Caenorhabditis elegans pseudouridine synthase 1 activity in vivo: tRNA is a substrate, but not U2 small nuclear RNA

Biochemical Journal

Volumn 372, Issue 2, 2003, Pages 595-602

  Patton, Jeffrey R ^a   Padgett, Richard W ^b  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Knockout; Primer extension; TruA

Indexed keywords

CATALYSIS; ENZYMES; GENES; RNA; SUBSTRATES; SYNTHESIS (CHEMICAL); YEAST;

GENE CODING;

BIOCHEMISTRY;

NUCLEAR RNA; NUCLEOTIDE; PSEUDOURIDINE; PSEUDOURIDINE SYNTHASE 1; SMALL NUCLEAR RNA; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE;

AMINO ACID SUBSTITUTION; ARTICLE; CAENORHABDITIS ELEGANS; ENZYME ACTIVITY; EXON; GENE DELETION; GENETIC CODE; KNOCKOUT GENE; METAZOON; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; WORM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BLOTTING, SOUTHERN; CAENORHABDITIS ELEGANS; CATALYSIS; DNA, HELMINTH; HYDRO-LYASES; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PSEUDOURIDINE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICING; RNA, HELMINTH; RNA, SMALL NUCLEAR; RNA, TRANSFER; SUBSTRATE SPECIFICITY;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; EUKARYOTA; INVERTEBRATA; METAZOA; NEMATODA;

EID: 0037662639     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021938     Document Type: Article

References (56)

1. Auffinger, P. and Westhof, E. (1998) Appendix 5: Location and distribution of modified nucleotides in tRNA. In Modification and Editing of RNA (Grosjean, H. and Benne, R., eds.), pp. 569-576, ASM Press, Washington DC
2. Bjork, G. R., Ericson, J. U., Gustafsson, C. E., Hagervall, T. G., Jonsson, Y. H. and Wikstrom, P. M. (1987) Transfer RNA modification. Annu. Rev. Biochem. 56, 263-287
3. Johnson, L. and Soll, D. (1970) In vitro biosynthesis of pseudouridine at the polynucleotide level by an enzyme extract from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 67, 943-950
4. Massenet, S. A., Mougin, A. and Branlant, C. (1998) Posttranscriptional modifications of the U small nuclear RNAs. In Modification and Editing of RNA (Grosjean, H. and Benne, R., eds.), pp. 201-227, ASM Press, Washington DC
5. Ofengand, J. and Fournier, M. J. (1998) The pseudouridine residues of rRNA: Number, location, biosynthesis, and function. In Modification and Editing of RNA (Grosjean, H. and Benne, R., eds.), pp. 229-253, ASM Press, Washington, D.C
6. Simos, G., Tekotte, H., Grosjean, H., Segref, A., Sharma, K., Tollervey, D. and Hurt, E. C. (1996) Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J. 15, 2270-2284
7. Motorin, Y., Keith, G., Simon, C., Foiret, D., Simos, G., Hurt, E. and Grosjean, H. (1998) The yeast tRNA: pseudouridine synthase Pus1p displays a multisite substrate specificity. RNA 4, 856-869
8. Chen, J. and Patton, J. R. (1999) Cloning and characterization of a mammalian pseudouridine synthase. RNA 5, 409-419
9. Chen, J. and Patton, J. R. (2000) Mouse pseudouridine synthase 1: gene structure and alternative splicing of pre-mRNA. Biochem. J. 352, 465-473
10. Massenet, S., Motorin, Y., Lafontaine, D. L., Hurt, E. C., Grosjean, H. and Branlant, C. (1999) Pseudouridine mapping in the Saccharomyces cerevisiae spliceosomal U small nuclear RNAs (snRNAs) reveals that pseudouridine synthase pus1p exhibits a dual substrate specificity for U2 snRNA and tRNA. Mol. Cell. Biol. 19, 2142-2154
11. Ganot, P., Bortolin, M. L. and Kiss, T. (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89, 799-809
12. Ni, J., Tien, A. L. and Fournier, M. J. (1997) Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 89, 565-573
13. Jady, B. E. and Kiss, T. (2001) A small nucleolar guide RNA functions both in 2′-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA. EMBO J. 20, 541-551
14. Ganot, P., Jady, B. E., Bortolin, M. L., Darzacq, X. and Kiss, T. (1999) Nucleolar factors direct the 2′-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA. Mol. Cell. Biol. 19, 6906-6917
15. Zhao, X., Li, Z.-H., Terns, R. M., Terns, M. P. and Yu, Y.-T. (2002) An H/ACA guide RNA directs U2 pseudouridylation at two different sites in the branch point recognition region in Xenopus oocytes. RNA 8, 1515-1525
16. 1-labeled pseudouridine. J. Biol. Chem. 260, 9734-9741
17. Davis, D. R. (1995) Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 23, 5020-5026
18. 15N NMR studies of Escherichia coli tRNA(Phe) from hisT mutants: a structural role for pseudouridine. Biochemistry 30, 4223-4231
19. Durant, P. C. and Davis, D. R. (1999) Stabilization of the anticodon stem-loop of tRNALys,3 by an A+C base-pair and by pseudouridine. J. Mol. Biol. 285, 115-131
20. Davis, D. R., Veltri, C. A. and Nielsen, L. (1998) An RNA model system for investigation of pseudouridine stabilization of the codon-anticodon interaction in tRNALys, tRNAHis and tRNATyr. J. Biomol. Struct. Dyn. 15, 1121-1132
21. Tomita, K., Ueda, T. and Watanabe, K. (1999) The presence of pseudouridine in the anticodon alters the genetic code: a possible mechanism for assignment of the AAA lysine codon as asparagine in echinoderm mitochondria. Nucleic Acids Res. 27, 1683-1689
22. Zerfass, K. and Beier, H. (1992) Pseudouridine in the anticodon G psi A of plant cytoplasmic tRNA(Tyr) is required for UAG and UAA suppression in the TMV-specific context. Nucleic Acids Res. 20, 5911-5918
23. Perret, V., Garcia, A., Grosjean, H., Ebel, J. P., Florentz, C. and Giege, R. (1990) Relaxation of a transfer RNA specificity by removal of modified nucleotides. Nature (London) 344, 787-789
24. Yu, Y. T., Shu, M. D. and Steitz, J. A. (1998) Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J. 17, 5783-5795
25. Segault, V., Will, C. L., Sproat, B. S. and Luhrmann, R. (1995) In vitro reconstitution of mammalian U2 and U5 snRNPs active in splicing: Sm proteins are functionally interchangeable and are essential for the formation of functional U2 and U5 snRNPs. EMBO J. 14, 4010-4021
26. Becker, H. F., Motorin, Y., Planta, R. J. and 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, 4493-4499
27. Grosshans, H., Lecointe, F., Grosjean, H., Hurt, E. and Simos, G. (2001) Pus1p-dependent tRNA pseudouridinylation becomes essential when tRNA biogenesis is compromised in yeast. J. Biol. Chem. 276, 46333-46339
28. Kinghorn, S. M., O'Byrne, C. P., Booth, I. R. and Stansfield, I. (2002) Physiological analysis of the role of truB in Escherichia coli: a role for tRNA modification in extreme temperature resistance. Microbiology 148, 3511-3520
29. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
30. Mullis, K., Faloona, F., Scharf, S., Saiki, R., Horn, G. and Erlich, H. (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb. Syrup. Quant. Biol. 51, 263-273
31. Mullis, K. B. and Faloona, F. A. (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155, 335-350
32. Sanger, F., Nicklen, S. and Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74, 5463-5467
33. Lewis, J. A. and Fleming, J. T. (1995) Basic culture methods. In Caenorhabditis elegans: Modern Biological Analysis of an Organism. Methods in Cell Biology, vol. 48 (Epstein, H. F. and Shakes, D. C., eds.), pp. 3-29, Academic Press, New York
34. Johnstone, I. L. (1999) Molecular Biology. In C. elegans: a Practical Approach (Hope, I. A., ed.) pp. 201-225, Oxford University Press, Oxford
35. Barstead, R. J., Kleiman, L. and Waterston, R. H. (1991) Cloning, sequencing, and mapping of an alpha-actinin gene from the nematode Caenorhabditis elegans. Cell Motil. Cytoskeleton 20, 69-78
36. Williams, B. D., Schrank, B., Huynh, C., Shownkeen, R. and Waterston, R. H. (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131, 609-624
37. Bakin, A. V. and Ofengand, J. (1998) Mapping of pseudouridine residues in RNA to nucleotide resolution. Methods Mol. Biol. 77, 297-309
38. Baumstark, T. and Ahlquist, P. (2001) The brome mosaic virus RNA3 intergenic replication enhancer folds to mimic a tRNA TpsiC-stem loop and is modified in vivo. RNA 7, 1652-1670
39. Sambrook, J. and Rusell, D. W. (2001) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Press, Cold Spring Harbor, NY
40. Melton, D. A., Krieg, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K. and Green, M. R. (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12, 7035-7056
41. Hill, A. A., Hunter, C. P., Tsung, B. T., Tucker-Kellogg, G. and Brown, E. L. (2000) Genomic analysis of gene expression in C. elegans. Science 290, 809-812
42. Raychaudhuri, S., Niu, L., Conrad, J., Lane, B. G. and Ofengand, J. (1999) Functional effect of deletion and mutation of the Escherichia coli ribosomal RNA and tRNA pseudouridine synthase RluA. J. Biol. Chem. 274, 18880-18886
43. Huang, L., Pookanjanatavip, M., Gu, X. and Santi, D. V. (1998) A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 37, 344-351
44. Foster, P. G., Huang, L., Santi, D. V. and Stroud, R. M. (2000) The structural basis for tRNA recognition and pseudouridine formation by pseudouridine synthase I. Nat. Struct. Biol. 7, 23-27
45. Sprinzl, M., Horn, C., Brown, M, Ioudovitch, A. and Steinberg, S. (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 26, 148-153
46. Lowe, T. M. and Eddy, S. R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964
47. Lecointe, F., Simos, G., Sauer, A., Hurt, E. C., Motorin, Y. and Grosjean, H. (1998) Characterization of yeast protein Deg1 as pseudouridine synthase (Pus3) catalyzing the formation of psi 38 and psi 39 in tRNA anticodon loop. J. Biol. Chem. 273, 1316-1323
48. Chen, J. and Patton, J. R. (2000) Pseudouridine synthase 3 from mouse modifies the anticodon loop of tRNA. Biochemistry 39, 12723-12730
49. Ma, X., Zhao, X. and Yu, Y.-T. (2003) Pseudouridylation (ψ) of U2 snRNA in S. cerevisiae is catalyzed by an RNA-independent mechanism. EMBO J. 22, in the press
50. Guthrie, C. and Patterson, B. (1988) Spliceosomal snRNAs. Annu. Rev. Genet. 22, 387-419
51. Kiss, A. M., Jady, B. E., Darzacq, X., Verheggen, C., Bertrand, E. and Kiss, T. (2002) A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. Nucleic Acids Res. 30, 4643-4649
52. Lafontaine, D. L. J., Bousquet-Antonelli, C., Henry, Y., Caizergues-Ferrer, M. and Tollervey, D. (1998) The box H+ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase. Genes Dev. 12, 527-537
53. Heiss, N. S., Knight, S. W., Vulliamy, T. J., Klauck, S. M., Wiemann, S., Mason, P. J., Poustka, A. and Dokal, I. (1998) X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat. Genet. 19, 32-38
54. Gu, J., Patton, J. R., Shimba, S. and Reddy, R. (1996) Localization of modified nucleotides in Schizosaccharomyces pombe spliceosomal small nuclear RNAs: modified nucleotides are clustered in functionally important regions. RNA 2, 909-918
55. Reddy, R. and Busch, H. (1988) Small nuclear RNAs: RNA sequences, structure, and modifications. In Structure and Function of Major and Minor snRNPs (Birnstiel, M., ed.), pp. 1-37, Springer Verlag, Berlin
56. Koonin, E. V. (1996) Pseudouridine synthases: four families of enzymes containing a putative uridine-binding motif also conserved in dUTPases and dCTP deaminases. Nucleic Acids Res. 24, 2411-2415