Ribosomal protein S14 of Saccharomyces cerevisiae regulates its expression by binding to RPS14B pre-mRNA and to 18S rRNA

Molecular and Cellular Biology

Volumn 19, Issue 1, 1999, Pages 826-834

  Fewell, Sheara W ^a   Woolford Jr , John L ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA PRECURSOR; RIBOSOME PROTEIN; RNA 18S;

ANTIBIOTIC RESISTANCE; ARTICLE; FUNGAL GENETICS; GENE CONTROL; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RIBOSOME; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 0032939495     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.1.826     Document Type: Article

References (70)

1. Allen, P. N., and H. F. Noller. 1989. Mutations in ribosomal proteins S4 and S12 influence the higher order structure of 16S ribosomal RNA. J. Mol. Biol. 208:457-468.
2. Bollen, A., R. L. Heimark, A. Cozzone, R. R. Traut, and J. W. B. Hershey. 1975. Cross-linking of initiation factor IF-2 to Escherichia coli 30S ribosomal proteins with dimethylsuberimidate. J. Biol. Chem. 250:4310-4314.
3. Bozzoni, I., P. Fragapane, F. Annesi, P. Pierandrei-Amaldi, F. Amaldi, and E. Beccari. 1984. Expression of two Xenopus laevis ribosomal protein genes in injected frog oocytes: a specific splicing block interferes with the L1 RNA maturation. J. Mol. Biol. 180:987-1005.
4. 1192 in 16S rRNA, thereby potentially freezing this molecule into an inactive conformation. Nucleic Acids Res. 22:325-331.
5. Bucher, K., and L. Skogerson. 1976. Cryptopleurine - an inhibitor of translocation. Biochemistry 15:4755-4759.
6. Caffarelli, E., P. Fragapane, C. Gehring, and I. Bozzoni. 1987. The accumulation of mature RNA for the X. laevis ribosomal protein L1 is controlled at the level of splicing and turnover of the precursor RNA. EMBO J. 6:3493-3498.
7. Chang, C., and G. R. Craven. 1977. Identification of several proteins involved in the messenger RNA binding site of the 30S ribosome by inactivation with 2-methoxy-5-nitrotropone. J. Mol. Biol. 117:401-418.
8. Chittum, H. S., and W. S. Champney. 1994. Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J. Bacteriol. 176:6192-6198.
9. Dabeva, M. D., and J. R. Warner. 1993. Ribosomal protein L32 of Saccharomyces cerevisiae regulates both splicing and translation of its own transcript. J. Biol. Chem. 268:19669-19674.
10. Davies, C., V. Ramakrishnan, and S. W. White. 1996 Structural evidence for specific S8-RNA and S8-protein interactions within the 30S subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9 Å resolution. Structure 4:1093-1104.
11. Draper, D. E. 1994. RNA-protein interactions in ribosomes, p. 82-102. In K. Nagai and I. W. Mattaj (ed.), RNA-protein interactions. Oxford University Press, Oxford, United Kingdom.
12. Draper, D. E. 1996. Ribosomal protein-RNA interactions, p. 171-198. In R. A. Zimmerman and A E. Dahlberg (ed.), Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis. CRC Press, Inc., Boca Raton, Fla.
13. El-Baradi, T. T. A. L., H. A. Raué, V. C. H. F. de Regt, E. C. Verbree, and R. J. Planta. 1985. Yeast ribosomal protein L25 binds to an evolutionary conserved site on yeast 26S and E. coli 23S rRNA. EMBO J. 4:2101-2107.
14. El-Baradi, T. T. A. L., V. C. H. F. de Regt, S. W. C. Einerhand, J. Teixido, R. J. Planta, J. P. G. Ballesta, and H. A. Raué. 1987 Ribosomal proteins EL11 from Escherichia coli and L15 from Saccharomyces cerevisiae bind to the same site in both yeast 26S and mouse 28S rRNA. J. Mol. Biol. 195:909-917.
15. Eng, F. J., and J. R. Warner. 1991. Structural basis for the regulation of splicing of a yeast messenger RNA. Cell 65:797-804.
16. Fanning, T. G., M. Cantrell, C. Y. Shin, and G. R. Craven. 1978. Evidence that proteins S1, S11, and S21 directly participate in the binding of transfer RNA to the 30S ribosome. Nucleic Acids Res. 5:933-950.
17. Fourmy, D., M. I. Recht, S. C. Blanchard, and J. D. Puglisi. 1996. Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274:1367-1371.
18. 15N NMR. Biochemistry 32:12812-12820.
19. Gorenstein, C., and J. R. Warner. 1976. Coordinate regulation of the synthesis of eukaryotic ribosomal proteins. Proc. Natl. Acad. Sci. USA 73:1547-1551.
20. Greuer, B., M. Osswald, R. Brimacombe, and G. Stöffler. 1987. RNA-protein cross-linking in Escherichia coli 30S ribosomal subunits: determination of sites on 16S rRNA that are cross-linked to proteins S3, S4, S7, S9, S10, S11, S17, S18 and S21 by treatment with bis-(2-chloroethyl)-methylamine. Nucleic Acids Res. 15:3241-3255.
21. Gutell, R. R. 1994. Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res. 22:3502-3507.
22. Heimark, R. L., L. Kahan, K. Johnston, J. W. B. Hershey, and R. R. Tract. 1976. Cross-linking of initiation factor IF3 to proteins of the Escherichia coli 30S ribosomal subunit. J. Mol. Biol. 105:219-230.
23. Jain, C., and J. G. Belasco. 1996. A structural model for the HIV-1 Rev-RRE complex deduced from altered-specificity Rev variants isolated by a rapid genetic strategy. Cell 87:115-125.
24. Kippert, F. 1995. A rapid permeabilization procedure for accurate quantitative determination of beta-galactosidase activity in yeast cells. FEMS Microbiol. Lett. 128:201-206.
25. Kooi, E. A., C. A. Rutgers, M. J. Kleijmeer, J. van't Riet, J. Venema, and H. A. Raué. 1994. Mutational analysis of the C-terminal region of Saccharomyces cerevisiae ribosomal protein L25 in vitro and in vivo demonstrates the presence of two distinct functional elements. J. Mol. Biol. 240:243-255.
26. Kruiswijk, T., R. J. Planta, and J. M. Krop. 1978. The course of the assembly of ribosomal subunits in yeast. Biochim. Biophys. Acta 517:378-389.
27. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
28. Laird-Offringa, I. A., and J. G. Belasco. 1995 Analysis of RNA-binding proteins by in vitro genetic selection: identification of an amino acid residue important for locking UlA onto its RNA target. Proc. Natl. Acad. Sci. USA 92:11859-11863.
29. Larkin, J. C., and J. L. Woolford, Jr. 1983. Molecular cloning and analysis of the CRY1 gene: a yeast ribosomal protein gene. Nucleic Acids Res. 11:403-420.
30. Larkin, J. C., J. R. Thompson, and J. L. Woolford, Jr. 1987. Structure and expression of the Saccharomyces cerevisiae CRY1 gene: a highly conserved ribosomal protein gene. Mol. Cell. Biol. 7:1764-1775.
31. Li, B., J. Vilardell, and J. R. Warner. 1996. An RNA structure involved in feedback regulation of splicing and of translation is critical for biological fitness. Proc. Natl. Acad. Sci. USA 93:1596-1600.
32. Li, Z. 1995. Feedback regulation of CRY2, a yeast ribosomal protein gene. Ph.D. thesis. Carnegie Mellon University, Pittsburgh, Pa.
33. Li, Z., A. G. Paulovich, and J. L. Woolford, Jr. 1995. Feedback inhibition of the yeast ribosomal protein gene CRY2 is mediated by the nucleotide sequence and secondary structure of CRY2 pre-mRNA. Mol. Cell. Biol. 15: 6454-6464.
34. Madjar, J.-J., K. Nielson-Smith, M. Frahm, and D. J. Roufa. 1982. Emetine resistance in Chinese hamster ovary cells is associated with an altered ribosomal protein S14 mRNA. Proc. Natl. Acad. Sci. USA 79:1003-1007.
35. Madjar, J.-J., M. Frahm, S. McGill, and D. J. Roufa. 1983. Ribosomal protein S14 is altered by two-step emetine resistance in Chinese hamster cells. Mol. Cell. Biol. 3:190-197.
36. Mager, W. H., R. J. Planta, J.-P. G. Ballesta, J. C. Lee, K. Mizuta, K. Suzuki, J. R. Warner, and J. Woolford. 1997. A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Res. 25: 4872-4875.
37. Martin, F., A. Schaller, S. Eglite, D. Schümperli, and B. Müller. 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.
38. Moazed, D., and H. F. Noller. 1987. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389-394.
39. Moritz, M., A. G. Paulovich, Y.-F. Tsay, and J. L. Woolford, Jr. 1990. Depletion of yeast ribosomal proteins L16 or rp59 disrupts ribosome assembly. J. Cell Biol. 111:2261-2274.
40. Mueller, F., and R. Brimacombe. 1997. A new model for the three-dimensional folding of Escherichia coli 16S ribosomal RNA. II. The RNA-protein interaction data. J. Mol. Biol. 271:545-565.
41. Nomura, M., and W. A. Held. 1974. Reconstitution of ribosomes: studies of ribosome structure, function and assembly, p. 193-223. In M. Nomura, A. Tissières, and P. Lengyel (ed.), Ribosomes. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Nomura, M. 1990. History of ribosome research: a personal account, p. 3-55. In W. Hill et al. (ed.), The ribosome: structure, function, and evolution. American Society for Microbiology, Washington, D.C.
43. Paulovich, A. G., J. R. Thompson, J. C. Larkin, Z. Li, and J. L. Woolford, Jr. 1993. Molecular genetics of cryptopleurine resistance in Saccharomyces cerevisiae: expression of a ribosomal protein gene family. Genetics 135:719-730.
44. Pongs, O., G. Stöffler, and E. Lanka. 1975. The codon binding site of the Escherichia coli ribosomes as studied with a chemically reactive A-U-G analog. J. Mol. Biol. 99:301-315.
45. Powers, T., and H. G. Noller. 1995. Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA. RNA 1:194-209.
46. Presutti, C., S.-A. Caifre, and I. Bozzoni. 1991. The ribosomal protein L2 in S. cerevisiae controls the level of accumulation of its own mRNA. EMBO J. 10:2215-2221.
47. Presutti, C., T. Villa, D. Hall, C. Pertica, and I. Bozzoni. 1995. Identification of the cis-acting elements mediating the autogenous control of ribosomal protein L2 mRNA stability in yeast. EMBO J. 14:101-109.
48. Puglisi, E. V., and J. D. Puglisi. 1998. Nuclear magnetic resonance spectroscopy of RNA, p. 117-146. In R. W. Simons and M. Grunberg-Manago (ed.), RNA structure and function. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Ramakrishnan, V., and S. W. White. 1992. The structure of ribosomal protein S5 reveals sites of interaction with 16S rRNA. Nature 358:768-771.
50. Ramakrishnan, V., and S. W. White. 1998. Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem. Sci. 23:208-212.
51. Ramakrishnan, V., C. Davies, S. E. Gerchman, B. L. Golden, D. W. Hoffman, T. N. Jaishree, J. H. Kycia, S. Porter, and S. W. White. 1995. Structures of prokaryotic ribosomal proteins: implications for RNA binding and evolution. Biochem. Cell Biol. 73:979-986.
52. Rhoads, D. D., and D. J. Roufa. 1985. Emetine resistance of Chinese hamster cells: structures of wild-type and mutant ribosomal protein S14 mRNAs. Mol. Cell. Biol. 5:1655-1659.
53. Rosendahl, G., and S. Douthwaite. 1995. The antibiotics micrococcin and thiostrepton interact directly with 23S rRNA mucleotides 1067A and 1095A. Nucleic Acids Res. 22:357-363.
54. Rutgers, C. A., J. M. J. Rientjes, J. van't Riet, and H. A. Raué. 1991. rRNA binding domain of yeast ribosomal protein L25: identification of its borders and a key leucine residue. J. Mol. Biol. 218:375-385.
55. SenGupta, D. J., B. Zhang, B. Kraemer, P. Pochart, S. Fields, and M. Wickens. 1996. A three-hybrid system to detect RNA-protein interactions in vivo. Proc. Natl. Acad. Sci. USA 93:8496-8501.
56. Stern, S., T. Powers, L.-M. Changchien, and H. F. Noller. 1989. RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science 244:783-790.
57. Tasheva, E. S., and D. J. Roufa. 1995. Regulation of human RPS14 transcription by intronic antisense RNAs and ribosomal protein S14. Genes Dev. 9:304-316.
58. Trapman, J., J. Retel, and R. J. Planta. 1975. Ribosomal precursor particles from yeast. Exp. Cell Res. 90:95-104.
59. Tsay, Y. F., J. R. Thompson, M. O. Rotenberg, J. C. Larkin, and J. L. Woolford, Jr. 1988. Ribosomal protein synthesis is not regulated at the translational level in Saccharomyces cerevisiae: balanced accumulation of ribosomal proteins L16 and rp59 is mediated by turnover of excess protein. Genes Dev 2:664-676.
60. Urlaub, H., V. Krufl, O. Bischof, E.-C. Müller, and B. Wittmann-Liebold. 1995. Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J. 14:4578-4588.
61. Urlaub, H., B. Thiede, E-.C. Miller, R. Brimacombe, and B. Wittmann-Liebold. 1997. Identification and sequence analysis of contact sites between ribosomal proteins and rRNA in Escherichia coli 30S subunits by a new approach using matrix-assisted laser desorption/ionization-mass spectrometry combined with N-terminal microsequencing. J. Biol. Chem. 272:14547-14555.
62. Varani, G., and K. Nagai. 1998. RNA recognition by RNP proteins during RNA processing. Annu. Rev. Biophys. Biomol. Struct. 27:407-445.
63. Vilardell, J., and J. R. Warner. 1994. Regulation of splicing at an intermediate step in the formation of the splicesome. Genes Dev. 8:211-220.
64. Vilardell, J., and J. R. Warner. 1997. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Mol. Cell. Biol. 17:1959-1965.
65. Wang, Z. F., M. L. Whitfield, T. C. Ingledue III, Z. Dominski, and W. F. Marzluff. 1996. The protein that binds the 3′ end of the histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev. 10:3028-3040.
66. Warner, J. R., G. Mitra, W. F. Schwindinger, M. Studeny, and H. M. Fried. 1985. Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Mol. Cell. Biol. 5:1512-1521.
67. Woolford, J. L. 1991. The structure and biogenesis of yeast ribosomes. Adv. Genet. 29:63-118.
68. Zengel, J. M., and L. Lindahl. 1994. Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Prog, Nucleic Acids Res. Mol. Biol. 47:331-370.
69. Zhang, B., M. Gallegos, A. Puoti, E. Durkin, S. Fields, J. Kimble, and M. P. Wickens. 1997. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390:477-484.
70. Zhen, L., and R. T. Swank. 1993. A simple and high yield method for recovering DNA from agarose gels. BioTechniques 14:894-898.