N-terminal region of Saccharomyces cerevisiae eRF3 is essential for the functioning of the eRF1/eRF3 complex beyond translation termination
10.1186/1471-2199-7-34
Crossref journal-article
Springer Science and Business Media LLC
BMC Molecular Biology (297)
Abstract

Abstract Background Termination of translation in eukaryotes requires two release factors, eRF1, which recognizes all three nonsense codons and facilitates release of the nascent polypeptide chain, and eRF3 stimulating translation termination in a GTP-depended manner. eRF3 from different organisms possess a highly conservative C region (eRF3C), which is responsible for the function in translation termination, and almost always contain the N-terminal extension, which is inessential and vary both in structure and length. In the yeast Saccharomyces cerevisiae the N-terminal region of eRF3 is responsible for conversion of this protein into the aggregated and functionally inactive prion form. Results Here, we examined functional importance of the N-terminal region of a non-prion form of yeast eRF3. The screen for mutations which are lethal in combination with the SUP35-C allele encoding eRF3C revealed the sup45 mutations which alter the N-terminal domain of eRF1 and increase nonsense codon readthrough. However, further analysis showed that synthetic lethality was not caused by the increased levels of nonsense codon readthrough. Dominant mutations in SUP35-C were obtained and characterized, which remove its synthetic lethality with the identified sup45 mutations, thus indicating that synthetic lethality was not due to a disruption of interaction with proteins that bind to this eRF3 region. Conclusion These and other data demonstrate that the N-terminal region of eRF3 is involved both in modulation of the efficiency of translation termination and functioning of the eRF1/eRF3 complex outside of translation termination.

Bibliography

Urakov, V. N., Valouev, I. A., Kochneva-Pervukhova, N. V., Packeiser, A. N., Vishnevsky, A. Y., Glebov, O. O., Smirnov, V. N., & Ter-Avanesyan, M. D. (2006). N-terminal region of Saccharomyces cerevisiae eRF3 is essential for the functioning of the eRF1/eRF3 complex beyond translation termination. BMC Molecular Biology, 7(1).

Authors 8
  1. Valery N Urakov (first)
  2. Igor A Valouev (additional)
  3. Natalia V Kochneva-Pervukhova (additional)
  4. Anna N Packeiser (additional)
  5. Alexander Yu Vishnevsky (additional)
  6. Oleg O Glebov (additional)
  7. Vladimir N Smirnov (additional)
  8. Michael D Ter-Avanesyan (additional)
References 49 Referenced 21
  1. Frolova L, Le Goff X, Rasmussen HH, Cheperegin S, Drugeon G, Kress M, Arman I, Haenni AL, Celis JE, Philippe M, Justesen J, Kisselev LL: A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature. 1994, 372: 701-703. 10.1038/372701a0 (10.1038/372701a0) / Nature by L Frolova (1994)
  2. Zhouravleva G, Frolova L, Le Goff X, Le Guellec R, Inge-Vechtomov SG, Kisselev LL, Philippe M: Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 1995, 14: 4065-4072. (10.1002/j.1460-2075.1995.tb00078.x) / EMBO J by G Zhouravleva (1995)
  3. Stansfield I, Jones KM, Kushnirov VV, Dagkesamanskaya AR, Poznyakovski AI, Paushkin SV, Nierras CR, Cox BS, Ter-Avanesyan MD, Tuite MF: The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 1995, 14: 4365-4373. (10.1002/j.1460-2075.1995.tb00111.x) / EMBO J by I Stansfield (1995)
  4. Frolova L, Le Goff X, Zhouravleva G, Davydova E, Philippe M, Kisselev L: Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA. 1996, 2: 334-341. / RNA by L Frolova (1996)
  5. Zavialov AV, Buckingham RH, Ehrenberg M: A posttermination ribosomal complex is the guanidine nucleotide exchange factor for peptide release factor RF3. Cell. 2001, 107: 115-124. 10.1016/S0092-8674(01)00508-6 (10.1016/S0092-8674(01)00508-6) / Cell by AV Zavialov (2001)
  6. Alkalaeva EZ, Pisarev AV, Frolova LY, Kisselev LL, Pestova TV: In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell. 2006, 125: 1125-1136. 10.1016/j.cell.2006.04.035 (10.1016/j.cell.2006.04.035) / Cell by EZ Alkalaeva (2006)
  7. Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA, Barford D: The crystal structure of human eukaryotic release factor eRF1 – mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell. 2000, 100: 311-321. 10.1016/S0092-8674(00)80667-4 (10.1016/S0092-8674(00)80667-4) / Cell by H Song (2000)
  8. Ter-Avanesyan MD, Kushnirov VV, Dagkesamanskaya AR, Didichenko SA, Chernoff YO, Inge-Vechtomov SG, Smirnov VN: Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol. 1993, 7: 683-692. (10.1111/j.1365-2958.1993.tb01159.x) / Mol Microbiol by MD Ter-Avanesyan (1993)
  9. Ter-Avanesyan MD, Dagkesamanskaya AR, Kushnirov VV, Smirnov VN: The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics. 1994, 137: 671-676. (10.1093/genetics/137.3.671) / Genetics by MD Ter-Avanesyan (1994)
  10. Liu JJ, Sondheimer N, Lindquist SL: Changes in the middle region of Sup35 profoundly alter the nature of epigenetic inheritance for the yeast prion [PSI+]. Proc Natl Acad Sci USA. 2002, 99: 16446-16453. 10.1073/pnas.252652099 (10.1073/pnas.252652099) / Proc Natl Acad Sci USA by JJ Liu (2002)
  11. Bradley ME, Liebman SW: The Sup35 domains required for maintenance of weak, strong or undifferentiated yeast [PSI+] prions. Mol Microbiol. 2004, 51: 1649-1659. 10.1111/j.1365-2958.2003.03955.x (10.1111/j.1365-2958.2003.03955.x) / Mol Microbiol by ME Bradley (2004)
  12. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD: Propagation of the yeast prion-like [PSI+] determinant is mediated by oligomerization of the SUP35 -encoded polypeptide chain release factor. EMBO J. 1996, 15: 3127-3134. (10.1002/j.1460-2075.1996.tb00675.x) / EMBO J by SV Paushkin (1996)
  13. Patino MM, Liu JJ, Glover JR, Lindquist SL: Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science. 1996, 273: 622-626. (10.1126/science.273.5275.622) / Science by MM Patino (1996)
  14. Valouev IA, Kushnirov VV, Ter-Avanesyan MD: Yeast polypeptide chain release factors eRF1 and eRF3 are involved in cytoskeleton organization and cell cycle regulation. Cell Motil Cytoskeleton. 2002, 52: 161-173. 10.1002/cm.10040 (10.1002/cm.10040) / Cell Motil Cytoskeleton by IA Valouev (2002)
  15. Kong C, Ito K, Walsh MA, Wada M, Liu Y, Kumar S, Barford D, Nakamura Y, Song H: Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 form S. pombe. Mol Cell. 2004, 14: 233-245. 10.1016/S1097-2765(04)00206-0 (10.1016/S1097-2765(04)00206-0) / Mol Cell by C Kong (2004)
  16. Gagny B, Silar P: Identification of the genes encoding the cytosolic translation release factors from Podospora anserina and analysis of their role during the life cycle. Genetics. 1988, 149: 1763-1775. (10.1093/genetics/149.4.1763) / Genetics by B Gagny (1988)
  17. Hoshino S, Imai M, Kobayashi T, Uchida N, Katada T: 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. 1999, 274: 16677-16680. 10.1074/jbc.274.24.16677 (10.1074/jbc.274.24.16677) / J Biol Chem by S Hoshino (1999)
  18. Cosson B, Couturier A, Chabelskaya S, Kiktev D, Inge-Vechtomov S, Philippe M, Zhouravleva G: Poly(A)-binding protein acts in translation termination via eukaryotic release factor interaction and does not influence [PSI+] propagation. Mol Cell Biol. 2002, 22: 3301-3315. 10.1128/MCB.22.10.3301-3315.2002 (10.1128/MCB.22.10.3301-3315.2002) / Mol Cell Biol by B Cosson (2002)
  19. Hosoda N, Kobayashi T, Uchida N, Funakoshi Y, Kikuchi Y, Hoshino S, Katada T: Translation termination factor eRF3 mediates mRNA decay through the regulation of deanylation. J Biol Chem. 2003, 278: 28287-38291. / J Biol Chem by N Hosoda (2003)
  20. Urakov VN, Valouev IA, Lewitin EI, Paushkin SV, Kosorukov VS, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD: Itt1p, a novel protein inhibiting translation termination in Saccharomyces cerevisiae. BMC Mol Biol. 2001, 2: 9-18. 10.1186/1471-2199-2-9 (10.1186/1471-2199-2-9) / BMC Mol Biol by VN Urakov (2001)
  21. Bailleul PA, Newnam GP, Steenbergen JN, Chernoff YO: Genetic study of interactions between the cytoskeletal assembly protein Sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics. 1999, 153: 81-94. (10.1093/genetics/153.1.81) / Genetics by PA Bailleul (1999)
  22. Glover JR, Kowal AS, Schirmer EC, Patino MM, Liu JJ, Lindquist S: Self-seeded fibers formed by Sup35 the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell. 1997, 89: 811-819. 10.1016/S0092-8674(00)80264-0 (10.1016/S0092-8674(00)80264-0) / Cell by JR Glover (1997)
  23. King C-Y, Tittmann P, Gross H, Gebert R, Aebi M, Wuthrich K: Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc Natl Acad Sci USA. 1997, 94: 6618-6622. 10.1073/pnas.94.13.6618 (10.1073/pnas.94.13.6618) / Proc Natl Acad Sci USA by C-Y King (1997)
  24. Breining P, Piepersberg W: Yeast omnipotent suppressor SUP1 (SUP45): nucleotide sequence of the wild type and a mutant gene. Nucleic Acids Res. 1986, 14: 5187-5197. (10.1093/nar/14.13.5187) / Nucleic Acids Res by P Breining (1986)
  25. Valouev IA, Urakov VN, Kochneva-Pervukhova NV, Ter-Avanesyan MD: Translation termination factors function outside of translation: yeast eRF1 interacts with myosin light chain, Mlc1p, to effect cytokinesis. Mol Microbiol. 2004, 53: 687-696. 10.1111/j.1365-2958.2004.04157.x (10.1111/j.1365-2958.2004.04157.x) / Mol Microbiol by IA Valouev (2004)
  26. Ebihara K, Nakamura Y: C-terminal interaction of translational release factors eRF1 and eRF3 of fission yeast: G-domain uncoupled binding and the role of conserved amino acids. RNA. 1999, 5: 739-750. 10.1017/S135583829998216X (10.1017/S135583829998216X) / RNA by K Ebihara (1999)
  27. Eurwilaichitr L, Graves FM, Stansfield I, Tuite MF: The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Mol Microbiol. 1999, 32: 485-496. 10.1046/j.1365-2958.1999.01346.x (10.1046/j.1365-2958.1999.01346.x) / Mol Microbiol by L Eurwilaichitr (1999)
  28. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD: Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Mol Cell Biol. 1997, 17: 2798-2805. (10.1128/MCB.17.5.2798) / Mol Cell Biol by SV Paushkin (1997)
  29. Santoso A, Chien P, Osherovich LZ, Weissman JS: Molecular basis of a yeast prion species barrier. Cell. 2000, 100: 277-288. 10.1016/S0092-8674(00)81565-2 (10.1016/S0092-8674(00)81565-2) / Cell by A Santoso (2000)
  30. Kushnirov VV, Kochneva-Pervukhova NV, Chechenova MB, Frolova NS, Ter-Avanesyan MD: Prion properties of the Sup35 protein of yeast Pichia methanolica. EMBO J. 2000, 19: 324-331. 10.1093/emboj/19.3.324 (10.1093/emboj/19.3.324) / EMBO J by VV Kushnirov (2000)
  31. Chernoff YO, Galkin AP, Lewitin E, Chernova TA, Newnam GP, Belenkiy SM: Evolutionary conservation of prion-forming abilities of the yeast Sup35 protein. Mol Microbiol. 2000, 35: 865-876. 10.1046/j.1365-2958.2000.01761.x (10.1046/j.1365-2958.2000.01761.x) / Mol Microbiol by YO Chernoff (2000)
  32. Nakayashiki T, Ebihara K, Bannai H, Nakamura Y: Yeast [PSI+] "prions" that are crosstransmissible and susceptible beyond a species barrier through a quasi-prion state. Mol Cell. 2001, 7: 1121-1130. 10.1016/S1097-2765(01)00259-3 (10.1016/S1097-2765(01)00259-3) / Mol Cell by T Nakayashiki (2001)
  33. Hara H, Nakayashiki T, Crist CG, Nakamura Y: Prion domain interaction responsible for species discrimination in yeast [PSI+] transmission. Genes to Cells. 2004, 8: 925-939. 10.1111/j.1365-2443.2003.00694.x. (10.1111/j.1365-2443.2003.00694.x) / Genes to Cells by H Hara (2004)
  34. Sherman F, Fink GR, Hicks JB: Methods in yeast genetics. 1986, Cold Spring Harbor Laboratory Press / Methods in yeast genetics by F Sherman (1986)
  35. Boeke JD, LaCroute F, Fink GR: A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984, 197: 345-346. 10.1007/BF00330984 (10.1007/BF00330984) / Mol Gen Genet by JD Boeke (1984)
  36. Sambrook J, Fritsch EE, Maniatis T: Molecular Cloning: A Laboratory Manual. 1989, Cold Spring Harbor Laboratory Press, 2 / Molecular Cloning: A Laboratory Manual by J Sambrook (1989)
  37. Gietz RD, Woods RA: Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002, 350: 87-96. (10.1016/S0076-6879(02)50957-5) / Methods Enzymol by RD Gietz (2002)
  38. Inoue H, Nojima H, Okayama H: High efficiency transformation of Escherichia coli with plasmids. Gene. 1990, 96: 23-28. 10.1016/0378-1119(90)90336-P (10.1016/0378-1119(90)90336-P) / Gene by H Inoue (1990)
  39. Lafontaine DLJ, Preiss T, Tollervey D: Yeast 18S rRNA dimethylase Dim1p: a quality control mechanism in ribosome synthesis?. Mol Cell Biol. 1998, 18: 2360-2370. (10.1128/MCB.18.4.2360) / Mol Cell Biol by DLJ Lafontaine (1998)
  40. Jones JS, Prakash L: Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast. 1990, 6: 363-366. 10.1002/yea.320060502 (10.1002/yea.320060502) / Yeast by JS Jones (1990)
  41. Rose MD, Novick P, Thomas JH, Botstein D, Fink GR: A Saccharomyces cerevisiae genomic bank based on a centromere-containing shuttle vector. Gene. 1987, 60: 237-243. 10.1016/0378-1119(87)90232-0 (10.1016/0378-1119(87)90232-0) / Gene by MD Rose (1987)
  42. Gari E, Piedrafita L, Aldea M, Herrero E: A set of vectors with tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast. 1997, 13: 837-848. 10.1002/(SICI)1097-0061(199707)13:9<837::AID-YEA145>3.0.CO;2-T (10.1002/(SICI)1097-0061(199707)13:9<837::AID-YEA145>3.0.CO;2-T) / Yeast by E Gari (1997)
  43. Miller JH: Experiments in Molecular Genetics. 1972, Cold Spring Harbor Laboratory Press / Experiments in Molecular Genetics by JH Miller (1972)
  44. Stansfield I, Akhmaloka , Tuite MF: A mutant allele of the SUP45 (SAL4) gene of Saccharomyces cerevisiae shows temperature-dependent allosuppressor and omnipotent suppressor phenotypes. Curr Genet. 1995, 27: 417-426. 10.1007/BF00311210 (10.1007/BF00311210) / Curr Genet by I Stansfield (1995)
  45. Roman H: Studies of gene mutation in Saccharomyces. Cold Spring Harbor Symp Quant Biol. 1956, 21: 175-185. (10.1101/SQB.1956.021.01.015) / Cold Spring Harbor Symp Quant Biol by H Roman (1956)
  46. Fortes P, Kufel J, Fornerod M, Policarpou-Schwarz M, Lafontaine D, Tollervey D, Mattaj IW: Genetic and physical interactions involving the yeast nuclear cap-binding complex. Mol Cell Biol. 1999, 19: 6543-6553. (10.1128/MCB.19.10.6543) / Mol Cell Biol by P Fortes (1999)
  47. Chernoff YO, Inge-Vechtomov SG, Derkach IL, Ptyushkina MV, Tarunina OV, Dagkesamanskaya AR, Ter-Avanesyan MD: Dosage-dependent translational suppression in yeast Saccharomyces cerevisiae. Yeast. 1992, 8: 489-499. 10.1002/yea.320080702 (10.1002/yea.320080702) / Yeast by YO Chernoff (1992)
  48. Gietz RD, Sugino A: New yeast- Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988, 74: 527-534. 10.1016/0378-1119(88)90185-0 (10.1016/0378-1119(88)90185-0) / Gene by RD Gietz (1988)
  49. Sikorski RS, Hieter P: A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989, 122: 19-27. (10.1093/genetics/122.1.19) / Genetics by RS Sikorski (1989)
Dates
Type When
Created 18 years, 10 months ago (Oct. 11, 2006, 2:28 p.m.)
Deposited 4 years ago (Aug. 31, 2021, 11:06 p.m.)
Indexed 1 year, 2 months ago (June 13, 2024, 3:55 p.m.)
Issued 18 years, 10 months ago (Oct. 11, 2006)
Published 18 years, 10 months ago (Oct. 11, 2006)
Published Online 18 years, 10 months ago (Oct. 11, 2006)
Published Print 18 years, 9 months ago (Dec. 1, 2006)
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@article{Urakov_2006, title={N-terminal region of Saccharomyces cerevisiae eRF3 is essential for the functioning of the eRF1/eRF3 complex beyond translation termination}, volume={7}, ISSN={1471-2199}, url={http://dx.doi.org/10.1186/1471-2199-7-34}, DOI={10.1186/1471-2199-7-34}, number={1}, journal={BMC Molecular Biology}, publisher={Springer Science and Business Media LLC}, author={Urakov, Valery N and Valouev, Igor A and Kochneva-Pervukhova, Natalia V and Packeiser, Anna N and Vishnevsky, Alexander Yu and Glebov, Oleg O and Smirnov, Vladimir N and Ter-Avanesyan, Michael D}, year={2006}, month=oct }