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Autoselection of Cytoplasmic Yeast Virus Like Elements Encoding Toxin/Antitoxin Systems Involves a Nuclear Barrier for Immunity Gene Expression


The rather wide-spread and extremely A/T rich yeast virus like elements (VLEs, also termed linear plasmids) which encode toxic anticodon nucleases (ACNases) ensure autoselection in the cytoplasm by preventing functional nuclear capture of the cognate immunity genes, but how? When expressed in the nucleus, the mRNA of the VLE immunity genes is split into fragments to which poly(A) tails are added. Consistently, lowering the A/T content by gene synthesis prevented transcript cleavage and permitted functional nuclear expression providing full immunity against the respective ACNase toxin. Thus, internal poly(A) cleavage is likely to prevent functional nuclear immunity gene expression.


Vyšlo v časopise: Autoselection of Cytoplasmic Yeast Virus Like Elements Encoding Toxin/Antitoxin Systems Involves a Nuclear Barrier for Immunity Gene Expression. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005005
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005005

Souhrn

The rather wide-spread and extremely A/T rich yeast virus like elements (VLEs, also termed linear plasmids) which encode toxic anticodon nucleases (ACNases) ensure autoselection in the cytoplasm by preventing functional nuclear capture of the cognate immunity genes, but how? When expressed in the nucleus, the mRNA of the VLE immunity genes is split into fragments to which poly(A) tails are added. Consistently, lowering the A/T content by gene synthesis prevented transcript cleavage and permitted functional nuclear expression providing full immunity against the respective ACNase toxin. Thus, internal poly(A) cleavage is likely to prevent functional nuclear immunity gene expression.


Zdroje

1. Worsham PL, Bolen PL (1990) Killer toxin production in Pichia acaciae is associated with linear DNA plasmids. Curr Genet 18: 77–80. 2245477

2. Gunge N, Tamaru A, Ozawa F, Sakaguchi K (1981) Isolation and characterization of linear deoxyribonucleic acid plasmids from Kluyveromyces lactis and the plasmid-associated killer character. J Bacteriol 145: 382–390. 6257636

3. Jeske S, Meinhardt F (2006) Autonomous cytoplasmic linear plasmid pPac1-1 of Pichia acaciae: molecular structure and expression studies. Yeast 23: 479–486. 16652393

4. Schaffrath R, Meinhardt F, editors (2005) Kluyveromyces lactis zymocin and other plasmid-encoded yeast killer toxins. Berlin: Springer. 337–352 p.

5. Jablonowski D, Fichtner L, Martin VJ, Klassen R, Meinhardt F, et al. (2001) Saccharomyces cerevisiae cell wall chitin, the Kluyveromyces lactis zymocin receptor. Yeast 18: 1285–1299. 11571753

6. Mehlgarten C, Schaffrath R (2004) After chitin docking, toxicity of Kluyveromyces lactis zymocin requires Saccharomyces cerevisiae plasma membrane H+-ATPase. Cell Microbiol 6: 569–580. 15104597

7. Zink S, Mehlgarten C, Kitamoto HK, Nagase J, Jablonowski D, et al. (2005) Mannosyl-diinositolphospho-ceramide, the major yeast plasma membrane sphingolipid, governs toxicity of Kluyveromyces lactis zymocin. Eukaryot Cell 4: 879–889. 15879522

8. Chakravarty AK, Smith P, Jalan R, Shuman S (2014) Structure, mechanism, and specificity of a eukaryal tRNA restriction enzyme involved in self-nonself discrimination. Cell Rep 7: 339–347. doi: 10.1016/j.celrep.2014.03.034 24726365

9. Klassen R, Paluszynski JP, Wemhoff S, Pfeiffer A, Fricke J, et al. (2008) The primary target of the killer toxin from Pichia acaciae is tRNA(Gln). Mol Microbiol 69: 681–697. doi: 10.1111/j.1365-2958.2008.06319.x 18532979

10. Lu J, Huang B, Esberg A, Johansson MJ, Byström AS (2005) The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. Rna 11: 1648–1654. 16244131

11. Jablonowski D, Zink S, Mehlgarten C, Daum G, 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. 16390459

12. Nandakumar J, Schwer B, Schaffrath R, Shuman S (2008) RNA repair: an antidote to cytotoxic eukaryal RNA damage. Mol Cell 31: 278–286. doi: 10.1016/j.molcel.2008.05.019 18657509

13. 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. doi: 10.1093/nar/gkq831 20855293

14. Meineke B, Kast A, Schwer B, Meinhardt F, Shuman S, et al. (2012) A fungal anticodon nuclease ribotoxin exploits a secondary cleavage site to evade tRNA repair. RNA 18: 1716–1724. doi: 10.1261/rna.034132.112 22836353

15. Klassen R, Meineke B, Kast A, Wünsche G, Krampe L, et al. (2013) A secondary cleavage site in tRNA prevents anticodon nuclease toxin resistance via RNA repair. Yeast 30: 230–230.

16. Paluszynski JP, Klassen R, Meinhardt F (2007) Pichia acaciae killer system: genetic analysis of toxin immunity. Appl Environ Microbiol 73: 4373–4378. 17483256

17. Tokunaga M, Wada N, Hishinuma F (1987) Expression and identification of immunity determinants on linear DNA killer plasmids pGKL1 and pGKL2 in Kluyveromyces lactis. Nucleic Acids Res 15: 1031–1046. 3029695

18. Satwika D, Klassen R, Meinhardt F (2012) Anticodon nuclease encoding virus-like elements in yeast. Appl Microbiol Biotechnol 96: 345–356. doi: 10.1007/s00253-012-4349-9 22899498

19. Kast A, Klassen R, Meinhardt F (2014) rRNA fragmentation induced by a yeast killer toxin. Mol Microbiol 91: 606–617. doi: 10.1111/mmi.12481 24308908

20. Klassen R, Kast A, Wünsche G, Paluszynski JP, Wemhoff S, et al. (2014) Immunity factors for two related tRNAGln targeting killer toxins distinguish cognate and non-cognate toxic subunits. Curr Genet 60: 213–222. doi: 10.1007/s00294-014-0426-1 24719080

21. Klassen R, Meinhardt F (2007) Linear protein-promed replicating plasmids in eukaryotic microbes. In: Meinhardt F, Klassen R, editors. Microbiology monographs Microbial linear plasmids. Berlin: Springer. pp. 187–226.

22. Gunge N, Sakaguchi K (1981) Intergeneric transfer of deoxyribonucleic acid killer plasmids, pGKl1 and pGKl2, from Kluyveromyces lactis into Saccharomyces cerevisiae by cell fusion. J Bacteriol 147: 155–160. 7016841

23. Proudfoot NJ (2011) Ending the message: poly(A) signals then and now. Genes Dev 25: 1770–1782. doi: 10.1101/gad.17268411 21896654

24. Wilson DW, Meacock PA (1988) Extranuclear gene expression in yeast: evidence for a plasmid-encoded RNA polymerase of unique structure. Nucleic Acids Res 16: 8097–8112. 3138657

25. Larsen M, Gunge N, Meinhardt F (1998) Kluyveromyces lactis killer plasmid pGKL2: evidence for a viral-like capping enzyme encoded by ORF3. Plasmid 40: 243–246. 9806862

26. Tiggemann M, Jeske S, Larsen M, Meinhardt F (2001) Kluyveromyces lactis cytoplasmic plasmid pGKL2: heterologous expression of Orf3p and proof of guanylyltransferase and mRNA-triphosphatase activities. Yeast 18: 815–825. 11427964

27. Meinhardt F, Wodara C, Larsen M, Schickel J (1994) A novel approach to express a heterologous gene on Kluyveromyces lactis linear killer plasmids: expression of the bacterial aph gene from a cytoplasmic promoter fragment without in-phase fusion to the plasmid open reading frame. Plasmid 32: 318–327. 7899517

28. Schickel J, Helmig C, Meinhardt F (1996) Kluyveromyces lactis killer system: analysis of cytoplasmic promoters of the linear plasmids. Nucleic Acids Res 24: 1879–1886. 8657569

29. Schaffrath R, Meinhardt F, Meacock PA (1996) Yeast killer plasmid pGKL2: molecular analysis of UCS5, a cytoplasmic promoter element essential for ORF5 gene function. Mol Gen Genet 250: 286–294. 8602143

30. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158–229. 17347522

31. Graber JH, Cantor CR, Mohr SC, Smith TF (1999) In silico detection of control signals: mRNA 3'-end-processing sequences in diverse species. Proc Natl Acad Sci U S A 96: 14055–14060. 10570197

32. Frank AC, Wolfe KH (2009) Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot Cell 8: 1521–1531. doi: 10.1128/EC.00110-09 19666779

33. Satwika D, Klassen R, Meinhardt F (2012) Repeated capture of a cytoplasmic linear plasmid by the host nucleus in Debaryomyces hansenii. Yeast 29: 145–154. doi: 10.1002/yea.2893 22434608

34. Butler AR, Porter M, Stark MJ (1991) Intracellular expression of Kluyveromyces lactis toxin gamma subunit mimics treatment with exogenous toxin and distinguishes two classes of toxin-resistant mutant. Yeast 7: 617–625. 1767590

35. Klassen R, Teichert S, Meinhardt F (2004) Novel yeast killer toxins provoke S-phase arrest and DNA damage checkpoint activation. Mol Microbiol 53: 263–273. 15225320

36. Guglielmini J, Van Melderen L (2011) Bacterial toxin-antitoxin systems: Translation inhibitors everywhere. Mob Genet Elements 1: 283–290. 22545240

37. Louis VL, Despons L, Friedrich A, Martin T, Durrens P, et al. (2012) Pichia sorbitophila, an interspecies yeast hybrid, reveals early steps of genome resolution after polyploidization. G3 (Bethesda) 2: 299–311. doi: 10.1534/g3.111.000745 22384408

38. Gietz RD, Schiestl RH, Willems AR, Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355–360. 7785336

39. Klassen R, Krampe S, Meinhardt F (2007) Homologous recombination and the yKu70/80 complex exert opposite roles in resistance against the killer toxin from Pichia acaciae. DNA Repair (Amst) 6: 1864–1875. 17765020

40. Scotto-Lavino E, Du G, Frohman MA (2006) 3' end cDNA amplification using classic RACE. Nat Protoc 1: 2742–2745. 17406530

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Genetika Reprodukčná medicína

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