A mutagenic analysis of the RNase mechanism of the bacterial Kid toxin by mass spectrometry

FEBS Journal

Volumn 276, Issue 17, 2009, Pages 4973-4986

  Diago Navarro, Elizabeth ^a   Kamphuis, Monique B ^b   Boelens, Rolf ^b   Barendregt, Arjan ^b   Heck, Albert J ^b   Van Den Heuvel, Robert H ^b   Díaz Orejas, Ramón ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Kid mutants; Kid RNase model; Native mass spectrometry; Protein RNA binding; Protein RNA cleavage

Indexed keywords

BACTERIAL TOXIN; KID TOXIN; RIBONUCLEASE; UNCLASSIFIED DRUG; URACIL;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; MASS SPECTROMETRY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; RNA CLEAVAGE;

ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; RIBONUCLEASES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 68849096027     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07199.x     Document Type: Article

References (35)

1. Ogura T Hiraga S (1983) Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci USA 80, 4784 4788.
2. Gerdes K, Rasmussen PB Molin S (1986) Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci USA 83, 3116 3120.
3. Bravo A, de Torrontegui G Diaz R (1987) Identification of components of a new stability system of plasmid R1, ParD, that is close to the origin of replication of this plasmid. Mol Gen Genet 210, 101 110.
4. Pandey DG Gerdes K (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 55, 78 89.
5. Gerdes K Wagner EG (2007) RNA antitoxins. Curr Opin Microbiol 10, 117 124.
6. Gerdes K, Christensen SK Lobner-Olensen A (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3, 371 382.
7. Van Melderen L Saavedra De Bast M (2009) Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet 5, e1000437, doi :.
8. Ruiz-Echevarria MJ, Berzal-Herranz A, Gerdes K Diaz-Orejas R (1991) The kis and kid genes of the parD maintenance system of plasmid R1 form an operon that is autoregulated at the level of transcription by the co-ordinated action of the Kis and Kid proteins. Mol Microbiol 5, 2685 2693.
9. Monti MC, Hernandez-Arriaga AM, Kamphuis MB, Lopez-Villarejo J, Heck AJ, Boelens R, Diaz-Orejas R Van den Heuvel RH (2007) Interactions of Kid-Kis toxin-antitoxin complexes with the parD operator-promoter region of plasmid R1 are piloted by the Kis antitoxin and tuned by the stoichiometry of Kid-Kis oligomers. Nucleic Acids Res 35, 1737 1749.
10. Ruiz-Echevarria MJ, de-la-Cueva G Diaz-Orejas R (1995) Translational coupling and limited degradation of a polycistronic messenger modulate differential gene expression in the parD stability system of plasmid R1. Mol Gen Genet 248, 599 609.
11. Tsuchimoto S, Nishimura Y Ohtsubo E (1992) The stable maintenance system pem of plasmid R100: degradation of PemI protein may allow PemK protein to inhibit cell growth. J Bacteriol 174, 4205 4211.
12. Munoz-Gomez AJ, Lemonnier M, Santos-Sierra S, Berzal-Herranz A Diaz-Orejas R (2005) RNase/anti-RNase activities of the bacterial parD toxin-antitoxin system. J Bacteriol 187, 3151 3157.
13. Tsuchimoto S, Ohtsubo H Ohtsubo E (1988) Two genes, pemK and pemI, responsible for stable maintenance of resistance plasmid R100. J Bacteriol 170, 1461 1466.
14. Zhang J, Zhang Y, Zhu L, Suzuki M Inouye M (2004) Interference of mRNA function by sequence-specific endoribonuclease PemK. J Biol Chem 279, 20678 20684.
15. Pimentel B, Madine MA de la Cueva-Mendez G (2005) Kid cleaves specific mRNAs at UUACU sites to rescue the copy number of plasmid R1. EMBO J 24, 3459 3469.
16. Ruiz-Echevarria MJ, de-la-Torre MA Diaz-Orejas R (1995) A mutation that decreases the efficiency of plasmid R1 replication leads to the activation of parD, a killer stability system of the plasmid. FEMS Microbiol Lett 130, 129 135.
17. Steyaert J (1997) A decade of protein engineering on ribonuclease T1 - atomic dissection of the enzyme-substrate interactions. Eur J Biochem 247, 1 11.
18. Lacadena J, Martinez del Pozo A, Lacadena V, Martinez-Ruiz A, Mancheno JM, Onaderra M Gavilanes JG (1998) The cytotoxin alpha-sarcin behaves as a cyclizing ribonuclease. FEBS Lett 424, 46 48.
19. Kamphuis MB, Bonvin AM, Monti MC, Lemonnier M, Munoz-Gomez A, Van den Heuvel RH, Diaz-Orejas R Boelens R (2006) Model for RNA binding and the catalytic site of the RNase Kid of the bacterial parD toxin-antitoxin system. J Mol Biol 357, 115 126.
20. Santos-Sierra S, Lemonnier M, Nunez B, Hargreaves D, Rafferty J, Giraldo R, Andreu JM Diaz-Orejas R (2003) Non-cytotoxic variants of the Kid protein that retain their auto-regulatory activity. Plasmid 50, 120 130.
21. Hargreaves D, Santos-Sierra S, Giraldo R, Sabariegos-Jareno R, de la Cueva-Mendez G, Boelens R, Diaz-Orejas R Rafferty JB (2002) Structural and functional analysis of the kid toxin protein from E. coli plasmid R1. Structure 10, 1425 1433.
22. Masuda Y, Miyakawa K, Nishimura Y Ohtsubo E (1993) chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100. J Bacteriol 175, 6850 6856.
23. Munoz Gomez A (2004) Identificación y caracterización de la actividad RNasa de las toxinas bacterianas Kid y ChpAK. PhD Thesis. Universidad Autónoma de Madrid, Madrid. M, Santos-Sierra S, Pardo-Abarrio C Diaz-Orejas R (2004) Identification of residues of the kid toxin involved in autoregulation of the parD system. J Bacteriol 186, 240 243.
24. Heck AJ (2008) Native mass spectrometry: a bridge between interactomics and structural biology. Nat Methods 5, 927 933.
25. Sharon M Robinson CV (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu Rev Biochem 76, 167 193.
26. Prysak MH, Mozdzierz CJ, Cook AM, Zhu L, Zhang Y, Inouye M Woychik NA (2009) Bacterial toxin YafQ is an endoribonuclease that associates with the ribosome and blocks translation elongation through sequence-specific and frame-dependent mRNA cleavage. Mol Microbiol 71, 1071 1087.
27. Christensen-Dalsgaard M Gerdes K (2008) Translation affects YoeB and MazF messenger RNA interferase activities by different mechanisms. Nucleic Acids Res 36, 6472 6481.
28. Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K Ehrenberg M (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112, 131 140.
29. Diago-Navarro E, Mora L, Buckingham RH, Diaz-Orejas R Lemonnier M (2009) Novel Escherichia coli RF1 mutants with decreased translation termination activity and increased sensitivity to the cytotoxic effect of the bacterial toxins Kid and RelE. Mol Microbiol 71, 66 78.
30. Miller J (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. van den Heuvel RH, van Duijn E, Mazon H, Synowsky SA, Lorenzen K, Versluis C, Brouns SJ, Langridge D, van der Oost J, Hoyes J et al. (2006) Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry. Anal Chem 78, 7473 7483.
32. van den Heuvel RH, Gato S, Versluis C, Gerbaux P, Kleanthous C Heck AJ (2005) Real-time monitoring of enzymatic DNA hydrolysis by electrospray ionization mass spectrometry. Nucleic Acids Res 33, e96.
33. Bravo A, Ortega S, de Torrontegui G Diaz R (1988) Killing of Escherichia coli cells modulated by components of the stability system ParD of plasmid R1. Mol Gen Genet 215, 146 151.
34. Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL Boyer HW (1977) Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2, 95 113. (Pubitemid 9021046)
35. De Lano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.