Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins

EMBO Journal

Volumn 23, Issue 8, 2004, Pages 1857-1867

  Wang, Chen ^a   Meier, U Thomas ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Dyskeratosis congenita; H ACA snoRNAs; Pseudouridine synthase; Ribonucleoprotein particle assembly; Telomerase RNA

Indexed keywords

CORE PROTEIN; DYSKERIN; PROTEIN GAR1; PROTEIN NHP2; PROTEIN NOP10; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; TELOMERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CROSS LINKING; CYTOSOL; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSCRIPTION; IMMUNOPRECIPITATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RNA SEQUENCE; RNA TRANSLATION;

ANIMALS; CELL EXTRACTS; HUMANS; MAMMALS; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; RATS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA; RNA, SMALL NUCLEOLAR; RNA-BINDING PROTEINS; TELOMERASE; ULTRAVIOLET RAYS; URIDINE;

ANIMALIA; MAMMALIA;

EID: 2442542173     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600181     Document Type: Article

References (59)

1. Aravind L, Koonin EV (1999) Novel predicted RNA-binding domains associated with the translation machinery. J Mol Evol 48: 291-302
2. Bachellerie JP, Cavaille J (1997) Guiding ribose methylation of rRNA. Trends Biochem Sci 22: 257-261
3. Bagni C, Lapeyre B (1998) Gar1p binds to the small nucleolar RNAs snR10 and snR30 in vitro through a nontypical RNA binding element. J Biol Chem 273: 10868-10873
4. Bonnerot C, Pintard L, Lutfalla G (2003) Functional redundancy of Spb1p and a snR52-dependent mechanism for the 2′-O-ribose methylation of a conserved rRNA position in yeast. Mol Cell 12: 1309-1315
5. Bortolin ML, 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: 457-469
6. Bousquet-Antonelli C, Henry Y, Gélugne J-P, Caizergues-Ferrer M, Kiss T (1997) A small nucleolar RNP protein is required for pseudouridylation of eukaryotic ribosomal RNAs. EMBO J 16: 4770-4776
7. Cahill NM, Friend K, Speckmann W, Li ZH, Terns RM, Terns MP, Steitz JA (2002) Site-specific cross-linking analyses reveal an asymmetric protein distribution for a box C/D snoRNP. EMBO J 21: 3816-3828
8. Chartrand P, Meng XH, Singer RH, Long RM (1999) Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo. Curr Biol 9: 333-336
9. Decatur WA, Fournier MJ (2003) RNA-guided nucleotide modification of ribosomal and other RNAs. J Biol Chem 278: 695-698
10. Dez C, Henras A, Faucon B, Lafontaine D, Caizergues-Ferrer M, Henry Y (2001) Stable expression in yeast of the mature form of human telomerase RNA depends on its association with the box H/ACA small nucleolar RNP proteins Cbf5p, Nhp2p and Nop10p. Nucleic Acids Res 29: 598-603
11. Dez C, Noaillac-Depeyre J, Caizergues-Ferrer M, Henry Y (2002) Naf1p, an essential nucleoplasmic factor specifically required for accumulation of box H/ACA small nucleolar RNPs. Mol Cell Biol 22: 7053-7065
12. Dokal I, Vulliamy T (2003) Dyskeratosis congenita: its link to telomerase and aplastic anaemia. Blood Rev 17: 217-225
13. Dragon F, Pogacic V, Filipowicz W (2000) In vitro assembly of human H/ ACA small nucleolar RNPs reveals unique features of U17 and telomerase RNAs. Mol Cell Biol 20: 3037-3048
14. Fatica A, Dlakic M, Tollervey D (2002) Naf1 p is a box H/ACA snoRNP assembly factor. RNA 8: 1502-1514
15. Feng J, Funk WD, Wang SS, Weinrich SL, Avilion AA, Chiu CP, Adams RR, Chang E, Allsopp RC, Yu J, Le S, West MD, Harley CB, Andrews WH, Greider CW, Villeponteau B (1995) The RNA component of human telomerase. Science 269: 1236-1241
16. Frankel A, Clarke S (1999) RNase treatment of yeast and mammalian cell extracts affects in vitro substrate methylation by type I protein arginine N-methyltransferases. Biochem Biophys Res Commun 259: 391-400
17. Ganot P, Bortolin M-L, Kiss T (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89: 799-809
18. Girard JP, Bagni C, Caizergues-Ferrer M, Amalric F, Lapeyre B (1994) Identification of a segment of the small nucleolar ribonucleoprotein-associated protein GAR1 that is sufficient for nucleolar accumulation. J Biol Chem 269: 18499-18506
19. 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: 673-682
20. Gu X, Liu Y, Santi DV (1999) The mechanism of pseudouridine synthase I as deduced from its interaction with 5-fluorouracil-tRNA. Proc Natl Acad Sci USA 96: 14270-14275
21. Heiss NS, Girod A, Salowsky R, Wiemann S, Pepperkok R, Poustka A (1999) Dyskerin localizes to the nucleolus and its mislocalization is unlikely to play a role in the pathogenesis of dyskeratosis congenita. Hum Mol Genet 8: 2515-2524
22. Heiss NS, Knight SW, Vulliamy TJ, Klauck SM, Wiemann S, Mason PJ, Poustka A, 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
23. Henras A, Dez C, Noaillac-Depeyre J, Henry Y, Caizergues-Ferrer M (2001) Accumulation of H/ACA snoRNPs depends on the integrity of the conserved central domain of the RNA-binding protein Nhp2p. Nucleic Acids Res 29: 2733-2746
24. Henras A, Henry Y, Bousquet-Antonelli C, Noaillac-Depeyre J, Gelugne JP, Caizergues-Ferrer M (1998) Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J 17: 7078-7090
25. Hoang C, Ferre-D'Amare AR (2001) Cocrystal structure of a tRNA Ψ55 pseudouridine synthase: nucleotide flipping by an RNA-modifying nzyme. Cell 107: 929-939
26. Huang L, Pookanjanatavip M, Gu X, Santi DV (1998) A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 37: 344-351
27. 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: 4884-4893
28. King TH, Decatur WA, Bertrand E, Maxwell ES, Fournier MJ (2001) A well-connected and conserved nucleoplasmic helicase is required for production of box C/D and H/ACA snoRNAs and localization of snoRNP proteins. Mol Cell Biol 21: 7731-7746
29. King TH, Liu B, McCully RR, Fournier MJ (2003) Ribosome structure nd activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11: 425-435
30. Knight SW, Heiss NS, Vulliamy TJ, Aalfs CM, McMahon C, Richmond P, Jones A, Hennekam RC, Poustka A, Mason PJ, Dokal I (1999) Unexplained aplastic anaemia, immunodeficiency, and cerebellar hypoplasia (Hoyeraal-Hreidarsson syndrome) due to mutations in the dyskeratosis congenita gene, DKC1. Br J Haematol 107: 335-339
31. Lafontaine DLJ, Bousquet-Antonelli C, Henry Y, Caizergues-Ferrer M, Tollervey D (1998) The box H+ACA snoRNAs carry Cbf5p, the putative rRNA pseuclouridine synthase. Genes Dev 12: 527-537
32. Liang XH, Liu L, Michaeli S (2001) Identification of the first trypanosome H/ACA RNA that guides pseudouridine formation on rRNA. J Biol Chem 276: 40313-40318
33. Long RM, Gu W, Lorimer E, Singer RH, Chartrand P (2000) She2p is a novel RNA-binding protein that recruits the Myo4p-She3p complex to ASH1 mRNA. EMBO J 19: 6592-6601
34. Lübben B, Fabrizio P, Kastner B, Lührmann R (1995) Isolation and characterization of the small nucleolar ribonucleoprotein particle snR30 from Saccharomyces cerevislae. J Biol Chem 270: 11549-11554
35. Marrone A, Mason PJ (2003) Dyskeratosis congenita. Cell Mol Life Sci 60: 507-517
36. Meier UT (2003) Dissecting dyskeratosis. Nat Genet 33: 116-117
37. Meier UT, Blobel G (1994) NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria. J Cell Biol (correction appeared in 140: 447) 127: 1505-1514
38. Mitchell JR, Cheng J, Collins K (1999a) A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol Cell Biol 19: 567-576
39. Mitchell JR, Wood E, Collins K (1999b) A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402: 551-555
40. Ni J, Tien AL, Fournier MJ (1997) Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 89: 565-573
41. Nottrott S, Hartmuth K, Fabrizio P, Urlaub H, Vidovic I, Ficner R, Luhrmann R (1999) Functional interaction of a novel 15.5 kD [U4/U6.U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J 18: 6119-6133
42. Nurse K, Wrzesinski J, Bakin A, Lane BG, Ofengand J (1995) Purification, cloning, and properties of the tRNA Ψ55 synthase from Escherichia coli. RNA 1: 102-112
43. Pogacic V, Dragon F, Filipowicz W (2000) Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol Cell Biol 20: 9028-9040
44. Rozhdestvensky TS, Tang TH, Tchirkova IV, Brosius J, Bachellerie JP, Huttenhofer 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: 869-877
45. Ruggero D, Grisendi S, Piazza F, Rego E, Mari F, Rao PH, Cordon-Cardo C, Pandolfi PP (2003) Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299: 259-262
46. Smith CM, Steitz JA (1997) Sno storm in the nucleolus: new roles for myriad small RNPs. Cell 89: 669-672
47. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, Drungowski M, Elge T, Brosius J, Huttenhofer A (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci USA 99: 7536-7541
48. Tollervey D, Kiss T (1997) Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 9: 337-342
49. Tremblay A, Lamontagne B, Catala M, Yam Y, Larose S, Good L, Elela SA (2002) A physical interaction between Gar1p and Rnt1pi is required for the nuclear import of H/ACA small nucleolar RNA-associated proteins. Mol Cell Biol 22: 4792-4802
50. Wang C, Query CC, Meier UT (2002) Immunopurified small nucleolar ribonucleoprotein particles pseudouridylate RRNA independently of their association with phosphorylated Nopp140. Mol Cell Biol 22: 8457-8466
51. Watanabe Y, Gray MW (2000) Evolutionary appearance of genes encoding proteins associated with box H/ACA snoRNAs: cbf5p in Euglena gracilis, an early diverging eukaryote, and candidate Gar1p and Nop10p homologs in archaebacteria. Nucleic Acids Res 28: 2342-2352
52. Watkins NJ, 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 box H/ACA-motif snoRNPs and constitute a common bipartite structure. RNA 4: 1549-1568
53. Watkins NJ, Segault V, Charpentier B, Nottratt S, Fabrizio P, Bachi A, Wilm M, Rosbash M, Branlant C, Luhrmann R (2000) A common core RNP structure shared between the small nuclear box C/D RNPs and the spliceosomal U4 snRNP. Cell 103: 457-466
54. Weinstein Szewczak LB, DeGregorio SJ, Strobel SA, Steitz JA (2002) Exclusive interaction of the 15.5 kD protein with the terminal box C/D motif of a methylation guide snoRNP. Chem Biol 9: 1095-1107
55. Xu C, Henry PA, Setya A, Henry MF (2003) In vivo analysis of nucleolar proteins modified by the yeast arginine methyltransferase Hmt1/Rmt1p. RNA 9: 746-759
56. Yang PK, Rotondo G, Porras T, Legrain P, Chanfreau G (2002) The Shq1p.Naf1p complex is required for box H/ACA small nucleolar ribonucleoprotein particle biogenesis. J Biol Chem 277: 45235-45242
57. Youssoufian H, Gharibyan V, Qatanani M (1999) Analysis of epitope-tagged forms of the dyskeratosis congenital protein (dyskerin); identification of a nuclear localization signal. Blood Cells Mol Dis 25: 305-309
58. Yu YT, Shu MD, Steitz JA (1998) Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17: 5783-5795
59. Zebarjadian Y, King T, Fournier MJ, Clarke L, Carbon J (1999) Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA. Mol Cell Biol 19: 7461-7472