Escherichia coli cytidine deaminase provides a molecular model for ApoB RNA editing and a mechanism for RNA substrate recognition

Journal of Molecular Biology

Volumn 275, Issue 4, 1998, Pages 695-714

  Navaratnam, Naveenan ^a   Fujino, Takahiro ^a   Bayliss, Jayne ^a   Jarmuz, Adam ^a   How, Alan ^a   Richardson, Nathan ^a   Somasekaram, Angelika ^a   Bhattacharya, Shoumo ^a   Carter, Charles ^b   Scott, James ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

ApoB; Cytidine deaminase; RNA editing

Indexed keywords

APOLIPOPROTEIN B; CYTIDINE DEAMINASE;

AMINO ACID SEQUENCE; ARTICLE; ENZYME ACTIVE SITE; ENZYME BINDING; ESCHERICHIA COLI; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RNA EDITING;

ESCHERICHIA COLI; PROKARYOTA;

EID: 13144259628     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1506     Document Type: Article

References (80)

1. Anant, S., MacGinnitie, A. J. & Davidson, N. O. (1995). Apobec-1, the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme, is a novel RNA-binding protein. J. Biol. Chem. 270, 14762-14767.
2. Backus, J. W. & Smith, H. C. (1991). Apolipoprotein B mRNA sequences 3′ of the editing site are necessary and sufficient for editing and editosome assembly. Nucl. Acids Res. 19, 6781-6786.
3. Backus, J. W. & Smith, H. C. (1992). Three distinct RNA sequence elements are required for efficient apolipoprotein B (apoB) RNA editing in vitro. Nucl. Acids Res. 20, 6007-6014.
4. Backus, J. W., Schock, D. & Smith, H. C. (1994). Only cytidines 5′ of the apolipoprotein B mRNA mooring sequence are edited. Biochim. Biophys. Acta, 1219, 1-14.
5. Betts, L., Xiang, S., Short, S. A., Wolfenden, R. & Carter, C. W. J. (1994). Cytidine deaminase. The 2.3 Å crystal structure of an enzyme: transition-state analog complex. J. Mol. Biol. 235, 635-656.
6. Bhattacharya, S., Navaratnam, N., Morrison, J. R., Scott, J. & Taylor, W. R. (1994). Cytosine nucleoside/nucleotide deaminases and apolipoprotein B mRNA editing. Trends Biochem. Sci. 19, 105-106.
7. Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L. & Wiley, D. C. (1987). Structure of the human class I histocompatibility antigen, HLA-A2. Nature, 329, 506-512.
8. Blundell, T. L. (1996). Structure-based drug design. Nature, 384(Suppl.), 23-26.
9. Borner, G. V. & Paabo, S. (1996). Evolutionary fixation of RNA editing. Nature, 383, 225.
10. Borner, G. V., Morl, M., Janke, A. & Paabo, S. (1996). RNA editing changes the identity of a mitochondrial tRNA in marsupials. EMBO J. 15, 5949-5957.
11. Bostrom, K., Lauer, S. J., Poksay, K. S., Garcia, Z., Taylor, J. M. & Innerarity, T. L. (1989). Apolipoprotein B48 RNA editing in chimeric apolipoprotein EB mRNA. J. Biol. Chem. 264, 15701-15708.
12. Chen, S.-H., Habib, G., Yang, C. Y., Gu, Z. W., Lee, B. R., Weng, S. A., Silberman, S. R., Cai, S. J., Deslypere, J. P., Rosseneu, M., Gotto, A. M. J., Li, W. H. & Chan, L. (1987). Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science, 238, 363-366.
13. Chen, S.-H., Li, X. X., Liao, W. S., Wu, J. H. & Chan, L. (1990). RNA editing of apolipoprotein B mRNA. Sequence specificity determined by in vitro coupled transcription editing. J. Biol. Chem. 265, 6811-6816.
14. Cohen, R. M. & Wolfenden, R. (1971a). Cytidine deaminase from Escherichia coli purification, properties, and inhibition by the potential transition state analog 3, 4, 5, 6-tetrahydrouridine. J. Biol. Chem. 246, 7561-7565.
15. Cohen, R. M. & Wolfenden, R. (1971b). The equilibrium of hydrolytic deamination of cytidine and N4-methylcytidine. J. Biol. Chem. 246, 7566-7568.
16. Covello, P. S. & Gray, M. W. (1989). RNA editing in plant mitochondria. Nature, 341, 662-666.
17. Davidson, N. O., Anant, S. & MacGinnitie, A. J. (1995). Apolipoprotein B messenger RNA editing: insights into the molecular regulation of post-transcriptional cytidine deamination. Curr. Opin. Lipidol. 6, 70-74.
18. Davies, M. S., Wallis, S. C., Driscoll, D. M., Wynne, J. K., Williams, G. W., Powell, L. M. & Scott, J. (1989). Sequence requirements for apolipoprotein B RNA editing in transfected rat hepatoma cells. J. Biol. Chem. 264, 13395-13398.
19. Doublié, S., Gilmore, C. J., Bricogne, G. & Carter, C. W., Jr (1995). Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase. Structure, 3, 17-31.
20. Driscoll, D. M. & Casanova, E. (1990). Characterization of the apolipoprotein B mRNA editing activity in enterocyte extracts. J. Biol. Chem. 265, 21401-21403.
21. Driscoll, D. M. & Zhang, Q. (1994). Expression and characterization of p27, the catalytic subunit of the apolipoprotein B mRNA editing enzyme. J. Biol. Chem. 269, 19843-19847.
22. Driscoll, D. M., Wynne, J. K., Wallis, S. C. & Scott, J. (1989). An in vitro system for the editing of apolipoprotein B mRNA. Cell, 58, 519-525.
23. Driscoll, D. M., Lakhe, Reddy S., Oleksa, L. M. & Martinez, D. (1993). Induction of RNA editing at heterologous sites by sequences in apolipoprotein B mRNA. Mol. Cell Biol. 13, 7288-7294.
24. Drugan, J. K., Khosravi-Far, R., White, M. A., Der, C. J., Sung, Y.-J., Hwang, Y.-W. & Campbell, S. L. (1996). Ras interaction with two distinct binding domains in Raf-1 may be required for ras transformation. J. Biol. Chem. 271, 233-237.
25. Eriani, G., Delarue, M., Poch, O., Gangloff, J. & Moras, D. (1990). Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature, 347(9), 203-206.
26. Fisher, D. & Eisenberg, D. (1996). Protein fold recognition using sequence-derived predictions. Protein Sci. 5, 947-955.
27. Gott, J. M., Visomirski, L. M. & Hunter, J. L. (1993). Substitutional and insertional RNA editing of the cytochrome c oxidase subunit 1 mRNA of physarum polycephalum. J. Biol. Chem. 268, 25483-25486.
28. Gray, M. W. (1996). RNA editing in plant organelles: a fertile field. Proc. Natl Acad. Sci. USA, 93, 8157-8159.
29. Greeve, J., Navaratnam, N. & Scott, J. (1991). Characterization of the apolipoprotein B mRNA editing enzyme: no similarity to the proposed mechanism of RNA editing in kinetoplastid protozoa. Nucl. Acids Res. 19, 3569-3576.
30. Gribskov, M., MacLachlan, A. D. & Eisenberg, D. (1987). Profile analysis: detection of distantly related proteins. Proc. Natl Acad. Sci. USA, 84, 4355-4358.
31. Gualberto, J. M., Lamattina, L., Bonnard, G., Weil, J.-H. & Grienenberger, J.-M. (1989). RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature, 341, 660-662.
32. Hadjiagapiou, C., Giannoni, F., Funahashi, T., Skarosi, S. F. & Davidson, N. O. (1994). Molecular cloning of a human small intestinal apolipoprotein B mRNA editing protein. Nucl. Acids Res. 22, 1874-1879.
33. Harris, S. G., Sabio, I., Mayer, E., Steinberg, M. F., Backus, J. W., Sparks, J. D., Sparks, C. E. & Smith, H. C. (1993). Extract-specific heterogeneity in high-order complexes containing apolipoprotein B mRNA editing activity and RNA-binding proteins. J. Biol. Chem. 268, 7382-7392.
34. Hasemann, C. A., Kurumbail, R. G., Boddupalli, S. S., Peterson, J. A. & Deisenhofer, J. (1995). Structure and function of cytochromes P450: a comparative analysis of three structures. Structure, 3, 41-62.
35. Hiesel, R., Wissinger, B., Schuster, W. & Brennicke, A. (1989). RNA editing in plant mitochondria. Science, 246, 1632-1634.
36. Higgins, D. G. & Sharp, P. M. (1988). CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene, 73(1), 237-244.
37. Hodges, P. & Scott, J. (1992). Apolipoprotein B mRNA editing: a new tier for the control of gene expression. Trends Biochem. Sci. 17, 77-81.
38. Hountondji, C., Dessen, P. & Blanquet, S. (1986). Sequence similarities among the family of aminoacyl-tRNA synthetases. Biochimie, 68, 1071-1078.
39. Hu, J. C., O'Shea, E. K., Kim, P. S. & Sauer, R. T. (1990). Sequence requirements for coiled-coils: analysis with lambda repressor-GCN4 leucine zipper fusions. Science, 250, 1400-1403.
40. Janke, A. & Paabo, S. (1993). Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucl. Acids. Res. 21, 1523-1525.
41. Kane, J. P. (1983). Apolipoprotein B: structural and metabolic heterogeneity. Annu. Rev. Physiol. 45, 637-650.
42. Kardar, M. (1996). Which came first, protein sequence or structure? Science, 273, 610.
43. Knott, T. J., Pease, R. J., Powell, L. M., Wallis, S. C., Rall, S. C. J., Innerarity, T. L., Blackhart, B., Taylor, W. H., Marcel, Y., Milne, R., Johnson, D., Fuller, M., Lusis, A. J., McCarthy, B. J., Mahley, R. W., Levy-Wilson, B. & Scott, J. (1986). Complete protein sequence and identification of structural domains of human apolipoprotein B. Nature, 323, 734-738.
44. Kuyper, L. & Carter, C. W. J. (1996). Resolving crystal polymorphisms by finding "stationary points" from quantitative analysis of crystal growth response surfaces. J. Crystal Growth, 168, 135-169.
45. Lau, P. P., Zhu, H.-J., Baldini, A., Charnsangevi, C. & Chan, L. (1994). Dimeric structure of a human apolipoprotein B mRNA editing protein and cloning and chromosomal localization of its gene. Proc. Natl Acad. Sci. USA, 91, 8522-8526.
46. MacGinnitie, A. J., Anant, S. & Davidson, N. O. (1995). Mutagenesis of apobec-1, the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme, reveals distinct domains that mediate cytosine nucleoside deaminase, RNA binding, and RNA editing activity. J. Biol. Chem. 270, 14768-14775.
47. Mahendran, R., Spottswood, M. R. & Miller, D. L. (1991). RNA editing by cytidine insertion in mitochondria of Physarum polycephalum. Nature, 349, 434-438.
48. Malek, O., Lattig, K., Hiesel, R., Brennicke, A. & Knoop, V. (1996). RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 15, 1403-1411.
49. Miklos, G. L. G. & Rubin, G. M. (1996). The role of the genome project in determining gene function: insights from model organisms. Cell, 86, 521-529.
50. Nakamuta, M., Oka, K., Krushkal, J., Kobayashi, K., Yamamoto, M., Li, W. H. & Chan, L. (1995). Alternative mRNA splicing and differential promoter utilization determine tissue-specific expression of the apolipoprotein B mRNA-editing protein (apo-bec1) gene in mice. Structure and evolution of apo-becl and related nucleoside/nucleotide deaminases. J. Biol. Chem. 270, 13042-13056.
51. Navaratnam, N., Morrison, J. R., Bhattacharya, S., Patel, D., Funahashi, T., Giannoni, F., Teng, B. B., Davidson, N. O. & Scott, J. (1993a). The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J. Biol. Chem. 268, 20709-20712.
52. Navaratnam, N., Shah, R., Patel, D., Fay, V. & Scott, J. (1993b). Apolipoprotein B mRNA editing is associated with UV crosslinking of proteins to the editing site. Proc. Natl Acad. Sci. USA, 90, 222-226.
53. Navaratnam, N., Bhattacharya, S., Fujino, T., Patel, D., Jarmuz, A. L. & Scott, J. (1995). Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell, 81, 187-195.
54. Powell, L. M., Wallis, S. C., Pease, R. J., Edwards, Y. H., Knott, T. J. & Scott, J. (1987). A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell, 50, 831-840.
55. Ravichandran, K. G., Boddupalli, S. S., Hasemann, C. A., Peterson, J. A. & Deisenhofer, J. (1993). Crystal structure of hemoprotein domain of P450BM-3 a prototype for microsomal P450's. Science, 261, 731-736.
56. Richards, F. M. (1974). The interpretation of protein structures: total volume, group volume distributions, & packing density. J. Mol. Biol. 82, 1-14.
57. Richards, F. M. (1977). Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6, 151-176.
58. Richards, F. M. (1985). Calculation of molecular volumes and areas for structures of known geometry. Methods Enzymol, 115, 445-464.
59. Richards, F. M. & Lim, W. A. (1993). An analysis of packing in the protein folding problem. Quart. Rev. Biophys. 26(4), 423-498.
60. Rost, B. & Sander, C. (1993). Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232, 584-599.
61. Russell, L., Finley, J. R. & Brent, R. (1996). Interaction trap cloning with yeast. In DNA Cloning 2 (Glover, D. M. & Hames, B. D., eds), 2nd edit, pp. 169-203, IRL Press, Oxford.
62. Schock, D., Kuo, S. R., Steinburg, M. F., Bolognino, M., Sparks, J. D., Sparks, C. E. & Smith, H. C. (1996). An auxiliary factor containing a 240-kDa protein complex is involved in apolipoprotein B RNA editing. Proc. Natl Acad. Sci. USA, 93, 1097-1102.
63. Scott, J. (1995). A place in the world for RNA editing. Cell, 81, 833-836.
64. Scott, J., Navaratnam, N., Bhattacharya, S. & Morrison, J. R. (1994). The apolipoprotein B messenger RNA editing enzyme. Curr. Opin. Lipidol. 5, 87-93.
65. Shah, R. R., Knott, T. J., Legros, J. E., Navaratnam, N., Greeve, J. C. & Scott, J. (1991). Sequence requirements for the editing of apolipoprotein B mRNA. J. Biol. Chem. 266, 16301-16304.
66. Singh, R. K., Tropsha, A. & Vaisman, I. I. (1996). Delaunay tessellation of proteins: four body nearest neighbor propensities of amino acid residues. J. Comput. Biol. 3, 213-222.
67. Smith, H. C. (1993). Apolipoprotein B mRNA editing: the sequence to the event. Semin. Cell Biol. 4, 267-278.
68. Smith, H. C. & Sowden, M. P. (1996). Base-modification mRNA editing through deamination - the good, the bad and the unregulated. Trends Genet. 12, 418-424.
69. Smith, H. C., Kuo, S. R., Backus, J. W., Harris, S. G., Sparks, C. E. & Sparks, J. D. (1991). In vitro apolipoprotein B mRNA editing: identification of a 27 S editing complex. Proc. Natl Acad. Sci. USA, 88, 1489-93.
70. Sowden, M., Hamm, J. K. & Smith, H. C. (1996). Overexpression of APOBEC-1 results in mooring sequence-dependent promiscuous RNA editing. J. Biol. Chem. 271, 3011-3017.
71. Stein, P. & Chothia, C. (1992). Serpin tertiary structure transformation. J. Mol. Biol. 221, 615-621.
72. Taubes, G. (1996). Software matchmakers help make sense of sequences. Science, 273, 588-590.
73. Teng, B., Burant, C. F. & Davidson, N. O. (1993). Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science, 260, 1816-1819.
74. Tropsha, A., Singh, R. K., Vaisman, I. I. & Zheng, W. (1996). Statistical geometry analysis of proteins: implications for inverted structure prediction. In Pacific Symposium on Biocomputing '96 (Hunter, L. & Klein, T. E., eds), pp. 614-623, World Scientific, Singapore.
75. Xiang, S., Short, S. A., Wolfenden, R. & Carter, C. W., Jr (1995). Transition state selectivity for a single hydroxyl group during catalysis by cytidine deaminase. Biochemistry, 34, 4516-4523.
76. Xiang, S., Short, S. A., Wolfenden, R. & Carter, C. W., Jr (1996). Cytidine deaminase complexed to 3-deazacytidine A "valence-buffer" in zinc enzyme catalysis. Biochemistry, 35(5), 1335-1341.
77. Xiang, S., Short, S. A., Wolfenden, R. & Carter, C. W., Jr (1997). Structure of the cytidine deaminase: product complex provides evidence for efficient proton transfer and ground-state destabilization. Biochemistry, 36, 4768-4774.
78. Yamanaka, S., Poksay, K. S., Balestra, M. E., Zeng, G. Q. & Innerarity, T. L. (1994). Cloning and mutagenesis of the rabbit ApoB mRNA editing protein. A zinc motif is essential for catalytic activity, and noncatalytic auxiliary factor(s) of the editing complex are widely distributed. J. Biol. Chem. 269, 21725-21734.
79. Yamanaka, S., Poksay, K. S., Driscoll, D. M. & Innerarity, T. L. (1996). Hyperediting of multiple cytidines of apolipoprotein B mRNA by APOBEC-1 requires auxiliary protein(s) but not a mooring sequence motif. J. Biol. Chem. 271, 11506-11510.
80. Yang, C. Y., Chen, S. H., Gianturco, S. H., Bradley, W. A., Sparrow, J. T., Tanimura, M., Li, W. H., Sparrow, D. A., DeLoof, H., Rosseneu, M. & et., al (1986). Sequence, structure, receptor-binding domains and internal repeats of human apolipoprotein B-100. Nature, 323, 738-742.