RNA-dependent pseudouridylation catalyzed by box H/ACA RNPs

Abstract

BACKGROUND: Pseudouridine (Y) is the most abundant post-transcriptionally modified nucleotide found in RNA. Y is clustered in functionally important and evolutionary conserved regions of RNAs in all three domains of life. Pseudouridylation is catalyzed by two distinct mechanisms: an RNA-independent and an RNA-dependent mechanism. The former involves a group of stand-alone protein enzymes, and the latter involves a family of complex enzymes called box H/ACA RNPs, each of which consists of one RNA (box H/ACA RNA) and a set of four core proteins. Over the years, the mechanism of RNA-dependent pseudouridylation has been extensively studied. The crystal structures of partial and complete box H/ACA RNP have been solved. However, the detailed picture of RNA-dependent pseudouridylation is still not entirely clear.

OBJECTIVE: In this work, we review what is known about box H/ACA RNP and the mechanism by which box H/ACA RNP catalyzes RNA-dependent pseudouridylation. We also discuss some examples of the dual nature and redundancy of box H/ACA RNPs that deviate from the usual mechanism.

METHODS: A methodical literature search was performed using the Pubmed central search engine and International Digital Publishing Forum (EPUB) using the following keywords: “pseudouridylation,” “pseudouridine,” and “box H/ACA RNP.” The necessary information was extracted and cited.

RESULTS: A detailed introduction is made including the discovery, mechanism and crystal structure of box H/ACA RNP. Three sequence/structural requirements for box H/ACA RNA-guided pseudouridylation are discussed and the exceptions to those rules are explored.

CONCLUSION: Over the years, box H/ACA RNP-catalyzed pseudouridylation has been extensively studied, generating fruitful results. However, a detailed picture regarding the mechanism of this reaction is still to be deciphered. More work is needed to fully understand box H/ACA RNP-catalyzed pseudouridylation.

Acknowledgments

We thank the members of the Yu laboratory for helpful discussions on the manuscript. The work carried out in the Yu laboratory was supported by grant GM104077 from NIH (to Y-T Yu).

Compliance with ethics guidelines

Yi-Tao Yu and Meemanage D. De Zoysa declare that they have no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

References

1 Baker D L, Youssef O A, Chastkofsky M I R, Dy D A, Terns R M, Terns M P (2005). RNA-guided RNA modification: functional organization of the archaeal H/ACA RNP. Genes Dev, 19(10): 1238–1248

PMID

2 Balakin A G, Smith L, Fournier M J (1996). The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell, 86(5): 823–834

PMID

3 Basak A, Query C C (2014). A pseudouridine residue in the spliceosome core is part of the filamentous growth program in yeast. Cell Reports, 8(4): 966–973

PMID

4 Becker H F, Motorin Y, Planta R J, Grosjean H (1997). The yeast gene YNL292w encodes a pseudouridine synthase (Pus4) catalyzing the formation of psi55 in both mitochondrial and cytoplasmic tRNAs. Nucleic Acids Res, 25(22): 4493–4499

PMID

5 Bortolin M L, Ganot P, Kiss T (1999). Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs. EMBO J, 18(2): 457–469

PMID

6 Branlant C, Krol A, Machatt M A, Pouyet J, Ebel J P, Edwards K, Kössel H (1981). Primary and secondary structures of Escherichia coli MRE 600 23S ribosomal RNA. Comparison with models of secondary structure for maize chloroplast 23S rRNA and for large portions of mouse and human 16S mitochondrial rRNAs. Nucleic Acids Res, 9(17): 4303–4324

PMID

7 Carlile T M, Rojas-Duran M F, Zinshteyn B, Shin H, Bartoli K M, Gilbert W V (2014). Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature, 515(7525): 143–146

PMID

8 Charette M, Gray M W (2000). Pseudouridine in RNA: what, where, how, and why. IUBMB Life, 49(5): 341–351

PMID

9 Charpentier B, Muller S, Branlant C (2005). Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res, 33(10): 3133–3144

PMID

10 Cohn W E (1959). 5-Ribosyl uracil, a carbon-carbon ribofuranosyl nucleoside in ribonucleic acids. Biochim Biophys Acta, 32: 569–571

PMID

11 Deryusheva S, Gall J G (2013). Novel small Cajal-body-specific RNAs identified in Drosophila: probing guide RNA function. RNA, 19(12): 1802–1814

PMID

12 Deryusheva S, Gall J G (2017). Dual nature of pseudouridylation in U2 snRNA: Pus1p-dependent and Pus1p-independent activities in yeasts and higher eukaryotes. RNA, 23(7): 1060–1067

PMID

13 Dönmez G, Hartmuth K, Lührmann R (2004). Modified nucleotides at the 5′ end of human U2 snRNA are required for spliceosomal E-complex formation. RNA, 10(12): 1925–1933

PMID

14 Duan J, Li L, Lu J, Wang W, Ye K (2009). Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol Cell, 34(4): 427–439

PMID

15 Ganot P, Bortolin M L, Kiss T (1997a). Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell, 89(5): 799–809

PMID

16 Ganot P, Caizergues-Ferrer M, Kiss T (1997b). The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. Genes Dev, 11(7): 941–956

PMID

17 Ge J, Yu Y T (2013). RNA pseudouridylation: new insights into an old modification. Trends Biochem Sci, 38(4): 210–218

PMID

18 Girard J P, Lehtonen H, Caizergues-Ferrer M, Amalric F, Tollervey D, Lapeyre B (1992). GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast. EMBO J, 11(2): 673–682

PMID

19 Grosjean H (2005). Modification and editing of RNA: historical overview and important facts to remember. In: H. Grosjean, ed. Fine-Tuning of RNA Functions by Modification and Editing. Berlin: Springer Berlin Heidelberg, pp. 1–22

20 Hamma T, Reichow S L, Varani G, Ferré-D’Amaré A R (2005). The Cbf5-Nop10 complex is a molecular bracket that organizes box H/ACA RNPs. Nat Struct Mol Biol, 12(12): 1101–1107

PMID

21 Henras A, Henry Y, Bousquet-Antonelli C, Noaillac-Depeyre J, Gélugne J P, Caizergues-Ferrer M (1998). Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J, 17(23): 7078–7090

PMID

22 Hopper A K, Phizicky E M (2003). tRNA transfers to the limelight. Genes Dev, 17(2): 162–180

PMID

23 Hüttenhofer A, Kiefmann M, Meier-Ewert S, O’Brien J, Lehrach H, Bachellerie J P, Brosius J (2001). RNomics: an experimental approach that identifies 201 candidates for novel, small, non-messenger RNAs in mouse. EMBO J, 20(11): 2943–2953

PMID

24 Jack K, Bellodi C, Landry D M, Niederer R O, Meskauskas A, Musalgaonkar S, Kopmar N, Krasnykh O, Dean A M, Thompson S R, Ruggero D, Dinman J D (2011). rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol Cell, 44(4): 660–666

PMID

25 Jiang W, Middleton K, Yoon H J, Fouquet C, Carbon J (1993). An essential yeast protein, CBF5p, binds in vitro to centromeres and microtubules. Mol Cell Biol, 13(8): 4884–4893

PMID

26 Khanna M, Wu H, Johansson C, Caizergues-Ferrer M, Feigon J (2006). Structural study of the H/ACA snoRNP components Nop10p and the 3′ hairpin of U65 snoRNA. RNA, 12(1): 40–52

PMID

27 King T H, Liu B, McCully R R, Fournier M J (2003). Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell, 11(2): 425–435

PMID

28 Li H (2008). Unveiling substrate RNA binding to H/ACA RNPs: one side fits all. Curr Opin Struct Biol, 18(1): 78–85

PMID

29 Li L, Ye K (2006a). Crystal structure of an H/ACA box ribonucleoprotein particle. Nature, 443(7109): 302–307

PMID

30 Li L, Ye K (2006b). Crystal structure of an H/ACA box ribonucleoprotein particle. Nature, 443(7109): 302–307

PMID

31 Li S, Duan J, Li D, Yang B, Dong M, Ye K (2011). Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev, 25(22): 2409–2421

PMID

32 Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C (2015). Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nat Chem Biol, 11(8): 592–597

PMID

33 Liang B, Xue S, Terns R M, Terns M P, Li H (2007). Substrate RNA positioning in the archaeal H/ACA ribonucleoprotein complex. Nat Struct Mol Biol, 14(12): 1189–1195

PMID

34 Liang B, Zhou J, Kahen E, Terns R M, Terns M P, Li H (2009a). Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA. Nat Struct Mol Biol, 16(7): 740–746

PMID

35 Liang X H, Liu Q, Fournier M J (2009b). Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. RNA, 15(9): 1716–1728

PMID

36 Lovejoy A F, Riordan D P, Brown P O (2014). Transcriptome-wide mapping of pseudouridines: pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLoS One, 9(10): e110799

PMID

37 Ma X, Zhao X, Yu Y T (2003). Pseudouridylation (Y) of U2 snRNA in S. cerevisiae is catalyzed by an RNA-independent mechanism. EMBO J, 22(8): 1889–1897

PMID

38 Manival X, Charron C, Fourmann J B, Godard F, Charpentier B, Branlant C (2006). Crystal structure determination and site-directed mutagenesis of the Pyrococcus abyssi aCBF5-aNOP10 complex reveal crucial roles of the C-terminal domains of both proteins in H/ACA sRNP activity. Nucleic Acids Res, 34(3): 826–839

PMID

39 Massenet S, Mougin A, Branlant C (1998). Posttranscriptional Modifications in the U Small Nuclear RNAs. In: Grosjean H, Benne R, eds. Modification and Editing of RNA. Washington D. C.: ASM Press

40 Meier U T (2005). The many facets of H/ACA ribonucleoproteins. Chromosoma, 114(1): 1–14

PMID

41 Mitchell J R, Wood E, Collins K (1999). A telomerase component is defective in the human disease dyskeratosis congenita. Nature, 402: 551

42 Ni J, Tien A L, Fournier M J (1997). Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell, 89(4): 565–573

PMID

43 Nurse K, Wrzesinski J, Bakin A, Lane B G, Ofengand J (1995). Purification, cloning, and properties of the tRNA psi 55 synthase from Escherichia coli. RNA, 1(1): 102–112

PMID

44 Ofengand J, Fournier M J (1998). The Pseudouridine Residues of rRNA: Number, Location, Biosynthesis, and Function. In: Grosjean H, Benne R., eds. Modification and Editing of RNA. Washington D. C.: ASM Press

45 Piekna-Przybylska D, Przybylski P, Baudin-Baillieu A, Rousset J P, Fournier M J (2008). Ribosome performance is enhanced by a rich cluster of pseudouridines in the A-site finger region of the large subunit. J Biol Chem, 283(38): 26026–26036

PMID

46 Rashid R, Liang B, Baker D L, Youssef O A, He Y, Phipps K, Terns R M, Terns M P, Li H (2006). Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol Cell, 21(2): 249–260

PMID

47 Reddy R, Busch H (1988). Small Nuclear RNAs: RNA Sequences, Structure, and Modifications. In: Birnstiel M L, ed. Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles. Berlin: Springer Berlin Heidelber, pp. 1–37

48 Reichow S L, Hamma T, Ferré-D’Amaré A R, Varani G (2007). The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res, 35(5): 1452–1464

PMID

49 Rozhdestvensky T S, Tang T H, Tchirkova I V, Brosius J, Bachellerie J P, Hüttenhofer A (2003). Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res, 31(3): 869–877

PMID

50 Schattner P, Barberan-Soler S, Lowe T M (2006). A computational screen for mammalian pseudouridylation guide H/ACA RNAs. RNA, 12(1): 15–25

PMID

51 Schattner P, Decatur W A, Davis C A, Ares M Jr, Fournier M J, Lowe T M (2004). Genome-wide searching for pseudouridylation guide snoRNAs: analysis of the Saccharomyces cerevisiae genome. Nucleic Acids Res, 32(14): 4281–4296

PMID

52 Schwartz S, Bernstein D A, Mumbach M R, Jovanovic M, Herbst R H, León-Ricardo B X, Engreitz J M, Guttman M, Satija R, Lander E S, Fink G, Regev A (2014). Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell, 159(1): 148–162

PMID

53 Sprinzl M, Vassilenko K S (2005). Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res, 33(Database issue): D139–D140

PMID

54 Terns M, Terns R (2006). Noncoding RNAs of the H/ACA family. Cold Spring Harb Symp Quant Biol, 71(0): 395–405

PMID

55 Torchet C, Badis G, Devaux F, Costanzo G, Werner M, Jacquier A (2005). The complete set of H/ACA snoRNAs that guide rRNA pseudouridylations in Saccharomyces cerevisiae. RNA, 11(6): 928–938

PMID

56 Vitali P, Royo H, Seitz H, Bachellerie J P, Hüttenhofer A, Cavaillé J (2003). Identification of 13 novel human modification guide RNAs. Nucleic Acids Res, 31(22): 6543–6551

PMID

57 Watkins N J, Gottschalk A, Neubauer G, Kastner B, Fabrizio P, Mann M, Lührmann R (1998). Cbf5p, a potential pseudouridine synthase, and Nhp2p, a putative RNA-binding protein, are present together with Gar1p in all H BOX/ACA-motif snoRNPs and constitute a common bipartite structure. RNA, 4(12): 1549–1568

PMID

58 Wu G, Adachi H, Ge J, Stephenson D, Query C C, Yu Y T (2016). Pseudouridines in U2 snRNA stimulate the ATPase activity of Prp5 during spliceosome assembly. EMBO J, 35(6): 654–667

PMID

59 Wu G, Xiao M, Yang C, Yu Y T (2011). U2 snRNA is inducibly pseudouridylated at novel sites by Pus7p and snR81 RNP. EMBO J, 30(1): 79–89

PMID

60 Wu G, Yu A T, Kantartzis A, Yu Y T (2011). Functions and mechanisms of spliceosomal small nuclear RNA pseudouridylation. Wiley Interdiscip Rev RNA, 2(4): 571–581

PMID

61 Xiao M, Yang C, Schattner P, Yu Y T (2009). Functionality and substrate specificity of human box H/ACA guide RNAs. RNA, 15(1): 176–186

PMID

62 Yang C, McPheeters D S, Yu Y T (2005). y35 in the branch site recognition region of U2 small nuclear RNA is important for pre-mRNA splicing in Saccharomyces cerevisiae. J Biol Chem, 280(8): 6655–6662

PMID

63 Ye K (2007). H/ACA guide RNAs, proteins and complexes. Curr Opin Struct Biol, 17(3): 287–292

PMID

64 Yu A T, Ge J, Yu Y T (2011). Pseudouridines in spliceosomal snRNAs. Protein Cell, 2(9): 712–725

PMID

65 Yu Y T, Meier U T (2014). RNA-guided isomerization of uridine to pseudouridine--pseudouridylation. RNA Biol, 11(12): 1483–1494

PMID

66 Yu Y T, Shu M D, Steitz J A (1998). Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J, 17(19): 5783–5795

PMID

67 Yu Y T, Terns R M, Terns M P (2005). Mechanisms and functions of RNA-guided RNA modification. In: Grosjean H. ed. Fine-Tuning of RNA Functions by Modification and Editing. Berlin: Springer Berlin Heidelberg, pp. 223–262

68 Zebarjadian Y, King T, Fournier M J, Clarke L, Carbon J (1999). Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA. Mol Cell Biol, 19(11): 7461–7472

PMID

69 Zhao X, Li Z H, Terns R M, Terns M P, Yu Y T (2002). An H/ACA guide RNA directs U2 pseudouridylation at two different sites in the branchpoint recognition region in Xenopus oocytes. RNA, 8(12): 1515–1525

PMID

70 Zhao X, Yu Y T (2004). Pseudouridines in and near the branch site recognition region of U2 snRNA are required for snRNP biogenesis and pre-mRNA splicing in Xenopus oocytes. RNA, 10(4): 681–690

PMID