The special Sm core structure of the U7 snRNP: Far-reaching significance of a small nuclear ribonucleoprotein

Cellular and Molecular Life Sciences

Volumn 61, Issue 19-20, 2004, Pages 2560-2570

  Schumperli D ^a   Pillai, R S ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Alternative splicing; Antisense gene therapy; Cajal bodies; Histone RNA 3 end processing; Sm core assembly; Sm like proteins; SMN complex; Symmetrical dimethyl arginine; U7 small nuclear ribonucleoprotein

Indexed keywords

ISOPROTEIN; MESSENGER RNA; METHYLTRANSFERASE; POLYPEPTIDE; PROTEIN DERIVATIVE; PROTEIN LSM 10; PROTEIN LSM 11; PROTEIN SM; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN U7; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; GENE THERAPY; NUCLEIC ACID PROBE; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; RNA PROCESSING; RNA SPLICING;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; ANIMALS; BINDING SITES; EXONS; GENE EXPRESSION REGULATION; GENE THERAPY; HISTONES; HUMANS; MODELS, GENETIC; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEIN, U7 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA; RNA, MESSENGER; RNA, SMALL NUCLEAR; SPLICEOSOMES;

EID: 9744246907     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-4190-0     Document Type: Review

References (98)

1. Schümperli D. (1988) Multilevel regulation of replication-dependent histone genes. Tr. Genet. 4: 187-191
2. Marzluff W. F. (1992) Histone 3′ ends: essential and regulatory functions. Gene Expr. 2: 93-97
3. Müller B. and Schümperli D. (1997) The U7 snRNP and the hairpin binding protein: key players in histone mRNA metabolism. Semin. Cell Dev. Biol. 8: 567-576
4. Dominski Z. and Marzluff W. F. (1999) Formation of the 3′ end of histone mRNA. Gene 239: 1-14
5. Marzluff W. F. and Duronio R. J. (2002) Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 14: 692-699
6. Martin F., Schaller A., Eglite S., Schümperli D. and Müller B. (1997) The gene for histone RNA hairpin binding protein is located on human chromosome 4 and encodes a novel type of RNA binding protein. EMBO J. 15: 769-778
7. Wang Z. F., Whitfield M. L., Ingledue T. C., Dominski Z. and Marzluff W. F. (1996) The protein that binds the 3′ end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev. 10: 3028-3040
8. Dominski Z., Sumerel J., Hanson R. J. and Marzluff W. F. (1995) The polyribosomal protein bound to the 3′ end of histone mRNA can function in histone pre-mRNA processing. RNA 1: 915-923
9. Hanson R. J., Sun J. Willis D. G. and Marzluff W. F. (1996) Efficient extraction and partial purification of the polyribosome-associated stem-loop binding protein bound to the 3′ end of histone mRNA. Biochemistry 35: 2146-2156
10. Pandey N. B. and Marzluff W. F. (1987) The stem-loop structure at the 3′ end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol. Cell. Biol. 7: 4557-4559
11. Williams A. S., Ingledue T. C., Kay B. K. and Marzluff W. F. (1994) Changes in the stem-loop at the 3′ terminus of histone mRNA affects its nucleocytoplasmic transport and cytoplasmic regulation. Nucl. Acids Res. 22: 4660-4666
12. Ling J., Morley S. J., Pain V. M., Marzluff W. F. and Gallie D. R. (2002) The histone 3′-terminal stem-loop-binding protein enhances translation through a functional and physical interaction with eukaryotic initiation factor 4G (eIF4G) and eIF3. Mol. Cell Biol. 22: 7853-7867
13. Sullivan E., Santiago C., Parker E. D., Dominski Z., Yang X., Lanzotti D. J. et al. (2001) Drosophila stem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression. Genes Dev. 15: 173-187
14. Kodama Y., Rothman J. H., Sugimoto A. and Yamamoto M. (2002) The stem-loop binding protein CDL-1 is required for chromosome condensation, progression of cell death and morphogenesis in Caenorhabditis elegans. Development 129: 187-196
15. Pettitt I, Crombie C., Schümperli D. and Müller B. (2002) The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division. J. Cell Sci. 115: 857-866
16. Martin F., Michel F., Zenklusen D., Müller B. and Schümperli D. (2000) Positive and negative mutant selection in the human histone hairpin-binding protein using the yeast three-hybrid system. Nucl. Acids Res. 28: 1594-1603
17. Michel F., Schümperli D. and Müller B. (2000) Specificities of Caenorhabditis elegans and human hairpin binding proteins for the first nucleotide in the histone mRNA hairpin loop. RNA 6: 1539-1550
18. Dominski Z., Erkmann J. A., Greenland J. A. and Marzluff W. F. (2001) Mutations in the RNA binding domain of stem-loop binding protein define separable requirements for RNA binding and for histone pre-mRNA processing. Mol. Cell. Biol. 21: 2008-2017
19. Jaeger S., Eriani G. and Martin F. (2004) Critical residues for RNA discrimination of the histone hairpin binding protein (HBP) investigated by the yeast three-hybrid system. FEBS Lett. 556: 265-270
20. Whitfield M. L., Zheng L. X., Baldwin A., Ohta T., Hurt M. M. and Marzluff W. F. (2000) Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol. Cell. Biol. 20: 4188-4198
21. Dominski Z., Zheng L. X., Sanchez R. and Marzluff W. F. (1999) Stem-loop binding protein facilitates 3′-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol. Cell. Biol. 19: 3561-3570
22. Streit A., Wittop Koning T. H., Soldati D., Melin L. and Schümperli D. (1993) Variable effects of the conserved RNA hairpin element upon 3′ end processing of histone pre-mRNA in vitro. Nucl. Acids Res. 21: 1569-1575
23. Spycher C., Streit A., Stefanovic B., Albrecht D., Wittop K. and Schümperli D. (1994) 3′ end processing of mouse histone pre-mRNA: evidence for additional base-pairing between U7 snRNA and pre-mRNA. Nucl. Acids Res. 22: 4023-4030
24. Dominski Z., Erkmarm J. A., Yang X., Sanchez R. and Marzluff W. F. (2002) A novel zinc finger protein is associated with U7 snRNP and interacts with the stem-loop binding protein in the histone pre-mRNP to stimulate 3′-end processing. Genes Dev. 16: 58-71
25. Gick O., Krämer A., Vasserot A. and Birnstiel M. L. (1987) Heat-labile regulatory factor is required for 3′ processing of histone precursor mRNAs. Proc. Natl. Acad. Sci. USA 84: 8937-8940
26. Galli G., Hofstetter H., Stunnenberg H. G. and Birnstiel M. L. (1983) Biochemical complementation with RNA in the Xenopus oocyte: a small RNA is required for the generation of 3′ histone mRNA termini. Cell 34: 823-828
27. Strub K., Galli G., Busslinger M. and Birnstiel M. L. (1984) The cDNA sequences of the sea urchin U7 small nuclear RNA suggest specific contacts between histone mRNA precursor and U7 RNA during RNA processing. EMBO J. 3: 2801-2807
28. Strub K. and Birnstiel M. L. (1986) Genetic complementation in the Xenopus oocyte: co-expression of sea urchin histone and U7 RNAs restores 3′ processing of H3 pre-mRNA in the oocyte. EMBO J. 5: 1675-1682
29. Gilmartin G. M., Schaufele F., Schaffner G. and Birnstiel M. E. (1988) Functional analysis of the sea urchin U7 small nuclear RNA. Mol. Cell. Biol. 8: 1076-1084
30. Schaufele F., Gilmartin G. M., Bannwarth W. and Birnstiel M. E. (1986) Compensatory mutations suggest that base-pairing with a small nuclear RNA is required to form the 3′ end of H3 messenger RNA. Nature 323: 777-781
31. Bond U. M., Yario T. A. and Steitz J. A. (1991) Multiple processing-defective mutations in a mammalian histone premessenger RNA are suppressed by compensatory changes in U7 RNA both in vivo and in vitro. Genes Dev. 5: 1709-1722
32. Scharl E. C. and Steitz J. A. (1994) The site of 3′ end formation of histone messenger RNA is a fixed distance from the downstream element recognized by the U7 snRNP. EMBO J. 13: 2432-2440
33. Scharl E. C. and Steitz J. A. (1996) Length suppression in histone messenger RNA 3′-end maturation: processing defects of insertion mutant premessenger RNAs can be compensated by insertions into the U7 small nuclear RNA. Proc. Natl. Acad. Sci. USA 93: 14659-14664
34. Furger A., Schaller A. and Schümperli D. (1998) Functional importance of conserved nucleotides at the histone RNA 3′ processing site. RNA 4: 246-256
35. Walther T. N., Wittop Koning T. H., Schümperli D. and Müller B. (1998) A 5′-3′ exonuclease activity involved in forming the 3′ products of histone pre-mRNA processing in vitro. RNA 4: 1034-1046
36. Pillai R. S., Will C. L., Lührmann R., Schümperli D. and Müller B. (2001) Purified UV snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J. 20: 5470-5479
37. Pillai R. S., Grimmler M., Meister G., Will C. L., Luhrmann R., Fischer U. et al. (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev. 17: 2321-2333
38. Grimm C., Stefanovic B. and Schümperli D. (1993) The low abundance of U7 snRNA is partly determined by its Sm binding site. EMBO J. 12: 1229-1238
39. Stefanovic B., Hackl W, Lührmann R. and Schümperli D. (1995) Assembly, nuclear import and function of U7 snRNPs studied by microinjection of synthetic U7 RNA into Xenopus oocytes. Nucl. Acids Res. 23: 3141-3151
40. Lerner E. A., Lerner M. R., Janeway C. A. and Steitz J. A. (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc. Natl. Acad. Sci. USA 78: 2737-2741
41. Lührmann R., Kastner B. and Bach M. (1990) Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim. Biophys. Acta 1087: 265-292
42. Cooper M., Johnston L. H. and Beggs J. D. (1995) Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J. 14: 2066-2075
43. Hermann H., Fabrizio P., Raker V. A. Foulaki K., Hornig H., Brahms H. et al. (1995) snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 14: 2076-2088
44. Seraphin B. (1995) Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J. 14: 2089-2098
45. Kambach C, Walke S., Young R., Avis J. M., de la Fortelle E., Raker V. A. et al. (1999) Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96: 375-387
46. Kambach C., Walke S. and Nagai K. (1999) Structure and assembly of the spliceosomal small nuclear ribonucleoprotein particles. Curr. Opin. Struct. Biol. 9: 222-230
47. Stark H., Dube P., Lührmann R. and Kastner B. (2001) Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonucleoprotein particle. Nature 409: 539-543
48. Achsel T., Brahms H., Kastner B., Bachi A., Wilm M. and Lührmann R. (1999) A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18: 5789-5802
49. Gottschalk A., Neubauer G., Banroques J., Mann M., Luhrmann R. and Fabrizio P. (1999) Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6.U5] tri-snRNP. EMBO J. 18: 4535-4548
50. Mayes A. E., Verdone L., Legrain P. and Beggs J. D. (1999) Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18: 4321-4331
51. Salgado-Garrido J. Bragado-Nilsson E., Kandels-Lewis S. and Seraphin B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J. 18: 3451-3462
52. He W. and Parker R. (2000) Functions of Lsm proteins in mRNA degradation and splicing. Curr. Opin. Cell Biol. 12: 346-350
53. Rader S. D. and Guthrie C. (2002) A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8: 1378-1392
54. Ryan D. E., Stevens S. W. and Abelson J. (2002) The 5′ and 3′ domains of yeast U6 snRNA: Lsm proteins facilitate binding of Prp24 protein to the U6 telestem region. RNA 8: 1011-1033
55. Bouveret E., Rigaut G., Shevchenko A., Wilm M. and Seraphin B. (2000) A Sm-like protein complex that participates in mRNA degradation. EMBO J. 19: 1661-1671
56. Tharun S., He W., Mayes A. E., Lennertz P., Beggs J. D. and Parker R. (2000) Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404: 515-518
57. Fernandez C. F., Pannone B. K., Chen X., Fuchs G. and Wolin S. L. (2004) An Lsm2-Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5. Mol. Biol. Cell 15: 2842-2852
58. Tomasevic N. and Peculis B. A. (2002) Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence. Mol. Cell. Biol. 22: 4101-4112
59. Kufel J., Allmang C., Verdone L., Beggs J. D. and Tollervey D. (2002) Lsm proteins are required for normal processing of pre-tRNAs and their efficient association with La-homologous protein Lhp1p. Mol. Cell. Biol. 22: 5248-5256
60. Achsel T., Stark H. and Lührmann R. (2001) The Sm domain is an ancient RNA-binding motif with oligo(U) specificity. Proc. Natl. Acad. Sci. USA 98: 3685-3689
61. Toro I., Thore S., Mayer C., Basquin J., Seraphin B. and Suck D. (2001) RNA binding in an Sm core domain: X-ray structure and functional analysis of an archaeal Sm protein complex. EMBO J. 20: 2293-2303
62. Moller T., Franch T., Hojrup P., Keene D. R., Bachinger H. P., Brennan R. G. et al. (2002) Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol. Cell 9: 23-30
63. Zhang A., Wassarman K. M., Ortega J., Steven A. C. and Storz G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell. 9: 11-22
64. Sauter C., Basquin J. and Suck D. (2003) Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucl. Acids Res. 31: 4091-4098
65. Raker V. A., Plessel G. and Lührmann R. (1996) The snRNP core assembly pathway: identification of stable core protein heteromeric complexes and an snRNP subcore particle in vitro. EMBO J. 15: 2256-2269
66. Raker V. A., Hartmuth K., Kastner B. and Lührmann R. (1999) Spliceosomal U snRNP core assembly: Sm proteins assemble onto an Sm site RNA nonanucleotide in a specific and thermodynamically stable manner. Mol. Cell. Biol. 19: 6554-6565
67. Azzouz T. N. and Schümperli D. (2003) Evolutionary conservation of the U7 small nuclear ribonucleoprotein in Drosophila melanogaster. RNA 9: 1532-1541
68. Pellizzoni L., Yong J. and Dreyfuss G. (2002) Essential role for the SMN complex in the specificity of snRNP assembly. Science 298: 1775-1779
69. Huber J., Cronshagen U., Kadokura M., Marshallsay C., Wada T., Sekine M. et al. (1998) Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 17: 4114-4126
70. Meister G., Eggert C. and Fischer U. (2002) SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol. 12: 472-478
71. Paushkin S., Gubitz A. K., Massenet S. and Dreyfuss G. (2002) The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 14: 305-312
72. Meister G., Bühler D., Pillai R., Lottspeich F. and Fischer U. (2001) A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs. Nat. Cell Biol. 3: 945-949
73. Meister G. and Fischer U. (2002) Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs. EMBO J. 21: 5853-5863
74. Yong J., Pellizzoni L. and Dreyfuss G. (2002) Sequence-specific interaction of U1 snRNA with the SMN complex. EMBO J. 21: 1188-1196
75. Yong J., Golembe T. J., Battle D. J., Pellizzoni L. and Dreyfuss G. (2004) snRNAs contain specific SMN-binding domains that are essential for snRNP assembly. Mol. Cell. Biol. 24: 2747-2756
76. Massenet S., Pellizzoni L., Paushkin S., Mattaj I. W. and Dreyfuss G. (2002) The SMN complex is associated with snRNPs throughout their cytoplasmic assembly pathway. Mol. Cell. Biol. 22: 6533-6541
77. Müller B., Link J. and Smythe C. (2000) Assembly of U7 small nuclear ribonucleoprotein particle and histone RNA 3′ processing in Xenopus egg extracts. J. Biol. Chem. 275: 24284-24293
78. Friesen W. J., Paushlcin S., Wyce A., Massenet S., Pesiridis S., Van Duyne G. et al. (2001) The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 21: 8289-8300
79. Meister G., Eggert C., Bühler D., Brahms H., Kambach C. and Fischer U. (2001) Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr. Biol. 11: 1990-1994
80. Lewis J. D. and Tollervey D. (2000) Like attracts like: getting RNA processing together in the nucleus. Science 288: 1385-1389
81. Sleeman J. E. and Lamond A. I. (1999) Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr. Biol. 9: 1065-1074
82. Jady B. E., Darzacq X., Tucker K. E., Matera A. G., Bertrand E. and Kiss T. (2003) Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J. 22: 1878-1888
83. Hebert M. D., Shpargel K. B., Ospina J. K., Tucker K. E. and Matera A. G. (2002) Coilin methylation regulates nuclear body formation. Dev. Cell 3: 329-337
84. Frey M. R. and Matera A. G. (1995) Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells [published erratum appears in Proc. Natl. Acad. Sci. USA 1995 Aug 29;92(18):8532]. Proc. Natl. Acad. Sci. USA 92: 5915-5919
85. Wu Z., Murphy C., Wu C. H., Tsvetkov A. and Gall J. G. (1993) Snurposomes and coiled bodies. Cold Spring Harb. Symp. Quant. Biol. 58: 747-754
86. Tuma R. S. and Roth M. B. (1999) Induction of coiled body-like structures inXenopus oocytes by U7 snRNA. Chromosoma 108: 337-344
87. Wu C. H., Murphy C. and Gall J. C. (1996) The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes. RNA 2: 811-823
88. Vacek M., Sazani P. and Kole R. (2003) Antisense-mediated redirection of mRNA splicing. Cell Mol. Life Sci. 60: 825-833
89. German L., Suter D., Emerick V., Schümperli D. and Kole R. (1998) Stable alteration of pre-mRNA splicing patterns by modified U7 small nuclear RNAs. Proc. Natl. Acad. Sci. USA 95: 4929-4934
90. Suter D., Tomasini R., Reber U., Gorman L., Kole R. and Schümperli D. (1999) Double-target antisense U7 snRNAs promote efficient skipping of an aberrant exon in three human beta-thalassemic mutations. Hum. Mol. Genet. 8: 2415-2423
91. Gorman L., Schümperli D. and Kole R. (2000) Alteration of pre-mRNA splicing patterns by modified small nuclear RNAs. In: Progress in Gene Therapy -Basic and Clinical Frontiers, pp. 455-473, Bertolotti R., Parvez S. H. and Nagatsu T. (eds), VSP Utrecht, The Netherlands
92. De Angelis F. G., Sthandier O., Berarducci B., Toso S., Galluzzi G., Ricci E. et al. (2002) Chimeric snRNA molecules carrying antisense sequences against the splice junctions of exon 51 of the dystrophin pre-mRNA induce exon skipping and restoration of a dystrophin synthesis in Delta 48-50 DMD cells. Proc. Natl. Acad. Sci. USA 99: 9456-9461
93. Brun C., Suter D. Pauli C., Dunant P., Lochmüller H., Burgunder J. M. et al. (2003) U7 snRNAs induce correction of mutated dystrophin pre-mRNA by exon skipping. Cell Mol. Life Sci. 60: 557-566
94. Liu S., Asparuhova M., Brondani V., Ziekau I., Klimkait T. and Schumperli D. (2004) Inhibition of HIV-1 multiplication by antisense U7 snRNAs and siRNAs targeting cyclophilin A. Nucl. Acids Res. 32: 3752-3759
95. Vacek M. M., Ma H., Gemignani F., Lacerra G., Kafri T. and Kole R. (2003) High-level expression of hemoglobin A in human thalassemic erythroid progenitor cells following lentiviral vector delivery of an antisense snRNA. Blood 101: 104-111
96. Stefanovic B., Schnabl B. and Brenner D. A. (2002) Inhibition of collagen alpha 1(I) expression by the 5′ stem-loop as a molecular decoy. J. Biol. Chem. 277: 18229-18237
97. German L., Mercatante D. R. and Kole R. (2000) Restoration of correct splicing of thalassemic beta-globin pre-mRNA by modified U1 snRNAs. J. Biol. Chem. 275: 35914-35919
98. Will C. L. and Lührmann R. (2001) Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13: 290-301