Determinants of the cytotoxicity of PrrC anticodon nuclease and its amelioration by tRNA repair

RNA

Volumn 18, Issue 1, 2012, Pages 145-154

  Meineke, Birthe ^a   Shuman, Stewart ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Polynucleotide kinase phosphatase; Ribotoxin; RNA ligase; tRNA breakage; Wobble uridine modification

Indexed keywords

ARGININE; ESCHERICHIA COLI TRNA ANTICODON NUCLEASE; LYSINE; RNA LIGASE; TRANSFER RNA; TRYPTOPHAN; UNCLASSIFIED DRUG; URIDINE;

5' UNTRANSLATED REGION; ALLELE; ANTICODON; ARTICLE; BACTERIAL SURVIVAL; BACTERIOPHAGE T4; CELL GROWTH; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ESCHERICHIA COLI; GAIN OF FUNCTION MUTATION; GROWTH INHIBITION; HYDROGEN BOND; MUTAGENESIS; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA ANALYSIS; RNA BINDING; RNA REPAIR; SACCHAROMYCES CEREVISIAE; TRANSESTERIFICATION; VIRUS CELL INTERACTION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARGININE; ESCHERICHIA COLI PROTEINS; GENE DOSAGE; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASES; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; TRYPTOPHAN; URIDINE;

EID: 84055212176     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.030171.111     Document Type: Article

References (29)

1. Amitsur M, Levitz R, Kaufman G. 1987. Bacteriophage T4 anticodon nuclease, polynucleotide kinase, and RNA ligase reprocess the host lysine tRNA. EMBO J 6: 2499-2503.
2. Amitsur M, Morad I, Kaufmann G. 1989. In vitro reconstitution of anticodon nuclease from components encoded by phage T4 and Escherichia coli CTr5X. EMBO J 8: 2411-2415. (Pubitemid 19273323)
3. Amitsur M, Morad I, Chapman-Shimshoni D, Kaufmann G. 1992. HSD restriction-modification proteins partake in latent anticodon nuclease. EMBO J 11: 3129-3134.
4. Amitsur M, Benjamin S, Rosner R, Chapman-Shimshoni D, Meidler R, Blanga S, Kaufmann G. 2003. Bacteriophage T4-encoded Stp can be replaced as activator of anticodon nuclease by a normal host cell metabolite. Mol Microbiol 50: 129-143. (Pubitemid 37222792)
5. Blanga-Kanfi S, Amitsur M, Azem A, Kaufmann G. 2006. PrrC-anticodon nuclease: Functional organization of a prototypical bacteria restriction RNase. Nucleic Acids Res 34: 3209-3219.
6. Davidov E, Kaufmann G. 2008. RloC: A wobble nucleotide-excising and zinc-responsive bacterial tRNase. Mol Microbiol 69: 1560-1574.
7. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. 2011. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 43: 613-623.
8. Jablonowski D, Schaffrath R. 2007. Zymocin, a composite chitinase and tRNase killer toxin from yeast. Biochem Soc Trans 35: 1533-1537.
9. Glu wobble uridine methylation by Trm9 identifies Elongator's key role for zymocin-induced cell death in yeast. Mol Microbiol 59: 677-688.
10. Jiang Y, Mediler R, Amitsur M, Kaufmann G. 2001. Specific interaction between anticodon nuclease and the tRNALys wobble base. J Mol Biol 305: 377-388. (Pubitemid 33032847)
11. Lys favored by anticodon nuclease as inferred from reactivities of anticodon stem and loop substrate analogs. J Biol Chem 277: 3836-3841.
12. Kaufmann G. 2000. Anticodon nucleases. Trends Biochem Sci 25: 70-74. (Pubitemid 30100369)
13. Klaiman D, Amitsur M, Blanga-Kanfi S, Chai M, Davis DR, Kaufmann G. 2007. Parallel dimerization of a PrrC-anticodon nuclease region implicated in tRNALys recognition. Nucleic Acids Res 35: 4704-4714. (Pubitemid 47250342)
14. Klassen R, Paluszynski JP, Emhoff S, Pfeiffer A, Fricke J, Meinhardt F. 2008. The primary target of the killer toxin from Pichia acaciae is tRNAGln. Mol Microbiol 69: 681-697. (Pubitemid 351962563)
15. Levitz R, Chapman D, Amitsur M, Green R, Snyder L, Kaufmann G. 1990. The optional E. coli prr locus encodes a latent form of phage T4-induced anticodon nuclease. EMBO J 9: 1383-1389.
16. Lu J, Huang B, Esberg A, Johanson MJO, Byström AS. 2005. The Kluyveromyces lactis γ-toxin targets tRNA anticodons. RNA 11: 1648-1654. (Pubitemid 41505539)
17. Lu J, Esberg A, Huang B, Byström AS. 2008. Kluyveromyces lactis γ-toxin, a ribonuclease that recognizes the anticodon stem loop of tRNA. Nucleic Acids Res 36: 1072-1080. (Pubitemid 351330926)
18. Meidler R, Morad I, Amitsur M, Inokuchi H, Kaufmann G. 1999. Detection of anticodon nuclease residues involved in tRNALyscleavage specificity. J Mol Biol 287: 499-510. (Pubitemid 29168429)
19. Meineke B, Schwer B, Schaffrath R, Shuman S. 2011. Determinants of eukaryal cell killing by the bacterial ribotoxin PrrC. Nucleic Acids Res 39: 687-700.
20. Nandakumar J, Schwer B, Schaffrath R, Shuman S. 2008. RNA repair: An antidote to cytotoxic eukaryal RNA damage. Mol Cell 31: 278-286. (Pubitemid 352001396)
21. Ogawa T, Tomita K, Ueda T, Watanabe K, Uozumi T, Masaki H. 1999. A cytotoxic ribonuclease targeting specific tRNA anticodons. Science 283: 2097-2100.
22. Ogawa T, Hidaka M, Kohno K, Masaki H. 2009. Colicin E5 ribonuclease domain cleaves Saccharomyces cerevisiae tRNAs leading to impairment of the cell growth. J Biochem 145: 461-466.
23. Penner M, Morad I, Snyder L, Kaufmann G. 1995. Phage T4-coded Stp: Double-edged effector of coupled DNA and tRNA-restriction systems. J Mol Biol 249: 857-868.
24. Shigematsu M, Ogawa T, Kido A, Kitamoto HK, Hidaka M, Masaki H. 2009. Cellular and transcriptional responses of yeast to the cleavage of cytosolic tRNAs by colicin D. Yeast 26: 663-673.
25. Thompson DM, Parker R. 2009. Stressing out over tRNA cleavage. Cell 138: 215-219.
26. Tomita K, Ogawa T, Uozumi T, Watanabe K, Masaki H. 2000. A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc Natl Acad Sci 97: 8278-8283. (Pubitemid 30639663)
27. Tyndall C, Meister J, Bickle TA. 1994. The Escherichia coli prr region encodes a functional type IC DNA restriction system closely integrated with an anticodon nuclease gene. J Mol Biol 237: 266-274. (Pubitemid 24144281)
28. Wang LK, Schwer B, Englert M, Beier H, Shuman S. 2006. Structure-function analysis of the kinase-CPD domain of yeast tRNA ligase (Trl1) and requirements for complementation of tRNA splicing by a plant Trl1 homolog. Nucleic Acids Res 34: 517-527. (Pubitemid 43240240)
29. Winther KS, Gerdes K. 2011. Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc Natl Acad Sci 108: 7403-7407.