Functional and structural analysis of HicA3-HicB3, a novel toxin-antitoxin system of yersinia pestis

Journal of Bacteriology

Volumn 196, Issue 21, 2014, Pages 3712-3723

  Bibi Triki, Sabrina ^a,b   de la Sierra Gallay, Inès Li ^c   Lazar, Noureddine ^c   Leroy, Arnaud ^d   Van Tilbeurgh, Herman ^c   Sebbane, Florent ^a,b   Pradel, Elizabeth ^a,b  

^a INSERM U1019   (France)

^b UNIV LILLE   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d EA 4529   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; HISTIDINE; RIBONUCLEASE; ANTITOXIN; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BIOCHEMICAL COMPOSITION; CRYSTAL STRUCTURE; GENE FUNCTION; GENETIC CODE; HICA3 GENE; HICB3 GENE; MUTAGENESIS; NONHUMAN; OPERON; PROMOTER REGION; STRUCTURE ANALYSIS; YERSINIA PESTIS; ANIMAL; CHEMICAL STRUCTURE; DNA BASE COMPOSITION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE; PATHOGENICITY; PHYSIOLOGY; PLAGUE; PROTEIN CONFORMATION; VIRULENCE;

ANIMALS; ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE COMPOSITION; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLAGUE; PROMOTER REGIONS, GENETIC; PROTEIN CONFORMATION; VIRULENCE; YERSINIA PESTIS;

EID: 84907842145     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01932-14     Document Type: Article

References (60)

1. Butler T. 2013. Plague gives surprises in the first decade of the 21st century in the United States and worldwide. Am. J. Trop. Med. Hyg. 89:788-793. http://dx.doi.org/10.4269/ajtmh.13-0191.
2. Lathem WW, Crosby SD, Miller VL, Goldman WE. 2005. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. U. S. A. 102:17786-17791. http://dx.doi.org/10.1073/pnas.0506840102.
3. Pradel E, Lemaître N, Merchez M, Ricard I, Reboul A, Dewitte A, Sebbane F. 2014. New insights into how Yersinia pestis adapts to its mammalian host during bubonic plague. PLoS Pathog. 10:e1004029. http://dx.doi.org/10.1371/journal.ppat.1004029.
4. Sebbane F, Lemaître N, Sturdevant DE, Rebeil R, Virtaneva K, Porcella SF, Hinnebusch BJ. 2006. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. U. S. A. 103:11766-11771. http://dx.doi.org/10.1073/pnas.0601182103.
5. Goulard C, Langrand S, Carniel E, Chauvaux S. 2010. The Yersinia pestis chromosome encodes active addiction toxins. J. Bacteriol. 192:3669-3677. http://dx.doi.org/10.1128/JB.00336-10.
6. Yamaguchi Y, Park J-H, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45:61-79. http://dx.doi.org/10.1146/annurev-genet-110410-132412.
7. Cook GM, Robson JR, Frampton RA, McKenzie J, Przybilski R, Fineran PC, Arcus VL. 2013. Ribonucleases in bacterial toxin-antitoxin systems. Biochim. Biophys. Acta 1829:523-531. http://dx.doi.org/10.1016/j.bbagrm.2013.02.007.
8. Unoson C, Wagner EGH. 2008. A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol. Microbiol. 70:258-270. http://dx.doi.org/10.1111/j.1365-2958.2008.06416.x.
9. Bernard P, Kézdy KE, Van Melderen L, Steyaert J, Wyns L, Pato ML, Higgins PN, Couturier M. 1993. The F plasmid CcdB protein induces efficient ATP-dependent DNA cleavage by gyrase. J. Mol. Biol. 234:534-541. http://dx.doi.org/10.1006/jmbi.1993.1609.
10. Zhang Y, Inouye M. 2011. RatA (YfjG), an Escherichia coli toxin, inhibits 70S ribosome association to block translation initiation. Mol. Microbiol. 79:1418-1429. http://dx.doi.org/10.1111/j.1365-2958.2010.07506.x.
11. Correia FF, D'Onofrio A, Rejtar T, Li L, Karger BL, Makarova K, Koonin EV, Lewis K. 2006. Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J. Bacteriol. 188:8360-8367. http://dx.doi.org/10.1128/JB.01237-06.
12. Germain E, Castro-Roa D, Zenkin N, Gerdes K. 2013. Molecular mechanism of bacterial persistence by HipA. Mol. Cell 52:248-254. http://dx.doi.org/10.1016/j.molcel.2013.08.045.
13. Yamaguchi Y, Inouye M. 2011. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 9:779-790. http://dx.doi.org/10.1038/nrmicro2651.
14. Fozo EM, Hemm MR, Storz G. 2008. Small toxic proteins and the antisense RNAs that repress them. Microbiol. Mol. Biol. Rev. 72:579-589. http://dx.doi.org/10.1128/MMBR.00025-08.
15. Hayes F, Van Melderen L. 2011. Toxins-antitoxins: diversity, evolution and function. Crit. Rev. Biochem. Mol. Biol. 46:386-408. http://dx.doi.org/10.3109/10409238.2011.600437.
16. Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GP. 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. U. S. A. 106: 894-899. http://dx.doi.org/10.1073/pnas.0808832106.
17. Samson JE, Bélanger M, Moineau S. 2013. Effect of the abortive infection mechanism and type III toxin/antitoxin system AbiQ on the lytic cycle of Lactococcus lactis phages. J. Bacteriol. 195:3947-3956. http://dx.doi.org/10.1128/JB.00296-13.
18. Zielenkiewicz U, Ceglowski P. 2005. The toxin-antitoxin system of the streptococcal plasmid pSM19035. J. Bacteriol. 187:6094-6105. http://dx.doi.org/10.1128/JB.187.17.6094-6105.2005.
19. Hallez R, Geeraerts D, Sterckx Y, Mine N, Loris R, Van Melderen L. New toxins homologous to ParE belonging to three-component toxin-antitoxin systems in Escherichia coli O157:H7. Mol. Microbiol. 76: 719-732. http://dx.doi.org/10.1111/j.1365-2958.2010.07129.x.
20. Pandey DP, Gerdes K. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 33:966-976. http://dx.doi.org/10.1093/nar/gki201.
21. Jørgensen MG, Pandey DP, Jaskolska M, Gerdes K. 2009. HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J. Bacteriol. 191:1191-1199. http://dx.doi.org/10.1128/JB.01013-08.
22. Sikkema DJ, Brubaker RR. 1987. Resistance to pesticin, storage of iron, and invasion of HeLa cells by yersiniae. Infect. Immun. 55:572-578.
23. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
24. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86. http://dx.doi.org/10.1016/S0378-1119(98)00130-9.
25. Fetherston JD, Schuetze P, Perry RD. 1992. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol. Microbiol. 6:2693-2704. http://dx.doi.org/10.1111/j.1365-2958.1992.tb01446.x.
26. Burke E, Barik S. 2003. Megaprimer PCR, p 525-531. In Bartlett JMS, Stirling D (ed), PCR protocols. Humana Press, Totowa, NJ. http://dx.doi.org/10.1385/1-59259-384-4:525.
27. Quevillon-Cheruel S, Collinet B, Trésaugues L, Minard P, Henckes G, Aufrère R, Blondeau K, Zhou C-Z, Liger D, Bettache N, Poupon A, Aboulfath I, Leulliot N, Janin J, van Tilbeurgh H. 2007. Cloning, production, and purification of proteins for a medium-scale structural genomics project, p 21-37. In Walker JM, Doublié S (ed), Macromolecular crystallography protocols. Humana Press, Totowa, NJ. http://dx.doi.org/10.1007/978-1-59745-209-0_2.
28. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, Margalit H, Altuvia S. 2001. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 11:941-950. http://dx.doi.org/10.1016/S0960-9822(01)00270-6.
29. Lohmann V, Körner F, Koch J-O, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113. http://dx.doi.org/10.1126/science.285.5424.110.
30. Lemaître N, Ricard I, Pradel E, Foligné B, Courcol R, Simonet M, Sebbane F. 2012. Efficacy of ciprofloxacin-gentamicin combination therapy in murine bubonic plague. PLoS One 7:e52503. http://dx.doi.org/10.1371/journal.pone.0052503.
31. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. DBiol. Crystallogr. 67:235-242. http://dx.doi.org/10.1107/S0907444910045749.
32. Park SJ, Son WS, Lee B-J. 2013. Structural overview of toxin- antitoxin systems in infectious bacteria: a target for developing antimicrobial agents. Biochim. Biophys. Acta 1834:1155-1167. http://dx.doi.org/10.1016/j.bbapap.2013.02.027.
33. Gazit E, Sauer RT. 1999. The Doc toxin and Phd antidote proteins of the bacteriophage P1 plasmid addiction system form a heterotrimeric complex. J. Biol. Chem. 274:16813-16818. http://dx.doi.org/10.1074/jbc.274.24.16813.
34. Loris R, Dao-Thi M-H, Bahassi EM, Van Melderen L, Poortmans F, Liddington R, Couturier M, Wyns L. 1999. Crystal structure of CcdB, a topoisomerase poison from E. coli. J. Mol. Biol. 285:1667-1677. http://dx.doi.org/10.1006/jmbi.1998.2395.
35. Overgaard M, Borch J, Gerdes K. 2009. RelB and RelE of Escherichia coli form a tight complex that represses transcription via the ribbon- helix- helix motif in RelB. J. Mol. Biol. 394:183-196. http://dx.doi.org/10.1016/j.jmb.2009.09.006.
36. Kamada K, Hanaoka F, Burley SK. 2003. Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. Mol. Cell 11:875-884. http://dx.doi.org/10.1016/S1097-2765(03)00097-2.
37. Anantharaman V, Aravind L. 2003. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsensemediated RNA decay system. Genome Biol. 4:R81. http://dx.doi.org/10.1186/gb-2003-4-12-r81.
38. Kamphuis M, Chiara Monti M, van den Heuvel HR, Lopez-Villarejo J, Diaz-Orejas R, Boelens R. 2007. Structure and function of bacterial Kid-Kis and related toxin-antitoxin systems. Protein Pept. Lett. 14:113-124. http://dx.doi.org/10.2174/092986607779816096.
39. Brown BM, Bowie JU, Sauer RT. 1990. Arc repressor is tetrameric when bound to operator DNA. Biochemistry (Mosc.) 29:11189-11195. http://dx.doi.org/10.1021/bi00503a006.
40. Bøggild A, Sofos N, Andersen KR, Feddersen A, Easter AD, Passmore LA, Brodersen DE. 2012. The crystal structure of the intact E. coli RelBE toxin-antitoxin complex provides the structural basis for conditional cooperativity. Structure 20:1641-1648. http://dx.doi.org/10.1016/j.str.2012.08.017.
41. van Helden J, André B, Collado-Vides J. 2000. A web site for the computational analysis of yeast regulatory sequences. Yeast 16:177-187. http://dx.doi.org/10.1002/(SICI)1097-0061(20000130)16:2<177::AID-YEA516>3.0.CO;2-9.
42. Overgaard M, Borch J, Jørgensen MG, Gerdes K. 2008. Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity. Mol. Microbiol. 69:841-857. http://dx.doi.org/10.1111/j.1365-2958.2008.06313.x.
43. Garcia-Pino A, Balasubramanian S, Wyns L, Gazit E, De Greve H, Magnuson RD, Charlier D, van Nuland NAJ, Loris R. 2010. Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell 142:101-111. http://dx.doi.org/10.1016/j.cell.2010.05.039.
44. Winther KS, Gerdes K. 2012. Regulation of enteric vapBC transcription: induction by VapC toxin dimer-breaking. Nucleic Acids Res. 40:4347-4357. http://dx.doi.org/10.1093/nar/gks029.
45. Brown BL, Lord DM, Grigoriu S, Peti W, Page R. 2013. The Escherichia coli toxin MqsR destabilizes the transcriptional repression complex formed between the antitoxin MqsA and the mqsRA operon promoter. J. Biol. Chem. 288:1286-1294. http://dx.doi.org/10.1074/jbc. M112.421008.
46. Butt A, Higman VA, Williams C, Crump MP, Hemsley CM, Harmer N, Titball RW. 2014. The HicA toxin from Burkholderia pseudomallei has a role in persister cell formation. Biochem. J. 459:333-344. http://dx.doi.org/10.1042/BJ20140073.
47. De la Cruz MA, Zhao W, Farenc C, Gimenez G, Raoult D, Cambillau C, Gorvel J-P, Méresse S. 2013. A toxin-antitoxin module of Salmonella promotes virulence in mice. PLoS Pathog. 9:e1003827. http://dx.doi.org/10.1371/journal.ppat.1003827.
48. Ren D, Walker AN, Daines DA. 2012. Toxin-antitoxin loci vapBC-1 and vapXD contribute to survival and virulence in nontypeable Haemophilus influenzae. BMC Microbiol. 12:263. http://dx.doi.org/10.1186/1471-2180-12-263.
49. Ramage HR, Connolly LE, Cox JS. 2009. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet. 5:e1000767. http://dx.doi.org/10.1371/journal.pgen.1000767.
50. Kim Y, Wang X, Ma Q, Zhang X-S, Wood TK. 2009. Toxin-antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae. J. Bacteriol. 191:1258-1267. http://dx.doi.org/10.1128/JB.01465-08.
51. Frampton R, Aggio RBM, Villas-Bôas SG, Arcus VL, Cook GM. 2012. Toxin-antitoxin systems of Mycobacterium smegmatis are essential for cell survival. J. Biol. Chem. 287:5340-5356. http://dx.doi.org/10.1074/jbc. M111.286856.
52. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130. http://dx.doi.org/10.1016/0022-2836(86)90385-2.
53. Herrero M, de Lorenzo V, Timmis KN. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
54. Grant SG, Jessee J, Bloom FR, Hanahan D. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylationrestriction mutants. Proc. Natl. Acad. Sci. U. S. A. 87:4645-4649. http://dx.doi.org/10.1073/pnas.87.12.4645.
55. Guyer MS, Reed RR, Steitz JA, Low KB. 1981. Identification of a sexfactor- affinity site in E. coli as gamma delta. Cold Spring Harb. Symp. Quant. Biol. 45(Part 1):135-140. http://dx.doi.org/10.1101/SQB.1981.045.01.022.
56. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1:784-791. http://dx.doi.org/10.1038/nbt1183-784.
57. Doll JM, Zeitz PS, Ettestad P, Bucholtz AL, Davis T, Gage K. 1994. Cat-transmitted fatal pneumonic plague in a person who traveled from Colorado to Arizona. Am. J. Trop. Med. Hyg. 51:109-114.
58. Veiga E, de Lorenzo V, Fernández LA. 1999. Probing secretion and translocation of a β-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol. Microbiol. 33:1232-1243. http://dx.doi.org/10.1046/j.1365-2958.1999.01571.x.
59. Guzman L-M, Belin D, Carson MJ, Beckwith JON. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
60. Kalogeraki VS, Winans SC. 1997. Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188:69-75. http://dx.doi.org/10.1016/S0378-1119(96)00778-0.