Genetic architectures of quantitative variation in RNA editing pathways

Genetics

Volumn 202, Issue 2, 2016, Pages 787-798

  Gu, Tongjun ^a   Gatti, Daniel M ^a   Srivastava, Anuj ^a   Snyder, Elizabeth M ^a   Raghupathy, Narayanan ^a   Simecek, Petr ^a   Svenson, Karen L ^a   Dotu, Ivan ^a,b   Chuang, Jeffrey H ^a   Keller, Mark P ^c   Attie, Alan D ^c   Braun, Robert E ^a   Churchill, Gary A ^a  

^a JACKSON LABORATORY   (United States)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apobec1; Diversity Outbred; Genetics; MPP; Multiparent advanced generation inter cross (MAGIC); Multiparental populations; RNA editing; Secondary structure

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; ARGININE; DECORIN; GABA TRANSPORTER 2; GLUTAMINE; GM10319 PROTEIN; M6PR PROTEIN; MUG1 PROTEIN; MUG2 PROTEIN; NECAP1 PROTEIN; PEX26 PROTEIN; PHC1 PROTEIN; PROTEIN; RNA; SLC6A12 PROTEIN; SPACER DNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; CYTIDINE DEAMINASE;

3' UNTRANSLATED REGION; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; CHROMOSOME 1; CHROMOSOME 6; DNA POLYMORPHISM; ENZYME ACTIVE SITE; FEMALE; FOUNDER EFFECT; GENE LOCUS; GENE MAPPING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC REGULATION; GENETIC VARIABILITY; GENETIC VARIATION; HAPLOTYPE; HEREDITY; INDEL MUTATION; INTRON; LOD SCORE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT; READING FRAME; RNA EDITING; RNA SEQUENCE; RNA STRUCTURE; STOP CODON; ANIMAL; CHEMISTRY; CHROMOSOMAL MAPPING; GENE EXPRESSION PROFILING; GENETICS; GENOME; MULTIFACTORIAL INHERITANCE; QUANTITATIVE TRAIT LOCUS;

ANIMALS; APOBEC-1 DEAMINASE; CHROMOSOME MAPPING; CYTIDINE DEAMINASE; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOME; MALE; MICE; MULTIFACTORIAL INHERITANCE; QUANTITATIVE TRAIT LOCI; RNA EDITING;

EID: 84979884843     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.179481     Document Type: Article

References (45)

1. Bailey, T. L., and C. Elkan, 1994 Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2: 28–36.
2. Bass, B. L., 2002 RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71: 817–846.
3. Bass, B., H. Hundley, J. B. Li, Z. Peng, J. Pickrell et al., 2012 The difficult calls in RNA editing. Nat. Biotechnol. 30: 1207–1209.
4. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289–300.
5. Bhogal, B., J. E. Jepson, Y. A. Savva, A. S. Pepper, R. A. Reenan et al., 2011 Modulation of dADAR-dependent RNA editing by the Drosophila fragile X mental retardation protein. Nat. Neurosci. 14: 1517–1524.
6. Chen, S. H., G. Habib, C. Y. Yang, Z. W. Gu, B. R. Lee et al., 1987 Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 238: 363–366.
7. Churchill, G. A., and R. W. Doerge, 1994 Empirical threshold values for quantitative trait mapping. Genetics 138: 963–971.
8. Churchill, G. A., and R. W. Doerge, 2008 Naive application of permutation testing leads to inflated type I error rates. Genetics 178: 609–610.
9. Daneck, P., C. Nellåker, E. R., J. E. McIntyre, S. Buendia-Buendia, Bumpstead et al., 2012 High levels of RNA-editing site conservation amongst 15 laboratory mouse strains. Genome Biol. 13: r26.
10. Daniel, C., M. T. Veno, Y. Ekdahl, J. Kjems, and M. Ohman, 2012 A distant cis-acting intronic element induces site-selective RNA editing. Nucleic Acids Res. 40: 9876–9886.
11. Davidson, N. O., and G. S. Shelness, 2000 APOLIPOPROTEIN B: mRNA editing, lipoprotein assembly, and presecretory degradation. Annu. Rev. Nutr. 20: 169–193.
12. Dawson, T. R., C. L. Sansam, and R. B. Emeson, 2004 Structure and sequence determinants required for the RNA editing of ADAR2 substrates. J. Biol. Chem. 279: 4941–4951.
13. Flicek, P., M. R. Amode, D. Barrell, K. Beal, S. Brent et al., 2012 Ensembl 2012. Nucleic Acids Res. 40: D84–D90.
14. Fossat, N., K. Tourle, T. Radziewic, D. Liebhold, J.B. Studdert et al., 2014 C to U RNA editing mediated by APOBEC1 requires RNA-binding protein RBM47. EMBO Rep. 15: 903–910.
15. Gatti, D. M., K. L. Svenson, A. Shabalin, L. Y. Wu, W. Valdar et al., 2014 Quantitative trait locus mapping methods for diversity outbred mice. G3 4: 1623–1633.
16. Greenberger, S., E. Y. Levanon, N. Paz-Yaacov, A. Barzilai, M. Safran et al., 2010 Consistent levels of A-to-I RNA editing across individuals in coding sequences and non-conserved Alu repeats. BMC Genomics 11: 608.
17. Gu, T., F. W. Buaas, A. K. Simons, C. L. Ackert-Bicknell, R. E. Braun et al., 2012 Canonical A-to-I and C-to-U RNA editing is enriched at 3,UTRs and microRNA target sites in multiple mouse tissues. PLoS One 7: e33720.
18. Gurevich, I., H. Tamir, V. Arango, A. J. Dwork, J. J. Mann et al., 2002 Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims. Neuron 34: 349–356.
19. Hassan, M. A., V. Butty, K. D. Jensen, and J. P. Saeij, 2014 The genetic basis for individual differences in mRNA splicing and APOBEC1 editing activity in murine macrophages. Genome Res. 24: 377–389.
20. Herbert, A., and A. Rich, 2001 The role of binding domains for dsRNA and Z-DNA in the in vivo editing of minimal substrates by ADAR1. Proc. Natl. Acad. Sci. USA 98: 12132–12137.
21. Hirano, K., S. G. Young, R. V. Farese, Jr., J. Ng, E. Sande et al., 1996 Targeted disruption of the mouse apobec-1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48. J. Biol. Chem. 271: 9887–9890.
22. Hofacker, I. L., B. Priwitzer, and P. F. Stadler, 2004 Prediction of locally stable RNA secondary structures for genome-wide surveys. Bioinformatics 20: 186–190.
23. Huang, S., J. Holt, C. Kao, L. McMillan, and W. Wang, 2014 A novel multi-alignment pipeline for high-throughput sequencing data. Database (Oxford), bau057: 1–12.
24. Keane, T. M., L. Goodstadt, P. Danecek, M. A. White, K. Wong et al., 2011 Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289–294.
25. Kiran, A. M., J. J. O’Mahony, K. Sanjeev, and P. V. Baranov, 2013 Darned in 2013: inclusion of model organisms and linking with Wikipedia. Nucleic Acids Res. 41: D258–D261.
26. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
27. Lehmann, K. A., and B. L. Bass, 1999 The importance of internal loops within RNA substrates of ADAR1. J. Mol. Biol. 291: 1–13.
28. Li, B., and C. N. Dewey, 2011 RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12: 323.
29. Li, J.B., E.Y. Levanon, J. K. Yoon, J. Aach, B. Xieet al., 2009 Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210–1213.
30. Lorenz, R., S.H. Bernhart, C. Honer Zu Siederdissen, H. Tafer, C. Flamm et al., 2011 ViennaRNA Package 2.0. Algorithms Mol. Biol. 6: 26.
31. Munger, S. C., N. Raghupathy, K. Choi, A. K. Simons, D. M. Gatti et al., 2014 RNA-seq alignment to individualized genomes improves transcript abundance estimates in multiparent populations. Genetics 198: 59–73.
32. Nakamuta, M., K. Oka, J. Krushkal, K. Kobayashi, M. Yamamoto et al., 1995 Alternative mRNA splicing and differential promoter utilization determine tissue-specific expression of the apolipoprotein B mRNA-editing protein (Apobec1) gene in mice: structure and evolution of Apobec1 and related nucleo-side/nucleotide deaminases. J. Biol. Chem. 270: 13042–13056.
33. Ota, H., M. Sakurai, R. Gupta, L. Valente, B. E. Wulff et al., 2013 ADAR1 forms a complex with Dicer to promote micro-RNA processing and RNA-induced gene silencing. Cell 153: 575–589.
34. Paz, N., E. Y. Levanon, N. Amariglio, A. B. Heimberger, Z. Ram et al., 2007 Altered adenosine-to-inosine RNA editing in human cancer. Genome Res. 17: 1586–1595.
35. Petersen-Mahrt, S. K., and M. S. Neuberger, 2003 In vitro deamination of cytosine to uracil in single-stranded DNA by apolipoprotein B editing complex catalytic subunit 1 (APOBEC1). J. Biol. Chem. 278: 19583–19586.
36. Pickrell, J. K., Y. Gilad, and J. K. Pritchard, 2012 Comment on “Widespread RNA and DNA sequence differences in the human transcriptome.” Science 335: 1302 (author reply: 1302).
37. Ramaswami, G., and J. B. Li, 2014 RADAR: a rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res. 42: D109–D113.
38. Rieder, L. E., and R. A. Reenan, 2012 The intricate relationship between RNA structure, editing, and splicing. Semin. Cell Dev. Biol. 23: 281–288.
39. Rosenberg, B. R., C. E. Hamilton, M. M. Mwangi, S. Dewell, and F. N. Papavasiliou, 2011 Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3, UTRs. Nat. Struct. Mol. Biol. 18: 230–236.
40. Sapiro, A. L., P. Deng, R. Zhang, and J. B. Li, 2015 Cis regulatory effects on A-to-I RNA editing in related Drosophila species. Cell Reports 11: 697–703.
41. Smith, H. C., R. P. Bennett, A. Kizilyer, W. M. McDougall, and K. M. Prohaska, 2012 Functions and regulation of the APOBEC family of proteins. Semin. Cell Dev. Biol. 23: 258–268.
42. Svenson, K. L., D. M. Gatti, W. Valdar, C. E. Welsh, R. Cheng et al., 2012 High-resolution genetic mapping using the Mouse Diversity outbred population. Genetics 190: 437–447.
43. Waterston, R. H., K. Lindblad-Toh, E. Birney, J. Rogers, J. F. Abril et al., 2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562.
44. Yalcin, B., K. Wong, A. Agam, M. Goodson, T. M. Keane et al., 2011 Sequence-based characterization of structural variation in the mouse genome. Nature 477: 326–329.
45. Yalcin, B., D. J. Adams, J. Flint, and T. M. Keane, 2012 Next-generation sequencing of experimental mouse strains. Mamm. Genome 23: 490–498.