A bacterial toxin inhibits DNA replication elongation through a direct interaction with the β sliding clamp

Molecular Cell

Volumn 52, Issue 5, 2013, Pages 617-628

  Aakre, Christopher D ^a   Phung, Tuyen N ^a   Huang, David ^a   Laub, Michael T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN; BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE GAMMA; GLUTATHIONE; PROTEASE CLPXP; PROTEINASE; SOCA; SOCB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BACTERIAL MUTATION; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; COLONY FORMATION; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ESCHERICHIA COLI; NONHUMAN; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STABILITY; TRANSPOSON;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES;

ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CAULOBACTER CRESCENTUS; CHROMOSOMES, BACTERIAL; DNA REPLICATION; DNA-BINDING PROTEINS; MUTATION; PROTEIN BINDING; PROTEOLYSIS;

EID: 84890203965     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.10.014     Document Type: Article

References (48)

1. Bhat N.H., Vass R.H., Stoddard P.R., Shin D.K., Chien P. Identification of ClpP substrates in Caulobacter crescentus reveals a role forregulated proteolysis in bacterial development. Mol. Microbiol. 2013, 88:1083-1092.
2. Bunting K.A., Roe S.M., Pearl L.H. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp. EMBO J. 2003, 22:5883-5892.
3. Bush K., Courvalin P., Dantas G., Davies J., Eisenstein B., Huovinen P., Jacoby G.A., Kishony R., Kreiswirth B.N., Kutter E., et al. Tackling antibiotic resistance. Nat. Rev. Microbiol. 2011, 9:894-896.
4. Castro-Roa D., Garcia-Pino A., De Geiter S., van Nuland N.A.J., Loris R., Zenkin N. The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu. Nat. Chem. Biol. 2013, in press. Published online October 20, 2013. 10.1038/nchembio.1364.
5. Chien P., Perchuk B.S., Laub M.T., Sauer R.T., Baker T.A. Direct and adaptor-mediated substrate recognition by an essential AAA+ protease. Proc. Natl. Acad. Sci. USA 2007, 104:6590-6595.
6. Christen B., Abeliuk E., Collier J.M., Kalogeraki V.S., Passarelli B., Coller J.A., Fero M.J., McAdams H.H., Shapiro L. The essential genome of a bacterium. Mol. Syst. Biol. 2011, 7:528.
7. Coates A.R., Halls G., Hu Y. Novel classes of antibiotics or more of the same?. Br. J. Pharmacol. 2011, 163:184-194.
8. Collier J., Shapiro L. Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J.Bacteriol. 2009, 191:5706-5716.
9. Dallmann H.G., Fackelmayer O.J., Tomer G., Chen J., Wiktor-Becker A., Ferrara T., Pope C., Oliveira M.T., Burgers P.M., Kaguni L.S., McHenry C.S. Parallel multiplicative target screening against divergent bacterial replicases: identification of specific inhibitors with broad spectrum potential. Biochemistry 2010, 49:2551-2562.
10. Dalrymple B.P., Kongsuwan K., Wijffels G., Dixon N.E., Jennings P.A. A universal protein-protein interaction motif in the eubacterial DNAreplication and repair systems. Proc. Natl. Acad. Sci. USA 2001, 98:11627-11632.
11. Dougan D.A., Weber-Ban E., Bukau B. Targeted delivery of anssrA-tagged substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol. Cell 2003, 12:373-380.
12. Farrell C.M., Baker T.A., Sauer R.T. Altered specificity of a AAA+ protease. Mol. Cell 2007, 25:161-166.
13. Flynn J.M., Neher S.B., Kim Y.I., Sauer R.T., Baker T.A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 2003, 11:671-683.
14. Georgescu R.E., Yurieva O., Kim S.S., Kuriyan J., Kong X.P., O'Donnell M. Structure of a small-molecule inhibitor of a DNA polymerase sliding clamp. Proc. Natl. Acad. Sci. USA 2008, 105:11116-11121.
15. Gerdes K., Maisonneuve E. Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol. 2012, 66:103-123.
16. Gora K.G., Tsokos C.G., Chen Y.E., Srinivasan B.S., Perchuk B.S., Laub M.T. A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus. Mol. Cell 2010, 39:455-467.
17. Indiani C., McInerney P., Georgescu R., Goodman M.F., O'Donnell M. A sliding-clamp toolbelt binds high- and low-fidelity DNA polymerases simultaneously. Mol. Cell 2005, 19:805-815.
18. Jenal U., Fuchs T. An essential protease involved in bacterial cell-cycle control. EMBO J. 1998, 17:5658-5669.
19. Johnson A., O'Donnell M. Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 2005, 74:283-315.
20. Jonas K., Chen Y.E., Laub M.T. Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication. Curr. Biol. 2011, 21:1092-1101.
21. Karimova G., Pidoux J., Ullmann A., Ladant D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. USA 1998, 95:5752-5756.
22. Kato J., Katayama T. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 2001, 20:4253-4262.
23. Kurz M., Dalrymple B., Wijffels G., Kongsuwan K. Interaction of the sliding clamp beta-subunit and Hda, a DnaA-related protein. J.Bacteriol. 2004, 186:3508-3515.
24. Lenhart J.S., Sharma A., Hingorani M.M., Simmons L.A. DnaN clamp zones provide a platform for spatiotemporal coupling of mismatch detection to DNA replication. Mol. Microbiol. 2013, 87:553-568.
25. Lenne-Samuel N., Wagner J., Etienne H., Fuchs R.P. The processivity factor beta controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis invivo. EMBO Rep. 2002, 3:45-49.
26. Levchenko I., Seidel M., Sauer R.T., Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 2000, 289:2354-2356.
27. Little J.W., Mount D.W. The SOS regulatory system of Escherichia coli. Cell 1982, 29:11-22.
28. López de Saro F.J., Marinus M.G., Modrich P., O'Donnell M. The beta sliding clamp binds to multiple sites within MutL and MutS. J.Biol. Chem. 2006, 281:14340-14349.
29. Maki S., Kornberg A. DNA polymerase III holoenzyme of Escherichia coli. II. A novel complex including the gamma subunit essential for processive synthesis. J.Biol. Chem. 1988, 263:6555-6560.
30. Martin A., Baker T.A., Sauer R.T. Diverse pore loops of the AAA+ ClpX machine mediate unassisted and adaptor-dependent recognition of ssrA-tagged substrates. Mol. Cell 2008, 29:441-450.
31. Modell J.W., Hopkins A.C., Laub M.T. A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev. 2011, 25:1328-1343.
32. Mutschler H., Gebhardt M., Shoeman R.L., Meinhart A. A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol. 2011, 9:e1001033.
33. Nakano M.M., Hajarizadeh F., Zhu Y., Zuber P. Loss-of-function mutations in yjbD result in ClpX- and ClpP-independent competence development of Bacillus subtilis. Mol. Microbiol. 2001, 42:383-394.
34. Pandey D.P., Gerdes K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 2005, 33:966-976.
35. Piotrowski A., Burghout P., Morrison D.A. spr1630 is responsible for the lethality of clpX mutations in Streptococcus pneumoniae. J.Bacteriol. 2009, 191:4888-4895.
36. Raju R.M., Unnikrishnan M., Rubin D.H., Krishnamoorthy V., Kandror O., Akopian T.N., Goldberg A.L., Rubin E.J. Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability invitro and during infection. PLoS Pathog. 2012, 8:e1002511.
37. Robinson A., Brzoska A.J., Turner K.M., Withers R., Harry E.J., Lewis P.J., Dixon N.E. Essential biological processes of an emerging pathogen: DNA replication, transcription, and cell division in Acinetobacter spp. Microbiol. Mol. Biol. Rev. 2010, 74:273-297.
38. Robinson A., Causer R.J., Dixon N.E. Architecture and conservation of the bacterial DNA replication machinery, an underexploited drug target. Curr. Drug Targets 2012, 13:352-372.
39. Sauer R.T., Baker T.A. AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 2011, 80:587-612.
40. Schweder T., Lee K.H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J.Bacteriol. 1996, 178:470-476.
41. Su'etsugu M., Errington J. The replicase sliding clamp dynamically accumulates behind progressing replication forks in Bacillus subtilis cells. Mol. Cell 2011, 41:720-732.
42. Walsh C. Antibiotics: Actions, Origins, Resistance 2003, ASM Press, Washington, D.C.
43. Wang J.D., Sanders G.M., Grossman A.D. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 2007, 128:865-875.
44. Wang X., Kim Y., Hong S.H., Ma Q., Brown B.L., Pu M., Tarone A.M., Benedik M.J., Peti W., Page R., Wood T.K. Antitoxin MqsA helpsmediate the bacterial general stress response. Nat. Chem. Biol. 2011, 7:359-366.
45. Yamaguchi Y., Inouye M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 2011, 9:779-790.
46. Yamaguchi Y., Park J.H., Inouye M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 2011, 45:61-79.
47. Yuan J., Sterckx Y., Mitchenall L.A., Maxwell A., Loris R., Waldor M.K. Vibrio cholerae ParE2 poisons DNA gyrase via a mechanism distinct from other gyrase inhibitors. J.Biol. Chem. 2010, 285:40397-40408.
48. Zhang Y., Zhang J., Hoeflich K.P., Ikura M., Qing G., Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 2003, 12:913-923.