SSB-1 of the Yeast Saccharomyces Cerevisiae is a Nucleolar-specific, Silver-binding Protein That is Associated with the SnR10 and SnR11 Small Nuclear RNAs

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1990 Nov 1

PMID 2121740

Citations 43

Authors

M W Clark

M L Yip

J Campbell

J Abelson

Affiliations

Soon will be listed here.

Abstract

SSB-1, the yeast single-strand RNA-binding protein, is demonstrated to be a yeast nucleolar-specific, silver-binding protein. In double-label immunofluorescence microscopy experiments antibodies to two other nucleolar proteins, RNA Pol I 190-kD and fibrillarin, were used to reveal the site of rRNA transcription; i.e., the fibrillar region of the nucleolus. SSB-1 colocalized with fibrillarin in a double-label immunofluorescence mapping experiment to the yeast nucleolus. SSB-1 is located, though, over a wider region of the nucleolus than the transcription site marker. Immunoprecipitations of yeast cell extracts with the SSB-1 antibody reveal that in 150 mM NaCl SSB-1 is bound to two small nuclear RNAs (snRNAs). These yeast snRNAs are snR10 and snR11, with snR10 being predominant. Since snR10 has been implicated in pre-rRNA processing, the association of SSB-1 and snR10 into a nucleolar snRNP particle indicates SSB-1 involvement in rRNA processing as well. Also, another yeast protein, SSB-36-kD, isolated by single-strand DNA chromatography, is shown to bind silver under the conditions used for nucleolar-specific staining. It is, most likely, another yeast nucleolar protein.

Citing Articles

Modopathies Caused by Mutations in Genes Encoding for Mitochondrial RNA Modifying Enzymes: Molecular Mechanisms and Yeast Disease Models.

Magistrati M, Gilea A, Ceccatelli Berti C, Baruffini E, Dallabona C Int J Mol Sci. 2023; 24(3).

PMID: 36768505 PMC: 9917222. DOI: 10.3390/ijms24032178.

Elucidation of the RNA-granule inducing sodium azide stress response through transcriptome analysis.

Garg M, Poornima G, Rajyaguru P Genomics. 2020; 112(5):2978-2989.

PMID: 32437849 PMC: 7116212. DOI: 10.1016/j.ygeno.2020.05.001.

Sbp1 modulates the translation of Pab1 mRNA in a poly(A)- and RGG-dependent manner.

Brandariz-Nunez A, Zeng F, Lam Q, Jin H RNA. 2017; 24(1):43-55.

PMID: 28986506 PMC: 5733569. DOI: 10.1261/rna.062547.117.

Identification of genes that function in the biogenesis and localization of small nucleolar RNAs in Saccharomyces cerevisiae.

Qiu H, Eifert J, Wacheul L, Thiry M, Berger A, Jakovljevic J Mol Cell Biol. 2008; 28(11):3686-99.

PMID: 18378690 PMC: 2423305. DOI: 10.1128/MCB.01115-07.

Sbp1p affects translational repression and decapping in Saccharomyces cerevisiae.

Segal S, Dunckley T, Parker R Mol Cell Biol. 2006; 26(13):5120-30.

PMID: 16782896 PMC: 1489156. DOI: 10.1128/MCB.01913-05.

References

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Jong A, Campbell J . Isolation of the gene encoding yeast single-stranded nucleic acid binding protein 1. Proc Natl Acad Sci U S A. 1986; 83(4):877-81. PMC: 322973. DOI: 10.1073/pnas.83.4.877. View

Lischwe M, Smetana K, Olson M, Busch H . Proteins C23 and B23 are the major nucleolar silver staining proteins. Life Sci. 1979; 25(8):701-8. DOI: 10.1016/0024-3205(79)90512-5. View

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

Fakan S, PUVION E . The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol. 1980; 65:255-99. DOI: 10.1016/s0074-7696(08)61962-2. View

Chooi W, Leiby K . An electron microscopic method for localization of ribosomal proteins during transcription of ribosomal DNA: a method for studying protein assembly. Proc Natl Acad Sci U S A. 1981; 78(8):4823-7. PMC: 320262. DOI: 10.1073/pnas.78.8.4823. View

Wray W, Boulikas T, Wray V, Hancock R . Silver staining of proteins in polyacrylamide gels. Anal Biochem. 1981; 118(1):197-203. DOI: 10.1016/0003-2697(81)90179-2. View

LaBonne S, Dumas L . Isolation of a yeast single-strand deoxyribonucleic acid binding protein that specifically stimulates yeast DNA polymerase I. Biochemistry. 1983; 22(13):3214-9. DOI: 10.1021/bi00282a027. View

Scheer U, Rose K . Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc Natl Acad Sci U S A. 1984; 81(5):1431-5. PMC: 344849. DOI: 10.1073/pnas.81.5.1431. View

10.

Spector D, Ochs R, Busch H . Silver staining, immunofluorescence, and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma. 1984; 90(2):139-48. DOI: 10.1007/BF00292451. View

11.

Hugle B, Hazan R, Scheer U, Franke W . Localization of ribosomal protein S1 in the granular component of the interphase nucleolus and its distribution during mitosis. J Cell Biol. 1985; 100(3):873-86. PMC: 2113517. DOI: 10.1083/jcb.100.3.873. View

12.

Hugle B, Scheer U, Franke W . Ribocharin: a nuclear Mr 40,000 protein specific to precursor particles of the large ribosomal subunit. Cell. 1985; 41(2):615-27. DOI: 10.1016/s0092-8674(85)80034-9. View

13.

Sentenac A . Eukaryotic RNA polymerases. CRC Crit Rev Biochem. 1985; 18(1):31-90. DOI: 10.3109/10409238509082539. View

14.

Lischwe M, Ochs R, Reddy R, Cook R, Yeoman L, Tan E . Purification and partial characterization of a nucleolar scleroderma antigen (Mr = 34,000; pI, 8.5) rich in NG,NG-dimethylarginine. J Biol Chem. 1985; 260(26):14304-10. View

15.

Ochs R, Lischwe M, Spohn W, Busch H . Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell. 1985; 54(2):123-33. DOI: 10.1111/j.1768-322x.1985.tb00387.x. View

16.

Riedel N, Wise J, SWERDLOW H, Mak A, Guthrie C . Small nuclear RNAs from Saccharomyces cerevisiae: unexpected diversity in abundance, size, and molecular complexity. Proc Natl Acad Sci U S A. 1986; 83(21):8097-101. PMC: 386874. DOI: 10.1073/pnas.83.21.8097. View

17.

Riedel N, Wolin S, Guthrie C . A subset of yeast snRNA's contains functional binding sites for the highly conserved Sm antigen. Science. 1987; 235(4786):328-31. DOI: 10.1126/science.2948278. View

18.

Reimer G, Pollard K, Penning C, Ochs R, Lischwe M, Busch H . Monoclonal autoantibody from a (New Zealand black x New Zealand white)F1 mouse and some human scleroderma sera target an Mr 34,000 nucleolar protein of the U3 RNP particle. Arthritis Rheum. 1987; 30(7):793-800. DOI: 10.1002/art.1780300709. View

19.

Benavente R, Rose K, Reimer G, Scheer U . Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells. J Cell Biol. 1987; 105(4):1483-91. PMC: 2114661. DOI: 10.1083/jcb.105.4.1483. View

20.

Clark M, Abelson J . The subnuclear localization of tRNA ligase in yeast. J Cell Biol. 1987; 105(4):1515-26. PMC: 2114637. DOI: 10.1083/jcb.105.4.1515. View