Determinants of eukaryal cell killing by the bacterial ribotoxin PrrC

Nucleic Acids Research

Volumn 39, Issue 2, 2011, Pages 687-700

  Meineke, Birthe ^a   Schwer, Beate ^b   Schaffrath, Raffael ^c   Shuman, Stewart ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RIBOTOXIN; BACTERIAL TOXIN; ESCHERICHIA COLI PROTEIN; PROTEIN PRRC; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL KILLING; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; FUNGAL STRAIN; GENE MUTATION; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; STREPTOCOCCUS MUTANS; TOXICITY; XANTHOMONAS CAMPESTRIS;

ALANINE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL TOXINS; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASES; RNA, TRANSFER; RNA, TRANSFER, LYS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; NEISSERIA; SACCHAROMYCETALES; STREPTOCOCCUS; XANTHOMONAS;

EID: 79551482322     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq831     Document Type: Article

References (56)

1. Ogawa, T., Tomita, K., Ueda, T., Watanabe, K., Uozumi, T. and Masaki, H. (1999) A cytotoxic ribonuclease targeting specific tRNA anticodons. Science, 283, 2097-2100.
2. Tomita, K., Ogawa, T., Uozumi, T., Watanabe, K. and Masaki, H. (2000) A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc. Natl Acad. Sci. USA, 97, 8278-8283.
3. Lu, J., Huang, B., Esberg, A., Johanson, M. and Byströ m, A.S. (2005) The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. RNA, 11, 1648-1654.
4. Lu, J., Esberg, A., Huang, B. and Byströ m, A.S. (2008) The Kluyveromyces lactis g-toxin, a ribonuclease that recognizes the anticodon stem loop of tRNA. Nucleic Acids Res., 36, 1072-1080.
5. Klassen, R., Paluszynski, J.P., Emhoff, S., Pfeiffer, A., Fricke, J. and Meinhardt, F. (2008) The primary target of the killer toxin from Pichia acaciae is tRNAGln. Mol. Microbiol., 69, 681-697.
6. Kaufmann, G. (2000) Anticodon nucleases. TIBS, 25, 70-74.
7. Condon, C. (2006) Shutdown decay of mRNA. Mol. Microbiol., 61, 573-583.
8. Nariya, H. and Inouye, M. (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell, 132, 55-66.
9. Levitz, R., Chapman, D., Amitsur, M., Green, R., Snyder, L. and Kaufmann, G. (1990) The optional E. coli prr locus encodes a latent form of phage T4-induced anticodon nuclease. EMBO J., 9, 1383-1389.
10. Tyndall, C., Meister, J. and Bickle, T.A. (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.
11. Amitsur, M., Morad, I. and Kaufmann, G. (1989) In vitro reconstitution of anticodon nuclease from components encoded by phage T4 and Escherichia coli CTr5X. EMBO J., 8, 2411-2415.
12. Amitsur, M., Morad, I., Chapman-Shimshoni, D. and Kaufmann, G. (1992) HSD restriction-modification proteins partake in latent anticodon nuclease. EMBO J., 11, 3129-3134.
13. Penner, M., Morad, I., Snyder, L. and Kaufmann, G. (1995) Phage T4-coded Stp: double-edged effector of coupled DNA and tRNA-restriction systems. J. Mol. Biol., 249, 857-868.
14. Amitsur, M., Levitz, R. and Kaufman, G. (1987) Bacteriophage T4 anticodon nuclease, polynucleotide kinase, and RNA ligase reprocess the host lysine tRNA. EMBO J., 6, 2499-2503.
15. Zhu, H., Yin, S. and Shuman, S. (2004) Characterization of polynucleotide kinase/phosphatase enzymes from mycobacteriophages Omega and Cjw1 and vibriophage KVP40. J. Biol. Chem., 279, 26358-26369.
16. Jiang, Y., Mediler, R., Amitsur, M. and Kaufmann, G. (2001) Specific interaction between anticodon nuclease and the tRNALys wobble base. J. Mol. Biol., 305, 377-388.
17. Jiang, Y., Blanga, S., Amitsur, M., Meidler, R., Krivosheyev, E., Sundaram, M., Bajii, A., Davis, D.R. and Kaufmann, G. (2002) Structural features of tRNALys favored by anticodon nuclease as inferred from reactivities of anticodon stem and loop substrate analogs. J. Biol. Chem., 277, 3826-3841.
18. Amitsur, M., Banjamin, S., Rosner, R., Chapman-Shimshoni, D., Meidler, R., Blanga, S. and 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.
19. Blanga-Kanfi, S., Amitsur, M., Azem, A. and Kaufmann, G. (2006) PrrC-anticodon nuclease: functional organization of a prototypical bacteria restriction RNase. Nucleic Acids Res., 34, 3209-3219.
20. Davidov, E. and Kaufmann, G. (2008) RloC: a wobble nucleotide-excising and zinc-responsive bacterial tRNase. Mol. Microbiol., 69, 1560-1574.
21. Meidler, R., Morad, I., Amitsur, M., Inokuchi, H. and Kaufmann, G. (1999) Detection of anticodon nuclease residues involved in tRNALys cleavage specificity. J. Mol. Biol., 287, 499-510.
22. Ogawa, T., Hidaka, M., Kohno, K. and Masaki, H. (2009) Colicin E5 ribonuclease domain cleaves Saccharomyces cerevisiae tRNAs leading to impairment of the cell growth. J. Biochem., 145, 461-466.
23. Shigematsu, M., Ogawa, T., Kido, A., Kitamoto, H.K., Hidaka, M. and Masaki, H. (2009) Cellular and transcriptional responses of yeast to the cleavage of cytosolic tRNAs by colicin D. Yeast, 26, 663-673.
24. Keppetipola, N., Jain, R., Meineke, B., Diver, M. and Shuman, S. (2009) Structure-activity relationships in Kluyveromyces lactis g-toxin, a eukaryal tRNA anticodon nuclease. RNA, 15, 1036-1044.
25. Jablonowski, D., Zink, S., Mehlgarten, C., Daum, G. and Schaffrath, R. (2006) tRNAGlu wobble uridine methylation by Trm9 identifies Elongator's key role for zymocin-induced cell death in yeast. Mol. Microbiol., 59, 677-688.
26. Huang, B., Johansson, M.J.O. and Byströ m, A. (2005) An early step in wobble uridine tRNA modification requires the Elongator complex. RNA, 11, 424-436.
27. Schiestl, R.H. and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet., 16, 339-346.
28. Smith, P.C., Karpowich, N., Millen, L., Moody, J.E., Rosen, J., Thomas, P.J. and Hunt, J.F. (2002) ATP binding to the motor domain of a ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell., 10, 139-149.
29. Zaitseva, J., Jenewein, S., Jumpertz, T., Holland, I.B. and Schmitt, L. (2005) A structural analysis of asymmetry required tor catalytic activity of an ABC-ATPase domain dimer. EMBO J., 25, 3432-3443.
30. Zaitseva, J., Oswald, C., Jumpertz, T., Jenewein, S., Wiedenmann, A., Holland, I.B. and Schmitt, L. (2006) H662 is the lynchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J., 24, 1901-1910.
31. Dawson, R.J.P. and Locher, K.P. (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMPPNP. FEBS Lett., 581, 935-938.
32. Atwell, S., Brouillette, C.G., Conners, K., Emtage, S., Gheyi, T., Guggino, W.B., Hendle, J., Hunt, J.F., Lewis, H.A., Lu, F. et al. (2010) Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng. Des. Sel., 23, 375-384.
33. Klaiman, D., Amitsur, M., Blanga-Kanfi, S., Chai, M., Davis, D.R. and Kaufmann, G. (2007) Parallel dimerization of a PrrC-anticodon nuclease region implicated in tRNALys recognition. Nucleic Acids Res., 35, 4704-4714.
34. Raines, R.T. (1998) Ribonuclease A. Chem Rev., 98, 1045-1065.
35. Steyaert, J. (1997) A decade of protein engineering on ribonuclease T1: atomic dissection of the enzyme-substrate interactions. Eur. J. Biochem., 247, 1-11.
36. Xue, S., Calvin, K. and Li, H. (2006) RNA recognition and cleavage by a splicing endonuclease. Science, 312, 906-910.
37. Yajima, S., Inoue, S., Ogawa, T., Nonaka, T., Ohsawa, K. and Masaki, H. (2006) Structural basis for sequence-dependent recognition of colicin E5 tRNase by mimicking the mRNA-tRNA interaction. Nucleic Acids Res., 34, 6074-6082.
38. Zegers, I., Loris, R., Dehollander, G., Haikal, A.F., Poortmans, F., Steyaert, J. and Wyns, L. (1998) Hydrolysis of a slow cyclic thiophosphate substrate of RNase T1 analyzed by time-resolved crystallography. Nature Struct. Biol., 5, 280-283.
39. Buckle, A.M. and Fersht, A.R. (1994) Subsite binding in an RNase: structure of a barnase-tetranucleotide complex at 1.76-A? resolution. Biochemistry, 33, 1644-1653.
40. Loverix, S. and Steyaert, J. (2001) Deciphering the mechanism of RNase T1. Meth. Enzymol., 341, 305-323.
41. Jablonowski, D. and Schaffrath, R. (2007) Zymocin, a composite chitinase and tRNase killer toxin from yeast. Biochem. Soc. Trans., 35, 1533-1537.
42. Sadler, A.J. and Williams, B.R. (2008) Interferon-inducible antiviral effectors. Nat. Rev. Immunol., 8, 559-568.
43. Lee, S.R. and Collins, K. (2005) Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J. Biol. Chem., 280, 42744-42749.
44. Li, Y., Zhou, H., Liao, J.Y., Ma, L.M., Chen, Y.Q. and Qu, L.H. (2008) Stress-induced tRNA-derived RNAs: a novel class of small RNAs in the primitive eukaryote Giardia lamblia. Nucleic Acids Res., 36, 6048-6055.
45. Thompson, D.M., Lu, C., Green, P.J. and Parker, R. (2008) tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA, 14, 2095-2103. Nucleic Acids Research, 2011, Vol. 39, No. 2 699.
46. Thompson, D.M. and Parker, R. (2009) The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol., 185, 43-50.
47. Fu, H., Feng, J., Liu, Q., Sun, F., Tie, Y., Zhu, J., Xing, R., Sun, Z. and Zheng, X. (2009) Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett., 583, 437-442.
48. Yamasaki, S., Ivanov, P., Gu, G. and Anderson, P. (2009) Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol., 185, 35-42.
49. Emara, M.M., Ivanov, P., Hickman, T., Dawra, N., Tosdale, S., Kedersha, N., Hu, G.F. and Anderson, P. (2010) Angiogenin-induced tRNA-derived stress-induced RNA promote stress-induced stress granule assembly. J. Biol. Chem., 285, 20959-10968.
50. Garcia-Silva, M.R., Frugier, M., Tosar, J.P., Correa-Dominguez, A., Ronalte-Alves, L., Parodi-Talice, A., Robira, C., Robello, C., Goldenberg, S., Cayota, A. et al. (2010) A population of tRNA-derived small RNAs is actively produced in Trypanosoma cruzi and recruited to specific cytoplasmic granules. Mol. Biochem. Parisitol., 171, 64-73.
51. Thompson, D.M. and Parker, R. (2009) Stressing out over tRNA cleavage. Cell, 138, 215-219.
52. Shterman, N., Elroy-Stein, O., Morad, I., Amitsur, M. and Kaufmann, G. (1995) Cleavage of the HIV replication primer tRNALys3, 3 in human cells expressing bacterial anticodon nuclease. Nucleic Acids Res., 23, 1744-1749.
53. Makarov, A.A., Kolchinsky, A. and Ilinskaya, O.N. (2008) Binase and other microbial RNases as potential anticancer agents. BioEssays, 30, 781-790.
54. Ardelt, W., Ardelt, B. and Darzynkiewicz, Z. (2009) Ribonucleases as potential modalities in anticancer therapy. Eur. J. Pharmacol., 625, 181-189.
55. Saxena, S.K., Sirdeshmukh, R., Ardelt, W., Mikulski, S.M., Shogen, K. and Youle, R.J. (2002) Entry into cells and selective degradation of tRNAs by a cytotoxic member of the RNase A family. J. Biol. Chem., 277, 15142-15146.
56. Nandakumar, J., Schwer, B., Schaffrath, R. and Shuman, S. (2008) RNA repair: an antidote to cytotoxic eukaryal RNA damage. Mol. Cell, 31, 278-286.