RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESs

Genes and Development

Volumn 23, Issue 23, 2009, Pages 2753-2764

  Landry, Dori M ^a   Hertz, Marla I ^a   Thompson, Sunnie R ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

Dicistroviridae; Hepatitis C virus; IRES; Ribosome; RPS25; Translation initiation

Indexed keywords

MESSENGER RNA; RIBOSOMAL PROTEIN S25; RIBOSOME PROTEIN; SPACER DNA; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; GENETICS; HEPATITIS C; HEPATITIS C VIRUS; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; MAMMAL CELL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RIBOSOMAL FRAMESHIFTING; RIBOSOME SUBUNIT; TRANSLATION INITIATION; VIRUS ENTRY; YEAST;

ANIMALS; DICISTROVIRIDAE; GENE DELETION; GENE EXPRESSION REGULATION; HELA CELLS; HEPACIVIRUS; HUMANS; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

CRICKET PARALYSIS VIRUS; DICISTROVIRIDAE; EUKARYOTA; HEPATITIS C VIRUS; MAMMALIA;

EID: 72549101167     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1832209     Document Type: Article

References (59)

1. Adilakshmi T, Laine RO. 2002. Ribosomal protein S25 mRNA partners with MTF-1 and La to provide a p53-mediated mechanism for survival or death. J Biol Chem 277: 4147-4151. (Pubitemid 34968675)
2. Angelastro JM, Torocsik B, Greene LA. 2002. Nerve growth factor selectively regulates expression of transcripts encoding ribosomal proteins. BMC Neurosci 3: 3. doi: 10.1186/ 1471-2202-3-3
3. Becker DM, Lundblad V. 1993. Manipulation of yeast genes. Curr Protoc Mol Biol 27: 13.17.11-13.17.10. doi: 10.1002/ 0471142727.mb1307s27.
4. Belcourt MF, Farabaugh PJ. 1990. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 62: 339-352. (Pubitemid 20233540)
5. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H. 2005. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: Remodeling of the HCV IRES. Structure 13: 1695-1706. (Pubitemid 41571833)
6. Bonetti B, Fu L, Moon J, Bedwell DM. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol 251: 334-345.
7. Brierley I, Dos Ramos FJ. 2006. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res 119: 29-42. (Pubitemid 43765977)
8. Bushell M, Sarnow P. 2002. Hijacking the translation apparatus by RNA viruses. J Cell Biol 158: 395-399. (Pubitemid 34851696)
9. Bushell M, Stoneley M, Kong YW, Hamilton TL, Spriggs KA, Dobbyn HC, Qin X, Sarnow P, Willis AE. 2006. Polypyrimidine tract binding protein regulates IRES-mediated gene expression during apoptosis. Mol Cell 23: 401-412. (Pubitemid 44128848)
10. Carter MS, Sarnow P. 2000. Distinct mRNAs that encode La autoantigen are differentially expressed and contain internal ribosome entry sites. J Biol Chem 275: 28301-28307. (Pubitemid 30688957)
11. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
12. Costantino D, Kieft JS. 2005. A preformed compact ribosome-binding domain in the cricket paralysis-like virus IRES RNAs. RNA 11: 332-343. (Pubitemid 40270825)
13. Costantino DA, Pfingsten JS, Rambo RP, Kieft JS. 2008. tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat Struct Mol Biol 15: 57-64.
14. Deniz N, Lenarcic EM, Landry DM, Thompson SR. 2009. Translation initiation factors are not required for Dicistroviridae IRES function in vivo. RNA 15: 932-946.
15. Dinos G, Kalpaxis DL, Wilson DN, Nierhaus KH. 2005. Deacylated tRNA is released from the E site upon A site occupation but before GTP is hydrolyzed by EF-Tu. Nucleic Acids Res 33: 5291-5296. (Pubitemid 41487832)
16. Doring T, Mitchell P, Osswald M, Bochkariov D, Brimacombe R. 1994. The decoding region of 16S RNA; A cross-linking study of the ribosomal A, P and E sites using tRNA derivatized at position 32 in the anticodon loop. EMBO J 13: 2677-2685. (Pubitemid 24188401)
17. Ferreira-Cerca S, Poll G, Gleizes PE, Tschochner H, Milkereit P. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol Cell 20: 263-275. (Pubitemid 41484171)
18. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425: 737-741. (Pubitemid 37314318)
19. Giedroc DP, Cornish PV. 2009. Frameshifting RNA pseudoknots: Structure and mechanism. Virus Res 139: 193-208.
20. Gilbert WV, Zhou K, Butler TK, Doudna JA. 2007. Cap-independent translation is required for starvation-induced differentiation in yeast. Science 317: 1224-1227.
21. Graber TE, Holcik M. 2007. Cap-independent regulation of gene expression in apoptosis. Mol Biosyst 3: 825-834. (Pubitemid 350115410)
22. Harger JW, Dinman JD. 2003. An in vivo dual-luciferase assay system for studying translational recoding in the yeast Saccharomyces cerevisiae. RNA 9: 1019-1024.
23. Hellen CU, Sarnow P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes & Dev 15: 1593-1612. (Pubitemid 32702581)
24. Jan E, Sarnow P. 2002. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J Mol Biol 324: 889-902. (Pubitemid 41782981)
25. Jan E, Kinzy TG, Sarnow P. 2003. Divergent tRNA-like element supports initiation, elongation, and termination of protein biosynthesis. Proc Natl Acad Sci 100: 15410-15415. (Pubitemid 38021003)
26. Kanamori Y, Nakashima N. 2001. A tertiary structure model of the internal ribosome entry site (IRES) for methionine-independent initiation of translation. RNA 7: 266-274. (Pubitemid 33590509)
27. Keeling KM, Lanier J, Du M, Salas-Marco J, Gao L, Kaenjak-Angeletti A, Bedwell DM. 2004. Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae. RNA 10: 691-703. (Pubitemid 38405947)
28. Kellis M, Birren BW, Lander ES. 2004. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624. (Pubitemid 38524797)
29. Kieft JS. 2008. Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 33: 274-283.
30. Laine RO, Shay NF, Kilberg MS. 1994. Nuclear retention of the induced mRNA following amino acid-dependent transcriptional regulation of mammalian ribosomal proteins L17 and S25. J Biol Chem 269: 9693-9697.
31. Lavery WL, Goyns MH. 2002. Increased expression of the S25 ribosomal protein gene occurs during ageing of the rat liver. Gerontology 48: 369-373. (Pubitemid 36152987)
32. Marion MJ, Marion C. 1988. Ribosomal proteins S2, S6, S10, S14, S15 and S25 are localized on the surface of mammalian 40 S subunits and stabilize their conformation. A study with immobilized trypsin. FEBS Lett 232: 281-285.
33. Marquez V, Wilson DN, Tate WP, Triana-Alonso F, Nierhaus KH. 2004. Maintaining the ribosomal reading frame: The influence of the E site during translational regulation of release factor 2. Cell 118: 45-55. (Pubitemid 38902813)
34. Namy O, Rousset JP, Napthine S, Brierley I. 2004. Reprogrammed genetic decoding in cellular gene expression. Mol Cell 13: 157-168. (Pubitemid 38183263)
35. Nierhaus KH. 1990. The allosteric three-site model for the ribosomal elongation cycle: Features and future. Biochemistry 29: 4997-5008.
36. Nierhaus KH. 2006. Decoding errors and the involvement of the E-site. Biochimie 88: 1013-1019.
37. Nishiyama T, Yamamoto H, Uchiumi T, Nakashima N. 2007. Eukaryotic ribosomal protein RPS25 interacts with the conserved loop region in a dicistroviral intergenic internal ribosome entry site. Nucleic Acids Res 35: 1514-1521. (Pubitemid 46592873)
38. Pestova TV, Hellen CU. 2003. Translation elongation after assembly of ribosomes on the cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes & Dev 17: 181-186.
39. Pfingsten JS, Costantino DA, Kieft JS. 2006. Structural basis for ribosome recruitment and manipulation by a viral IRES RNA. Science 314: 1450-1454. (Pubitemid 44871950)
40. Robledo S, Idol RA, Crimmins DL, Ladenson JH, Mason PJ, Bessler M. 2008. The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA 14: 1918-1929.
41. Rotenberg MO, Moritz M, Woolford JL Jr. 1988. Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of halfmer polyribosomes. Genes & Dev 2: 160-172.
42. Salas-Marco J, Bedwell DM. 2005. Discrimination between defects in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J Mol Biol 348: 801-815. (Pubitemid 40544383)
43. Schilling-Bartetzko S, Franceschi F, Sternbach H, Nierhaus KH. 1992. Apparent association constants of tRNAs for the ribosomal A, P, and E sites. J Biol Chem 267: 4693-4702.
44. Schuler M, Connell SR, Lescoute A, Giesebrecht J, Dabrowski M, Schroeer B, Mielke T, Penczek PA, Westhof E, Spahn CM. 2006. Structure of the ribosome-bound cricket paralysis virus IRES RNA. Nat Struct Mol Biol 13: 1092-1096. (Pubitemid 44885919)
45. Semenkov YP, Rodnina MV, Wintermeyer W. 1996. The "allosteric three-site model" of elongation cannot be confirmed in a well-defined ribosome system from Escherichia coli. Proc Natl Acad Sci 93: 12183-12188.
46. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
47. Spahn CM, Kieft JS, Grassucci RA, Penczek PA, Zhou K, Doudna JA, Frank J. 2001. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291: 1959-1962. (Pubitemid 32216995)
48. Spahn CM, Gomez-Lorenzo MG, Grassucci RA, Jorgensen R, Andersen GR, Beckmann R, Penczek PA, Ballesta JP, Frank J. 2004a. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J 23: 1008-1019. (Pubitemid 38436866)
49. Spahn CM, Jan E, Mulder A, Grassucci RA, Sarnow P, Frank J. 2004b. Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: The IRES functions as an RNA-based translation factor. Cell 118: 465-475. (Pubitemid 39485666)
50. Spriggs KA, Stoneley M, Bushell M, Willis AE. 2008. Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol Cell 100: 27-38. (Pubitemid 351201431)
51. Sung D, Kang H. 1998. The N-terminal amino acid sequences of the firefly luciferase are important for the stability of the enzyme. Photochem Photobiol 68: 749-753. (Pubitemid 128472306)
52. Thompson SR, Gulyas KD, Sarnow P. 2001. Internal initiation in Saccharomyces cerevisiae mediated by an initiator tRNA/eIF2-independent internal ribosome entry site element. Proc Natl Acad Sci 98: 12972-12977. (Pubitemid 33051303)
53. Treco DA, Lundblad V. 1993. Basic techniques of yeast genetics. Cur Protoc Mol Biol 23: 13.11.11-13.11.17. doi: 10.1002/ 0471142727.mb1301s23.
54. Treco DA, Winston F. 2008. Growth and manipulation of yeast. Curr Protoc Mol Biol 82: 13.12.11-13.12.12. doi: 10.1002/0471142727.mb1302s82.
55. Uchiumi T, Terao K, Ogata K. 1981. Identification of neighboring protein pairs cross-linked with dimethyl 3,3′-dithiobispropionimidate in rat liver 40S ribosomal subunits. J Biochem (Tokyo) 90: 185-193.
56. Wilson JE, Pestova TV, Hellen CU, Sarnow P. 2000. Initiation of protein synthesis from the A site of the ribosome. Cell 102: 511-520.
57. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906. (Pubitemid 29381993)
58. Wower J, Scheffer P, Sylvers LA, Wintermeyer W, Zimmermann RA. 1993. Topography of the E site on the Escherichia coli ribosome. EMBO J 12: 617-623. (Pubitemid 23073708)
59. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. 2001. Crystal structure of the ribosome at 5.5 A resolution. Science 292: 883-896. (Pubitemid 32422479)