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. 1995 May;177(10):2887–2891. doi: 10.1128/jb.177.10.2887-2891.1995

Translation and M1 double-stranded RNA propagation: MAK18 = RPL41B and cycloheximide curing.

K Carroll 1, R B Wickner 1
PMCID: PMC176963  PMID: 7751301

Abstract

MAK18 is one of nearly 30 chromosomal genes of Saccharomyces cerevisiae necessary for propagation of the killer toxin-encoding M1 double-stranded RNA satellite of the L-A double-stranded RNA virus. We have cloned and sequenced MAK18 and find that it is identical to RPL41B, one of the two genes encoding large ribosomal subunit protein L41. The mak18-1 mutant is deficient in 60S subunits, which we suggest results in a preferential decrease in translation of viral poly(A)-deficient mRNA. We have reexamined the curing of M1 by low concentrations of cycloheximide (G. R. Fink and C. A. Styles, Proc. Natl. Acad. Sci. USA 69:2846-2849, 1972), which is known to act on ribosomal large subunit protein L29. We find that when M1 is supported by L-A proteins made from the poly(A)+ mRNA of a cDNA clone of L-A, cycloheximide does not decrease the M1 copy number, consistent with our hypothesis.

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Selected References

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  1. Ball S. G., Tirtiaux C., Wickner R. B. Genetic Control of L-a and L-(Bc) Dsrna Copy Number in Killer Systems of SACCHAROMYCES CEREVISIAE. Genetics. 1984 Jun;107(2):199–217. doi: 10.1093/genetics/107.2.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bostian K. A., Sturgeon J. A., Tipper D. J. Encapsidation of yeast killer double-stranded ribonucleic acids: dependence of M on L. J Bacteriol. 1980 Jul;143(1):463–470. doi: 10.1128/jb.143.1.463-470.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bussey H. K1 killer toxin, a pore-forming protein from yeast. Mol Microbiol. 1991 Oct;5(10):2339–2343. doi: 10.1111/j.1365-2958.1991.tb02079.x. [DOI] [PubMed] [Google Scholar]
  5. Cheng R. H., Caston J. R., Wang G. J., Gu F., Smith T. J., Baker T. S., Bozarth R. F., Trus B. L., Cheng N., Wickner R. B. Fungal virus capsids, cytoplasmic compartments for the replication of double-stranded RNA, formed as icosahedral shells of asymmetric Gag dimers. J Mol Biol. 1994 Dec 2;244(3):255–258. doi: 10.1006/jmbi.1994.1726. [DOI] [PubMed] [Google Scholar]
  6. Cooper T. G., Bossinger J. Selective inhibition of protein synthesis initiation in Saccharomyces cerevisiae by low concentrations of cycloheximide. J Biol Chem. 1976 Nov 25;251(22):7278–7280. [PubMed] [Google Scholar]
  7. Deshmukh M., Tsay Y. F., Paulovich A. G., Woolford J. L., Jr Yeast ribosomal protein L1 is required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol Cell Biol. 1993 May;13(5):2835–2845. doi: 10.1128/mcb.13.5.2835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dinman J. D., Icho T., Wickner R. B. A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):174–178. doi: 10.1073/pnas.88.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dinman J. D., Wickner R. B. Translational maintenance of frame: mutants of Saccharomyces cerevisiae with altered -1 ribosomal frameshifting efficiencies. Genetics. 1994 Jan;136(1):75–86. doi: 10.1093/genetics/136.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erickson J. R., Johnston M. Direct cloning of yeast genes from an ordered set of lambda clones in Saccharomyces cerevisiae by recombination in vivo. Genetics. 1993 May;134(1):151–157. doi: 10.1093/genetics/134.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fink G. R., Styles C. A. Curing of a killer factor in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2846–2849. doi: 10.1073/pnas.69.10.2846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fried H. M., Fink G. R. Electron microscopic heteroduplex analysis of "killer" double-stranded RNA species from yeast. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4224–4228. doi: 10.1073/pnas.75.9.4224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fried H. M., Warner J. R. Molecular cloning and analysis of yeast gene for cycloheximide resistance and ribosomal protein L29. Nucleic Acids Res. 1982 May 25;10(10):3133–3148. doi: 10.1093/nar/10.10.3133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fujimura T., Wickner R. B. Gene overlap results in a viral protein having an RNA binding domain and a major coat protein domain. Cell. 1988 Nov 18;55(4):663–671. doi: 10.1016/0092-8674(88)90225-5. [DOI] [PubMed] [Google Scholar]
  15. Icho T., Wickner R. B. The MAK11 protein is essential for cell growth and replication of M double-stranded RNA and is apparently a membrane-associated protein. J Biol Chem. 1988 Jan 25;263(3):1467–1475. [PubMed] [Google Scholar]
  16. Icho T., Wickner R. B. The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames. J Biol Chem. 1989 Apr 25;264(12):6716–6723. [PubMed] [Google Scholar]
  17. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kawai S., Murao S., Mochizuki M., Shibuya I., Yano K., Takagi M. Drastic alteration of cycloheximide sensitivity by substitution of one amino acid in the L41 ribosomal protein of yeasts. J Bacteriol. 1992 Jan;174(1):254–262. doi: 10.1128/jb.174.1.254-262.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lee Y. J., Wickner R. B. MAK10, a glucose-repressible gene necessary for replication of a dsRNA virus of Saccharomyces cerevisiae, has T cell receptor alpha-subunit motifs. Genetics. 1992 Sep;132(1):87–96. doi: 10.1093/genetics/132.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Masison D. C., Blanc A., Ribas J. C., Carroll K., Sonenberg N., Wickner R. B. Decoying the cap- mRNA degradation system by a double-stranded RNA virus and poly(A)- mRNA surveillance by a yeast antiviral system. Mol Cell Biol. 1995 May;15(5):2763–2771. doi: 10.1128/mcb.15.5.2763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Munroe D., Jacobson A. Tales of poly(A): a review. Gene. 1990 Jul 16;91(2):151–158. doi: 10.1016/0378-1119(90)90082-3. [DOI] [PubMed] [Google Scholar]
  22. Nam H. G., Fried H. M. Effects of progressive depletion of TCM1 or CYH2 mRNA on Saccharomyces cerevisiae ribosomal protein accumulation. Mol Cell Biol. 1986 May;6(5):1535–1544. doi: 10.1128/mcb.6.5.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ohtake Y., Wickner R. B. Yeast virus propagation depends critically on free 60S ribosomal subunit concentration. Mol Cell Biol. 1995 May;15(5):2772–2781. doi: 10.1128/mcb.15.5.2772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Olson M. V., Dutchik J. E., Graham M. Y., Brodeur G. M., Helms C., Frank M., MacCollin M., Scheinman R., Frank T. Random-clone strategy for genomic restriction mapping in yeast. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7826–7830. doi: 10.1073/pnas.83.20.7826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ridley S. P., Sommer S. S., Wickner R. B. Superkiller mutations in Saccharomyces cerevisiae suppress exclusion of M2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN. Mol Cell Biol. 1984 Apr;4(4):761–770. doi: 10.1128/mcb.4.4.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Riles L., Dutchik J. E., Baktha A., McCauley B. K., Thayer E. C., Leckie M. P., Braden V. V., Depke J. E., Olson M. V. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs. Genetics. 1993 May;134(1):81–150. doi: 10.1093/genetics/134.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rotenberg M. O., Moritz M., Woolford J. L., Jr Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of half-mer polyribosomes. Genes Dev. 1988 Feb;2(2):160–172. doi: 10.1101/gad.2.2.160. [DOI] [PubMed] [Google Scholar]
  28. Sachs A. B., Davis R. W. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell. 1989 Sep 8;58(5):857–867. doi: 10.1016/0092-8674(89)90938-0. [DOI] [PubMed] [Google Scholar]
  29. Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. doi: 10.1016/0076-6879(91)94004-v. [DOI] [PubMed] [Google Scholar]
  30. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sommer S. S., Wickner R. B. Yeast L dsRNA consists of at least three distinct RNAs; evidence that the non-Mendelian genes [HOK], [NEX] and [EXL] are on one of these dsRNAs. Cell. 1982 Dec;31(2 Pt 1):429–441. doi: 10.1016/0092-8674(82)90136-2. [DOI] [PubMed] [Google Scholar]
  32. Tercero J. C., Wickner R. B. MAK3 encodes an N-acetyltransferase whose modification of the L-A gag NH2 terminus is necessary for virus particle assembly. J Biol Chem. 1992 Oct 5;267(28):20277–20281. [PubMed] [Google Scholar]
  33. Thrash C., Voelkel K., DiNardo S., Sternglanz R. Identification of Saccharomyces cerevisiae mutants deficient in DNA topoisomerase I activity. J Biol Chem. 1984 Feb 10;259(3):1375–1377. [PubMed] [Google Scholar]
  34. Toh-E A., Guerry P., Wickner R. B. Chromosomal superkiller mutants of Saccharomyces cerevisiae. J Bacteriol. 1978 Dec;136(3):1002–1007. doi: 10.1128/jb.136.3.1002-1007.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Toh-E A., Wickner R. B. "Superkiller" mutations suppress chromosomal mutations affecting double-stranded RNA killer plasmid replication in saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jan;77(1):527–530. doi: 10.1073/pnas.77.1.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Valle R. P., Wickner R. B. Elimination of L-A double-stranded RNA virus of Saccharomyces cerevisiae by expression of gag and gag-pol from an L-A cDNA clone. J Virol. 1993 May;67(5):2764–2771. doi: 10.1128/jvi.67.5.2764-2771.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wickner R. B. Double-stranded RNA virus replication and packaging. J Biol Chem. 1993 Feb 25;268(6):3797–3800. [PubMed] [Google Scholar]
  38. Wickner R. B. Double-stranded and single-stranded RNA viruses of Saccharomyces cerevisiae. Annu Rev Microbiol. 1992;46:347–375. doi: 10.1146/annurev.mi.46.100192.002023. [DOI] [PubMed] [Google Scholar]
  39. Wickner R. B. Host function of MAK16: G1 arrest by a mak16 mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6007–6011. doi: 10.1073/pnas.85.16.6007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wickner R. B., Icho T., Fujimura T., Widner W. R. Expression of yeast L-A double-stranded RNA virus proteins produces derepressed replication: a ski- phenocopy. J Virol. 1991 Jan;65(1):155–161. doi: 10.1128/jvi.65.1.155-161.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wickner R. B. Mapping chromosomal genes of Saccharomyces cerevisiae using an improved genetic mapping method. Genetics. 1979 Jul;92(3):803–821. doi: 10.1093/genetics/92.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wickner R. B., Ridley S. P., Fried H. M., Ball S. G. Ribosomal protein L3 is involved in replication or maintenance of the killer double-stranded RNA genome of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4706–4708. doi: 10.1073/pnas.79.15.4706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Widner W. R., Wickner R. B. Evidence that the SKI antiviral system of Saccharomyces cerevisiae acts by blocking expression of viral mRNA. Mol Cell Biol. 1993 Jul;13(7):4331–4341. doi: 10.1128/mcb.13.7.4331. [DOI] [PMC free article] [PubMed] [Google Scholar]

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