Plumbagin inhibits cytokinesis in Bacillus subtilis by inhibiting FtsZ assembly - A mechanistic study of its antibacterial activity

FEBS Journal

Volumn 280, Issue 18, 2013, Pages 4585-4599

  Bhattacharya, Anusri ^a   Jindal, Bhavya ^a   Singh, Parminder ^a   Datta, Anindya ^a   Panda, Dulal ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

antibacterial agent; bacterial cell division; FtsZ assembly; plumbagin; Z ring

Indexed keywords

FTSZ PROTEIN; GUANOSINE TRIPHOSPHATASE; PLUMBAGIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; BINDING AFFINITY; BINDING SITE; CELL ELONGATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINESIS; DRUG BINDING SITE; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL;

ANTIBACTERIAL AGENT; BACTERIAL CELL DIVISION; FTSZ ASSEMBLY; PLUMBAGIN; Z-RING;

ANTI-BACTERIAL AGENTS; ASPARTIC ACID; BACILLUS SUBTILIS; BACTERIAL LOAD; BACTERIAL PROTEINS; BINDING SITES; CYTOKINESIS; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DOCKING SIMULATION; MUTATION; NAPHTHOQUINONES; PROTEIN BINDING; RECOMBINANT PROTEINS; SPECIES SPECIFICITY; VALINE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84883458216     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12429     Document Type: Article

References (51)

1. Singh P, &, Panda D, (2010) FtsZ inhibition: a promising approach for antistaphylococcal therapy. Drug News Perspect 23, 295-304.
2. Adams DW, &, Errington J, (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7, 642-653.
3. Kapoor S, &, Panda D, (2009) Targeting FtsZ for antibacterial therapy: a promising avenue. Expert Opin Ther Targets 13, 1037-1051.
4. Graumann PL, (2009) Dynamics of bacterial cytoskeletal elements. Cell Motil Cytoskeleton 66, 909-914.
5. Harry E, Monahan L, &, Thompson L, (2006) Bacterial cell division: the mechanism and its precison. Int Rev Cytol 253, 27-94.
6. Weiss DS, (2004) Bacterial cell division and the septal ring. Mol Microbiol 54, 588-597.
7. Margolin W, (2009) Sculpting the bacterial cell. Curr Biol 19, 812-822.
8. Nogales E, Downing KH, Amos LA, &, Lowe J, (1998) Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 5, 451-458.
9. Plaza A, Keffer JL, Bifulco G, Lloyd JR, &, Bewley CA, (2010) Chrysophaentins A-H, antibacterial bisdiarylbutene macrocycles that inhibit the bacterial cell division protein FtsZ. J Am Chem Soc 132, 9069-9077.
10. Stokes NR, Sievers J, Barker S, Bennett JM, Brown DR, Collins I, Errington VM, Foulger D, Hall M, Halsey R, et al,. (2005) Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J Biol Chem 280, 39709-39715.
11. Corton JC, Ward JE Jr, &, Lutkenhaus J, (1987) Analysis of cell division gene ftsZ (sulB) from gram-negative and gram-positive bacteria. J Bacteriol 169, 1-7.
12. Huang Q, Kirikae F, Kirikae T, Pepe A, Amin A, Respicio L, Slayden RA, Tonge PJ, &, Ojima I, (2006) Targeting FtsZ for antituberculosis drug discovery: noncytotoxic taxanes as novel antituberculosis agents. J Med Chem 49, 463-466.
13. Huang Q, Tonge PJ, Slayden RA, Kirikae T, &, Ojima I, (2007) FtsZ: a novel target for tuberculosis drug discovery. Curr Top Med Chem 7, 527-543.
14. Respicio L, Nair PA, Huang Q, Anil B, Tracz S, Truglio JJ, Kisker C, Releigh DP, Ojima I, Knudson DL, et al,. (2008) Characterizing septum inhibition in Mycobacterium tuberculosis for novel drug discovery. Tuberculosis 88, 420-429.
15. Kumar K, Awasthi D, Lee SY, Zanardi I, Ruzsicska B, Knuson S, Tonge PJ, Slayen RA, &, Ojima I, (2011) Novel trisubstituted benzimidazoles, targeting Mtb FtsZ, as a new class of antitubercular agents. J Med Chem 54, 374-381.
16. Ahmad A, Banerjee S, Wang Z, Kong D, &, Sarkar FH, (2008) Plumbagin-induced apoptosis of human breast cancer cells is mediated by inactivation of NF-κB and Bcl-2. J Cell Biochem 105, 1461-1471.
17. Powolny AA, &, Singh SV, (2008) Plumbagin-induced apoptosis in human prostate cancer cells is associated with modulation of cellular redox status and generation of reactive oxygen species. Pharm Res 25, 2171-2180.
18. Dzoyem JP, Kechia FA, Kuete V, Pieme AC, Akak CM, Tangmouo JG, &, Lohoue PJ, (2011) Phytotoxic, antifungal activities and acute toxicity studies of the crude extract and compounds from Diospyros canaliculata. Nat Prod Res 25, 741-749.
19. Kuete V, Alibert-Franco S, Eyong KO, Ngameni B, Folefoc GN, Nguemeving JR, Tangmouo JG, Fotso GW, Komguem J, Ouahouo BM, et al,. (2011) Antibacterial activity of some natural products against bacteria expressing a multidrug-resistant phenotype. Int J Antimicrob Agents 37, 156-161.
20. Borges-Argáez R, Canche-Chay CI, Peña-Rodríguez LM, Said-Fernández S, &, Molina-Salinas GM, (2007) Antimicrobial activity of Diospyros anisandra. Fitoterapia 78, 370-372.
21. Ferreira DT, Andrei CC, Saridakis HO, Faria Tde J, Vinhato E, Carvalho KE, Daniel JF, Machado SL, Saridakis DP, &, Braz-Filho R, (2004) Antimicrobial activity and chemical investigation of Brazilian Drosera. Mem Inst Oswaldo Cruz 99, 753-755.
22. de Paiva SR, Figueiredo MR, Aragão TV, &, Kaplan MA, (2003) Antimicrobial activity in vitro of plumbagin isolated from Plumbago species. Mem Inst Oswaldo Cruz 98, 959-961.
23. Mathew R, Kruthiventi AK, Prasad JV, Kumar SP, Srinu G, &, Chatterji D, (2010) Inhibition of mycobacterial growth by plumbagin derivatives. Chem Biol Drug Des 76, 34-42.
24. Beuria TK, Santra MK, &, Panda D, (2005) Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44, 16584-16593.
25. Jaiswal R, Beuria TK, Mohan R, Mahajan SK, &, Panda D, (2007) Totarol inhibits bacterial cytokinesis by perturbing the assembly dynamics of FtsZ. Biochemistry 46, 4211-4220.
26. Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM, Brown DR, Baker PJ, Barynin VV, Rice DW, Sedelnikova SE, et al,. (2008) An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321, 1673-1675.
27. Beuria TK, Singh P, Surolia A, &, Panda D, (2009) Promoting assembly and bundling of FtsZ as a strategy to inhibit bacterial cell division: a new approach for developing novel antibacterial drugs. Biochem J 423, 61-69.
28. Singh P, Jindal B, Surolia A, &, Panda D, (2012) A rhodanine derivative CCR-11 inhibits bacterial proliferation by inhibiting the assembly and GTPase activity of FtsZ. Biochemistry 51, 5434-5442.
29. Acharya BR, Bhattacharyya B, &, Chakrabarti G, (2008) The natural naphthoquinone plumbagin exhibits antiproliferative activity and disrupts the microtubule network through tubulin binding. Biochemistry 47, 7838-7845.
30. Wiegand I, Hilpert K, &, Hancock RE, (2008) Agar and broth dilution methods to determine the minimum inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3, 163-175.
31. Bhattacharyya B, Kapoor S, &, Panda D, (2010) Fluorescence spectroscopic methods to analyze drug-tubulin interactions. Methods Cell Biol 95, 301-329.
32. Lee JC, Harrison D, &, Timasheff SN, (1975) Interaction of vinblastine with calf brain microtubule protein. J Biol Chem 250, 9276-9282.
33. Chen JW, Sun CM, Sheng WL, Wang YC, &, Syu WJ, (2006) Expression analysis of up-regulated genes responding to plumbagin in Escherichia coli. J Bacteriol 188, 456-463.
34. Lin CN, Syu WJ, Sun WS, Chen JW, Chen TH, Don MJ, &, Wang SH, (2010) A role of ygfZ in the Escherichia coli response to plumbagin challenge. J Biomed Sci 17, 84.
35. Martín-Galiano AJ, Buey RM, Cabezas M, &, Andreu JM, (2010) Mapping flexibility and the assembly switch of cell division protein FtsZ by computational and mutational approaches. J Biol Chem 285, 22554-22565.
36. Andreu JM, Schaffner-Barbero C, Huecas S, Alonso D, Lopez-Rodriguez ML, Ruiz-Avila LB, Núńez-Ramírez R, Llorca O, &, Martín-Galiano AJ, (2010) The antibacterial cell division inhibitor PC190723 is an FtsZ polymer-stabilizing agent that induces filament assembly and condensation. J Biol Chem 285, 14239-14246.
37. Jaiswal R, Patel RY, Asthana J, Jindal B, Balaji PV, &, Panda D, (2010) E93R substitution of Escherichia coli FtsZ induces bundling of protofilaments, reduces GTPase activity, and impairs bacterial cytokinesis. J Biol Chem 285, 31796-31805.
38. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
39. 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.
40. Santra MK, &, Panda D, (2007) Acid-induced loss of functional properties of bacterial cell division protein FtsZ: evidence for an alternative conformation at acidic pH. Proteins 67, 177-188.
41. Jaiswal R, &, Panda D, (2008) Cysteine 155 plays an important role in the assembly of Mycobacterium tuberculosis FtsZ. Protein Sci 17, 846-854.
42. 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.
43. Geladopoulos TP, Sotiroudis TG, &, Evangelopoulos AE, (1991) A malachite green colorimetric assay for protein phosphatase activity. Anal Biochem 192, 112-116.
44. Lakowicz JR, (1999) Principles of Fluorescence Spectroscopy, 2nd edn, pp. 27-61. Kluwer Academic/Plenum Publishers, New York.
45. Ray S, Kumar A, &, Panda D, (2013) GTP regulates the interaction between MciZ and FtsZ: a possible role of MciZ in bacterial cell division. Biochemistry 52, 392-401.
46. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, &, Olson AJ, (1998) Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J Comput Chem 19, 1639-1662.
47. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, &, Bourne PE, (2000) The Protein Data Bank. Nucleic Acids Res 28, 235-242.
48. SchÇ̃ttelkopf AW, &, van Aalten DM, (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr D Biol Crystallogr 60, 1355-1363.
49. Nielsen M, Lundegaard C, Lund O, &, Petersen TN, (2010) CPHmodels 3.0-remote homology modeling using structure guided sequence profiles. Nucleic Acids Res 38, W576-W581.
50. Laskowski RA, MacArthur MW, Moss DS, &, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291.
51. DeLano WL, (2002) The PyMOL Molecular Genetics Graphics System. DeLano Scientific, San Carlos, CA.