Skip to main content
SpringerLink
Log in

Role of Proteins Interacting with the eRF1 and eRF3 Release Factors in the Regulation of Translation and Prionization

  • REVIEWS
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

The review discusses the role that proteins interacting with the translation termination factors eRF1 and eRF3 play in the control of protein synthesis and prionization. These proteins interact not only with each other, but also with many other proteins involved in controlling the efficiency of translation termination, and associate translation termination with other cell processes. The termination of translation is directly related not only to translation re-initiation and ribosome recycling, but also to mRNA stability and protein quality control. This connection is ensured by the interaction of eRF1 and eRF3 with proteins participating in various cell metabolic processes, such as mRNA transport from the nucleus into the cytoplasm (Dbp5/DDX19 and Gle1), ribosome recycling (Rli1/ABCE1), mRNA degradation (Upf proteins), and translation initiation (Pab1/PABP). In addition to genetic control, there is epigenetic control of translation termination. This mechanism is associated with prion polymerization of the Sup35 protein to form the [PSI+] prion. The maintenance of the [PSI+] prion, like other yeast prions, requires the operation of a system of molecular chaperones and protein sorting factors. The review considers in detail the interaction of the translation termination factors with proteins involved in various cellular processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Inge-Vechtomov S., Zhouravleva G., Philippe M. 2003. Eukaryotic release factors (eRFs) history. Biol. Cell. 95, 195–209.

    Article  CAS  PubMed  Google Scholar 

  2. Patino M.M., Liu J.J., Glover J.R., Lindquist S. 1996. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science. 273, 622–626.

    Article  CAS  PubMed  Google Scholar 

  3. Paushkin S.V., Kushnirov V.V., Smirnov V.N., Ter-Avanesyan M.D. 1996. Propagation of the yeast prion-like [PSI +] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15, 3127–3134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Glover J.R., Kowal A.S., Schirmer E.C., Patino M.M., Liu J.J., Lindquist S. 1997. Self-seeded fibers formed by Sup35, the protein determinant of [PSI +], a heritable prion-like factor of S. cerevisiae. Cell. 89, 811–819.

    Article  CAS  PubMed  Google Scholar 

  5. King C.Y., Tittmann P., Gross H., Gebert R., Aebi M., Wüthrich K. 1997. Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc. Natl. Acad. Sci. U. S. A. 94, 6618–6622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Liebman S.W., Chernoff Y.O. 2012. Prions in yeast. Genetics. 191, 1041–1072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Stansfield I., Jones K.M., Kushnirov V.V., Dagkesamanskaya A.R., Poznyakovski A.I., Paushkin S.V., Nierras C.R., Cox B.S., Ter-Avanesyan M.D., Tuite M.F. 1995. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14, 4365–4373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhouravleva G., Frolova L., Le Goff X., Le Guellec R., Inge-Vechtomov S., Kisselev L., Philippe M. 1995. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 14, 4065–4072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Doma M.K., Parker R. 2006. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature. 440, 561–564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cheng Z., Saito K., Pisarev A.V., Wada M., Pisareva V.P., Pestova T.V., Gajda M., Round A., Kong C., Lim M., Nakamura Y., Svergun D.I., Ito K., Song H. 2009. Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev. 23, 1106–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chen L., Muhlrad D., Hauryliuk V., Cheng Z., Lim M.K., Shyp V., Parker R., Song H. 2010. Structure of the Dom34-Hbs1 complex and implications for no-go decay. Nat. Struct. Mol. Biol. 17, 1233–1240.

    Article  CAS  PubMed  Google Scholar 

  12. Becker T., Armache J.-P., Jarasch A., Anger A.M., Villa E., Sieber H., Motaal B.A., Mielke T., Berninghausen O., Beckmann R. 2011. Structure of the no-go mRNA decay complex Dom34–Hbs1 bound to a stalled 80S ribosome. Nat. Struct. Mol. Biol. 18, 715–720.

    Article  CAS  PubMed  Google Scholar 

  13. Frolova L., Le Goff X., Rasmussen H.H., Cheperegin S., Drugeon G., Kress M., Arman I., Haenni A.L., Celis J.E., Philippe M. 1994. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature. 372, 701–703.

    Article  CAS  PubMed  Google Scholar 

  14. Song H., Mugnier P., Das A.K., Webb H.M., Evans D.R., Tuite M.F., Hemmings B.A., Barford D. 2000. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell. 100, 311–321.

    Article  CAS  PubMed  Google Scholar 

  15. Ito K. 1996. Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: tRNA-protein mimicry hypothesis. Proc. Natl. Acad. Sci. U. S. A. 93, 5443–5448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hellen C.U.T. 2018. Translation termination and ribosome recycling in eukaryotes. Cold Spring Harb. Perspect. Biol. 10, a032656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Mantsyzov A.B., Ivanova E.V., Birdsall B., Kolosov P.M., Kisselev L.L., Polshakov V.I. 2007. NMR assignments of the C-terminal domain of human polypeptide release factor eRF1. Biomol. NMR Assign. 1, 183–185.

    Article  CAS  PubMed  Google Scholar 

  18. Frolova L.Y., Tsivkovskii R.Y., Sivolobova G.F., Oparina N.Y., Serpinsky O.I., Blinov V.M., Tatkov S.I., Kisselev L.L. 1999. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA. 5, 1014–1020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ito K., Ebihara K., Nakamura Y. 1998. The stretch of C-terminal acidic amino acids of translational release factor eRF1 is a primary binding site for eRF3 of fission yeast. RNA. 4, 958–972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Merkulova T.I., Frolova L.Y., Lazar M., Camonis J., Kisselev L.L. 1999. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett. 443, 41–47.

    Article  CAS  PubMed  Google Scholar 

  21. Moskalenko S.E., Chabelskaya S.V., Inge-Vechtomov S.G., Philippe M., Zhouravleva G.A. 2003. Viable nonsense mutants for the essential gene SUP45 of Saccharomyces cerevisiae. BMC Mol. Biol. 4, 2.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Eurwilaichitr L., Graves F.M., Stansfield I., Tuite M.F. 1999. The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Mol. Microbiol. 32, 485–496.

    Article  CAS  PubMed  Google Scholar 

  23. Andjelković N., Zolnierowicz S., Van Hoof C., Goris J., Hemmings B.A. 1996. The catalytic subunit of protein phosphatase 2A associates with the translation termination factor eRF1. EMBO J. 15, 7156–7167.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kononenko A.V., Mitkevich V.A., Dubovaya V.I., Kolosov P.M., Makarov A.A., Kisselev L.L. 2008. Role of the individual domains of translation termination factor eRF1 in GTP binding to eRF3. Proteins. 70, 388–393.

    Article  CAS  PubMed  Google Scholar 

  25. Mitkevich V.A., Kononenko A.V., Petrushanko I.Y., Yanvarev D.V., Makarov A.A., Kisselev L.L. 2006. Termination of translation in eukaryotes is mediated by the quaternary eRF1*eRF3*GTP*Mg2+ complex. The biological roles of eRF3 and prokaryotic RF3 are profoundly distinct. Nucleic Acids Res. 34, 3947–3954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Alkalaeva E.Z., Pisarev A.V., Frolova L.Y., Kisselev L.L., Pestova T.V. 2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell. 125, 1125–1136.

    Article  CAS  PubMed  Google Scholar 

  27. Hauryliuk V., Zavialov A., Kisselev L., Ehrenberg M. 2006. Class-1 release factor eRF1 promotes GTP binding by class-2 release factor eRF3. Biochimie. 88, 747–757.

    Article  CAS  PubMed  Google Scholar 

  28. Frolova L., Le Goff X., Zhouravleva G., Davydova E., Philippe M., Kisselev L. 1996. Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA. 2, 334–341.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Pisareva V.P., Pisarev A.V., Hellen C.U.T., Rodnina M.V., Pestova T.V. 2006. Kinetic analysis of interaction of eukaryotic release factor 3 with guanine nucleotides. J. Biol. Chem. 281, 40224–40235.

    Article  CAS  PubMed  Google Scholar 

  30. Hoshino S., Imai M., Mizutani M., Kikuchi Y., Hanaoka F., Ui M., Katada T. 1998. Molecular cloning of a novel member of the eukaryotic polypeptide chain-releasing factors (eRF). J. Biol. Chem. 273, 22254–22259.

    Article  CAS  PubMed  Google Scholar 

  31. Zhouravleva G., Schepachev V., Petrova A., Tarasov O., Inge-Vechtomov S. 2006. Evolution of translation termination factor eRF3: is GSPT2 generated by retrotransposition of GSPT1’s mRNA? IUBMB Life. 58, 199–202.

    Article  CAS  PubMed  Google Scholar 

  32. Kushnirov V.V., Ter-Avanesyan M.D., Telckov M.V., Surguchov A.P., Smirnov V.N., Inge-Vechtomov S.G. 1988. Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene. 66, 45–54.

    Article  CAS  PubMed  Google Scholar 

  33. Cosson B., Couturier A., Chabelskaya S., Kiktev D., Inge-Vechtomov S., Philippe M., Zhouravleva G. 2002. Poly(A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI +] propagation. Mol. Cell. Biol. 22, 3301–3315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Urakov V.N., Mitkevich O.V., Safenkova I.V., Ter-Avanesyan M.D. 2017. Ribosome-bound Pub1 modulates stop codon decoding during translation termination in yeast. FEBS J. 284, 1914–1930.

    Article  CAS  PubMed  Google Scholar 

  35. Paushkin S.V., Kushnirov V.V., Smirnov V.N., Ter-Avanesyan M.D. 1997. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: Implications for prion-dependent regulation. Mol. Cell. Biol. 17, 2798–2805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kong C., Ito K., Walsh M.A., Wada M., Liu Y., Kumar S., Barford D., Nakamura Y., Song H. 2004. Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe. Mol. Cell. 14, 233–234.

    Article  CAS  PubMed  Google Scholar 

  37. des Georges A., Hashem Y., Unbehaun A., Grassucci R.A., Taylor D., Hellen C.U.T., Pestova T.V., Frank J. 2014. Structure of the mammalian ribosomal pre-termination complex associated with eRF1.eRF3.GDPNP. Nucleic Acids Res. 42, 3409–3418.

    Article  CAS  PubMed  Google Scholar 

  38. Taylor D., Unbehaun A., Li W., Das S., Lei J., Liao H.Y., Grassucci R.A., Pestova T.V., Frank J. 2012. Cryo-EM structure of the mammalian eukaryotic release factor eRF1–eRF3-associated termination complex. Proc. Natl. Acad. Sci. U. S. A. 109, 18413–18418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Culbertson M.R., Underbrink K.M., Fink G.R. 1980. Frameshift suppression Saccharomyces cerevisiae: 2. Genetic properties of group II suppressors. Genetics. 95, 833–853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Leeds P., Peltz S.W., Jacobson A., Culbertson M.R. 1991. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5, 2303–2314.

    Article  CAS  PubMed  Google Scholar 

  41. Leeds P., Wood J.M., Lee B.S., Culbertson M.R. 1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 2165–2177.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Pulak R., Anderson P. 1993. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7, 1885–1897.

    Article  CAS  PubMed  Google Scholar 

  43. Cali B.M., Anderson P. 1998. mRNA surveillance mitigates genetic dominance in Caenorhabditis elegans. Mol. Gen. Genet. 260, 176–184.

    Article  CAS  PubMed  Google Scholar 

  44. Page M.F., Carr B., Anders K.R., Grimson A., Anderson P. 1999. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19, 5943–5951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Aronoff R., Baran R., Hodgkin J. 2001. Molecular identification of smg-4, required for mRNA surveillance in C. elegans. Gene. 268, 153–164.

    Article  CAS  PubMed  Google Scholar 

  46. Kashima I., Yamashita A., Izumi N., Kataoka N., Morishita R., Hoshino S., Ohno M., Dreyfuss G., Ohno S. 2006. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 20, 355–367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lloyd J.P.B., Davies B. 2013. SMG1 is an ancient nonsense-mediated mRNA decay effector. Plant J. 76, 800–810.

    Article  CAS  PubMed  Google Scholar 

  48. Causier B., Li Z., De Smet R., Lloyd J.P.B., Van de Peer Y., Davies B. 2017. Conservation of nonsense-mediated mRNA decay complex components throughout eukaryotic evolution. Sci. Rep. 7, 16692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lloyd J.P.B. 2018. The evolution and diversity of the nonsense-mediated mRNA decay pathway. F1000Research. 7, 1299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Culbertson M.R., Leeds P.F. 2003. Looking at mRNA decay pathways through the window of molecular evolution. Curr. Opin. Genet. Dev. 13, 207–214.

    Article  CAS  PubMed  Google Scholar 

  51. Atkin A.L., Schenkman L.R., Eastham M., Dahlseid J.N., Lelivelt M.J., Culbertson M.R. 1997. Relationship between yeast polyribosomes and Upf proteins required for nonsense mRNA decay. J. Biol. Chem. 272, 22163–22172.

    Article  CAS  PubMed  Google Scholar 

  52. Altamura N., Groudinsky O., Dujardin G., Slonimski P.P. 1992. NAM7 nuclear gene encodes a novel member of a family of helicases with a Zn-ligand motif and is involved in mitochondrial functions in Saccharomyces cerevisiae. J. Mol. Biol. 224, 575–587.

    Article  CAS  PubMed  Google Scholar 

  53. Weng Y., Czaplinski K., Peltz S.W. 1996. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol. 16, 5477–5490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Johansson M.J.O., Jacobson A. 2010. Nonsense-mediated mRNA decay maintains translational fidelity by limiting magnesium uptake. Genes Dev. 24, 1491–1495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. He F., Jacobson A. 1995. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9, 437–454.

    Article  CAS  PubMed  Google Scholar 

  56. He F., Brown A.H., Jacobson A. 1997. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 17, 1580–1594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Weng Y., Czaplinski K., Peltz S.W. 1996. Identification and characterization of mutations in the UPF1 gene that affect nonsense suppression and the formation of the Upf protein complex but not mRNA turnover. Mol. Cell. Biol. 16, 5491–5506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Czaplinski K., Ruiz-Echevarria M.J., Paushkin S. V, Han X., Weng Y., Perlick H.A., Dietz H.C., Ter-Avanesyan M.D., Peltz S.W. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12, 1665–1677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ivanov P.V., Gehring N.H., Kunz J.B., Hentze M.W., Kulozik A.E. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27, 736–747.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhouravleva G.A., Gryzina V.A. 2012. Influence of UPF genes on severity of SUP45 mutations.Mol. Biol. (Moscow). 46 (2), 258–269.

    Article  CAS  Google Scholar 

  61. Wang W., Czaplinski K., Rao Y., Peltz S.W. 2001. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J. 20, 880–890.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Serdar L.D., Whiteside D.L., Baker K.E. 2016. ATP hydrolysis by UPF1 is required for efficient translation termination at premature stop codons. Nat. Commun. 7, 14021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Schuller A.P., Zinshteyn B., Enam S.U., Green R. 2018. Directed hydroxyl radical probing reveals Upf1 binding to the 80S ribosomal E site rRNA at the L1 stalk. Nucleic Acids Res. 46, 2060–2073.

    Article  CAS  PubMed  Google Scholar 

  64. Neu-Yilik G., Raimondeau E., Eliseev B., Yeramala L., Amthor B., Deniaud A., Huard K., Kerschgens K., Hentze M.W., Schaffitzel C., Kulozik A.E. 2017. Dual function of UPF3B in early and late translation termination. EMBO J. 36, 2968–2986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kadlec J., Guilligay D., Ravelli R.B., Cusack S. 2006. Crystal structure of the UPF2-interacting domain of nonsense-mediated mRNA decay factor UPF1. RNA. 12, 1817–1824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kim Y.K., Maquat L.E. 2019. UPFront and center in RNA decay: UPF1 in nonsense-mediated mRNA decay and beyond. RNA. 25, 407–422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Min E.E., Roy B., Amrani N., He F., Jacobson A. 2013. Yeast Upf1 CH domain interacts with Rps26 of the 40S ribosomal subunit. RNA. 19, 1105–1115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cui Y., Hagan K.W., Zhang S., Peltz S.W. 1995. Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes Dev. 9, 423–436.

    Article  CAS  PubMed  Google Scholar 

  69. Mendell J.T., Medghalchi S.M., Lake R.G., Noensie E.N., Dietz H.C. 2000. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20, 8944–8957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Fourati Z., Roy B., Millan C., Coureux P.-D., Kervestin S., van Tilbeurgh H., He F., Usón I., Jacobson A., Graille M. 2014. A highly conserved region essential for NMD in the Upf2 N-terminal domain. J. Mol. Biol. 426, 3689–3702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. He F., Brown A.H., Jacobson A. 1996. Interaction between Nmd2p and Upf1p is required for activity but not for dominant-negative inhibition of the nonsense-mediated mRNA decay pathway in yeast. RNA. 2, 153–170.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. López-Perrote A., Castaño R., Melero R., Zamarro T., Kurosawa H., Ohnishi T., Uchiyama A., Aoyagi K., Buchwald G., Kataoka N., Yamashita A., Llorca O. 2016. Human nonsense-mediated mRNA decay factor UPF2 interacts directly with eRF3 and the SURF complex. Nucleic Acids Res. 44, 1909–1923.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Lykke-Andersen J., Shu M.D., Steitz J.A. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell. 103, 1121–1131.

    Article  CAS  PubMed  Google Scholar 

  74. Shirley R.L., Lelivelt M.J., Schenkman L.R., Dahlseid J.N., Culbertson M.R. 1998. A factor required for nonsense-mediated mRNA decay in yeast is exported from the nucleus to the cytoplasm by a nuclear export signal sequence. J. Cell Sci. 111, 3129–3143.

    Article  CAS  PubMed  Google Scholar 

  75. Shirley R.L., Ford A.S., Richards M.R., Albertini M., Culbertson M.R. 2002. Nuclear import of Upf3p is mediated by importin-alpha/-beta and export to the cytoplasm is required for a functional nonsense-mediated mRNA decay pathway in yeast. Genetics. 161, 1465–1482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chabelskaya S., Kiktev D., Inge-Vechtomov S., Philippe M., Zhouravleva G. 2004. Nonsense mutations in the essential gene SUP35 of Saccharomyces cerevisiae are non-lethal. Mol. Genet. Genomics. 272, 297–307.

    Article  CAS  PubMed  Google Scholar 

  77. Chabelskaya S., Gryzina V., Moskalenko S., Le Goff C., Zhouravleva G. 2007. Inactivation of NMD increases viability of sup45 nonsense mutants in Saccharomyces cerevisiae. BMC Mol. Biol. 8, 71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Chabelskaya S.V., Zhouravleva G.A. 2010. Mutations in the SUP35 gene impair nonsense-mediated mRNA decay. Mol Biol (Moscow). 44 (1), 45–53.

    Article  CAS  Google Scholar 

  79. Chamieh H., Ballut L., Bonneau F., Le Hir H. 2008. NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat. Struct. Mol. Biol. 15, 85–93.

    Article  CAS  PubMed  Google Scholar 

  80. Blobel G. 1973. A protein of molecular weight 78,000 bound to the polyadenylate region of eukaryotic messenger RNAs. Proc. Natl. Acad. Sci. U. S. A. 70, 924–928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Adam S.A., Nakagawa T., Swanson M.S., Woodruff T.K., Dreyfuss G. 1986. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol. 6, 2932–2943.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Sachs A.B., Bond M.W., Kornberg R.D. 1986. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: Domain structure and expression. Cell. 45, 827–835.

    Article  CAS  PubMed  Google Scholar 

  83. Mangus D.A., Evans M.C., Jacobson A. 2003. Poly(A)-binding proteins: Multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4, 223.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Kühn U., Wahle E. 2004. Structure and function of poly(A)-binding proteins. Biochim. Biophys. Acta. 1678, 67–84.

    Article  CAS  PubMed  Google Scholar 

  85. Sachs A.B., Davis R.W., Kornberg R.D. 1987. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol. Cell. Biol. 7, 3268–3276.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Kozlov G., Siddiqui N., Coillet-Matillon S., Trempe J.-F., Ekiel I., Sprules T., Gehring K. 2002. Solution structure of the orphan PABC domain from Saccharomyces cerevisiae poly(A)-binding protein. J. Biol. Chem. 277, 22822–22828.

    Article  CAS  PubMed  Google Scholar 

  87. Tarun S.Z., Sachs A.B. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15, 7168–7177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wells S.E., Hillner P.E., Vale R.D., Sachs A.B. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell. 2, 135–140.

    Article  CAS  PubMed  Google Scholar 

  89. Sachs A.B., Davis R.W. 1989. The poly(A)-binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell. 58, 857–867.

    Article  CAS  PubMed  Google Scholar 

  90. Munroe D., Jacobson A. 1990. mRNA poly(A) tail, a 3′-enhancer of translational initiation. Mol. Cell. Biol. 10, 3441–3455.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Gallie D.R. 1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5, 2108–2116.

    Article  CAS  PubMed  Google Scholar 

  92. Tarun S.Z., Wells S.E., Deardorff J.A., Sachs A.B. 1997. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. U. S. A. 94, 9046–9051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Imataka H., Gradi A., Sonenberg N. 1998. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17, 7480–7489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kessler S.H., Sachs A.B. 1998. RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 18, 51–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Otero L.J., Ashe M.P., Sachs A.B. 1999. The yeast poly(A)-binding protein Pab1p stimulates in vitro poly(A)-dependent and cap-dependent translation by distinct mechanisms. EMBO J. 18, 3153–3163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Richardson R., Denis C.L., Zhang C., Nielsen M.E.O., Chiang Y.-C., Kierkegaard M., Wang X., Lee D.J., Andersen J.S., Yao G. 2012. Mass spectrometric identification of proteins that interact through specific domains of the poly(A)-binding protein. Mol. Genet. Genomics. 287, 711–730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Hoshino S., Imai M., Kobayashi T., Uchida N., Katada T. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3'-Poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J. Biol. Chem. 274, 16677–16680.

    Article  CAS  PubMed  Google Scholar 

  98. Cosson B., Couturier A., Le Guellec R., Moreau J., Chabelskaya S., Zhouravleva G., Philippe M. 2002. Characterization of the poly(A) binding proteins expressed during oogenesis and early development of Xenopus laevis. Biol. Cell. 94, 217–231.

    Article  CAS  PubMed  Google Scholar 

  99. Cosson B., Berkova N., Couturier A., Chabelskaya S., Philippe M., Zhouravleva G. 2002. Poly(A)-binding protein and eRF3 are associated in vivo in human and Xenopus cells. Biol. Cell. 94, 205–216.

    Article  CAS  PubMed  Google Scholar 

  100. Uchida N., Hoshino S.-I., Imataka H., Sonenberg N., Katada T. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in cap/poly(A)-dependent translation. J. Biol. Chem. 277, 50286–50292.

    Article  CAS  PubMed  Google Scholar 

  101. Ivanov A., Mikhailova T., Eliseev B., Yeramala L., Sokolova E., Susorov D., Shuvalov A., Schaffitzel C., Alkalaeva. E. 2016. PABP enhances release factor recruitment and stop codon recognition during translation termination. Nucleic Acids Res. 44, 7766–7776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Albrecht M., Lengauer T. 2004. Survey on the PABC recognition motif PAM2. Biochem. Biophys. Res. Commun. 316, 129–138.

    Article  CAS  PubMed  Google Scholar 

  103. Brito M., Malta-Vacas J., Carmona B., Aires C., Costa P., Martins A.P., Ramos S., Conde A.R., Monteiro C. 2005. Polyglycine expansions in eRF3/GSPT1 are associated with gastric cancer susceptibility. Carcinogenesis. 26, 2046–2049.

    Article  CAS  PubMed  Google Scholar 

  104. Malta-Vacas J., Chauvin C., Gonçalves L., Nazaré A., Carvalho C., Monteiro C., Bagrel D., Jean-Jean O., Brito M. 2009. eRF3a/GSPT1 12-GGC allele increases the susceptibility for breast cancer development. Oncol. Rep. 21, 1551–1558.

    CAS  PubMed  Google Scholar 

  105. Miri M., Hemati S., Safari F., Tavassoli M. 2012. GGCn polymorphism of eRF3a/GSPT1 gene and breast cancer susceptibility. Med. Oncol. 29, 1581–1585.

    Article  CAS  PubMed  Google Scholar 

  106. Jerbi S., Jolles B., Bouceba T., Jean-Jean O. 2016. Studies on human eRF3–PABP interaction reveal the influence of eRF3a N-terminal glycin repeat on eRF3-PABP binding affinity and the lower affinity of eRF3a 12-GGC allele involved in cancer susceptibility. RNA Biol. 13, 306–315.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Kozlov G., Trempe J.F., Khaleghpour K., Kahvejian A., Ekiel I., Gehring K. 2001. Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl. Acad. Sci. U. S. A. 98, 4409–4413.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Xie J., Kozlov G., Gehring K. 2014. The “tale” of poly(A) binding protein: The MLLE domain and PAM2-containing proteins. Biochim. Biophys. Acta. 1839, 1062–1068.

    Article  CAS  PubMed  Google Scholar 

  109. Kozlov G., De Crescenzo G., Lim N.S., Siddiqui N., Fantus D., Kahvejian A., Trempe J-F., Elias D., Ekiel I., Sonenberg N., O’Connor-McCourt M., Gehring K. 2004. Structural basis of ligand recognition by PABC, a highly specific peptide-binding domain found in poly(A)-binding protein and a HECT ubiquitin ligase. EMBO J. 23, 272–281.

    Article  CAS  PubMed  Google Scholar 

  110. Kononenko A.V., Mitkevich V.A., Atkinson G.C., Tenson T., Dubovaya V.I., Frolova L.Y., Makarov A.A., Hauryliuk V. 2010. GTP-dependent structural rearrangement of the eRF1:eRF3 complex and eRF3 sequence motifs essential for PABP binding. Nucleic Acids Res. 38, 548–558.

    Article  CAS  PubMed  Google Scholar 

  111. Kozlov G., Gehring K. 2010. Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS One. 5, e10169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Hegde R., Srinivasula S.M., Datta P., Madesh M., Wassell R., Zhang Z., Cheong N., Nejmeh J., Fernandes-Alnemri T.,Hoshino S., Alnemri E.S. 2003. The polypeptide chain-releasing factor GSPT1/eRF3 is proteolytically processed into an IAP-binding protein. J. Biol. Chem. 278, 38699–38706.

    Article  CAS  PubMed  Google Scholar 

  113. Hosoda N., Kobayashi T., Uchida N., Funakoshi Y., Kikuchi Y., Hoshino S., Katada T. 2003. Translation termination factor eRF3 mediates mRNA decay through the regulation of deadenylation. J. Biol. Chem. 278, 38287–38291.

    Article  CAS  PubMed  Google Scholar 

  114. Funakoshi Y., Doi Y., Hosoda N., Uchida N., Osawa M., Shimada I., Tsujimoto M., Suzuki T., Katada T., Hoshino S. 2007. Mechanism of mRNA deadenylation: Evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev. 21, 3135–3148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Osawa M., Hosoda N., Nakanishi T., Uchida N., Kimura T., Imai S., Machiyama A., Katada T., Hoshino S., Shimada I. 2012. Biological role of the two overlapping poly(A)-binding protein interacting motifs 2 (PAM2) of eukaryotic releasing factor eRF3 in mRNA decay. RNA. 18, 1957–1967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Mangus D.A., Evans M.C., Agrin N.S., Smith M., Gongidi P., Jacobson A. 2004. Positive and negative regulation of poly(A) nuclease. Mol. Cell. Biol. 24, 5521–5533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Ivanov A., Shuvalova E., Egorova T., Shuvalov A., Sokolova E., Bizyaev N., Shatsky I., Terenin I., Alkalaeva E. 2019. Polyadenylate–binding protein–interacting proteins PAIP1 and PAIP2 affect translation termination. J. Biol. Chem. 294, 8630–8639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Geourjon C., Deléage G. 1994. SOPM: A self-optimized method for protein secondary structure prediction. Protein Eng. 7, 157–164.

    Article  CAS  PubMed  Google Scholar 

  119. Pisarev A.V., Skabkin M.A., Pisareva V.P., Skabkina O.V., Rakotondrafara A.M., Hentze M.W., Hellen C.U.T., Pestova T.V. 2010. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell. 37, 196–210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Shoemaker C.J., Green R. 2011. Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proc. Natl. Acad. Sci. U. S. A. 108, E1392–E1398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Barthelme D., Scheele U., Dinkelaker S., Janoschka A., Macmillan F., Albers S.-V., Driessen A.J.M., Stagni M.S., Bill E., Meyer-Klaucke W., Schünemann V., Tampé R. 2007. Structural organization of essential iron-sulfur clusters in the evolutionarily highly conserved ATP-binding cassette protein ABCE1. J. Biol. Chem. 282, 14598–14607.

    Article  CAS  PubMed  Google Scholar 

  122. Khoshnevis S., Gross T., Rotte C., Baierlein C., Ficner R., Krebber H. 2010. The iron-sulphur protein RNase L inhibitor functions in translation termination. EMBO Rep. 11, 214–219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Becker T., Franckenberg S., Wickles S., Shoemaker C.J., Anger A.M., Armache J.-P., Sieber H., Ungewickell C., Berninghausen O., Daberkow I., Karcher A., Thomm M., Hopfner K-P., Green R., Beckmann R. 2012. Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature. 482, 501–506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Snay-Hodge C.A., Colot H.V., Goldstein A.L., Cole C.N. 1998. Dbp5p/Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO J. 17, 2663–2676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Tseng S.S., Weaver P.L., Liu Y., Hitomi M., Tartakoff A.M., Chang T.H. 1998. Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export. EMBO J. 17, 2651–2662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Tieg B., Krebber H. 2013. Dbp5—from nuclear export to translation. Biochim. Biophys. Acta. 1829, 791–798.

    Article  CAS  PubMed  Google Scholar 

  127. Estruch F., Hodge C., Gómez-Navarro N., Peiró-Chova L., Heath C.V., Cole C.N. 2012. Insights into mRNP biogenesis provided by new genetic interactions among export and transcription factors. BMC Genet. 13, 80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Schmitt C., von Kobbe C., Bachi A., Panté N., Rodrigues J.P., Boscheron C., Rigaut G., Wilm M., Séraphin B., Carmo-Fonseca M., Izaurralde E. 1999. Dbp5, a DEAD-box protein required for mRNA export, is recruited to the cytoplasmic fibrils of nuclear pore complex via a conserved interaction with CAN/Nup159p. EMBO J. 18, 4332–4347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Gross T., Siepmann A., Sturm D., Windgassen M., Scarcelli J.J., Seedorf M., Cole C.N., Krebber H. 2007. The DEAD-box RNA helicase Dbp5 functions in translation termination. Science. 315, 646–649.

    Article  CAS  PubMed  Google Scholar 

  130. Murphy R., Wente S.R. 1996. An RNA-export mediator with an essential nuclear export signal. Nature. 383, 357–360.

    Article  CAS  PubMed  Google Scholar 

  131. Watkins J.L., Murphy R., Emtage J.L., Wente S.R. 1998. The human homologue of Saccharomyces cerevisiae Gle1p is required for poly(A)+ RNA export. Proc. Natl. Acad. Sci. U. S. A. 95, 6779–6784.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Alcázar-Román A.R., Tran E.J., Guo S., Wente S.R. 2006. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat. Cell Biol. 8, 711–716.

    Article  CAS  PubMed  Google Scholar 

  133. Adams R.L., Mason A.C., Glass L., Aditi, Wente S.R. 2017. Nup42 and IP6 coordinate Gle1 stimulation of Dbp5/DDX19B for mRNA export in yeast and human cells. Traffic. 18, 776–790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Montpetit B., Thomsen N.D., Helmke K.J., Seeliger M.A., Berger J.M., Weis K. 2011. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature. 472, 238–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Bolger T.A., Folkmann A.W., Tran E.J., Wente S.R. 2008. The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell. 134, 624–633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Hinnebusch A.G. 2006. eIF3: A versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31, 553–562.

    Article  CAS  PubMed  Google Scholar 

  137. Pisarev A.V., Hellen C.U.T., Pestova T.V. 2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell. 131, 286–299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Beznosková P., Cuchalová L., Wagner S., Shoemaker C.J., Gunišová S., von der Haar T., Valášek L.S. 2013. Translation initiation factors eIF3 and HCR1 control translation termination and stop codon read-through in yeast cells. PLoS Genet. 9, e1003962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Kikuchi Y., Shimatake H., Kikuchi A. 1988. A yeast gene required for the G1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J. 7, 1175–1182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Tikhomirova V.L., Inge-Vechtomov S.G. 1996. Sensitivity of sup35 and sup45 suppressor mutants in Saccharomyces cerevisiae to the anti-microtubule drug benomyl. Curr. Genet. 30, 44–49.

    Article  CAS  PubMed  Google Scholar 

  141. Basu J., Williams B.C., Li Z., Williams E.V., Goldberg M.L. 1998. Depletion of a Drosophila homolog of yeast Sup35p disrupts spindle assembly, chromosome segregation, and cytokinesis during male meiosis. Cell Motil. Cytoskeleton. 39, 286–302.

    Article  CAS  PubMed  Google Scholar 

  142. Borchsenius A.S., Tchourikova A.A., Inge-Vechtomov S.G. 2000. Recessive mutations in SUP35 and SUP45 genes coding for translation release factors affect chromosome stability in Saccharomyces cerevisiae. Curr. Genet. 37, 285–291.

    Article  CAS  PubMed  Google Scholar 

  143. Valouev I.A., Kushnirov V.V., Ter-Avanesyan M.D. 2002. Yeast polypeptide chain release factors eRF1 and eRF3 are involved in cytoskeleton organization and cell cycle regulation. Cell Motil. Cytoskeleton. 52, 161–173.

    Article  CAS  PubMed  Google Scholar 

  144. Stevens R.C., Davis T.N. 1998. Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae. J. Cell Biol. 142, 711–722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Valouev I.A., Urakov V.N., Kochneva-Pervukhova N.V., Smirnov V.N., Ter-Avanesyan M.D. 2004. Translation termination factors function outside of translation: Yeast eRF1 interacts with myosin light chain, Mlc1p, to effect cytokinesis. Mol. Microbiol. 53, 687–696.

    Article  CAS  PubMed  Google Scholar 

  146. Bailleul P.A., Newnam G.P., Steenbergen J.N., Chernoff Y.O. 1999. Genetic study of interactions between the cytoskeletal assembly protein Sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics. 153, 81–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ganusova E.E., Ozolins L.N., Bhagat S., Newnam G.P., Wegrzyn R.D., Sherman M.Y., Chernoff Y.O. 2006. Modulation of prion formation, aggregation, and toxicity by the actin cytoskeleton in yeast. Mol. Cell. Biol. 26, 617–629.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Manogaran A.L., Hong J.Y., Hufana J., Tyedmers J., Lindquist S., Liebman S.W. 2011. Prion formation and polyglutamine aggregation are controlled by two classes of genes. PLoS Genet. 7, e1001386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Moosavi B., Mousavi B., Yang G.-F. 2016. Actin, membrane trafficking and the control of prion induction, propagation and transmission in yeast. Traffic. 17, 5–20.

    Article  CAS  PubMed  Google Scholar 

  150. Tyedmers J., Madariaga M.L., Lindquist S. 2008. Prion switching in response to environmental stress. PLoS Biol. 6, e294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Speldewinde S.H., Doronina V.A., Tuite M.F., Grant C.M. 2017. Disrupting the cortical actin cytoskeleton points to two distinct mechanisms of yeast [PSI +] prion formation. PLoS Genet. 13, e1006708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Chernova T.A., Romanyuk A.V., Karpova T.S., Shanks J.R., Ali M., Moffatt N., Howie R.L., O’Dell A., McNally J.G., Liebman S.W., Chernoff Y.O., Wilkinson K.D. 2011. Prion induction by the short-lived, stress-induced protein Lsb2 is regulated by ubiquitination and association with the actin cytoskeleton. Mol. Cell. 43, 242–252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Chernova T.A., Kiktev D.A., Romanyuk A.V., Shanks J.R., Laur O., Ali M., Ghosh A., Kim D., Yang Z., Mang M., Chernoff Y.O., Wilkinson K.D. 2017. Yeast short-lived actin-associated protein forms a metastable prion in response to thermal stress. Cell Rep. 18, 751–761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Ali M., Chernova T.A., Newnam G.P., Yin L., Shanks J., Karpova T.S., Lee A., Laur O., Subramanian S., Kim D., McNally J.G., Seyfried N.T., Chernoff Y.O., Wilkinson K.D. 2014. Stress-dependent proteolytic processing of the actin assembly protein Lsb1 modulates a yeast prion. J. Biol. Chem. 289, 27625–27639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Li X., Rayman J.B., Kandel E.R., Derkatch I.L. 2014. Functional role of Tia1/Pub1 and Sup35 prion domains: directing protein synthesis machinery to the tubulin cytoskeleton. Mol. Cell. 55, 305–318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Derkatch I.L., Bradley M.E., Zhou P., Chernoff Y.O., Liebman S.W. 1997. Genetic and environmental factors affecting the de novo appearance of the [PSI +] prion in Saccharomyces cerevisiae. Genetics. 147, 507–519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Sondheimer N., Lindquist S. 2000. Rnq1: An epigenetic modifier of protein function in yeast. Mol. Cell. 5, 163–172.

    Article  CAS  PubMed  Google Scholar 

  158. Derkatch I.L., Bradley M.E., Hong J.Y., Liebman S.W. 2001. Prions affect the appearance of other prions: The story of [PIN +]. Cell. 106, 171–182.

    Article  CAS  PubMed  Google Scholar 

  159. Derkatch I.L., Bradley M.E., Masse S.V., Zadorsky S.P., Polozkov G.V., Inge-Vechtomov S.G., Liebman S.W. 2000. Dependence and independence of [PSI +] and [PIN +]: A two-prion system in yeast? EMBO J. 19, 1942–1952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Derkatch I.L., Uptain S.M., Outeiro T.F., Krishnan R., Lindquist S.L., Liebman S.W. 2004. Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI +] prion in yeast and aggregation of Sup35 in vitro. Proc. Natl. Acad. Sci. U. S. A. 101, 12934–12939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Bagriantsev S., Liebman S.W. 2004. Specificity of prion assembly in vivo: [PSI +] and [PIN +] form separate structures in yeast. J. Biol. Chem. 279, 51042–51048.

    Article  CAS  PubMed  Google Scholar 

  162. Bondarev S.A., Likholetova D.V., Belousov M.V., Zhouravleva G.A. 2017. Rnq1 protein protects [PSI +] prion from effect of the PNM mutation. Mol. Biol. (Moscow). 51 (2), 323–327.

    Article  CAS  Google Scholar 

  163. Osherovich L.Z., Weissman J.S. 2001. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI +] prion. Cell. 106, 183–194.

    Article  CAS  PubMed  Google Scholar 

  164. Wickner R. 1994. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science. 264, 566–569.

    Article  CAS  PubMed  Google Scholar 

  165. Du Z., Park K.-W., Yu H., Fan Q., Li L. 2008. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat. Genet. 40, 460–465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Du Z., Li L. 2014. Investigating the interactions of yeast prions: [SWI +], [PSI +], and [PIN +]. Genetics. 197, 685–700.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Patel B.K., Gavin-Smyth J., Liebman S.W. 2009. The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat Cell Biol. 11, 344–349.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Kurahashi H., Oishi K., Nakamura Y. 2011. A bipolar personality of yeast prion proteins. Prion. 5, 305–310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Yang Z., Hong J.Y., Derkatch I.L., Liebman S.W. 2013. Heterologous Gln/Asn-rich proteins impede the propagation of yeast prions by altering chaperone availability. PLoS Genet. 9, e1003236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Derkatch I.L., Liebman S.W. 2013. The story of stolen chaperones: How overexpression of Q/N proteins cures yeast prions. Prion. 7, 294–300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Bagriantsev S.N., Gracheva E.O., Richmond J.E., Liebman S.W. 2008. Variant-specific [PSI +] infection is transmitted by Sup35 polymers within [PSI +] aggregates with heterogeneous protein composition. Mol. Biol. Cell. 19, 2433–2443.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Nevzglyadova O.V., Artemov A.V., Mittenberg A.G., Solovyov K.V., Kostyleva E.I., Mikhailova E.V., Kuznetsova I.M., Turoverov K.K., Soidla T.R. 2009. Prion-associated proteins in yeast: Comparative analysis of isogenic [PSI +] and [psi –] strains. Yeast. 26, 611–631.

    Article  CAS  PubMed  Google Scholar 

  173. Chernova T.A., Wilkinson K.D., Chernoff Y.O. 2014. Physiological and environmental control of yeast prions. FEMS Microbiol. Rev. 38, 326–344.

    Article  CAS  PubMed  Google Scholar 

  174. Kushnirov V.V., Ter-Avanesyan M.D. 1998. Structure and replication of yeast prions. Cell. 94, 13–16.

    Article  CAS  PubMed  Google Scholar 

  175. Matveenko A.G., Barbitoff Y.A., Jay-Garcia L.M., Chernoff Y.O., Zhouravleva G.A. 2018. Differential effects of chaperones on yeast prions: CURrent view. Curr. Genet. 64, 317–325.

    Article  CAS  PubMed  Google Scholar 

  176. Chernoff Y., Lindquist S., Ono B., Inge-Vechtomov S., Liebman S. 1995. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [PSI +]. Science. 268, 880–884.

    Article  CAS  PubMed  Google Scholar 

  177. Ferreira P.C., Ness F., Edwards S.R., Cox B.S., Tuite M.F. 2001. The elimination of the yeast [PSI +] prion by guanidine hydrochloride is the result of Hsp104 inactivation. Mol. Microbiol. 40, 1357–1369.

    Article  CAS  PubMed  Google Scholar 

  178. Higurashi T., Hines J.K., Sahi C., Aron R., Craig E.A. 2008. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc. Natl. Acad. Sci. U. S. A. 105, 16596–16601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Kryndushkin D.S., Smirnov V.N., Ter-Avanesyan M.D., Kushnirov V.V. 2002. Increased expression of Hsp40 chaperones, transcriptional factors, and ribosomal protein Rpp0 can cure yeast prions. J. Biol. Chem. 277, 23702–23708.

    Article  CAS  PubMed  Google Scholar 

  180. Barbitoff Y.A., Matveenko A.G., Moskalenko S.E., Zemlyanko O.M., Newnam G.P., Patel A., Chernova T.A., Chernoff Y.O., Zhouravleva G.A. 2017. To CURe or not to CURe? Differential effects of the chaperone sorting factor Cur1 on yeast prions are mediated by the chaperone Sis1. Mol. Microbiol. 105, 242–257.

    Article  CAS  PubMed  Google Scholar 

  181. Kiktev D.A., Patterson J.C., Muller S., Bariar B., Pan T., Chernoff Y.O. 2012. Regulation of chaperone effects on a yeast prion by cochaperone Sgt2. Mol. Cell. Biol. 32, 4960–4970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Liu B., Larsson L., Caballero A., Hao X., Oling D., Grantham J., Nyström T. 2010. The polarisome is required for segregation and retrograde transport of protein aggregates. Cell. 140, 257–267.

    Article  CAS  PubMed  Google Scholar 

  183. Newnam G.P., Birchmore J.L., Chernoff Y.O. 2011. Destabilization and recovery of a yeast prion after mild heat shock. J. Mol. Biol. 408, 432–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Newnam G.P., Wegrzyn R.D., Lindquist S.L., Chernoff Y.O. 1999. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol. Cell. Biol. 19, 1325–1333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Chernoff Y.O., Newnam G.P., Kumar J., Allen K., Zink A.D. 1999. Evidence for a protein mutator in yeast: Role of the Hsp70-related chaperone ssb in formation, stability, and toxicity of the [PSI +] prion. Mol. Cell. Biol. 19, 8103–8112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Allen K.D., Wegrzyn R.D., Chernova T.A., Müller S., Newnam G.P., Winslett P.A., Wittich, K.B., Wilkinson K.D., Chernoff Y.O. 2005. Hsp70 chaperones as modulators of prion life cycle: Novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI +]. Genetics. 169, 1227–1242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Kiktev D.A., Melomed M.M., Lu C.D., Newnam G.P., Chernoff Y.O. 2015. Feedback control of prion formation and propagation by the ribosome-associated chaperone complex. Mol. Microbiol. 96, 621–632.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Wickner R.B., Edskes H.K., Son M., Wu S., Niznikiewicz M. 2020. How do yeast cells contend with prions? Int. J. Mol. Sci. 21, 4742.

    Article  CAS  PubMed Central  Google Scholar 

  189. Wickner R.B., Kelly A.C., Bezsonov E.E., Edskes H.K. 2017. [PSI +] prion propagation is controlled by inositol polyphosphates. Proc. Natl. Acad. Sci. U. S. A. 114, E8402–E8410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Son M., Wickner R.B. 2018. Nonsense-mediated mRNA decay factors cure most [PSI +] prion variants. Proc. Natl. Acad. Sci. U. S. A. 115, E1184–E1193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Matveenko A.G., Belousov M.V., Bondarev S.A., Moskalenko S.E., Zhouravleva G.A. 2016. Identification of new genes that affect [PSI +] prion toxicity in Saccharomyces cerevisiae yeast. Mol. Biol. (Moscow). 50 (5), 710–718.

    Article  CAS  Google Scholar 

  192. Matveenko A.G., Drozdova P.B., Belousov M.V, Moskalenko S.E., Bondarev S.A., Barbitoff Y.A., Nizhnikov A.A., Zhouravleva G.A. 2016. SFP1-mediated prion-dependent lethality is caused by increased Sup35 aggregation and alleviated by Sis1. Genes Cells. 21, 1290–1308.

    Article  CAS  PubMed  Google Scholar 

  193. Urakov V.N., Mitkevich O.V., Dergalev A.A., Ter-Avanesyan M.D. 2018. The Pub1 and Upf1 proteins act in concert to protect yeast from toxicity of the [PSI +]. Int. J. Mol. Sci. 19, 3663.

    Article  CAS  PubMed Central  Google Scholar 

  194. Sergeeva A.V., Sopova J.V., Belashova T.A., Siniukova V.A., Chirinskaite A.V., Galkin A.P., Zadorsky S.P. 2019. Amyloid properties of the yeast cell wall protein Toh1 and its interaction with prion proteins Rnq1 and Sup35. Prion. 13, 21–32.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 20-14-50271).

Author information

Authors and Affiliations

  1. Department of Genetics and Biotechnology, St. Petersburg State University, 199034, St. Petersburg, Russia

    G. A. Zhouravleva, S. A. Bondarev, O. M. Zemlyanko & S. E. Moskalenko

  2. Laboratory of Amyloid Biology, St. Petersburg State University, 199034, St. Petersburg, Russia

    G. A. Zhouravleva, S. A. Bondarev & O. M. Zemlyanko

  3. St. Petersburg Branch, Vavilov Institute of General Genetics, Russian Academy of Sciences, 199034, St. Petersburg, Russia

    S. E. Moskalenko

Authors
  1. G. A. Zhouravleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. A. Bondarev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. M. Zemlyanko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. E. Moskalenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. A. Zhouravleva.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

This work does not contain any studies involving animals or human subjects performed by any of the authors.

Additional information

Translated by T. Tkacheva

Abbreviations: aa, amino acid residues (with digits); RRM, RNA recognition motif; NMD, nonsense-mediated decay; IPOD, insoluble protein deposit.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhouravleva, G.A., Bondarev, S.A., Zemlyanko, O.M. et al. Role of Proteins Interacting with the eRF1 and eRF3 Release Factors in the Regulation of Translation and Prionization. Mol Biol 56, 147–165 (2022). https://doi.org/10.1134/S0026893322010101

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893322010101

Keywords:

Search

Navigation