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. 1992 Sep;132(1):87–96. doi: 10.1093/genetics/132.1.87

Mak10, a Glucose-Repressible Gene Necessary for Replication of a Dsrna Virus of Saccharomyces Cerevisiae, Has T Cell Receptor α-Subunit Motifs

Y J Lee 1, R B Wickner 1
PMCID: PMC1205132  PMID: 1398065

Abstract

The MAK10 gene is necessary for the propagation of the L-A dsRNA virus of the yeast Saccharomyces cerevisiae. We have isolated MAK10 from selected phage λ genomic DNA clones that map near MAK10. This gene encodes a 733-amino acid protein with several regions of similarity to T cell receptor α-subunit V (variable) regions. We show that MAK10 is essential for optimal growth on nonfermentable carbon sources independent of its effect on L-A. Although loss of L-A by mak10-1 mutants is partially suppressed by loss of the mitochondrial genome, no such suppression of a mak10::URA3 mutation was observed. Using MAK10-lacZ fusions we show that MAK10 is expressed at a very low level and that it is glucose repressed. The highest levels of expression were seen in tup1 and cyc8 mutants, known to be defective in glucose repression. These results suggest that the mitochondrial genome and L-A dsRNA compete for the MAK10 protein.

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Selected References

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  1. Becker D. M., Pattern P., Chien Y., Yokota T., Eshhar Z., Giedlin M., Gascoigne N. R., Goodnow C., Wolf R., Arai K. Variability and repertoire size of T-cell receptor V alpha gene segments. Nature. 1985 Oct 3;317(6036):430–434. doi: 10.1038/317430a0. [DOI] [PubMed] [Google Scholar]
  2. Bussey H. Proteases and the processing of precursors to secreted proteins in yeast. Yeast. 1988 Mar;4(1):17–26. doi: 10.1002/yea.320040103. [DOI] [PubMed] [Google Scholar]
  3. Carlson M., Osmond B. C., Neigeborn L., Botstein D. A suppressor of SNF1 mutations causes constitutive high-level invertase synthesis in yeast. Genetics. 1984 May;107(1):19–32. doi: 10.1093/genetics/107.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Dmochowska A., Dignard D., Henning D., Thomas D. Y., Bussey H. Yeast KEX1 gene encodes a putative protease with a carboxypeptidase B-like function involved in killer toxin and alpha-factor precursor processing. Cell. 1987 Aug 14;50(4):573–584. doi: 10.1016/0092-8674(87)90030-4. [DOI] [PubMed] [Google Scholar]
  6. Esteban R., Fujimura T., Wickner R. B. Internal and terminal cis-acting sites are necessary for in vitro replication of the L-A double-stranded RNA virus of yeast. EMBO J. 1989 Mar;8(3):947–954. doi: 10.1002/j.1460-2075.1989.tb03456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fujimura T., Esteban R., Esteban L. M., Wickner R. B. Portable encapsidation signal of the L-A double-stranded RNA virus of S. cerevisiae. Cell. 1990 Aug 24;62(4):819–828. doi: 10.1016/0092-8674(90)90125-x. [DOI] [PubMed] [Google Scholar]
  8. Fujimura T., Wickner R. B. L-A double-stranded RNA viruslike particle replication cycle in Saccharomyces cerevisiae: particle maturation in vitro and effects of mak10 and pet18 mutations. Mol Cell Biol. 1987 Jan;7(1):420–426. doi: 10.1128/mcb.7.1.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fujimura T., Wickner R. B. Reconstitution of template-dependent in vitro transcriptase activity of a yeast double-stranded RNA virus. J Biol Chem. 1989 Jun 25;264(18):10872–10877. [PubMed] [Google Scholar]
  10. Fujimura T., Wickner R. B. Replicase of L-A virus-like particles of Saccharomyces cerevisiae. In vitro conversion of exogenous L-A and M1 single-stranded RNAs to double-stranded form. J Biol Chem. 1988 Jan 5;263(1):454–460. [PubMed] [Google Scholar]
  11. Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Iwamoto A., Ohashi P. S., Pircher H., Walker C. L., Michalopoulos E. E., Rupp F., Hengartner H., Mak T. W. T cell receptor variable gene usage in a specific cytotoxic T cell response. Primary structure of the antigen-MHC receptor of four hapten-specific cytotoxic T cell clones. J Exp Med. 1987 Mar 1;165(3):591–600. doi: 10.1084/jem.165.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ju Q. D., Morrow B. E., Warner J. R. REB1, a yeast DNA-binding protein with many targets, is essential for growth and bears some resemblance to the oncogene myb. Mol Cell Biol. 1990 Oct;10(10):5226–5234. doi: 10.1128/mcb.10.10.5226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kimura N., Toyonaga B., Yoshikai Y., Du R. P., Mak T. W. Sequences and repertoire of the human T cell receptor alpha and beta chain variable region genes in thymocytes. Eur J Immunol. 1987 Mar;17(3):375–383. doi: 10.1002/eji.1830170312. [DOI] [PubMed] [Google Scholar]
  17. Liu Y. X., Dieckmann C. L. Overproduction of yeast viruslike particles by strains deficient in a mitochondrial nuclease. Mol Cell Biol. 1989 Aug;9(8):3323–3331. doi: 10.1128/mcb.9.8.3323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mukai Y., Harashima S., Oshima Y. AAR1/TUP1 protein, with a structure similar to that of the beta subunit of G proteins, is required for a1-alpha 2 and alpha 2 repression in cell type control of Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jul;11(7):3773–3779. doi: 10.1128/mcb.11.7.3773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nehlin J. O., Ronne H. Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J. 1990 Sep;9(9):2891–2898. doi: 10.1002/j.1460-2075.1990.tb07479.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Rothstein R. J., Sherman F. Genes affecting the expression of cytochrome c in yeast: genetic mapping and genetic interactions. Genetics. 1980 Apr;94(4):871–889. doi: 10.1093/genetics/94.4.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  25. Saito H., Kranz D. M., Takagaki Y., Hayday A. C., Eisen H. N., Tonegawa S. A third rearranged and expressed gene in a clone of cytotoxic T lymphocytes. Nature. 1984 Nov 1;312(5989):36–40. doi: 10.1038/312036a0. [DOI] [PubMed] [Google Scholar]
  26. Schuler G. D., Altschul S. F., Lipman D. J. A workbench for multiple alignment construction and analysis. Proteins. 1991;9(3):180–190. doi: 10.1002/prot.340090304. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Smeekens S. P., Avruch A. S., LaMendola J., Chan S. J., Steiner D. F. Identification of a cDNA encoding a second putative prohormone convertase related to PC2 in AtT20 cells and islets of Langerhans. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):340–344. doi: 10.1073/pnas.88.2.340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Smeekens S. P., Steiner D. F. Identification of a human insulinoma cDNA encoding a novel mammalian protein structurally related to the yeast dibasic processing protease Kex2. J Biol Chem. 1990 Feb 25;265(6):2997–3000. [PubMed] [Google Scholar]
  30. Somers J. M., Bevan E. A. The inheritance of the killer character in yeast. Genet Res. 1969 Feb;13(1):71–83. doi: 10.1017/s0016672300002743. [DOI] [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. Stark H. C., Fugit D., Mowshowitz D. B. Pleiotropic properties of a yeast mutant insensitive to catabolite repression. Genetics. 1980 Apr;94(4):921–928. doi: 10.1093/genetics/94.4.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sternberg N., Weisberg R. Packaging of coliphage lambda DNA. II. The role of the gene D protein. J Mol Biol. 1977 Dec 15;117(3):733–759. doi: 10.1016/0022-2836(77)90067-5. [DOI] [PubMed] [Google Scholar]
  34. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Toh-e A., Sahashi Y. The PET18 locus of Saccharomyces cerevisiae: a complex locus containing multiple genes. Yeast. 1985 Dec;1(2):159–171. doi: 10.1002/yea.320010204. [DOI] [PubMed] [Google Scholar]
  36. Trumbly R. J. Glucose repression in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1992 Jan;6(1):15–21. doi: 10.1111/j.1365-2958.1992.tb00832.x. [DOI] [PubMed] [Google Scholar]
  37. Trumbly R. J. Isolation of Saccharomyces cerevisiae mutants constitutive for invertase synthesis. J Bacteriol. 1986 Jun;166(3):1123–1127. doi: 10.1128/jb.166.3.1123-1127.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wickner R. B. Deletion of mitochondrial DNA bypassing a chromosomal gene needed for maintenance of the killer plasmid of yeast. Genetics. 1977 Nov;87(3):441–452. doi: 10.1093/genetics/87.3.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  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., Leibowitz M. J. Chromosomal genes essential for replication of a double-stranded RNA plasmid of Saccharomyces cerevisiae: the killer character of yeast. J Mol Biol. 1976 Aug 15;105(3):427–443. doi: 10.1016/0022-2836(76)90102-9. [DOI] [PubMed] [Google Scholar]
  42. Wickner R. B., Leibowitz M. J. Two chromosomal genes required for killing expression in killer strains of Saccharomyces cerevisiae. Genetics. 1976 Mar 25;82(3):429–442. doi: 10.1093/genetics/82.3.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wickner R. B. Mutants of Saccharomyces cerevisiae that incorporate deoxythymidine-5'-monophosphate into deoxyribonucleic acid in vivo. J Bacteriol. 1974 Jan;117(1):252–260. doi: 10.1128/jb.117.1.252-260.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wickner R. B., Toh-e A. [HOK], a new yeast non-Mendelian trait, enables a replication-defective killer plasmid to be maintained. Genetics. 1982 Feb;100(2):159–174. doi: 10.1093/genetics/100.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Williams F. E., Varanasi U., Trumbly R. J. The CYC8 and TUP1 proteins involved in glucose repression in Saccharomyces cerevisiae are associated in a protein complex. Mol Cell Biol. 1991 Jun;11(6):3307–3316. doi: 10.1128/mcb.11.6.3307. [DOI] [PMC free article] [PubMed] [Google Scholar]

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