The Drosophila U7 snRNP proteins Lsm10 and Lsm11 are required for histone pre-mRNA processing and play an essential role in development

RNA

Volumn 15, Issue 9, 2009, Pages 1661-1672

  Godfrey, Ashley C ^a   White, Anne E ^a   Tatomer, Deirdre C ^a   Marzluff, William F ^a,b   Duronio, Robert J ^a,b  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Histone; Lsm10; Lsm11; RNA processing; snRNP; U7

Indexed keywords

DIMER; HISTONE; MESSENGER RNA PRECURSOR; POLYADENYLATED RNA; PROTEIN LSM10; PROTEIN LSM11; SMALL NUCLEAR RIBONUCLEOPROTEIN; U7 SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; FERTILITY; GENE DISRUPTION; GENE MUTATION; LETHALITY; NONHUMAN; PHENOTYPE; POLYADENYLATION; PRECURSOR; PRIORITY JOURNAL; RNA PROCESSING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; FERTILITY; GENES, DEVELOPMENTAL; GENES, LETHAL; HISTONES; MALE; MUTATION; RIBONUCLEOPROTEIN, U7 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

METAZOA;

EID: 69049101138     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1518009     Document Type: Article

References (58)

1. Achsel T, Brahms H, Kastner B, Bachi A, Wilm M, 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.
2. Azzouz TN, Schumperli D. 2003. Evolutionary conservation of the U7 small nuclear ribonucleoprotein in Drosophila melanogaster. RNA 9: 1532-1541.
3. Azzouz TN, Gruber A, Schumperli D. 2005. U7 snRNP-specific Lsm11 protein: Dual binding contacts with the 100 kDa zinc finger processing factor (ZFP100) and a ZFP100-independent function in histone RNA 3′ end processing. Nucleic Acids Res 33: 2106-2117.
4. Beggs JD. 2005. Lsm proteins and RNA processing. Biochem Soc Trans 33: 433-438.
5. Bond UM, Yario TA, Steitz JA. 1991. Multiple processing-defective mutations in a mammalian histone pre-mRNA are suppressed by compensatory changes in U7 RNA both in vivo and in vitro. Genes & Dev 5: 1709-1722.
6. Bouveret E, Rigaut G, Shevchenko A, Wilm M, Seraphin B. 2000. A Sm-like protein complex that participates in mRNA degradation. EMBO J 19: 1661-1671.
7. Branlant C, Krol A, Ebel JP, Lazar E, Haendler B, Jacob M. 1982. U2 RNA shares a structural domain with U1, U4, and U5 RNAs. EMBO J 1: 1259-1265.
8. Carmo-Fonseca M. 2002. New clues to the function of the Cajal body. EMBO Rep 3: 726-727.
9. Cioce M, Lamond AI. 2005. Cajal bodies: A long history of discovery. Annu Rev Cell Dev Biol 21: 105-131.
10. Collins BM, Harrop SJ, Kornfeld GD, Dawes IW, Curmi PM, Mabbutt BC. 2001. Crystal structure of a heptameric Sm-like protein complex from archaea: Implications for the structure and evolution of snRNPs. J Mol Biol 309: 915-923.
11. Dominski Z, Erkmann JA, Yang X, Sanchez R, Marzluff WF. 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.
12. Dominski Z, Yang XC, Purdy M, Marzluff WF. 2003. Cloning and characterization of the Drosophila U7 small nuclear RNA. Proc Natl Acad Sci 100: 9422-9427.
13. Dominski Z, Yang XC, Marzluff WF. 2005. The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell 123: 37-48.
14. Fernandez CF, Pannone BK, Chen X, Fuchs G, Wolin SL. 2004. An Lsm2-Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5. Mol Biol Cell 15: 2842-2852.
15. Gall JG. 2000. Cajal bodies: The first 100 years. Annu Rev Cell Dev Biol 16: 273-300.
16. Gall JG. 2003. The centennial of the Cajal body. Nat Rev Mol Cell Biol 4: 975-980.
17. Galli G, Hofstetter H, Stunnenberg HG, Birnstiel ML. 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.
18. Gick O, Kramer A, Keller W, Birnstiel ML. 1986. Generation of histone mRNA 3′ ends by endonucleolytic cleavage of the pre-mRNA in a snRNP-dependent in vitro reaction. EMBO J 5: 1319-1326.
19. Godfrey AC, Kupsco JM, Burch BD, Zimmerman RM, Dominski Z, Marzluff WF, Duronio RJ. 2006. U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis. RNA 12: 396-409.
20. Grimm C, Stefanovic B, Schumperli D. 1993. The low abundance of U7 snRNA is partly determined by its Sm binding site. EMBO J 12: 1229-1238.
21. Harris ME, Bohni R, Schneiderman MH, Ramamurthy L, Schumperli D, Marzluff WF. 1991. Regulation of histone mRNA in the unperturbed cell cycle: Evidence suggesting control at two post-transcriptional steps. Mol Cell Biol 11: 2416-2424.
22. Hermann H, Fabrizio P, Raker VA, Foulaki K, Hornig H, Brahms H, Lührmann R. 1995. snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J 14: 2076-2088.
23. Jones MH, Guthrie C. 1990. Unexpected flexibility in an evolutionarily conserved protein-RNA interaction: Genetic analysis of the Sm binding site. EMBO J 9: 2555-2561.
24. Kambach C, Walke S, Young R, Avis JM, de la Fortelle E, Raker VA, Lührmann R, Li J, Nagai K. 1999. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96: 375-387.
25. Kolev NG, Steitz JA. 2005. Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes & Dev 19: 2583-2592.
26. Koundakjian EJ, Cowan DM, Hardy RW, Becker AH. 2004. The Zuker collection: A resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167: 203-206.
27. Lanzotti DJ, Kaygun H, Yang X, Duronio RJ, Marzluff WF. 2002. Developmental control of histone mRNA and dSLBP synthesis during Drosophila embryogenesis and the role of dSLBP in histone mRNA 3′ end processing in vivo. Mol Cell Biol 22: 2267-2282.
28. Liu JL, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG. 2006. The Drosophila melanogaster Cajal body. J Cell Biol 172: 875-884.
29. Loughney K, Kreber R, Ganetzky B. 1989. Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58: 1143-1154.
30. Lührmann R, Kastner B, Bach M. 1990. Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim Biophys Acta 1087: 265-292.
31. Luscher B, Schumperli D. 1987. RNA 3′ processing regulates histone mRNA levels in a mammalian cell cycle mutant. A processing factor becomes limiting in G1-arrested cells. EMBO J 6: 1721-1726.
32. Martin F, Schaller A, Eglite S, Schumperli D, Muller 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 16: 769-778.
33. Marzluff WF, Wagner EJ, Duronio RJ. 2008. Metabolism and regulation of canonical histone mRNAs: Life without a poly(A) tail. Nat Rev Genet 9: 843-854.
34. Matera AG. 2003. Cajal bodies. Curr Biol 13: R503. doi: 10.1016/S0960-9822(03)00438-X.
35. Matera AG, Terns RM, Terns MP. 2007. Noncoding RNAs: Lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol 8: 209-220.
36. Mattaj IW. 1986. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell 46: 905-911.
37. Mowry KL, Steitz JA. 1987a. Both conserved signals on mammalian histone pre-mRNAs associate with small nuclear ribonucleoproteins during 3′ end formation in vitro. Mol Cell Biol 7: 1663-1672.
38. Mowry KL, Steitz JA. 1987b. Identification of the human U7 snRNP as one of several factors involved in the 3′ end maturation of histone premessenger RNA's. Science 238: 1682-1687.
39. Park JW, Parisky K, Celotto AM, Reenan RA, Graveley BR. 2004. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc Natl Acad Sci 101: 15974-15979.
40. Pillai RS, Will CL, Lührmann R, Schumperli D, Muller B. 2001. Purified U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J 20: 5470-5479.
41. Pillai RS, Grimmler M, Meister G, Will CL, Lührmann R, Fischer U, Schumperli D. 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.
42. Sanchez R, Marzluff WF. 2002. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol Cell Biol 22: 7093-7104.
43. Schaufele F, Gilmartin GM, Bannwarth W, Birnstiel ML. 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.
44. Schumperli D, Pillai RS. 2004. The special Sm core structure of the U7 snRNP: Far-reaching significance of a small nuclear ribonucleoprotein. Cell Mol Life Sci 61: 2560-2570.
45. 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.
46. Stauber C, Schumperli D. 1988. 3′ Processing of pre-mRNA plays a major role in proliferation-dependent regulation of histone gene expression. Nucleic Acids Res 16: 9399-9414.
47. Stefanovic B, Hackl W, Lührmann R, Schumperli D. 1995. Assembly, nuclear import and function of U7 snRNPs studied by microinjection of synthetic U7 RNA into Xenopus oocytes. Nucleic Acids Res 23: 3141-3151.
48. Sullivan E, Santiago C, Parker ED, Dominski Z, Yang X, Lanzotti DJ, Ingledue TC, Marzluff WF, Duronio RJ. 2001. Drosophila stem-loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression. Genes & Dev 15: 173-187.
49. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, et al. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36: 283-287.
50. Till BJ, Colbert T, Tompa R, Enns LC, Codomo CA, Johnson JE, Reynolds SH, Henikoff JG, Greene EA, Steine MN, et al. 2003. High-throughput TILLING for functional genomics. Methods Mol Biol 236: 205-220.
51. Tomasevic N, Peculis BA. 2002. Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence. Mol Cell Biol 22: 4101-4112.
52. Toro I, Thore S, Mayer C, Basquin J, Seraphin B, 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.
53. Toro I, Basquin J, Teo-Dreher H, Suck D. 2002. Archaeal Sm proteins form heptameric and hexameric complexes: Crystal structures of the Sm1 and Sm2 proteins from the hyperthermophile Archaeoglobus fulgidus. J Mol Biol 320: 129-142.
54. Wagner EJ, Ospina JK, Hu Y, Dundr M, Matera AG, Marzluff WF. 2006. Conserved zinc fingers mediate multiple functions of ZFP100, a U7snRNP associated protein. RNA 12: 1206-1218.
55. Wagner EJ, Burch BD, Godfrey AC, Salzler HR, Duronio RJ, Marzluff WF. 2007. A genome-wide RNA interference screen reveals that variant histones are necessary for replication-dependent histone pre-mRNA processing. Mol Cell 28: 692-699.
56. Wang ZF, Whitfield ML, Ingledue TC 3rd, Dominski Z, Marzluff WF. 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.
57. Wang P, Palfi Z, Preusser C, Lucke S, Lane WS, Kambach C, Bindereif A. 2006. Sm core variation in spliceosomal small nuclear ribonucleoproteins from Trypanosoma brucei. EMBO J 25: 4513-4523.
58. White AE, Leslie ME, Calvi BR, Marzluff WF, Duronio RJ. 2007. Developmental and cell cycle regulation of the Drosophila histone locus body. Mol Biol Cell 18: 2491-2502.