Mycobacterium tuberculosis ClpX interacts with FtsZ and interferes with FtsZ assembly

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Dziedzic, Renata ^a   Kiran, Manjot ^a   Plocinski, Przemyslaw ^a   Ziolkiewicz, Malgorzata ^b   Brzostek, Anna ^b   Moomey, Meredith ^a   Vadrevu, Indumati S ^a   Dziadek, Jaroslaw ^b   Madiraju, Murty ^a   Rajagopalan, Malini ^a  

^a UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^b INSTITUTE OF MEDICAL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPEPTIDASE CLPX; FTSZ PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; CELL DIVISION; COLONY FORMING UNIT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; TWO HYBRID SYSTEM; UPREGULATION; WILD TYPE; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CYTOSKELETAL PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 77955374003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011058     Document Type: Article

References (52)

1. Gandhi NR, Moll A, Sturm AW, Pawinski R, Govender T, et al. (2006) Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368: 1575-1580.
2. Smith I (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16: 463-496.
3. Margolin W (2000) Themes and variations in prokaryotic cell division. FEMS Microbiol Rev 24: 531-548.
4. Romberg L, Levin PA (2003) Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu Rev Microbiol 57: 125-154.
5. Chauhan A, Lofton H, Maloney E, Moore J, Fol M, et al. (2006) Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase. Mol Microbiol 62: 132-147.
6. Dziadek J, Rutherford SA, Madiraju MV, Atkinson MA, Rajagopalan M (2003) Conditional expression of Mycobacterium smegmatis ftsZ, an essential cell division gene. Microbiology 149: 1593-1603.
7. Errington J, Daniel RA, Scheffers D J(2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52-65, table of contents.
8. Del Sol R, Mullins JG, Grantcharova N, Flardh K, Dyson P (2006) Influence of CrgA on assembly of the cell division protein FtsZ during development of Streptomyces coelicolor. J Bacteriol 188: 1540-1550.
9. Frees D, Savijoki K, Varmanen P, Ingmer H (2007) Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol Microbiol 63: 1285-1295.
10. Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19: 565-587.
11. Jenal U, Fuchs T (1998) An essential protease involved in bacterial cell-cycle control. EMBOJ 17: 5658-5669.
12. Hanson PI, Whiteheart SW (2005) AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 6: 519-529.
13. Kannan N, Haste N, Taylor SS, Neuwald AF (2007) The hallmark of AGC kinase functional divergence is its C-terminal tail, a cis-acting regulatory module. Proc Natl Acad Sci U S A 104: 1272-1277.
14. Singh SK, Rozycki J, Ortega J, Ishikawa T, Lo J, et al. (2001) Functional domains of the ClpA and ClpX molecular chaperones identified by limited proteolysis and deletion analysis. J Biol Chem 276: 29420-29429.
15. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
16. Engels S, Schweitzer JE, Ludwig C, Bott M, Schaffer S (2004) clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor sigmaH. Mol Microbiol 52: 285-302.
17. Viala J, Mazodier P (2002) ClpP-dependent degradation of PopR allows tightly regulated expression of the clpP3 clpP4 operon in Streptomyces lividans. Mol Microbiol 44: 633-643.
18. Chien P, Perchuk BS, Laub MT, Sauer RT, Baker TA (2007) Direct and adaptor-mediated substrate recognition by an essential AAA+ protease. Proc Natl Acad Sci U S A 104: 6590-6595.
19. Camberg JL, Hoskins JR, Wickner S (2009) ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc Natl Acad Sci U S A.
20. Sugimoto S, Yamanaka K, Nishikori S, Miyagi A, Ando T, et al. (2010) AAA+ chaperone ClpX regulates dynamics of prokaryotic cytoskeletal protein FtsZ. J Biol Chem 285: 6648-6657.
21. Farrell CM, Grossman AD, Sauer RT (2005) Cytoplasmic degradation ofssrA-tagged proteins. Mol Microbiol 57: 1750-1761.
22. Lu C, Stricker J, Erickson HP (1998) FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima-quantitation, GTP hydrolysis, and assembly. Cell Motil Cytoskeleton 40: 71-86.
23. Flynn JM, Neher SB, Kim YI, Sauer RT, Baker TA (2003) Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell 11: 671-683.
24. Haeusser DP, Lee AH, Weart RB, Levin PA (2009) ClpX inhibits FtsZ assembly in a manner that does not require its ATP hydrolysis-dependent chaperone activity. J Bacteriol 191: 1986-1991.
25. Weart RB, Nakano S, Lane BE, Zuber P, Levin PA (2005) The ClpX chaperone modulates assembly ofthe tubulin-like protein FtsZ. Mol Microbiol 57: 238-249.
26. Chauhan A, Madiraju MV, Fol M, Lofton H, Maloney E, et al. (2006) Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J Bacteriol 188: 1856-1865.
27. Mukherjee A, Lutkenhaus J(1999) Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J Bacteriol 181: 823-832.
28. Rajagopalan M, Atkinson MA, Lofton H, Chauhan A, Madiraju MV (2005) Mutations in the GTP-binding and synergy loop domains of Mycobacterium tuberculosis ftsZ compromise its function in vitro and in vivo. Biochem Biophys Res Commun 331: 1171-1177.
29. Galletto R, Kowalczykowski SC (2007) RecA. Curr Biol 17: R395-397.
30. Dajkovic A, Lan G, Sun SX, Wirtz D, Lutkenhaus J (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18: 235-244.
31. Dajkovic A, Mukherjee A, Lutkenhaus J (2008) Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. JBacteriol 190: 2513-2526.
32. White EL, Ross LJ, Reynolds RC, Seitz LE, Moore GD, et al. (2000) Slow polymerization of Mycobacterium tuberculosis FtsZ. J Bacteriol 182: 4028-4034.
33. Hett EC, Chao MC, Deng LL, Rubin EJ (2008) A mycobacterial enzyme essential for cell division synergizes with resuscitation-promoting factor. PLoS Pathog 4: e1000001.
34. Rajagopalan M, Maloney E, Dziadek J, Poplawska M, Lofton H, et al. (2005) Genetic evidence that mycobacterial FtsZ and FtsW proteins interact, and colocalize to the division site in Mycobacterium smegmatis. FEMS Microbiol Lett 250: 9-17.
35. Karimova G, Dautin N, Ladant D (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187: 2233-2243.
36. Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, et al. (2006) Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62: 1655-1673.
37. Singh A, Mai D, Kumar A, Steyn AJ(2006) Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 103: 11346-11351.
38. Datta P, Dasgupta A, Bhakta S, Basu J (2002) Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. JBiol Chem 277: 24983-24987.
39. Ma X, Margolin W (1999) Genetic and functional analyses of the conserved C-terminal core domain ofEscherichia coli FtsZ. J Bacteriol 181: 7531-7544.
40. Mosyak L, Zhang Y, Glasfeld E, Haney S, Stahl M, et al. (2000) The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J19: 3179-3191.
41. Corbin BD, Wang Y, Beuria TK, Margolin W (2007) Interaction between cell division proteins FtsE and FtsZ. J Bacteriol 189: 3026-3035.
42. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
43. Sureka K, Hossain T, Mukherjee P, Chatterjee P, Datta P, et al. (2010) Novel role of phosphorylation-dependent interaction between FtsZ and FipA in mycobacterial cell division. PLoS One 5: e8590.
44. Goley ED, Iniesta AA, Shapiro L (2007) Cell cycle regulation in Caulobacter: location, location, location. J Cell Sci 120: 3501-3507.
45. Kelly AJ, Sackett MJ, Din N, Quardokus E, Brun YV (1998) Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev 12: 880-893.
46. Gerth U, Kirstein J, Mostertz J, Waldminghaus T, Miethke M, et al. (2004) Fine- tuning in regulation of Clp protein content in Bacillus subtilis. J Bacteriol 186: 179-191.
47. Chen Y, Anderson DE, Rajagopalan M, Erickson HP (2007) Assembly dynamics of Mycobacterium tuberculosis FtsZ. JBiol Chem 282: 27736-27743.
48. Anderson DE, Gueiros-Filho FJ, Erickson HP (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. JBacteriol 186: 5775-5781.
49. Stricker J, Maddox P, Salmon ED, Erickson HP (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci U S A 99: 3171-3175.
50. Dziadek J, Madiraju MV, Rutherford SA, Atkinson MA, Rajagopalan M (2002) Physiological consequences associated with overproduction of Mycobacterium tuberculosis FtsZ in mycobacterial hosts. Microbiology 148: 961-971.
51. Fol M, Chauhan A, Nair NK, Maloney E, Moomey M, et al. (2006) Modulation of Mycobacterium tuberculosis proliferation by MtrA, an essential two-component response regulator. Mol Microbiol 60: 643-657.
52. Nair N, Dziedzic R, Greendyke R, Muniruzzaman S, Rajagopalan M, et al. (2009) Synchronous replication initiation in novel Mycobacterium tuberculosis dnaA cold-sensitive mutants. Mol Microbiol 71: 291-304.