein kinase in Streptococcus pneumoniae. J Bacteriol 2010, 192:3629-3638.
67. Kang C.M., Abbott D.W., Park S.T., Dascher C.C., Cantley L.C., Husson R.N. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 2005, 19:1692-1704.
68. Parikh A., Verma S.K., Khan S., Prakash B., Nandicoori V.K. PknB-mediated phosphorylation of a novel substrate, N-acetylglucosamine-1-phosphate uridyltransferase, modulates its acetyltransferase activity. J Mol Biol 2009, 386:451-464.
69. Thakur M., Chakraborti P.K. GTPase activity of mycobacterial FtsZ is impaired due to its transphosphorylation by the eukaryotic-type Ser/Thr kinase, PknA. J Biol Chem 2006, 281:40107-40113.
70. Archambaud C., Nahori M.A., Pizarro-Cerda J., Cossart P., Dussurget O. Control of Listeria superoxide dismutase by phosphorylation. J Biol Chem 2006, 281:31812-31822.