RNA-guided Nucleotide Modification of Ribosomal and Other RNAs
Year: 2003
Type: review
Abstract: ribonucleoprotein ribosomal RNA ribose-methylated nucleotide pseudouridine small nucleolar RNA small nucleolar ribonucleoprotein complex small nuclear RNA snoRNA-like RNA/RNP Cajal body nucleolar body small Cajal body RNA/RNP RNA polymerase II nucleotide(s) spliced leader One of the exciting frontiers in the field of RNA editing is the phenomenon of RNA-guided nucleotide modification. In this type of editing, a nucleotide in a precursor RNA is converted to another form by an RNA-protein complex (RNP)1 (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar). The RNPs that mediate these reactions include a guide RNA that provides site specificity through base pairing with the substrate and a set of proteins, one of which catalyzes the modification reaction. The phenomenon was first discovered in the modification of ribosomal RNA (rRNA) in the nucleolus of eukaryotic cells (Fig. 1). Two common alterations are relevant, formation of 2′-O-methylated nucleosides (Nm; the guided mechanism was reported in 1996) and conversion of uridine to pseudouridine (Ψ; the guided process was reported in 1997) (2Kiss-Laszlo Z. Henry Y. Bachellerie J.P. Caizergues-Ferrer M. Kiss T. Cell. 1996; 85: 1077-1088Abstract Full Text Full Text PDF PubMed Scopus (662) Google Scholar, 3Ni J. Tien A.L. Fournier M.J. Cell. 1997; 89: 565-573Abstract Full Text Full Text PDF PubMed Scopus (423) Google Scholar, 4Ganot P. Bortolin M.L. Kiss T. Cell. 1997; 89: 799-809Abstract Full Text Full Text PDF PubMed Scopus (494) Google Scholar). These modifications are mediated by two large, heterogeneous populations of RNPs that are modification type-specific and site-specific. The RNPs contain a small nucleolar RNA (snoRNA) and several associated proteins, and the snoRNA-protein complexes are called snoRNPs (“snorps”). The snoRNA provides the guide function, and an integral snoRNP protein catalyzes the modification reaction. When discovered, this type of reaction scheme was not only novel but in sharp contrast to the rRNA modification schemes used by Eubacteria, where the synthesis of Nm and Ψ is mediated (thus far) by protein enzymes that do not include an RNA co-factor (5Ofengand J. Rudd K. Garrett R.A. Douthwaite S.R. Liljas A. Matheson A.T. Moore P.B. Noller H.F. The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions. ASM Press, Washington, D. C.2000: 175-189Google Scholar). Guided modification was subsequently discovered to apply to the U6 snRNA (small nuclear RNA in vertebrates and Caenorhabditis elegans) and likely to mRNA (mammals, trypanosomes) (6Tycowski K.T. You Z.H. Graham P.J. Steitz J.A. Mol. Cell. 1998; 2: 629-638Abstract Full Text Full Text PDF PubMed Scopus (171) Google Scholar, 7Ganot P. Jady B.E. Bortolin M.L. Darzacq X. Kiss T. Mol. Cell. Biol. 1999; 19: 6906-6917Crossref PubMed Scopus (131) Google Scholar, 8Cavaille J. Buiting K. Kiefmann M. Lalande M. Brannan C.I. Horsthemke B. Bachellerie J.P. Brosius J. Huttenhofer A. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 14311-14316Crossref PubMed Scopus (471) Google Scholar, 9Liang X.H., Xu, Y.X. Michaeli S. RNA. 2002; 8: 237-246Crossref PubMed Scopus (56) Google Scholar). Strikingly, from an evolutionary perspective, the new paradigm was also discovered (in 2000) to apply to Archaeal organisms where substrates include tRNA as well as rRNA (10Dennis P.P. Omer A. Lowe T. Mol. Microbiol. 2001; 40: 509-519Crossref PubMed Scopus (112) Google Scholar). Recent advances have revealed guided modification to be more complex and widespread and are almost certainly a harbinger of exciting new developments to come. Key developments include: 1) identification of new guide RNAs that reside in mammalian Cajal bodies (these RNAs are specific for the four snRNAs transcribed by RNA polymerase II (pol II), which are thought to undergo maturation and possibly RNP assembly at this location (11Darzacq X. Jady B.E. Verheggen C. Kiss A.M. Bertrand E. Kiss T. EMBO J. 2002; 21: 2746-2756Crossref PubMed Scopus (371) Google Scholar)); 2) evidence that the trypanosome trans-spliced leader is a substrate for guided modification (9Liang X.H., Xu, Y.X. Michaeli S. RNA. 2002; 8: 237-246Crossref PubMed Scopus (56) Google Scholar); and 3) successful development of the first cell-free Nm modification system, using recombinant archaeal components (12Omer A.D. Ziesche S. Ebhardt H. Dennis P.P. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: 5289-5294Crossref PubMed Scopus (160) Google Scholar). Taken together, these findings argue that additional modifying RNPs and substrates subjected to RNA-guided modification will be discovered. In this minireview we describe the present state of knowledge about the various RNP-modifying complexes, the processes they mediate, where in the cell these reactions occur, and the range of substrates. Because of limited space the reader is also referred to other recent reviews (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar, 13Weinstein L.B. Steitz J.A. Curr. Opin. Cell Biol. 1999; 11: 378-384Crossref PubMed Scopus (252) Google Scholar, 14Warner J.R. Cell. 2001; 107: 133-136Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar, 15Fatica A. Tollervey D. Curr. Opin. Cell Biol. 2002; 14: 313-318Crossref PubMed Scopus (425) Google Scholar, 16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google Scholar, 17Kiss T. Cell. 2002; 109: 145-148Abstract Full Text Full Text PDF PubMed Scopus (612) Google Scholar, 18Terns M.P. Terns R.M. Gene Expr. 2002; 10: 17-39PubMed Google Scholar). The Nm and Ψ nucleotides appear to be universal among rRNAs and small stable RNAs such as splicing snRNAs, tRNAs, and snoRNAs; however, the abundance and locations of these nucleotides vary phylogenetically (19Grosjean, H., and Benne, R. (eds) (1998) Modification and Editing of RNA, ASM Press, Washington, D. C.Google Scholar, 20Gu J. Chen Y. Reddy R. Nucleic Acids Res. 1998; 26: 160-162Crossref PubMed Scopus (19) Google Scholar, 21Rozenski J. Crain P.F. McCloskey J.A. Nucleic Acids Res. 1999; 27: 196-197Crossref PubMed Scopus (349) Google Scholar). Although the modifications are believed to be beneficial, evidence is still sparse. Blocking Nm or Ψ modification at a global level in yeast rRNA has strong negative effects on growth rate (22Tollervey D. Lehtonen H. Jansen R. Kern H. Hurt E.C. Cell. 1993; 72: 443-457Abstract Full Text PDF PubMed Scopus (407) Google Scholar,23Zebarjadian Y. King T. Fournier M.J. Clarke L. Carbon J. Mol. Cell. Biol. 1999; 19: 7461-7472Crossref PubMed Scopus (191) Google Scholar), and the absence of Nm and Ψ in U2 snRNA impairs its assembly into an active spliceosome in Xenopus oocytes (24Yu Y.T. Shu M.D. Steitz J.A. EMBO J. 1998; 17: 5783-5795Crossref PubMed Scopus (207) Google Scholar). New three-dimensional modification maps of rRNA show the modifications are heavily concentrated in regions of the ribosome known or predicted to be functionally important, suggesting that the modifications benefit ribosome activity, either directly or indirectly (25Decatur W.A. Fournier M.J. Trends Biochem. Sci. 2002; 27: 344-351Abstract Full Text Full Text PDF PubMed Scopus (463) Google Scholar, 26Hansen M.A. Kirpekar F. Ritterbusch W. Vester B. RNA (N. Y.). 2002; 8: 202-213Crossref PubMed Scopus (50) Google Scholar, 27Ofengand J. FEBS Lett. 2002; 514: 17-25Crossref PubMed Scopus (145) Google Scholar). At the level of individual modifications blocking Nm or Ψ synthesis in bacterial or yeast rRNA has, thus far, resulted in either no detectable effect or only a slight effect on growth rate, implying that many (perhaps most) modifications affect ribosome structure and function in a synergistic way (25Decatur W.A. Fournier M.J. Trends Biochem. Sci. 2002; 27: 344-351Abstract Full Text Full Text PDF PubMed Scopus (463) Google Scholar, 27Ofengand J. FEBS Lett. 2002; 514: 17-25Crossref PubMed Scopus (145) Google Scholar, 28King, T. H., Liu, B., McCully, R. R., and Fournier, M. J. (2003) Mol. Cell, in pressGoogle Scholar). The changes in RNA structure caused by modification could “fine-tune” many events in rRNA folding, rRNP assembly, or ribosome activity as well as trafficking and half-life. The same reasoning applies to modification of the small RNAs (e.g.Ref. 29Newby M.I. Greenbaum N.L. RNA. 2001; 7: 833-845Crossref PubMed Scopus (92) Google Scholar). Since their discovery, scores of guide snoRNAs have been identified for rRNA, primarily in yeast and human cells, and it seems likely that most Nm and Ψ modifications in cytoplasmic rRNA are formed by snoRNPs (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar). In support of this view, candidate guide snoRNAs have been identified in yeast for 51 of 55 known Nm sites and 30 of 44 Ψs (30Lowe T.M. Eddy S.R. Science. 1999; 283: 1168-1171Crossref PubMed Scopus (386) Google Scholar, 31Samarsky D.A. Fournier M.J. Nucleic Acids Res. 1999; 27: 161-164Crossref PubMed Scopus (69) Google Scholar). 2W. A. Decatur and M. J. Fournier, unpublished data. However, it is possible that some modifications are created by enzymes without an RNA cofactor. The snoRNPs are thought to act early in rRNA synthesis as the modification level of uncleaved, primary transcripts is high (14Warner J.R. Cell. 2001; 107: 133-136Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar,15Fatica A. Tollervey D. Curr. Opin. Cell Biol. 2002; 14: 313-318Crossref PubMed Scopus (425) Google Scholar, 32Udem S.A. Warner J.R. J. Mol. Biol. 1972; 65: 227-242Crossref PubMed Scopus (226) Google Scholar, 33Salim M. Maden B.E. Nature. 1973; 244: 334-336Crossref PubMed Scopus (41) Google Scholar, 34Peculis B.A. RNA (N. Y.). 2001; 7: 207-219Crossref PubMed Scopus (20) Google Scholar). This situation is consistent with modification occurring co-transcriptionally or in large pre-ribosome complexes that evolve into the individual subunits (15Fatica A. Tollervey D. Curr. Opin. Cell Biol. 2002; 14: 313-318Crossref PubMed Scopus (425) Google Scholar) (Fig. 1 A). In addition to mediating modification reactions, a few snoRNPs are required for processing (cleavage) of pre-rRNA (17Kiss T. Cell. 2002; 109: 145-148Abstract Full Text Full Text PDF PubMed Scopus (612) Google Scholar). The corresponding snoRNAs interact directly with rRNA, but the actual functions of the snoRNPs in processing are not known in most cases. Additional roles for snoRNAs also seem possible. For example, in the context of guided modification, a snoRNP could affect other aspects of RNA synthesis or function in addition to modification (see below). Each general class of guide snoRNAs and snoRNPs is both modification type-specific and site-specific (Fig. 1, B andC). Each class of snoRNA contains one or two targeting motifs that act independently at sites in the same or different pre-rRNA(s), and each class of snoRNP contains a different set of four common core proteins. During modification, the guide sequence selects (by complementary base pairing) a target sequence in the substrate RNA, and modification occurs within this target sequence at a characteristic distance from a short “box” element in the interacting snoRNA. The Nm guide snoRNAs contain one or two pairs of small, distinguishing sequence elements called boxes C and D, and C′ and D′. These elements define the C/D family of snoRNAs, which also includes a few species involved in rRNA processing (16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google Scholar, 17Kiss T. Cell. 2002; 109: 145-148Abstract Full Text Full Text PDF PubMed Scopus (612) Google Scholar). Boxes C/D the and of the RNA and boxes are The guide sequence is of the element and of nucleotides (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar, J.P. B. M. J. Fournier M.J. Trends Biochem. Sci. 20: Full Text PDF PubMed Scopus Google Scholar). The C/D boxes are required for snoRNA and formation that snoRNAs are from of protein (16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google the C/D elements are also and for snoRNAs to the which occurs by way of the Cajal bodies in cells and in at some functionally nucleolar bodies in yeast (11Darzacq X. Jady B.E. Verheggen C. Kiss A.M. Bertrand E. Kiss T. EMBO J. 2002; 21: 2746-2756Crossref PubMed Scopus (371) Google Scholar, 18Terns M.P. Terns R.M. Gene Expr. 2002; 10: 17-39PubMed Google Scholar, C. J. M. Tollervey D. R. Bertrand E. EMBO J. 2001; 20: PubMed Scopus Google Scholar) (see below). These findings that snoRNA synthesis and are (16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google Scholar). The snoRNPs have four common core proteins. The of in a is not known is it known modifying snoRNPs are for the RNA The core in yeast and to a characteristic structure that includes the C/D elements in the (Fig. 1 is also of the where it a common RNA called the V. B. S. P. A. M. M. C. R. Cell. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar, T.M. Moore P.B. Steitz EMBO J. 2001; 20: PubMed Scopus Google Scholar). and are to each other and both interact with snoRNA (16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google Scholar, K. Z.H. Terns R.M. Terns M.P. Steitz J.A. EMBO J. 2002; 21: PubMed Scopus Google Scholar). is to be the In support of this in elements have been to in yeast In a structure of an archaeal that contains the elements that most of the protein has a three-dimensional structure that of many H. D. R. EMBO J. 2000; 19: PubMed Scopus Google Scholar). In a process to be but the snoRNP on a of a nucleotide that is base with the snoRNA guide The target site is nucleotides of nucleotides within the of (Fig. 1 Key to be include base pairing occurs the of the guide sequence base pairs are required for to J. Bachellerie J.P. Nucleic Acids Res. 1998; 26: PubMed Scopus Google and to the target nucleotide the of other snoRNP or such as a Each type of element is required for boxes and they are and the C/D and pairs they affect protein (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar, V. B. S. P. A. M. M. C. R. Cell. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar, K. Z.H. Terns R.M. Terns M.P. Steitz J.A. EMBO J. 2002; 21: PubMed Scopus Google Scholar). The Ψ guide snoRNAs have characteristic small sequence elements referred to as boxes and and are of a family of snoRNAs (1Kiss T. EMBO J. 2001; 20: 3617-3622Crossref PubMed Scopus (354) Google Scholar, 27Ofengand J. FEBS Lett. 2002; 514: 17-25Crossref PubMed Scopus (145) Google Scholar, L. Fournier M.J. Cell. 1996; Full Text Full Text PDF PubMed Scopus Google Scholar) (Fig. 1 the C/D the and boxes and are required for processing of snoRNA protein and (16Filipowicz W. Pogacic V. Curr. Opin. Cell Biol. 2002; 14: 319-327Crossref PubMed Scopus (323) Google M.P. Terns R.M. Gene Expr. 2002; 10: 17-39PubMed Google Scholar). snoRNAs are guide However, as with the C/D snoRNA a few in rRNA and RNA but not formation (17Kiss T. Cell. 2002; 109: 145-148Abstract Full Text Full Text PDF PubMed Scopus (612) Google Scholar, 18Terns M.P. Terns R.M. Gene Expr. 2002; 10: 17-39PubMed Google Scholar). The snoRNAs that guide Ψ formation have a structure of The and boxes in the and targeting base pairing through two short guide in a of the and a distance of nucleotides from the or J. Tien A.L. Fournier M.J. Cell. 1997; 89: 565-573Abstract Full Text Full Text PDF PubMed Scopus (423) Google P. Bortolin M.L. Kiss T. Cell. 1997; 89: 799-809Abstract Full Text Full Text PDF PubMed Scopus (494) Google Scholar). the uridine to be in a the The four core of the snoRNPs from in the C/D and the same about the and of among the individual The core in yeast include: and is to be the pseudouridine In support of this view, and contain elements among known Ψ and in two such elements in yeast Ψ formation in rRNA in a global Y. King T. Fournier M.J. Clarke L. Carbon J. Mol. Cell. Biol. 1999; 19: 7461-7472Crossref PubMed Scopus (191) Google Scholar). in human have been to a in but with function be the of the Ψ synthesis (17Kiss T. Cell. 2002; 109: 145-148Abstract Full Text Full Text PDF PubMed Scopus (612) Google Scholar). the protein in the snoRNPs and the protein in the C/D snoRNPs are to each other (in and suggesting the have The of the snoRNAs is in of two yeast where two are at one to form a structure at and A. B. P. M. R. RNA (N. Y.). 1998; PubMed Scopus Google Scholar). 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The small Cajal called have the of the snoRNAs, that some have an and of guide the set of species with both Nm and Ψ modification motifs and species that the guide have been identified thus in the for known modifications in snRNAs and snoRNAs that in modification of pre-rRNA are also known to to Cajal bodies the nucleolar complex (11Darzacq X. Jady B.E. Verheggen C. Kiss A.M. Bertrand E. Kiss T. EMBO J. 2002; 21: 2746-2756Crossref PubMed Scopus (371) Google Scholar, D.A. Fournier M.J. Bertrand E. EMBO J. 1998; 17: PubMed Scopus Google Scholar, A. W. Terns R. Terns M.P. Mol. Biol. Cell. 1999; 10: PubMed Scopus Google Scholar, Z.H. Terns R.M. Terns M.P. RNA (N. Y.). 2001; 7: Google Scholar). These that the nucleolar specific guide RNAs possibly additional also undergo modification in Cajal bodies The new in of snoRNA-like guide RNAs in the for RNA in the Cajal could substrate or with that are specific for the to the new with yeast have identified novel called nucleolar bodies which have functions with Cajal bodies C. J. M. Tollervey D. R. Bertrand E. EMBO J. 2001; 20: PubMed Scopus Google Scholar, C. D. J. R. Bertrand E. EMBO J. 2002; 21: PubMed Scopus Google Scholar) (Fig. and snoRNAs, and C/D and snoRNP have been in the evidence that both snoRNAs and snRNAs undergo maturation events in nucleolar bodies from the that an that the of a of snoRNAs and the II snRNAs to be to this structure J. Verheggen C. Bertrand E. J. R. Mol. Cell. 2002; Full Text Full Text PDF PubMed Scopus Google Scholar). with functions of and the of occurs in the Cajal suggesting that formation of snoRNAs in this nuclear C. D. J. R. Bertrand E. 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The mRNA transcripts undergo splicing and to editing at four sites to with different Guided is predicted to at one of the editing of which are to each other a and to an site from the editing modification at such an editing site could have several effects on and function of the protein this guide RNA and several are at suggesting they have a in J. Buiting K. Kiefmann M. Lalande M. Brannan C.I. Horsthemke B. Bachellerie J.P. Brosius J. Huttenhofer A. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 14311-14316Crossref PubMed Scopus (471) Google Scholar, J. H. M. Bachellerie J.P. Mol. 2002; 11: PubMed Scopus Google Scholar). are that a trypanosome spliced leader guided Ψ modification (9Liang X.H., Xu, Y.X. Michaeli S. RNA. 2002; 8: 237-246Crossref PubMed Scopus (56) Google Scholar). a candidate guide RNA was identified (in both the nucleolus and that is predicted to target a site known to undergo modification, and the of in the RNA this modification. Because the RNA is spliced to a modification could affect the synthesis and activity of many proteins. These two with the that RNA-guided modification roles in the structure and function of as well as stable The Archaeal contains components of the eukaryotic Nm and Ψ snoRNPs (10Dennis P.P. Omer A. Lowe T. Mol. Microbiol. 2001; 40: 509-519Crossref PubMed Scopus (112) Google Scholar). of candidate Nm guide RNAs for rRNA and tRNA have been and the first Ψ guide RNAs have also been reported RNA Bachellerie J.P. T. Bortolin M.L. H. M. T. Brosius J. Huttenhofer A. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: PubMed Scopus Google Scholar). 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This that an complex only the core and guide RNA is to site-specific the also the that is the Nm This to eukaryotic for Ψ modification. is to that the of RNAs subjected to RNA-guided modification will in for eukaryotic RNAs that through the Cajal bodies or In addition to and snRNAs, Cajal bodies also contain and splicing snRNAs and snRNA in formation of the of RNAs that appear to have a nucleolar is also and includes the U6 RNA, RNA, RNA, and transcripts T. Nucleic Acids Res. 1998; 26: PubMed Scopus Google Scholar, A. L. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: PubMed Scopus Google Scholar). the many small RNAs discovered are also for guided modifications Science. 2002; PubMed Scopus Google Scholar). The of the recent that the field of RNA-guided modification will an exciting of the RNA for many
Source: Journal of Biological Chemistry
Authors: Wayne A. Decatur, Maurille J. Fournier
Institution: University of Massachusetts Amherst
Language: English
Topic: RNA modifications and cancer
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: hybrid
Estimated APC paid: $3,430
OpenAlex ID: W2028400272