Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3′ UTRs

Nature Structural and Molecular Biology

Volumn 18, Issue 2, 2011, Pages 230-238

  Rosenberg, Brad R ^a   Hamilton, Claire E ^a   Mwangi, Michael M ^a   Dewell, Scott ^a   Papavasiliou, F Nina ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; MESSENGER RNA; TRANSCRIPTOME;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENETIC VARIABILITY; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; RNA EDITING; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTOMICS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CYTIDINE DEAMINASE; GENE EXPRESSION PROFILING; MICE; MICE, INBRED C57BL; RNA EDITING; RNA, MESSENGER;

EID: 79551638596     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1975     Document Type: Article

References (59)

1. Grosjean, H. et al. Enzymatic conversion of adenosine to inosine and to N1-methylinosine in transfer RNAs: a review. Biochimie 78, 488-501 (1996).
2. Gray, M.W. Diversity and evolution of mitochondrial RNA editing systems. IUBMB Life 55, 227-233 (2003).
3. Pullirsch, D. & Jantsch, M.F. Proteome diversifcation by adenosine to inosine RNA-editing. RNA Biol. 7, 205-212 (2010).
4. Kumar, M. & Carmichael, G.G. Nuclear antisense RNA induces extensive adenosine modifcations and nuclear retention of target transcripts. Proc. Natl. Acad. Sci. USA 94, 3542-3547 (1997).
5. Prasanth, K.V. et al. Regulating gene expression through RNA nuclear retention. Cell 123, 249-263 (2005).
6. Zhang, Z. & Carmichael, G.G. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 106, 465-475 (2001).
7. Chen, L.-L., DeCerbo, J.N. & Carmichael, G.G. Alu element-mediated gene silencing. EMBO J. 27, 1694-1705 (2008).
8. Chen, S.H. et al. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specifc in-frame stop codon. Science 238, 363-366 (1987).
9. Powell, L.M. et al. A novel form of tissue-specifc RNA processing produces apolipoprotein-B48 in intestine. Cell 50, 831-840 (1987).
10. Teng, B., Burant, C.F. & Davidson, N.O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260, 1816-1819 (1993).
11. Navaratnam, N. et al. The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J. Biol. Chem. 268, 20709-20712 (1993).
12. Conticello, S.G., Thomas, C.J.F., Petersen-Mahrt, S.K. & Neuberger, M.S. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol. 22, 367-377 (2005).
13. Navaratnam, N. et al. 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 (1995).
14. Anant, S., MacGinnitie, A.J. & Davidson, N.O. 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 (1995).
15. Mehta, A., Kinter, M.T., Sherman, N.E. & Driscoll, D.M. Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA. Mol. Cell. Biol. 20, 1846-1854 (2000).
16. Lellek, H. et al. Purifcation and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex. J. Biol. Chem. 275, 19848-19856 (2000).
17. Shah, R.R. et al. Sequence requirements for the editing of apolipoprotein B mRNA. J. Biol. Chem. 266, 16301-16304 (1991).
18. Backus, J.W. & Smith, H.C. Apolipoprotein B mRNA sequences 3′ of the editing site are necessary and suffcient for editing and editosome assembly. Nucleic Acids Res. 19, 6781-6786 (1991).
19. Hirano, K. et al. Targeted disruption of the mouse apobec-1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48. J. Biol. Chem. 271, 9887-9890 (1996).
20. Morrison, J.R. et al. Apolipoprotein B RNA editing enzyme-defcient mice are viable despite alterations in lipoprotein metabolism. Proc. Natl. Acad. Sci. USA 93, 7154-7159 (1996).
21. Yamanaka, S. et al. Apolipoprotein B mRNA-editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals. Proc. Natl. Acad. Sci. USA 92, 8483-8487 (1995).
22. Li, J.B. et al. Genome-wide identifcation of human RNA editing sites by parallel DNA capturing and sequencing. Science 324, 1210-1213 (2009).
23. Nagalakshmi, U. et al. The transcriptional landscape of the yeast genome defned by RNA sequencing. Science 320, 1344-1349 (2008).
24. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).
25. Sultan, M. et al. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321, 956-960 (2008).
26. Heap, G.A. et al. Genome-wide analysis of allelic expression imbalance in human primary cells by high-throughput transcriptome resequencing. Hum. Mol. Genet. 19, 122-134 (2010).
27. Chepelev, I., Wei, G., Tang, Q. & Zhao, K. Detection of single nucleotide variations in expressed exons of the human genome using RNA-Seq. Nucleic Acids Res. 37, e106 (2009).
28. Yamanaka, S., Poksay, K.S., Driscoll, D.M. & Innerarity, T.L. 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 (1996).
29. Sowden, M., Hamm, J.K. & Smith, H.C. Overexpression of APOBEC-1 results in mooring sequence-dependent promiscuous RNA editing. J. Biol. Chem. 271, 3011-3017 (1996).
30. Sowden, M.P., Eagleton, M.J. & Smith, H.C. Apolipoprotein B RNA sequence 3′ of the mooring sequence and cellular sources of auxiliary factors determine the location and extent of promiscuous editing. Nucleic Acids Res. 26, 1644-1652 (1998).
31. Davidson, N.O. The challenge of target sequence specifcity in C→U RNA editing. J. Clin. Invest. 109, 291-294 (2002).
32. Bass, B.L. RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71, 817-846 (2002).
33. Beale, R.C.L. et al. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J. Mol. Biol. 337, 585-596 (2004).
34. Bailey, T.L. & Elkan, C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36 (1994).
35. Backus, J.W. & Smith, H.C. Three distinct RNA sequence elements are required for effcient apolipoprotein B (apoB) RNA editing in vitro. Nucleic Acids Res. 20, 6007-6014 (1992).
36. Duret, L., Dorkeld, F. & Gautier, C. Strong conservation of non-coding sequences during vertebrates evolution: potential involvement in post-transcriptional regulation of gene expression. Nucleic Acids Res. 21, 2315-2322 (1993).
37. Siepel, A. et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050 (2005).
38. Hadjiagapiou, C., Giannoni, F., Funahashi, T., Skarosi, S.F. & Davidson, N.O. Molecular cloning of a human small intestinal apolipoprotein B mRNA editing protein. Nucleic Acids Res. 22, 1874-1879 (1994).
39. Lau, P.P., Zhu, H.J., Baldini, A., Charnsangavej, C. & Chan, L. 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 (1994).
40. Mukhopadhyay, D. et al. C→U editing of neurofbromatosis 1 mRNA occurs in tumors that express both the type II transcript and apobec-1, the catalytic subunit of the apolipoprotein B mRNA-editing enzyme. Am. J. Hum. Genet. 70, 38-50 (2002).
41. Skuse, G.R., Cappione, A.J., Sowden, M., Metheny, L.J. & Smith, H.C. The neurofbromatosis type I messenger RNA undergoes base-modifcation RNA editing. Nucleic Acids Res. 24, 478-485 (1996). (Pubitemid 26085812)
42. Lomeli, H. et al. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713 (1994).
43. Levanon, E.Y. et al. Systematic identifcation of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol. 22, 1001-1005 (2004).
44. Osenberg, S., Dominissini, D., Rechavi, G. & Eisenberg, E. Widespread cleavage of A-to-I hyperediting substrates. RNA 15, 1632-1639 (2009).
45. Borchert, G.M. et al. Adenosine deamination in human transcripts generates novel microRNA binding sites. Hum. Mol. Genet. 18, 4801-4807 (2009).
46. Liang, H. & Landweber, L.F. Hypothesis: RNA editing of microRNA target sites in humans? RNA 13, 463-467 (2007).
47. Barreau, C., Paillard, L. & Osborne, H.B. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138-7150 (2005).
48. Grimson, A. et al. MicroRNA targeting specifcity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (2007).
49. Kendrick, J.S., Chan, L. & Higgins, J.A. Superior role of apolipoprotein B48 over apolipoprotein B100 in chylomicron assembly and fat absorption: an investigation of apobec-1 knock-out and wild-type mice. Biochem. J. 356, 821-827 (2001).
50. Hirano, K., Min, J., Funahashi, T. & Davidson, N.O. Cloning and characterization of the rat apobec-1 gene: a comparative analysis of gene structure and promoter usage in rat and mouse. J. Lipid Res. 38, 1103-1119 (1997).
51. Nakamuta, M. et al. Alternative mRNA splicing and differential promoter utilization determine tissue-specifc expression of the apolipoprotein B mRNA-editing protein (Apobec1) gene in mice. Structure and evolution of Apobec1 and related nucleoside/ nucleotide deaminases. J. Biol. Chem. 270, 13042-13056 (1995).
52. Xie, Y., Nassir, F., Luo, J., Buhman, K. & Davidson, N.O. Intestinal lipoprotein assembly in apobec-1-/-mice reveals subtle alterations in triglyceride secretion coupled with a shift to larger lipoproteins. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G735-G746 (2003).
53. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-effcient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
54. Trapnell, C., Pachter, L. & Salzberg, S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
55. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
56. Li, H., Ruan, J. & Durbin, R. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18, 1851-1858 (2008).
57. Taylor, J., Schenck, I., Blankenberg, D. & Nekrutenko, A. Using galaxy to perform large-scale interactive data analyses. Curr. Protoc. Bioinformatics, 19:10.5.1-10.5.25 (2007).
58. Crooks, G.E., Hon, G., Chandonia, J.-M. & Brenner, S.E. WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (2004).
59. Marass, F. & Upton, C. Sequence Searcher: A Java tool to perform regular expression and fuzzy searches of multiple DNA and protein sequences. BMC Res Notes 2, 14 (2009).