Retrograde transfer RNA nuclear import provides a new level of tRNA quality control in Saccharomyces cerevisiae

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 21042-21047

  Kramer, Emily B ^a,b   Hopper, Anita K ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b SHIPPENSBURG UNIVERSITY   (United States)

Author keywords

Los1; Mtr10; Quality control pathways; TRNA processing errors; TRNA retrograde pathway

Indexed keywords

TRANSFER RNA;

ARTICLE; CELL MUTANT; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASMIC RAPID TRNA DECAY; NONHUMAN; NUCLEAR EXPORT; NUCLEAR IMPORT; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; QUALITY CONTROL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA DEGRADATION; RNA METABOLISM; RNA REPAIR; SACCHAROMYCES CEREVISIAE; YEAST CELL;

EID: 84891368395     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316579110     Document Type: Article

References (55)

1. Thompson M, Haeusler RA, Good PD, Engelke DR (2003) Nucleolar clustering of dispersed tRNA genes. Science 302(5649): 1399-1401.
2. Kufel J, Tollervey D (2003) 3'-Processing of yeast tRNATrp precedes 5'-processing. RNA 9(2): 202-208.
3. Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR (1998) Nucleolar localization of early tRNA processing. Genes Dev 12(16): 2463-2468.
4. Takaku H, Minagawa A, Takagi M, Nashimoto M (2003) A candidate prostate cancer susceptibility gene encodes tRNA 3' processing endoribonuclease. Nucleic Acids Res 31(9): 2272-2278.
5. Chen Y, et al. (2005) Characterization of TRZ1, a yeast homolog of the human candidate prostate cancer susceptibility gene ELAC2 encoding tRNase Z. BMC Mol Biol 6:12.
6. Vogel A, Schilling O, Späth B, Marchfelder A (2005) The tRNase Z family of proteins: Physiological functions, substrate specificity and structural properties. Biol Chem 386(12): 1253-1264.
7. Copela LA, Fernandez CF, Sherrer RL, Wolin SL (2008) Competition between the Rex1 exonuclease and the La protein affects both Trf4p-mediated RNA quality control and pre-tRNA maturation. RNA 14(6): 1214-1227.
8. Ozanick SG, et al. (2009) Rex1p deficiency leads to accumulation of precursor initiator tRNAMet and polyadenylation of substrate RNAs in Saccharomyces cerevisiae. Nucleic Acids Res 37(1): 298-308.
9. Hopper AK (2013) Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae. Genetics 194(1): 43-67.
10. Dhungel N, Hopper AK (2012) Beyond tRNA cleavage: Novel essential function for yeast tRNA splicing endonuclease unrelated to tRNA processing. Genes Dev 26(5): 503-514.
11. Yoshihisa T, Yunoki-Esaki K, Ohshima C, Tanaka N, Endo T (2003) Possibility of cytoplasmic pre-tRNA splicing: The yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol Biol Cell 14(8): 3266-3279.
12. Yoshihisa T, Ohshima C, Yunoki-Esaki K, Endo T (2007) Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells 12(3): 285-297.
13. Sarkar S, Hopper AK (1998) tRNA nuclear export in Saccharomyces cerevisiae: in situ hybridization analysis. Mol Biol Cell 9(11): 3041-3055.
14. Hellmuth K, et al. (1998) Yeast Los1p has properties of an exportin-like nucleocytoplasmic transport factor for tRNA. Mol Cell Biol 18(11): 6374-6386.
15. Murthi A, et al. (2010) Regulation of tRNA bidirectional nuclear-cytoplasmic trafficking in Saccharomyces cerevisiae. Mol Biol Cell 21(4): 639-649.
16. Hurt DJ, Wang SS, Lin YH, Hopper AK (1987) Cloning and characterization of LOS1, a Saccharomyces cerevisiae gene that affects tRNA splicing. Mol Cell Biol 7(3): 1208-1216.
17. Phizicky EM, Hopper AK (2010) tRNA biology charges to the front. Genes Dev 24(17): 1832-1860.
18. Jackman JE, Alfonzo JD (2013) Transfer RNA modifications: Nature's combinatorial chemistry playground. Wiley Interdiscip Rev RNA 4(1): 35-48.
19. El Yacoubi B, Bailly M, de Crécy-Lagard V (2012) Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 46: 69-95.
20. Barhoom S, et al. (2011) Quantitative single cell monitoring of protein synthesis at subcellular resolution using fluorescently labeled tRNA. Nucleic Acids Res 39(19):e129.
21. Shaheen HH, Hopper AK (2005) Retrograde movement of tRNAs from the cytoplasm to the nucleus in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102(32): 11290-11295.
22. Shaheen HH, et al. (2007) Retrograde nuclear accumulation of cytoplasmic tRNA in rat hepatoma cells in response to amino acid deprivation. Proc Natl Acad Sci USA 104(21): 8845-8850.
23. Zaitseva L, Myers R, Fassati A (2006) tRNAs promote nuclear import of HIV-1 intracellular reverse transcription complexes. PLoS Biol 4(10):e332.
24. Takano A, Endo T, Yoshihisa T (2005) tRNA actively shuttles between the nucleus and cytosol in yeast. Science 309(5731): 140-142.
25. Miyagawa R, Mizuno R, Watanabe K, Ijiri K (2012) Formation of tRNA granules in the nucleus of heat-induced human cells. Biochem Biophys Res Commun 418(1): 149-155.
26. Ohira T, Suzuki T (2011) Retrograde nuclear import of tRNA precursors is required for modified base biogenesis in yeast. Proc Natl Acad Sci USA 108(26): 10502-10507.
27. Chu HY, Hopper AK (2013) Genome-wide investigation of the role of the tRNA nuclear- cytoplasmic trafficking pathway in regulation of the yeast Saccharomyces cerevisiae transcriptome and proteome. Mol Cell Biol 33(21): 4241-4254.
28. Hurto RL, Tong AH, Boone C, Hopper AK (2007) Inorganic phosphate deprivation causes tRNA nuclear accumulation via retrograde transport in Saccharomyces cerevisiae. Genetics 176(2): 841-852.
29. Whitney ML, Hurto RL, Shaheen HH, Hopper AK (2007) Rapid and reversible nuclear accumulation of cytoplasmic tRNA in response to nutrient availability. Mol Biol Cell 18(7): 2678-2686.
30. Arts GJ, Kuersten S, Romby P, Ehresmann B, Mattaj IW (1998) The role of exportin-t in selective nuclear export of mature tRNAs. EMBO J 17(24): 7430-7441.
31. Lipowsky G, et al. (1999) Coordination of tRNA nuclear export with processing of tRNA. RNA 5(4): 539-549.
32. Cook AG, Fukuhara N, Jinek M, Conti E (2009) Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 461(7260): 60-65.
33. Feng W, Hopper AK (2002) A Los1p-independent pathway for nuclear export of intronless tRNAs in Saccharomycescerevisiae. Proc Natl Acad Sci USA 99(8): 5412-5417.
34. Grosshans H, Hurt E, Simos G (2000) An aminoacylation-dependent nuclear tRNA export pathway in yeast. Genes Dev 14(7): 830-840.
35. Sarkar S, Azad AK, Hopper AK (1999) Nuclear tRNA aminoacylation and its role in nuclear export of endogenous tRNAs in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96(25): 14366-14371.
36. Lund E, Dahlberg JE (1998) Proofreading and aminoacylation of tRNAs before export from the nucleus. Science 282(5396): 2082-2085.
37. Kadaba S, et al. (2004) Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev 18(11): 1227-1240.
38. Kadaba S, Wang X, Anderson JT (2006) Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. RNA 12(3): 508-521.
39. Alexandrov A, et al. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21(1): 87-96.
40. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM (2008) Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5'-3' exonucleases Rat1 and Xrn1. Genes Dev 22(10): 1369-1380.
41. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM (2011) The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and Tstems of mature tRNA. Genes Dev 25(11): 1173-1184.
42. O'Connor JP, Peebles CL (1991) In vivo pre-tRNA processing in Saccharomyces cerevisiae. Mol Cell Biol 11(1): 425-439.
43. Machnicka MA, et al. (2013) MODOMICS: A database of RNA modification pathways - 2013 update. Nucleic Acids Res 41(Database issue):D262-D267.
44. Motorin Y, Muller S, Behm-Ansmant I, Branlant C (2007) Identification of modified residues in RNAs by reverse transcription-based methods. Methods Enzymol 425: 21-53.
45. Pemberton LF, Rosenblum JS, Blobel G (1997) A distinct and parallel pathway for the nuclear import of an mRNA-binding protein. J Cell Biol 139(7): 1645-1653.
46. Senger B, et al. (1998) Mtr10p functions as a nuclear import receptor for the mRNAbinding protein Npl3p. EMBO J 17(8): 2196-2207.
47. Ferrezuelo F, Steiner B, Aldea M, Futcher B (2002) Biogenesis of yeast telomerase depends on the importin mtr10. Mol Cell Biol 22(17): 6046-6055.
48. Hurto RL, Hopper AK (2011) P-body components, Dhh1 and Pat1, are involved in tRNA nuclear-cytoplasmic dynamics. RNA 17(5): 912-924.
49. Li JM, Hopper AK, Martin NC (1989) N2, N2-dimethylguanosine-specific tRNA methyltransferase contains both nuclear and mitochondrial targeting signals in Saccharomyces cerevisiae. J Cell Biol 109(4 Pt 1): 1411-1419.
50. Dewe JM, Whipple JM, Chernyakov I, Jaramillo LN, Phizicky EM (2012) The yeast rapid tRNA decay pathway competes with elongation factor 1A for substrate tRNAs and acts on tRNAs lacking one or more of several modifications. RNA 18(10): 1886-1896.
51. Boeke JD, LaCroute F, Fink GR (1984) A positive selection for mutants lacking orotidine- 5'-phosphate decarboxylase activity in yeast: 5-Fluoro-orotic acid resistance. Mol Gen Genet 197(2): 345-346.
52. Ghavidel A, et al. (2007) Impaired tRNA nuclear export links DNA damage and cellcycle checkpoint. Cell 131(5): 915-926.
53. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30(6):e23.
54. Shen WC, Selvakumar D, Stanford DR, Hopper AK (1993) The Saccharomyces cerevisiae LOS1 gene involved in pre-tRNA splicing encodes a nuclear protein that behaves as a component of the nuclear matrix. J Biol Chem 268(26): 19436-19444.
55. Gelperin DM, et al. (2005) Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19(23): 2816-2826.