RNA as the substrate for epigenome-environment interactions: RNA guidance of epigenetic processes and the expansion of RNA editing in animals underpins development, phenotypic plasticity, learning, and cognition

BioEssays

Volumn 32, Issue 7, 2010, Pages 548-552

  Mattick, John S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

ADARs; APOBECs; Immune system; Nervous system; RNA modification

Indexed keywords

RNA;

COGNITION; DEVELOPMENT; ENVIRONMENT; EPIGENETICS; GENE INTERACTION; HEREDITY; HUMAN; LEARNING; MEMORY; NONHUMAN; PHENOTYPIC PLASTICITY; REVIEW; RNA EDITING; RNA STRUCTURE;

ANIMALS; COGNITION; ENVIRONMENT; EPIGENESIS, GENETIC; GENOME; LEARNING; PHENOTYPE; RNA; RNA EDITING;

ANIMALIA;

EID: 77954849146     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000028     Document Type: Review

References (90)

1. Levenson JM, Sweatt JD. 2005. Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6: 108-18.
2. Ling C, Groop L. 2009. Epigenetics: A molecular link between environmental factors and type 2 diabetes. Diabetes 58: 2718-25.
3. Schanen NC. 2006. Epigenetics of autism spectrum disorders. Hum Mol Genet 15: R138-50.
4. Feinberg AP. 2007. Phenotypic plasticity and the epigenetics of human disease. Nature 447: 433-40.
5. Hewagama A, Richardson B. 2009. The genetics and epigenetics of autoimmune diseases. J Autoimmun 33: 3-11.
6. Kong A, Steinthorsdottir V, Masson G, et al. 2009. Parental origin of sequence variants associated with complex diseases. Nature 462: 868-74.
7. Cernilogar FM, Orlando V. 2005. Epigenome programming by polycomb and trithorax proteins. Biochem Cell Biol 83: 322-31.
8. Kiefer JC. 2007. Epigenetics in development. Dev Dyn 236: 1144-56.
9. Schwartz YB, Pirrotta V. 2008. Polycomb complexes and epigenetic states. Curr Opin Cell Biol 20: 266-73.
10. Fraga MF, Ballestar E, Paz MF, et al. 2005. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102: 10604-9.
11. Petronis A. 2006. Epigenetics and twins: three variations on the theme. Trends Genet 22: 347-50. (Pubitemid 44015966)
12. Haque FN, Gottesman II, Wong AHC. 2009. Not really identical: epigenetic differences in monozygotic twins and implications for twin studies in psychiatry. Am J Med Genet C Semin Med Genet 151C: 136-41.
13. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
14. Barski A, Cuddapah S, Cui K, et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-37.
15. Meissner A, Mikkelsen TS, Gu H, et al. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-70.
16. Kolasinska-Zwierz P, Down T, Latorre I, et al. 2009. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41: 376-81.
17. Laurent L, Wong E, Li G, et al. 2010. Dynamic changes in the human methylome during differentiation. Genome Res 20: 320-31.
18. Maegawa S, Hinkal G, Kim HS, et al. 2010. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res 20: 332-40.
19. Andersson R, Enroth S, Rada-Iglesias A, et al. 2009. Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome Res 19: 1732-41.
20. Nahkuri S, Taft RJ, Mattick JS. 2009. Nucleosomes are preferentially positioned at exons in somatic and sperm cells. Cell Cycle 8: 3420-4.
21. Schwartz S, Meshorer E, Ast G. 2009. Chromatin organization marks exon-intron structure. Nat Struct Mol Biol 16: 990-5.
22. Spies N, Nielsen CB, Padgett RA, et al. 2009. Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36: 245-54.
23. Tilgner H, Nikolaou C, Althammer S, et al. 2009. Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol 16: 996-1001.
24. Luco RF, Pan Q, Tominaga K, et al. 2010. Regulation of alternative splicing by histone modifications. Science 327: 996-1000.
25. Mattick JS, Amaral PP, Dinger ME, et al. 2009. RNA regulation of epigenetic processes. Bioessays 31: 51-9.
26. Amaral PP, Mattick JS. 2008. Noncoding RNA in development. Mamm Genome 19: 454-92.
27. Mattick JS. 2007. A new paradigm for developmental biology. J Exp Biol 210: 1526-47.
28. Tang G. 2005. siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30: 106-14.
29. Bachellerie JP, Cavaille J, Huttenhofer A. 2002. The expanding snoRNA world. Biochimie 84: 775-90.
30. Dinger ME, Amaral PP, Mercer TR, et al. 2008. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18: 1433-45.
31. Khalil AM, Guttman M, Huarte M, et al. 2009. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106: 11667-72.
32. Gluckman PD, Hanson MA, Beedle AS. 2007. Non-genomic transgenerational inheritance of disease risk. Bioessays 29: 145-54.
33. Chandler VL. 2007. Paramutation: from maize to mice. Cell 128: 641-5.
34. Cuzin F, Grandjean V, Rassoulzadegan M. 2008. Inherited variation at the epigenetic level: Paramutation from the plant to the mouse. Curr Opin Genet Dev 18: 193-6.
35. Costa FF. 2008. Non-coding RNAs, epigenetics and complexity. Gene 410: 9-17.
36. Suter CM, Martin DI. Paramutation: The tip of an epigenetic iceberg? Trends Genet 26: 9-14.
37. Bass BL. 2002. RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71: 817-46.
38. Valente L, Nishikura K. 2005. ADAR gene family and A-to-I RNA editing: Diverse roles in posttranscriptional gene regulation. Prog Nucleic Acid Res Mol Biol 79: 299-338. (Pubitemid 43574881)
39. Navaratnam N, Sarwar R. 2006. An overview of cytidine deaminases. Int J Hematol 83: 195-200.
40. Conticello SG. 2008. The AID/APOBEC family of nucleic acid mutators. Genome Biol 9: 229.
41. Teng B, Burant CF, Davidson NO. 1993. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260: 1816-9.
42. Muramatsu M, Sankaranand VS, Anant S, et al. 1999. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem 274: 18470-6.
43. Macbeth MR, Schubert HL, Vandemark AP, et al. 2005. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309: 1534-9.
44. Morse DP, Aruscavage PJ, Bass BL. 2002. RNA hairpins in noncoding regions of human brain and Caenorhabditis elegans mRNA are edited by adenosine deaminases that act on RNA. Proc Natl Acad Sci U S A 99: 7906-11.
45. Athanasiadis A, Rich A, Maas S. 2004. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol 2: e391.
46. Blow M, Futreal PA, Wooster R, et al. 2004. A survey of RNA editing in human brain. Genome Res 14: 2379-87.
47. Kim DD, Kim TT, Walsh T, et al. 2004. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res 14: 1719-25.
48. Levanon EY, Eisenberg E, Yelin R, et al. 2004. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 22: 1001-5.
49. Li JB, Levanon EY, Yoon JK, et al. 2009. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210-3.
50. Blow MJ, Grocock RJ, van Dongen S, et al. 2006. RNA editing of human microRNAs. Genome Biol 7: R27.
51. Nishikura K. 2006. Editor meets silencer: crosstalk between RNA editing and RNA interference. Nat Rev Mol Cell Biol 7: 919-31. (Pubitemid 44871418)
52. Kawahara Y, Megraw M, Kreider E, et al. 2008. Frequency and fate of microRNA editing in human brain. Nucleic Acids Res 36: 5270-80.
53. Huang J, Liang Z, Yang B, et al. 2007. Derepression of microRNA-mediated protein translation inhibition by apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G (APOBEC3G) and its family members. J Biol Chem 282: 33632-40.
54. Lander ES, Linton LM, Birren B, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
55. Umylny B, Presting G, Efird JT, et al. 2007. Most human Alu and murine B1 repeats are unique. J Cell Biochem 102: 110-21.
56. Mattick JS, Mehler MF. 2008. RNA editing, DNA recoding and the evolution of human cognition. Trends Neurosci 31: 227-33.
57. Labuda D, Zietkiewicz E. 1994. Evolution of secondary structure in the family of 7SL-like RNAs. J Mol Evol 39: 506-18.
58. Hasler J, Strub K. 2006. Alu elements as regulators of gene expression. Nucleic Acids Res 34: 5491-7. (Pubitemid 44742437)
59. Paz N, Levanon EY, Amariglio N, et al. 2007. Altered adenosine-to-inosine RNA editing in human cancer. Genome Res 17: 1586-95.
60. Shah SP, Morin RD, Khattra J, et al. 2009. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461: 809-13.
61. Sawyer SL, Emerman M, Malik HS. 2004. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: E275.
62. Conticello SG, Thomas CJ, Petersen-Mahrt SK, et al. 2005. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol 22: 367-77.
63. Hill MS, Mulcahy ER, Gomez ML, et al. 2006. APOBEC3G expression is restricted to neurons in the brains of pigtailed macaques. AIDS Res Hum Retroviruses 22: 541-50.
64. Bhutani N, Brady JJ, Damian M, et al. 2010. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463: 1042-7.
65. Sato Y, Probst HC, Tatsumi R, et al. 2010. Deficiency in APOBEC2 leads to a shift in muscle fiber type, diminished body mass, and myopathy. J Biol Chem 285: 7111-8.
66. Schumann GG. 2007. APOBEC3 proteins: Major players in intracellular defence against LINE-1-mediated retrotransposition. Biochem Soc Trans 35: 637-42.
67. Aguiar RS, Peterlin BM. 2008. APOBEC3 proteins and reverse transcription. Virus Res 134: 74-85.
68. Dunlap KA, Palmarini M, Varela M, et al. 2006. Endogenous retroviruses regulate peri-implantation placental growth and differentiation. Proc Natl Acad Sci U S A 103: 14390-5.
69. Faulkner GJ, Kimura Y, Daub CO, et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563-71.
70. Coufal NG, Garcia-Perez JL, Peng GE, et al. 2009. L1 retrotransposition in human neural progenitor cells. Nature 460: 1127-31.
71. Habibi L, Ebtekar M, Jameie SB. 2009. Immune and nervous systems share molecular and functional similarities: memory storage mechanism. Scand J Immunol 69: 291-301.
72. Kioussis D, Pachnis V. 2009. Immune and nervous systems: more than just a superficial similarity? Immunity 31: 705-10.
73. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10: 19-26.
74. McAfoose J, Baune BT. 2009. Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev 33: 355-66.
75. Yu D, Cook MC, Shin DM, et al. 2008. Axon growth and guidance genes identify T-dependent germinal centre B cells. Immunol Cell Biol 86: 3-14.
76. Clatworthy MR, Lyons PA, Smith KG. 2008. The nervous spleen. Immunol Cell Biol 86: 1-2.
77. Zhang H, Yang B, Pomerantz RJ, et al. 2003. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94-8.
78. Pancer Z, Cooper MD. 2006. The evolution of adaptive immunity. Annu Rev Immunol 24: 497-518.
79. Cavaille J, Buiting K, Kiefmann M, et al. 2000. Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc Natl Acad Sci U S A 97: 14311-6.
80. Rogelj B, Hartmann CE, Yeo CH, et al. 2003. Contextual fear conditioning regulates the expression of brain-specific small nucleolar RNAs in hippocampus. Eur J Neurosci 18: 3089-96.
81. Taft RJ, Glazov EA, Lassmann T, et al. 2009. Small RNAs derived from snoRNAs. RNA 15: 1233-40.
82. Ender C, Krek A, Friedlander MR, et al. 2008. A human snoRNA with microRNA-like functions. Mol Cell 32: 519-28.
83. Saraiya AA, Wang CC. 2008. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4: e1000224.
84. Politz JC, Hogan EM, Pederson T. 2009. MicroRNAs with a nucleolar location. RNA 15: 1705-15.
85. Chen PY, Weinmann L, Gaidatzis D, et al. 2008. Strand-specific 5′-O-methylation of siRNA duplexes controls guide strand selection and targeting specificity. RNA 14: 263-74.
86. Jurkowski TP, Meusburger M, Phalke S, et al. 2008. Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism. RNA 14: 1663-70.
87. Schaefer M, Hagemann S, Hanna K, et al. 2009. Azacytidine inhibits RNA methylation at DNMT2 target sites in human cancer cell lines. Cancer Res 69: 8127-32.
88. Rai K, Chidester S, Zavala CV, et al. 2007. Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebra-fish. Genes Dev 21: 261-6. (Pubitemid 46246775)
89. Phalke S, Nickel O, Walluscheck D, et al. 2009. Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2. Nat Genet 41: 696-702.
90. Squires JL, Liu AH, Nousch M, et al. 2010. Mapping 5-methylcytosine in RNA using bisuphite sequencing. 31st Lorne Genome Conference. Volume 31. Lorne, Australia; p Abstract 18.