Balancing at survival's edge: The structure and adaptive benefits of prokaryotic toxin-antitoxin partners

Current Opinion in Structural Biology

Volumn 21, Issue 1, 2011, Pages 109-118

  Blower, Tim R ^a   Salmond, George PC ^a   Luisi, Ben F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN; DOC PROTEIN; HIPA PROTEIN; KID PROTEIN; RELE PROTEIN; RIBONUCLEASE; RIBOSOME RNA; UNCLASSIFIED DRUG; VAPC PROTEIN; ZETA PROTEIN;

BACTERIAL SURVIVAL; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA BINDING MOTIF; EVOLUTIONARY ADAPTATION; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROKARYOTE; REVIEW; RNA BINDING; RNA CLEAVAGE; STRUCTURAL HOMOLOGY; TOXIN ANALYSIS; TOXIN STRUCTURE; TRANSCRIPTION REGULATION;

ADAPTATION, PHYSIOLOGICAL; MULTIGENE FAMILY; PROKARYOTIC CELLS; PROTEIN BINDING; TOXINS, BIOLOGICAL;

PROKARYOTA;

EID: 79551671757     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2010.10.009     Document Type: Review

References (53)

1. Yarmolinsky M.B. Programmed cell death in bacterial populations. Science 1995, 267:836-837.
2. Gerdes K., Christensen S.K., Lobner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 2005, 3:371-382.
3. Rotem E., Loinger A., Ronin I., Levin-Reisman I., Gabay C., Shoresh N., Biham O., Balaban N.Q. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc Natl Acad Sci U S A 2010, 107:12541-12546.
4. Fineran P.C., Blower T.R., Foulds I.J., Humphreys D.P., Lilley K.S., Salmond G.P. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 2009, 106:894-899.
5. Mattison K., Wilbur J.S., So M., Brennan R.G. Structure of FitAB from Neisseria gonorrhoeae bound to DNA reveals a tetramer of toxin-antitoxin heterodimers containing PIN domains and ribbon-helix-helix motifs. J Biol Chem 2006, 281:37942-37951.
6. Magnuson R.D. Hypothetical functions of toxin-antitoxin systems. J Bacteriol 2007, 189:6089-6092.
7. Van Melderen L., Saavedra De Bast M. Bacterial toxin-antitoxin systems: more than selfish entities?. PLoS Genet 2009, 5:e1000437.
8. Fozo E.M., Hemm M.R., Storz G. Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 2008, 72:579-589. Table of Contents.
9. Blower T.R., Fineran P.C., Johnson M.J., Toth I.K., Humphreys D.P., Salmond G.P. Mutagenesis and functional characterisation of the RNA and protein components of the toxIN abortive infection and toxin-antitoxin locus of Erwinia. J Bacteriol 2009, 191:6029-6039.
10. 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.
11. Makarova K.S., Wolf Y.I., Koonin E.V. Comprehensive comparative-genomic analysis of Type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct 2009, 4:19.
12. Jorgensen M.G., Pandey D.P., Jaskolska M., Gerdes K. HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J Bacteriol 2009, 191:1191-1199.
13. Fozo E.M., Makarova K.S., Shabalina S.A., Yutin N., Koonin E.V., Storz G. Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 2010, 38:3743-3759.
14. Buts L., Lah J., Dao-Thi M.H., Wyns L., Loris R. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem Sci 2005, 30:672-679.
15. Hargreaves D., Santos-Sierra S., Giraldo R., Sabariegos-Jareno R., de la Cueva-Mendez G., Boelens R., Diaz-Orejas R., Rafferty J.B. Structural and functional analysis of the Kid toxin protein from E. coli plasmid R1. Structure 2002, 10:1425-1433.
16. Blower T.R., Pei X.Y., Short F.L., Fineran P.C., Humphreys D.P., Luisi B.F., Salmond G.P.C. A processed non-coding RNA regulates an altruistic bacterial antiviral system. Nat Struct Mol Biol 2011, 10.1038/nsmb.1981.
17. Zhang Y., Zhang J., Hara H., Kato I., Inouye M. Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J Biol Chem 2005, 280:3143-3150.
18. Diago-Navarro E., Hernandez-Arriaga A.M., Lopez-Villarejo J., Munoz-Gomez A.J., Kamphuis M.B., Boelens R., Lemonnier M., Diaz-Orejas R. parD toxin-antitoxin system of plasmid R1-basic contributions, biotechnological applications and relationships with closely-related toxin-antitoxin systems. FEBS J 2010, 277:3097-3117.
19. Dao-Thi M.H., Van Melderen L., De Genst E., Afif H., Buts L., Wyns L., Loris R. Molecular basis of gyrase poisoning by the addiction toxin CcdB. J Mol Biol 2005, 348:1091-1102.
20. Neubauer C., Gao Y.G., Andersen K.R., Dunham C.M., Kelley A.C., Hentschel J., Gerdes K., Ramakrishnan V., Brodersen D.E. The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 2009, 139:1084-1095.
21. Kamada K., Hanaoka F. Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol Cell 2005, 19:497-509.
22. Zhang Y., Inouye M. The inhibitory mechanism of protein synthesis by YoeB, an Escherichia coli toxin. J Biol Chem 2009, 284:6627-6638.
23. Christensen-Dalsgaard M., Jorgensen M.G., Gerdes K. Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses. Mol Microbiol 2010, 75:333-348.
24. Garcia-Pino A., Christensen-Dalsgaard M., Wyns L., Yarmolinsky M., Magnuson R.D., Gerdes K., Loris R. Doc of prophage P1 is inhibited by its antitoxin partner Phd through fold complementation. J Biol Chem 2008, 283:30821-30827.
25. Liu M., Zhang Y., Inouye M., Woychik N.A. Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit. Proc Natl Acad Sci U S A 2008, 105:5885-5890.
26. Miallau L., Faller M., Chiang J., Arbing M., Guo F., Cascio D., Eisenberg D. Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis. J Biol Chem 2009, 284:276-283.
27. Bunker R.D., McKenzie J.L., Baker E.N., Arcus V.L. Crystal structure of PAE0151 from Pyrobaculum aerophilum, a PIN-domain (VapC) protein from a toxin-antitoxin operon. Proteins 2008, 72:510-518.
28. Schumacher M.A., Piro K.M., Xu W., Hansen S., Lewis K., Brennan R.G. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 2009, 323:396-401.
29. Meinhart A., Alonso J.C., Strater N., Saenger W. Crystal structure of the plasmid maintenance system e{open}/ζ: functional mechanism of toxin ζ and inactivation by e{open}2ζ2 complex formation. Proc Natl Acad Sci U S A 2003, 100:1661-1666.
30. Khoo S.K., Loll B., Chan W.T., Shoeman R.L., Ngoo L., Yeo C.C., Meinhart A. Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 2007, 282:19606-19618.
31. Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010, 8:317-327.
32. Kamphuis M.B., Bonvin A.M., Monti M.C., Lemonnier M., Munoz-Gomez A., van den Heuvel R.H., Diaz-Orejas R., Boelens R. Model for RNA binding and the catalytic site of the RNase Kid of the bacterial parD toxin-antitoxin system. J Mol Biol 2006, 357:115-126.
33. Santos-Sierra S., Lemonnier M., Nunez B., Hargreaves D., Rafferty J., Giraldo R., Andreu J.M., Diaz-Orejas R. Non-cytotoxic variants of the Kid protein that retain their auto-regulatory activity. Plasmid 2003, 50:120-130.
34. Diago-Navarro E., Kamphuis M.B., Boelens R., Barendregt A., Heck A.J., van den Heuvel R.H., Diaz-Orejas R. A mutagenic analysis of the RNase mechanism of the bacterial Kid toxin by mass spectrometry. FEBS J 2009, 276:4973-4986.
35. Agarwal S., Mishra N.K., Bhatnagar S., Bhatnagar R. PemK toxin of Bacillus anthracis is a ribonuclease: an insight into its active site, structure, and function. J Biol Chem 2010, 285:7254-7270.
36. Gogos A., Mu H., Bahna F., Gomez C.A., Shapiro L. Crystal structure of YdcE protein from Bacillus subtilis. Proteins 2003, 53:320-322.
37. Li G.Y., Zhang Y., Chan M.C., Mal T.K., Hoeflich K.P., Inouye M., Ikura M. Characterization of dual substrate binding sites in the homodimeric structure of Escherichia coli mRNA interferase MazF. J Mol Biol 2006, 357:139-150.
38. Kamada K., Hanaoka F., Burley S.K. Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. Mol Cell 2003, 11:875-884.
39. Francuski D., Saenger W. Crystal structure of the antitoxin-toxin protein complex RelB-RelE from Methanococcus jannaschii. J Mol Biol 2009, 393:898-908.
40. Takagi H., Kakuta Y., Okada T., Yao M., Tanaka I., Kimura M. Crystal structure of archaeal toxin-antitoxin RelE-RelB complex with implications for toxin activity and antitoxin effects. Nat Struct Mol Biol 2005, 12:327-331.
41. Dalton K.M., Crosson S. A conserved mode of protein recognition and binding in a ParD-ParE toxin-antitoxin complex. Biochemistry 2010, 49:2205-2215.
42. Li G.Y., Zhang Y., Inouye M., Ikura M. Inhibitory mechanism of Escherichia coli RelE-RelB toxin-antitoxin module involves a helix displacement near an mRNA interferase active site. J Biol Chem 2009, 284:14628-14636.
43. Brown B.L., Grigoriu S., Kim Y., Arruda J.M., Davenport A., Wood T.K., Peti W., Page R. Three dimensional structure of the MqsR:MqsA complex: a novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties. PLoS Pathog 2009, 5:e1000706.
44. Madl T., Van Melderen L., Mine N., Respondek M., Oberer M., Keller W., Khatai L., Zangger K. Structural basis for nucleic acid and toxin recognition of the bacterial antitoxin CcdA. J Mol Biol 2006, 364:170-185.
45. Li G.Y., Zhang Y., Inouye M., Ikura M. Structural mechanism of transcriptional autorepression of the Escherichia coli RelB/RelE antitoxin/toxin module. J Mol Biol 2008, 380:107-119.
46. Kamphuis M.B., Monti M.C., van den Heuvel R.H., Santos-Sierra S., Folkers G.E., Lemonnier M., Diaz-Orejas R., Heck A.J., Boelens R. Interactions between the toxin Kid of the bacterial parD system and the antitoxins Kis and MazE. Proteins 2007, 67:219-231.
47. Garcia-Pino A., Balasubramanian S., Wyns L., Gazit E., De Greve H., Magnuson R.D., Charlier D., van Nuland N.A., Loris R. Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell 2010, 142:101-111.
48. Loris R., Marianovsky I., Lah J., Laeremans T., Engelberg-Kulka H., Glaser G., Muyldermans S., Wyns L. Crystal structure of the intrinsically flexible addiction antidote MazE. J Biol Chem 2003, 278:28252-28257.
49. De Jonge N., Hohlweg W., Garcia-Pino A., Respondek M., Buts L., Haesaerts S., Lah J., Zangger K., Loris R. Structural and thermodynamic characterization of Vibrio fischeri CcdB. J Biol Chem 2010, 285:5606-5613.
50. De Jonge N., Garcia-Pino A., Buts L., Haesaerts S., Charlier D., Zangger K., Wyns L., De Greve H., Loris R. Rejuvenation of CcdB-poisoned gyrase by an intrinsically disordered protein domain. Mol Cell 2009, 35:154-163.
51. Loris R., Dao-Thi M.H., Bahassi E.M., Van Melderen L., Poortmans F., Liddington R., Couturier M., Wyns L. Crystal structure of CcdB, a topoisomerase poison from E. coli. J Mol Biol 1999, 285:1667-1677.
52. Kumar P., Issac B., Dodson E.J., Turkenburg J.P., Mande S.C. Crystal structure of Mycobacterium tuberculosis YefM antitoxin reveals that it is not an intrinsically unstructured protein. J Mol Biol 2008, 383:482-493.
53. Oberer M., Zangger K., Gruber K., Keller W. The solution structure of ParD, the antidote of the ParDE toxin antitoxin module, provides the structural basis for DNA and toxin binding. Protein Sci 2007, 16:1676-1688.