Emerging themes in non-coding RNA quality control

Current Opinion in Structural Biology

Volumn 17, Issue 2, 2007, Pages 209-214

  Reinisch, Karin M ^a   Wolin, Sandra L ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RIBOSOME RNA; RNA BINDING PROTEIN; TRANSFER RNA; UNTRANSLATED RNA;

CELL STRUCTURE; EUKARYOTE; EXOSOME; GENE TARGETING; GENETIC CODE; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; QUALITY CONTROL; REVIEW; RNA DEGRADATION; RNA STRUCTURE;

ANIMALS; EUKARYOTIC CELLS; HUMANS; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; POLYADENYLATION; PROKARYOTIC CELLS; RIBONUCLEOPROTEINS; RNA, UNTRANSLATED;

EUKARYOTA; PROKARYOTA;

EID: 34147151804     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.03.012     Document Type: Review

References (41)

1. Henras A.K., Dez C., and Henry Y. RNA structure and function in C/D and H/ACA s(no)RNPs. Curr Opin Struct Biol 14 (2004) 335-343
2. Storz G., Altuvia S., and Wassarman K.M. An abundance of RNA regulators. Annu Rev Biochem 74 (2005) 199-217
3. Theimer C.A., and Feigon J. Structure and function of telomerase RNA. Curr Opin Struct Biol 16 (2006) 307-318
4. Tycowski K.T., Kolev N.G., Conrad N.K., Fok V., and Steitz J.A. The ever-growing world of small nuclear ribonucleoproteins. In: Gesteland R.F., Cech T.R., and Atkins J.F. (Eds). The RNA World (2006), Cold Spring Harbor Laboratory Press 327-368
5. Maquat L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5 (2004) 89-99
6. Amrani N., Sachs M.S., and Jacobson A. Early nonsense: mRNA decay solves a translational problem. Nat Rev Mol Cell Biol 7 (2006) 415-425
7. Behm-Ansmant I., and Izaurralde E. Quality control of gene expression: a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev 20 (2006) 391-398
8. Li Z., Reimers S., Pandit S., and Deutscher M.P. RNA quality control: degradation of defective transfer RNA. EMBO J 21 (2002) 1132-1138
9. Cheng Z.F., and Deutscher M.P. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc Natl Acad Sci USA 100 (2003) 6388-6393
10. Mohanty B.K., and Kushner S.R. Analysis of the function of Escherichia coli poly(A) polymerase I in RNA metabolism. Mol Microbiol 34 (1999) 1094-1108
11. Cheng Z.F., and Deutscher M.P. An important role for RNase R in mRNA decay. Mol Cell 17 (2005) 313-318
12. Li Z., Pandit S., and Deutscher M.P. Polyadenylation of stable RNA precursors in vivo. Proc Natl Acad Sci USA 95 (1998) 12158-12162
13. Met in S. cerevisiae. Genes Dev 18 (2004) 1227-1240
14. LaCava J., Houseley J., Saveanu C., Petfalski E., Thompson E., Jacquier A., and Tollervey D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121 (2005) 713-724. The poly(A) polymerase Trf4p forms a complex with the zinc knuckle protein Air2p and the putative helicase Mtr4p. The purified complex, called TRAMP, possesses polyadenylation activity and stimulates RNA decay by the exosome in vitro. In yeast strains lacking Trf4p, 3′-extended forms of several non-coding RNAs accumulate, indicating that Trf4p is required for their maturation and/or degradation. As an aberrant rRNA processing intermediate also accumulates, Trf4p is required for the exosome-mediated decay of this RNA.
15. ••], Trf4p was found to co-purify with the zinc knuckle proteins Air1p and Air2p and the Mtr4p helicase. A recombinant complex generated by co-expressing Air1p and Trf4p in E. coli is active in polyadenylation.
16. Vanacova S., Wolf J., Martin G., Blank D., Dettwiler S., Friedlein A., Langen H., Keith G., and Keller W. A New Yeast Poly(A) Polymerase Complex Involved in RNA Quality Control. PLoS Biol 3 (2005) e189. Trf4p was found to co-purify with Air1p, Air2p and Mtr4p, and the complex was demonstrated to have poly(A) polymerase activity and to stimulate degradation by the exosome. The Trf4p-containing complex preferentially polyadenylates aberrant forms of two mature tRNAs in vitro, suggesting that it might recognize structural features unique to misfolded tRNAs. Trf4p-Air1p and Trf4p-Air2p complexes formed from recombinant proteins retain the specificity for abnormal tRNAs.
17. Houseley J., and Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep 7 (2006) 205-211. The Trf5 protein, which is closely related in sequence to Trf4p, is shown to be complexed with Air1p and Mtr4p. In vivo, Trf5p overlaps in function with the Trf4p-containing complex.
18. Met described in Kadaba et al. [13] reveals that, in vivo, Trf4p polyadenylates nascent pre-tRNAs containing both 5′ leader and 3′ trailer sequences. Trf4p and the exosome are also shown to be involved in the degradation of a mutant spliceosomal U6 snRNA and a truncated 5S rRNA.
19. ••], microarray analyses reveal that yeast contain a large class of normally unstable RNAs generated by RNA polymerase II transcription of intergenic regions. Degradation of these RNAs requires Trf4p and the nuclear exosome.
20. Dez C., Houseley J., and Tollervey D. Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J 25 (2006) 1534-1546. In yeast containing a mutation that blocks nuclear export of 60S ribosomal subunits, the newly matured 25S rRNA and its precursors are degraded through a pathway involving Trf4p and the nuclear exosome. During the block in export, the preribosomal subunits, the TRAMP components Trf4p, Air2p and Mtr4p, and the exosome all concentrate in a subnucleolar focus, called the No-body, that might be the site of degradation.
21. Egecioglu D.E., Henras A.K., and Chanfreau G.F. Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12 (2006) 26-32. For many yeast snRNAs and snoRNAs, 3′ maturation involves endonucleolytic cleavage of the precursor by RNase III and processing by the nuclear exosome. In cells lacking the nuclear exosome protein Rrp6p, polyadenylated 3′-extended forms of these RNAs accumulate (see van Hoof et al. [22]). As Trf4p and Trf5p are shown to be required for the observed polyadenylation, these polymerases might function in the normal maturation of snRNAs and snoRNAs. It is also possible, however, that the polyadenylated precursors represent defective RNAs destined for degradation.
22. van Hoof A., Lennertz P., and Parker R. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 20 (2000) 441-452
23. Allmang C., Kufel J., Chanfreau G., Mitchell P., Petfalski E., and Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18 (1999) 5399-5410
24. Houseley J., LaCava J., and Tollervey D. RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7 (2006) 529-539
25. Midtgaard S.F., Assenholt J., Jonstrup A.T., Van L.B., Jensen T.H., and Brodersen D.E. Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc Natl Acad Sci USA 103 (2006) 11898-11903
26. Buttner K., Wenig K., and Hopfner K.P. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell 20 (2005) 461-471. Crystal structures of exosome core complexes from Archaeoglobus fulgidus are presented. Complexes include a heterohexameric ring of RNase PH-like subunits, Rrp41 and Rrp42, and three associated RNA-binding subunits, either Csl4 or Rrp4. The three phosphorolytic active sites (located in Rrp41 at the interfaces with Rrp42 on the face of the ring opposite Csl4 or Rrp4) were identified by soaking crystals with the phosphate analog tungstate.
27. 8 are bound at the catalytic active sites. Biochemical experiments are used to determine that RNA must thread through the Rrp41/Rrp42 hexamer before accessing the active sites.
28. Lorentzen E., Walter P., Fribourg S., Evguenieva-Hackenberg E., Klug G., and Conti E. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 12 (2005) 575-581. The structure of the exosome core from the archaeon S. solfataricus is presented. The core comprises three heterodimers of the RNase PH-like subunits Rrp41 and Rrp42 arranged into a ring. Possible locations for the phosphorolytic sites are identified by analogy with RNase PH from bacteria and mutational analysis is used to show that the active sites reside within the Rrp41 subunit. Rrp42 is catalytically inactive, but is important for structuring of the Rrp41 active site.
29. Mitchell P., Petfalski E., Shevchenko A., Mann M., and Tollervey D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91 (1997) 457-466
30. Val is degraded through a pathway that does not require Trf4p, Trf5p, Rrp6p or Ski2p, a putative RNA helicase required for function of the cytoplasmic exosome. Thus, S. cerevisiae contains at least one additional pathway for degrading defective non-coding RNAs.
31. •], degradation of the mutant tRNA was found to be independent of Trf4p. Thus, yeast possess additional pathways for degrading aberrant non-coding RNAs.
32. LaRiviere F.J., Cole S.E., Ferullo D.J., and Moore M.J. A late-acting quality control process for mature eukaryotic rRNAs. Mol Cell 24 (2006) 619-626
33. Chen X., and Wolin S.L. The Ro 60 kDa autoantigen: insights into cellular function and role in autoimmunity. J Mol Med 82 (2004) 232-239
34. O'Brien C.A., and Wolin S.L. A possible role for the 60 kd Ro autoantigen in a discard pathway for defective 5S ribosomal RNA precursors. Genes Dev 8 (1994) 2891-2903
35. Shi H., O'Brien C.A., Van Horn D.J., and Wolin S.L. A misfolded form of 5S rRNA is associated with the Ro and La autoantigens. RNA 2 (1996) 769-784
36. Chen X., Smith J.D., Shi H., Yang D.D., Flavell R.A., and Wolin S.L. The Ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation. Curr Biol 13 (2003) 2206-2211
37. Stein A.J., Fuchs G., Fu C., Wolin S.L., and Reinisch K.M. Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity. Cell 121 (2005) 529-539. Structures of unliganded Ro and Ro complexed with a fragment of Y RNA and a single-stranded RNA are presented. Ro forms an elliptical toroid with a central cavity that binds single-stranded RNA. Mutagenesis suggests that the single-stranded ends of misfolded RNAs insert into the cavity, while helical portions bind to a positively charged surface region that overlaps the Y RNA binding site.
38. Fuchs G., Stein A.J., Fu C., Reinisch K.M., and Wolin S.L. Structural and biochemical basis for misfolded RNA recognition by the Ro protein. Nat Struct Mol Biol 13 (2006) 1002-1009. The features by which X. laevis Ro recognizes misfolded RNAs are investigated. Ro binding to a misfolded pre-5S rRNA requires a single-stranded 3′ end of at least five nucleotides and also helical elements. The sequences of the helices and the tail are largely unimportant, indicating that Ro might be able to interact with many different structured RNAs. A crystal structure of Ro complexed with a misfolded pre-5S rRNA fragment confirms that the tail inserts into the central cavity while a helix binds to the outer surface of the ring.
39. Shimaoka M., Takagi J., and Springer T.A. Conformational regulation of integrin structure and function. Annu Rev Biophys Biomol Struct 31 (2002) 485-516
40. Liu Q., Greimann J.C., and Lima C.D. Reconstitution, activities, and structure of the eukaryotic exosome. Cell 127 (2006) 1223-1237. This paper presents the structure of the heterononameric human exosome. Additionally, nine-, ten- and eleven-subunit yeast exosomes were reconstituted. Biochemical analyses with both these larger subassemblies, as well as with smaller subassemblies, such as human Rrp41/Rrp45, were used in identifying and characterizing the roles of different human and yeast subunits in catalysis.
41. Dziembowski A., Lorentzen E., Conti E., and Séraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14 (2007) 15-22. The purified yeast exosome is found to have hydrolytic, but not phosphorolytic, exoribonuclease activity. Biochemical and genetic experiments indicate that Rrp44p/Dis3p is the only one of the ten subunits of the core exosome that has enzymatic activity, while the subunits containing RNase PH-like domains are catalytically inactive.