• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of embojLink to Publisher's site
EMBO J. Jun 15, 1999; 18(12): 3451–3462.
PMCID: PMC1171424

Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin.

Abstract

A group of seven Sm proteins forms a complex that binds to several RNAs in metazoans. All Sm proteins contain a sequence signature, the Sm domain, also found in two yeast Sm-like proteins associated with the U6 snRNA. We have performed database searches revealing the presence of 16 proteins carrying an Sm domain in the yeast genome. Analysis of this protein family confirmed that seven of its members, encoded by essential genes, are homologues of metazoan Sm proteins. Immunoprecipitation revealed that an evolutionarily related subgroup of seven Sm-like proteins is directly associated with the nuclear U6 and pre-RNase P RNAs. The corresponding genes are essential or required for normal vegetative growth. These proteins appear functionally important to stabilize U6 snRNA. The two last yeast Sm-like proteins were not found associated with RNA, and neither was essential for vegetative growth. To investigate whether U6-associated Sm-like protein function is widespread, we cloned several cDNAs encoding homologous human proteins. Two representative human proteins were shown to associate with U6 snRNA-containing complexes. We also identified archaeal proteins related to Sm and Sm-like proteins. Our results demonstrate that Sm and Sm-like proteins assemble in at least two functionally conserved complexes of deep evolutionary origin.

Full Text

The Full Text of this article is available as a PDF (274K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bacchetti S, Graham FL. Transfer of the gene for thymidine kinase to thymidine kinase-deficient human cells by purified herpes simplex viral DNA. Proc Natl Acad Sci U S A. 1977 Apr;74(4):1590–1594. [PMC free article] [PubMed]
  • Baudin A, Ozier-Kalogeropoulos O, Denouel A, Lacroute F, Cullin C. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 1993 Jul 11;21(14):3329–3330. [PMC free article] [PubMed]
  • Behrens SE, Lührmann R. Immunoaffinity purification of a [U4/U6.U5] tri-snRNP from human cells. Genes Dev. 1991 Aug;5(8):1439–1452. [PubMed]
  • Birney E, Thompson JD, Gibson TJ. PairWise and SearchWise: finding the optimal alignment in a simultaneous comparison of a protein profile against all DNA translation frames. Nucleic Acids Res. 1996 Jul 15;24(14):2730–2739. [PMC free article] [PubMed]
  • Boeck R, Lapeyre B, Brown CE, Sachs AB. Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol Cell Biol. 1998 Sep;18(9):5062–5072. [PMC free article] [PubMed]
  • Bordonné R, Tarassov I. The yeast SME1 gene encodes the homologue of the human E core protein. Gene. 1996 Oct 17;176(1-2):111–117. [PubMed]
  • Brahms H, Raker VA, van Venrooij WJ, Lührmann R. A major, novel systemic lupus erythematosus autoantibody class recognizes the E, F, and G Sm snRNP proteins as an E-F-G complex but not in their denatured states. Arthritis Rheum. 1997 Apr;40(4):672–682. [PubMed]
  • Branlant C, Krol A, Ebel JP, Lazar E, Haendler B, Jacob M. U2 RNA shares a structural domain with U1, U4, and U5 RNAs. EMBO J. 1982;1(10):1259–1265. [PMC free article] [PubMed]
  • Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, et al. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. [PubMed]
  • Camasses A, Bragado-Nilsson E, Martin R, Séraphin B, Bordonné R. Interactions within the yeast Sm core complex: from proteins to amino acids. Mol Cell Biol. 1998 Apr;18(4):1956–1966. [PMC free article] [PubMed]
  • Chen HJ, Remmler J, Delaney JC, Messner DJ, Lobel P. Mutational analysis of the cation-independent mannose 6-phosphate/insulin-like growth factor II receptor. A consensus casein kinase II site followed by 2 leucines near the carboxyl terminus is important for intracellular targeting of lysosomal enzymes. J Biol Chem. 1993 Oct 25;268(30):22338–22346. [PubMed]
  • Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene. 1992 Jan 2;110(1):119–122. [PubMed]
  • Chu JL, Elkon KB. The small nuclear ribonucleoproteins, SmB and B', are products of a single gene. Gene. 1991 Jan 15;97(2):311–312. [PubMed]
  • Cooper M, Johnston LH, Beggs JD. Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J. 1995 May 1;14(9):2066–2075. [PMC free article] [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. [PMC free article] [PubMed]
  • Felici F, Cesareni G, Hughes JM. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol Cell Biol. 1989 Aug;9(8):3260–3268. [PMC free article] [PubMed]
  • Fischer U, Heinrich J, van Zee K, Fanning E, Lührmann R. Nuclear transport of U1 snRNP in somatic cells: differences in signal requirement compared with Xenopus laevis oocytes. J Cell Biol. 1994 Jun;125(5):971–980. [PMC free article] [PubMed]
  • Fischer U, Liu Q, Dreyfuss G. The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell. 1997 Sep 19;90(6):1023–1029. [PubMed]
  • Fromont-Racine M, Rain JC, Legrain P. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet. 1997 Jul;16(3):277–282. [PubMed]
  • Fu YH. Identification of a novel protein, DMAP, which interacts with the myotonic dystrophy protein kinase and shows strong homology to D1 snRNP. Genetica. 1996 Jan;97(1):117–125. [PubMed]
  • Fury MG, Zhang W, Christodoulopoulos I, Zieve GW. Multiple protein: protein interactions between the snRNP common core proteins. Exp Cell Res. 1997 Nov 25;237(1):63–69. [PubMed]
  • Gottschalk A, Tang J, Puig O, Salgado J, Neubauer G, Colot HV, Mann M, Séraphin B, Rosbash M, Lührmann R, et al. A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA. 1998 Apr;4(4):374–393. [PMC free article] [PubMed]
  • Guthrie C, Patterson B. Spliceosomal snRNAs. Annu Rev Genet. 1988;22:387–419. [PubMed]
  • Hermann H, Fabrizio P, Raker VA, Foulaki K, Hornig H, Brahms H, Lührmann R. snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 1995 May 1;14(9):2076–2088. [PMC free article] [PubMed]
  • Huber J, Cronshagen U, Kadokura M, Marshallsay C, Wada T, Sekine M, Lührmann R. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 1998 Jul 15;17(14):4114–4126. [PMC free article] [PubMed]
  • Izaurralde E, Mattaj IW. Transport of RNA between nucleus and cytoplasm. Semin Cell Biol. 1992 Aug;3(4):279–288. [PubMed]
  • Jarmolowski A, Mattaj IW. The determinants for Sm protein binding to Xenopus U1 and U5 snRNAs are complex and non-identical. EMBO J. 1993 Jan;12(1):223–232. [PMC free article] [PubMed]
  • Kambach C, Walke S, Young R, Avis JM, de la Fortelle E, Raker VA, Lührmann R, Li J, Nagai K. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell. 1999 Feb 5;96(3):375–387. [PubMed]
  • Kawarabayasi Y, Sawada M, Horikawa H, Haikawa Y, Hino Y, Yamamoto S, Sekine M, Baba S, Kosugi H, Hosoyama A, et al. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res. 1998 Apr 30;5(2):55–76. [PubMed]
  • Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997 Nov 27;390(6658):364–370. [PubMed]
  • Längle-Rouault F, Jacobs E. A method for performing precise alterations in the yeast genome using a recycable selectable marker. Nucleic Acids Res. 1995 Aug 11;23(15):3079–3081. [PMC free article] [PubMed]
  • Lee JY, Evans CF, Engelke DR. Expression of RNase P RNA in Saccharomyces cerevisiae is controlled by an unusual RNA polymerase III promoter. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6986–6990. [PMC free article] [PubMed]
  • Lee SI, Murthy SC, Trimble JJ, Desrosiers RC, Steitz JA. Four novel U RNAs are encoded by a herpesvirus. Cell. 1988 Aug 26;54(5):599–607. [PubMed]
  • Lennon G, Auffray C, Polymeropoulos M, Soares MB. The I.M.A.G.E. Consortium: an integrated molecular analysis of genomes and their expression. Genomics. 1996 Apr 1;33(1):151–152. [PubMed]
  • Lerner EA, Lerner MR, Janeway CA, Jr, Steitz JA. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A. 1981 May;78(5):2737–2741. [PMC free article] [PubMed]
  • Liu Q, Fischer U, Wang F, Dreyfuss G. The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell. 1997 Sep 19;90(6):1013–1021. [PubMed]
  • Lührmann R, Kastner B, Bach M. Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim Biophys Acta. 1990 Nov 30;1087(3):265–292. [PubMed]
  • Lygerou Z, Mitchell P, Petfalski E, Séraphin B, Tollervey D. The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins. Genes Dev. 1994 Jun 15;8(12):1423–1433. [PubMed]
  • Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR. The RDP (Ribosomal Database Project). Nucleic Acids Res. 1997 Jan 1;25(1):109–111. [PMC free article] [PubMed]
  • Mattaj IW. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell. 1986 Sep 12;46(6):905–911. [PubMed]
  • Mattaj IW, Tollervey D, Séraphin B. Small nuclear RNAs in messenger RNA and ribosomal RNA processing. FASEB J. 1993 Jan;7(1):47–53. [PubMed]
  • McAllister G, Roby-Shemkovitz A, Amara SG, Lerner MR. cDNA sequence of the rat U snRNP-associated protein N: description of a potential Sm epitope. EMBO J. 1989 Apr;8(4):1177–1181. [PMC free article] [PubMed]
  • Nelissen RL, Will CL, van Venrooij WJ, Lührmann R. The association of the U1-specific 70K and C proteins with U1 snRNPs is mediated in part by common U snRNP proteins. EMBO J. 1994 Sep 1;13(17):4113–4125. [PMC free article] [PubMed]
  • Neubauer G, Gottschalk A, Fabrizio P, Séraphin B, Lührmann R, Mann M. Identification of the proteins of the yeast U1 small nuclear ribonucleoprotein complex by mass spectrometry. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):385–390. [PMC free article] [PubMed]
  • Palfi Z, Günzl A, Cross M, Bindereif A. Affinity purification of Trypanosoma brucei small nuclear ribonucleoproteins reveals common and specific protein components. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9097–9101. [PMC free article] [PubMed]
  • Pannone BK, Xue D, Wolin SL. A role for the yeast La protein in U6 snRNP assembly: evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts. EMBO J. 1998 Dec 15;17(24):7442–7453. [PMC free article] [PubMed]
  • Plessel G, Fischer U, Lührmann R. m3G cap hypermethylation of U1 small nuclear ribonucleoprotein (snRNP) in vitro: evidence that the U1 small nuclear RNA-(guanosine-N2)-methyltransferase is a non-snRNP cytoplasmic protein that requires a binding site on the Sm core domain. Mol Cell Biol. 1994 Jun;14(6):4160–4172. [PMC free article] [PubMed]
  • Pühler G, Leffers H, Gropp F, Palm P, Klenk HP, Lottspeich F, Garrett RA, Zillig W. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4569–4573. [PMC free article] [PubMed]
  • Puig O, Rutz B, Luukkonen BG, Kandels-Lewis S, Bragado-Nilsson E, Séraphin B. New constructs and strategies for efficient PCR-based gene manipulations in yeast. Yeast. 1998 Sep 15;14(12):1139–1146. [PubMed]
  • Raker VA, Plessel G, Lührmann R. The snRNP core assembly pathway: identification of stable core protein heteromeric complexes and an snRNP subcore particle in vitro. EMBO J. 1996 May 1;15(9):2256–2269. [PMC free article] [PubMed]
  • Rokeach LA, Jannatipour M, Haselby JA, Hoch SO. Mapping of the immunoreactive domains of a small nuclear ribonucleoprotein-associated Sm-D autoantigen. Clin Immunol Immunopathol. 1992 Dec;65(3):315–324. [PubMed]
  • Roy J, Zheng B, Rymond BC, Woolford JL., Jr Structurally related but functionally distinct yeast Sm D core small nuclear ribonucleoprotein particle proteins. Mol Cell Biol. 1995 Jan;15(1):445–455. [PMC free article] [PubMed]
  • Rymond BC. Convergent transcripts of the yeast PRP38-SMD1 locus encode two essential splicing factors, including the D1 core polypeptide of small nuclear ribonucleoprotein particles. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):848–852. [PMC free article] [PubMed]
  • Rymond BC, Rokeach LA, Hoch SO. Human snRNP polypeptide D1 promotes pre-mRNA splicing in yeast and defines nonessential yeast Smd1p sequences. Nucleic Acids Res. 1993 Jul 25;21(15):3501–3505. [PMC free article] [PubMed]
  • Schweinfest CW, Graber MW, Chapman JM, Papas TS, Baron PL, Watson DK. CaSm: an Sm-like protein that contributes to the transformed state in cancer cells. Cancer Res. 1997 Jul 15;57(14):2961–2965. [PubMed]
  • Séraphin B. 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. 1995 May 1;14(9):2089–2098. [PMC free article] [PubMed]
  • Seraphin B, Rosbash M. Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell. 1989 Oct 20;59(2):349–358. [PubMed]
  • Smith CM, Steitz JA. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell. 1997 May 30;89(5):669–672. [PubMed]
  • Smith DR, Doucette-Stamm LA, Deloughery C, Lee H, Dubois J, Aldredge T, Bashirzadeh R, Blakely D, Cook R, Gilbert K, et al. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol. 1997 Nov;179(22):7135–7155. [PMC free article] [PubMed]
  • Tan EM. Antinuclear antibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Adv Immunol. 1989;44:93–151. [PubMed]
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. [PMC free article] [PubMed]
  • Toh-e A, Sahashi Y. The PET18 locus of Saccharomyces cerevisiae: a complex locus containing multiple genes. Yeast. 1985 Dec;1(2):159–171. [PubMed]
  • Tollervey D, Mattaj IW. Fungal small nuclear ribonucleoproteins share properties with plant and vertebrate U-snRNPs. EMBO J. 1987 Feb;6(2):469–476. [PMC free article] [PubMed]
  • Yu YT, Tarn WY, Yario TA, Steitz JA. More Sm snRNAs from vertebrate cells. Exp Cell Res. 1996 Dec 15;229(2):276–281. [PubMed]

Articles from The EMBO Journal are provided here courtesy of The European Molecular Biology Organization

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Conserved Domains
    Conserved Domains
    Link to related CDD entry
  • Gene
    Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • HomoloGene
    HomoloGene
    HomoloGene links
  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • OMIM
    OMIM
    OMIM record citing PubMed
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...