Purification and characterization of the nuclear RNase P holoenzyme complex reveals extensive subunit overlap with RNase MRP

Genes and Development

Volumn 12, Issue 11, 1998, Pages 1678-1690

  Chamberlain, Joel R ^a   Lee, Yoon ^a   Lane, William S ^b   Engelke, David R ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Ribonuclease MRP; Ribonuclease P; RNP; TRNA

Indexed keywords

RIBONUCLEASE P;

ARTICLE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME SUBUNIT; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE;

BACTERIA (MICROORGANISMS); EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 2642635832     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.11.1678     Document Type: Article

References (78)

1. Alifano, P., F. Rivellini, C. Piscitelli, C.M. Arraiano, C.B. Bruni, and M.S. Carlomagno. 1994. Ribonuclease E provides substrates for ribonuclease P-dependent processing of a polycistronic mRNA. Genes & Dev. 8: 3021-3031.
2. Altman, S., L. Kirsebom, and S.J. Talbot. 1995. Recent studies of RNase P. In tRNA: Structure, biosynthesis, and function (ed. D. Söll and U.L. RajBhandary), pp. 67-78. American Society of Microbiology, Washington, D.C.
3. Altschul, S.F., W. Gish, W. Miller, E.W. Myers, and D.J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
4. Bairoch, A., P. Bucher, and K. Hofmann. 1995. The PROSITE database, its status in 1995. Nucleic Acids Res. 24: 189-196.
5. Bartkiewicz, M., H. Gold, and S. Altman. 1989. Identification and characterization of an RNA molecule that copurifies with RNase P activity from HeLa cells. Genes & Dev. 3: 488-199.
6. Baudin-Baillieu, A., D. Tollervey, C. Cullin, and F. Lacroute. 1997. Functional analysis of Rrp7p, an essential yeast protein involved in pre-rRNA processing and ribosome assembly. Mol. Cell Biol. 17: 5023-5032.
7. Bothwell, A.L., R.L. Garber, and S. Altman. 1976. Nucleotide sequence and in vitro processing of a precursor molecule to Escherichia coli 4.5 S RNA. J. Biol. Chem. 251: 7709-7716.
8. Brown, J.W., D.A. Hunt, and N.R. Pace. 1990. Nucleotide sequence of the 10Sa RNA gene of the β-purple eubacterium Alcaligenes eutrophus. Nucleic Acids Res. 18: 2820.
9. Burd, C.G. and G. Dreyfuss. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 256: 615-621.
10. Burton, Z.F., C.A. Gross, K.K. Watanabe, and R.R. Burgess. 1983. The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell 32: 335-349.
11. Chamberlain, J.R., E. Pagán-Ramos, D.W. Kindelberger, and D.R. Engelke. 1996a. An RNase P RNA subunit mutation that affects ribosomal RNA processing. Nucleic Acids Res. 24: 3158-3166.
12. Chamberlain, J.R., A.J. Tranguch, E. Pagán-Ramos, and D.R. Engelke 1996b. Eukaryotic nuclear RNase P: Structures and functions. In Progress in nucleic acids research and molecular biology (ed. K. Moldave and W. Cohn), pp. 87-119. Academic Press, San Diego, CA.
13. Chen, J.L. and N.R. Pace. 1997. Identification of the universally conserved core of ribonuclease P RNA. RNA 3: 557-560.
14. Cherry, J.M., C. Adler, C. Ball, S. Dwight, S. Chervitz, Y. Jia, G. Juvik, S. Weng, and D. Botstein. 1996. Saccharomyces Genome Database. http://genome-www.stanford.edu/Saccharomyces/1996.
15. Chervitz, S.A., J.M. Cherry, and D. Botstein. 1997. Saccharomyces genome database on-line pattern matching program. http://genome-www.stanford.edu/Sacch3D/pat-match.html.
16. Chu, S., R.H. Archer, J.M. Zengel, and L. Lindahl. 1994. The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc. Natl. Acad. Sci. 91: 659-663.
17. Chu, S., J.M. Zengel, and L. Lindahl. 1997. A novel protein snared by RNase MRP and RNase P. RNA 3: 382-391.
18. Dang, Y.L. and N.C. Martin. 1993. Yeast mitochondrial RNase P. sequence of the RPM2 gene and demonstration that its product is a protein subunit of the enzyme. J. Biol. Chem. 268: 19791-19796.
19. Dichtl, B. and D. Tollervey. 1997. Pop3p is essential for the activity of the RNase MRP and RNase P ribonucleoproteins in vivo. EMBO J. 16: 417-429.
20. Dingwall, C. and R. Laskey. 1992. Nuclear targeting sequences - a consensus? Trends Biochem. Sci. 16: 478-481.
21. Doersen, C.J., C. Guerrier Takada, S. Altman, and G. Attardi. 1985. Characterization of an RNase P activity from HeLa cell mitochondria. Comparison with the cytosol RNase P activity. J. Biol. Chem. 260: 5942-5949.
22. Doria, M., G. Carrara, P. Calandra, and G.P. Tocchini Valentini. 1991. An RNA molecule copurifies with RNase P activity from Xenopus laevis oocytes. Nucleic Acids Res. 19: 2315-2320
23. Eder, P.S., R. Kekuda, V. Stolc, and S. Altman. 1997. Characterization of two scleroderma autoimmune antigens that copu-rify with human ribonuclease P. Proc. Natl Acad. Sci. 94: 1101-1106.
24. Eng, J.K., A.L. McCormick, and J.R.I. Yates. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom 5: 976-989.
25. Engemann, S., E. Herfurth, U. Briesemeister, and B. Wittmann-Liebold. 1995. Amino acid sequence of the ribosomal protein HS23 from the halophilic Haloarcula marismortui and homology studies to other ribosomal proteins. J. Protein Chem. 14: 189-195.
26. Evans, C.F. and D.R. Engelke. 1990. Yeast extracts for transfer RNA gene transcription and processing. Methods Enzymol. 181: 439-450.
27. Felici, F., G. Cesareni, and J.M. Hughes. 1989. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol. Cell. Biol. 9: 3260-3268.
28. Forster, A.C. and S. Altman. 1990. Similar cage-shaped structures for the RNA components of all ribonuclease P and ribonuclease MRP enzymes. Cell 62: 407-409.
29. Garcia-Bustos, J., J. Heitman, and M.N. Hall. 1991. Nuclear protein localization. Biochim. Biophys. Acta 1071: 83-101.
30. Goffeau, A., B.G. Barrell, H. Bussey, R.W. Davis, B. Dujon, H. Feldman, F. Galibert, J.D. Hoheisel, C. Jacq, M. Johnston, E.J. Louis, H.W. Mewes, Y. Murakami, P. Philippsen, H. Tettelin, and S.G. Oliver. 1996. Life with 6000 genes. Science 274: 563-567.
31. Gold, H.A., J.N. Topper, D.A. Clayton, and J. Craft. 1989. The RNA processing enzyme RNase MRP is identical to the Th RNP and related to RNase P. Science 245: 1377-1380.
32. Gopalan, V., A.D. Baxevanis, D. Landsman, and S. Altman. 1997. Analysis of the functional role of conserved residues in the protein subunit of ribonuclease P from Escherichia coli. J. Mol. Biol. 267: 818-829.
33. Green, C.J., B.S. Vold, M.D. Morch, R.L. Joshi, and A.L. Haenni. 1988. Ionic conditions for the cleavage of the tRNA-like structure of turnip yellow mosaic virus by the catalytic RNA of RNase P. J. Biol. Chem. 263: 11617-11620.
34. Guerrier-Takada, C., K. Gardiner, T. Marsh, N. Pace, and S. Altman. 1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35: 849-857.
35. Hansen, F.G., E.B. Hansen, and T. Atlung. 1985. Physical mapping and nucleotide sequence of the rnpA gene that encodes the protein component of ribonuclease P in Escherichia coli. Gene 38: 85-93.
36. Harris, M.E., A.V. Kazantsev, J.L. Chen, and N.R. Pace. 1997. Analysis of the tertiary structure of the ribonuclease P ribozyme-substrate complex by site-specific photoaffinity crosslinking. RNA 3: 561-576.
37. Harris, S.D., J. Cheng, T.A. Pugh, and J.R. Pringle. 1992. Molecular analysis of Saccharomyces cerevisiae chromosome I. On the number of genes and the identification of essential genes using temperature-sensitive-lethal mutations. J. Mol. Biol. 225: 53-65.
38. Hollingsworth, M.J. and N.C. Martin. 1986. RNase P activity in the mitochondria of Saccharomyces cerevisiae depends on both mitochondrion and nucleus-encoded components. Mol. Cell Biol. 6: 1058-1064.
39. _. 1987. Alteration of a mitochondrial tRNA precursor 5′ leader abolishes its cleavage by yeast mitochondrial RNase P. Nucleic Acids Res. 15: 8845-8860.
40. Jacobson, M.R., L.G. Cao, Y.L. Wang, and T. Pederson. 1995. Dynamic localization of RNase MRP RNA in the nucleolus observed by fluorescent RNA cytochemistry in living cells. J. Cell. Biol. 131: 1649-1658.
41. Jacobson, M.R., L.G. Cao, K. Taneja, R.H. Singer, Y.L. Wang, and T. Pederson. 1997. Nuclear domains of the RNA subunit of RNase P. J. Cell Sci. 110: 829-837.
42. Jayanthi, G.P. and G.C. Van Tuyle. 1992. Characterization of ribonuclease P isolated from rat liver cytosol. Arch. Biochem. Biophys. 296: 264-270.
43. Kikuchi, Y., N. Sasaki, and Y. Ando-Yamagami. 1990. Cleavage of tRNA within the mature tRNA sequence by the catalytic RNA of RNase P: Implication for the formation of the primer tRNA fragment for reverse transcription in copia retrovirus-like particles. Proc. Natl. Acad. Sci. 87: 8105-8109.
44. Komine Y., M. Kitabatake, T. Yokogawa, K. Nishikawa, and H. Inokuchi. 1994. A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc. Natl. Acad. Sci. 91: 9223-9227.
45. Lawrence, N., D. Wesolowski, H. Gold, M. Bartkiewicz, C. Guerrier-Takada, W.H. McClain, and S. Altman. 1987. Characteristics of ribonuclease P from various organisms. Cold Spring Harbor Symp. Quant. Biol. 52: 233-238.
46. Lee, B., A.G. Matera, D.C. Ward, and J. Craft. 1996. Association of RNase mitochondrial RNA processing enzyme with ribonuclease P in higher ordered structures in the nucleolus: A possible coordinate role in ribosome biogenesis. Proc. Natl. Acad. Sci. 93: 11471-11476.
47. Lee, J.Y. and D.R. Engelke. 1989. Partial characterization of an RNA component that copurifies with Saccharomyces cerevisiae RNase P. Mol. Cell Biol. 9: 2536-2543.
48. Lee, J.Y., C.E. Rohlman, L.A. Molony, and D.R. Engelke. 1991. Characterization of RPR1, an essential gene encoding the RNA component of Saccharomyces cerevisiae nuclear RNase P. Mol. Cell Biol. 11: 721-730.
49. Lee, Y.C., B.J. Lee, D.S. Hwang, and H.S. Kang. 1996. Purification and characterization of mitochondrial ribonuclease P from Aspergillus nidulans. Eur. J. Biochem. 235: 289-296.
50. Lipman, D.J. and W.R. Pearson. 1985. Rapid and sensitive protein similarity searches. Science 227: 1435-1441.
51. Liu, F. and S. Altman. 1994. Differential evolution of substrates for an RNA enzyme in the presence and absence of its protein cofactor. Cell 77: 1093-1100.
52. Lygerou, Z., P. Mitchell, E. Petfalski, B. Seraphin, and D. Tollervey. 1994. The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins. Genes & Dev. 8: 1423-1433.
53. Lygerou, Z., C. Allmang, D. Tollervey, and B. Séraphin. 1996. Accurate processing of a eukaryotic precursor ribosomal RNA by ribonuclease MRP in vitro. Science 272: 268-270.
54. Mans, R.M., C. Guerrier Takada, S. Altman, and C.W. Pleij. 1990. Interaction of RNase P from Escherichia coli with pseudoknotted structures in viral RNAs. Nucleic Acids Res. 18: 3479-3487.
55. Matera, A.G., M.R. Frey, K. Margelot, and S.L. Wolin. 1995. A perinucleolar compartment contains several RNA polymer-ase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J. Cell Biol. 129: 1181-1193.
56. Morales, M.J., Y.L. Dang, Y.C. Lou, P. Sulo, and N.C. Martin. 1992. A 105-kDa protein is required for yeast mitochondrial RNase P activity. Proc. Natl. Acad. Sci. 89: 9875-9879.
57. Morrissey, J.P. and D. Tollervey. 1995. Birth of the snoRNPs: The evolution of RNase MRP and the eukaryotic pre-rRNA-processing system. Trends Biochem. Sci. 20: 78-82.
58. Mumberg, D., R. Müller, and M. Funk. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
59. Nash, H.M., S.D. Bruner, O.D. Scharer, T. Kawate, T.A. Addona, E. Spooner, W.S. Lane, and G.L. Verdine. 1996. Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base-excision DNA-repair protein superfamily. Curr. Biol. 6: 968-980.
60. Pace, N.R. and J.W. Brown. 1995. Evolutionary perspective on the structure and function of ribonuclease P, a ribozyme. J. Bacteriol. 177: 1919-1928.
61. Pearson, W.R. and D.J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. 85: 2444-2448.
62. Reich, C., G.J. Olsen, B. Pace, and N.R. Pace. 1988. Role of the protein moiety of ribonuclease P, a ribonucleoprotein enzyme. Science 239: 178-181.
63. Rodriguez-Tome, P., P.J. Stoehr, G.N. Cameron, and T.P. Flores. 1996. The European Bioinformatics Institute (EBI) databases. Nucleic Acids Res. 24: 6-12.
64. Rose, M.D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
65. Rutgers, C.A., J.M.J. Rientjes, J. van't Reit, 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.
66. Salazar, C.E., D.M. Mills-Hamm, V. Kumar, and F.H. Collins. 1993. Sequence of a cDNA from the mosquito Anopheles gambiae encoding a homologue of human ribosomal protein S7. Nucleic Acids Res. 21: 4147.
67. Schmitt, M.E. and D.A. Clayton. 1993. Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol. Cell Biol 13: 7935-7941.
68. _. 1994. Characterization of a unique protein component of yeast RNase MRP: An RNA-binding protein with a zinc-cluster domain. Genes &. Dev. 8: 2617-2628.
69. Shuai, K. and J.R. Warner. 1991. A temperature sensitive mutant of Saccharomyces cerevisiae defective in pre-rRNA processing. Nucleic Acid Res. 19: 5059-5064.
70. Sidman, K.E., D.G. George, W.C. Barker, and L.T. Hunt. 1988. The protein identification resource (PIR). Nucleic Acids Res. 16: 1869-1871.
71. Stohl, L.L. and D.A. Clayton. 1992. Saccharomyces cerevisiae contains an RNase MRP that cleaves at a conserved mitochondrial RNA sequence implicated in replication priming. Mol. Cell Biol. 12: 2561-2569.
72. Stole, V. and S. Altman. 1997. Rpp1, an essential protein subunit of nuclear RNase P required for processing of precursor tRNA and 35S precursor rRNA in Saccharomyces cerevisiae. Genes & Dev. 11: 2414-2425.
73. Thomas, B.C., L. Gao, D. Stomp, X. Li, and P.A. Gegenheimer 1995. Spinach chloroplast RNase P: A putative protein enzyme. Nucleic Acids Symp. Ser. 33: 95-98.
74. Tranguch, A.J., D.W. Kindelberger, C.E. Rohlman, J.Y. Lee, and D.R. Engelke. 1994. Structure-sensitive RNA footprinting of yeast nuclear ribonuclease P. Biochemistry 33: 1778-1787.
75. Wach, A., A. Brachat, R. Pohlmann, and P. Philippsen. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
76. Wessel, D. and U.I. Flügge. 1984. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138: 141-143.
77. Westhof, E. and S. Altman. 1994. Three-dimensional working model of M1 RNA, the catalytic RNA subunit of ribonuclease P from Escherichia coli. Proc. Natl. Acad. Sci. 91: 5133-5137.
78. Zimmerly, S., D. Drainas, L.A. Sylvers, and D. Söll. 1993. Identification of a 100-kDa protein associated with nuclear ribonuclease P activity in Schizosaccharomyces pombe. Eur. J. Biochem. 217: 501-507.