Sm and Sm-like Proteins Assemble in Two Related Complexes of Deep Evolutionary Origin

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1999 Jun 16

PMID 10369684

Citations 126

Authors

B Seraphin

Affiliations

Soon will be listed here.

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.

Citing Articles

Alternative splicing regulation and its therapeutic potential in bladder cancer.

Li L, Jin T, Hu L, Ding J Front Oncol. 2024; 14:1402350.

PMID: 39132499 PMC: 11310127. DOI: 10.3389/fonc.2024.1402350.

Oncofetal SNRPE promotes HCC tumorigenesis by regulating the FGFR4 expression through alternative splicing.

Wu Q, Liao R, Miao C, Hasnat M, Li L, Sun L Br J Cancer. 2024; 131(1):77-89.

PMID: 38796598 PMC: 11231362. DOI: 10.1038/s41416-024-02689-5.

Deregulated circRNAs in Epithelial Ovarian Cancer With Activity in Preclinical Models: Identification of Targets and New Modalities for Therapeutic Intervention.

Weidle U, Birzele F Cancer Genomics Proteomics. 2024; 21(3):213-237.

PMID: 38670587 PMC: 11059596. DOI: 10.21873/cgp.20442.

Growth-regulated co-occupancy of Mediator and Lsm3 at intronic ribosomal protein genes.

Abdel-Fattah W, Carlsson M, Hu G, Singh A, Vergara A, Aslam R Nucleic Acids Res. 2024; 52(11):6220-6233.

PMID: 38613396 PMC: 11194063. DOI: 10.1093/nar/gkae266.

Analysis of Lsm Protein-Mediated Regulation in the Haloarchaeon .

Paya G, Bautista V, Pastor-Soler S, Camacho M, Esclapez J, Bonete M Int J Mol Sci. 2024; 25(1).

PMID: 38203750 PMC: 10779274. DOI: 10.3390/ijms25010580.

References

Gottschalk A, Tang J, Puig O, Salgado J, Neubauer G, Colot H . A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA. 1998; 4(4):374-93. PMC: 1369625. View

Seraphin 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; 14(9):2089-98. PMC: 398309. DOI: 10.1002/j.1460-2075.1995.tb07200.x. View

Bacchetti S, Graham F . 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; 74(4):1590-4. PMC: 430836. DOI: 10.1073/pnas.74.4.1590. View

Lerner E, Lerner M, Janeway Jr C, Steitz J . Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A. 1981; 78(5):2737-41. PMC: 319432. DOI: 10.1073/pnas.78.5.2737. View

Huber J, Cronshagen U, Kadokura M, Marshallsay C, Wada T, Sekine M . Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 1998; 17(14):4114-26. PMC: 1170744. DOI: 10.1093/emboj/17.14.4114. View

Kawarabayasi Y, Sawada M, Horikawa H, Haikawa Y, Hino Y, Yamamoto S . Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res. 1998; 5(2):55-76. DOI: 10.1093/dnares/5.2.55. View

Boeck R, Lapeyre B, Brown C, Sachs A . Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol Cell Biol. 1998; 18(9):5062-72. PMC: 109091. DOI: 10.1128/MCB.18.9.5062. View

Puig O, Rutz B, Luukkonen B, Seraphin B . New constructs and strategies for efficient PCR-based gene manipulations in yeast. Yeast. 1998; 14(12):1139-46. DOI: 10.1002/(SICI)1097-0061(19980915)14:12<1139::AID-YEA306>3.0.CO;2-B. View

Pannone B, Xue D, Wolin S . 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; 17(24):7442-53. PMC: 1171088. DOI: 10.1093/emboj/17.24.7442. View

10.

Kambach C, Walke S, Young R, Avis J, de La Fortelle E, Raker V . Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell. 1999; 96(3):375-87. DOI: 10.1016/s0092-8674(00)80550-4. View

11.

Chen H, Remmler J, Delaney J, Messner D, 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.... J Biol Chem. 1993; 268(30):22338-46. View

12.

Fischer U, Heinrich J, Van Zee K, Fanning E, Luhrmann R . Nuclear transport of U1 snRNP in somatic cells: differences in signal requirement compared with Xenopus laevis oocytes. J Cell Biol. 1994; 125(5):971-80. PMC: 2120059. DOI: 10.1083/jcb.125.5.971. View

13.

Plessel G, Fischer U, Luhrmann 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; 14(6):4160-72. PMC: 358782. DOI: 10.1128/mcb.14.6.4160-4172.1994. View

14.

Nelissen R, Will C, van Venrooij W, Luhrmann 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; 13(17):4113-25. PMC: 395334. DOI: 10.1002/j.1460-2075.1994.tb06729.x. View

15.

Lygerou Z, Mitchell P, Petfalski E, Seraphin B, Tollervey D . The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins. Genes Dev. 1994; 8(12):1423-33. DOI: 10.1101/gad.8.12.1423. View

16.

Roy J, Zheng B, Rymond B, Woolford Jr J . Structurally related but functionally distinct yeast Sm D core small nuclear ribonucleoprotein particle proteins. Mol Cell Biol. 1995; 15(1):445-55. PMC: 231989. DOI: 10.1128/MCB.15.1.445. View

17.

Cooper M, Johnston L, Beggs J . 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; 14(9):2066-75. PMC: 398307. DOI: 10.1002/j.1460-2075.1995.tb07198.x. View

18.

Hermann H, Fabrizio P, Raker V, Foulaki K, HORNIG H, Brahms H . snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 1995; 14(9):2076-88. PMC: 398308. DOI: 10.1002/j.1460-2075.1995.tb07199.x. View

19.

Dignam J, Lebovitz R, Roeder R . Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983; 11(5):1475-89. PMC: 325809. DOI: 10.1093/nar/11.5.1475. View

20.

Devereux J, Haeberli P, SMITHIES O . A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984; 12(1 Pt 1):387-95. PMC: 321012. DOI: 10.1093/nar/12.1part1.387. View