APOBEC3A is implicated in a novel class of G-to-A mRNA editing in WT1 transcripts

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Niavarani, Ahmadreza ^a,b   Currie, Erin ^a   Reyal, Yasmin ^c   Anjos Afonso, Fernando ^a   Horswell, Stuart ^a   Griessinger, Emmanuel ^d   Sardina, Jose Luis ^e   Bonnet, Dominique ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^d CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^e UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3A; COMPLEMENTARY DNA; GLYCINE; HYDROLASE; MESSENGER RNA; UNCLASSIFIED DRUG; ADENOSINE; APOBEC3A PROTEIN, HUMAN; CYTIDINE DEAMINASE; GUANINE; PROTEIN; SMALL INTERFERING RNA; WT1 PROTEIN; WT1 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; GENE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOLECULAR CLONING; MONONUCLEAR CELL; PROTEIN FUNCTION; RNA EDITING; RNA INTERFERENCE; UMBILICAL CORD BLOOD; WT1 GENE; ACUTE MYELOID LEUKEMIA; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CYTOLOGY; DNA SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NEPHROBLASTOMA; NUCLEOTIDE SEQUENCE; PATHOLOGY; UMBILICAL CORD;

ADENOSINE; BASE SEQUENCE; CYTIDINE DEAMINASE; GUANINE; HUMANS; LEUKEMIA, MYELOID, ACUTE; LEUKOCYTES, MONONUCLEAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEINS; RNA EDITING; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; UMBILICAL CORD; WILMS TUMOR; WT1 PROTEINS;

EID: 84926289051     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120089     Document Type: Article

References (48)

1. Powell LM, Wallis SC, Pease RJ, Edwards YH, Knott TJ, Scott J. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell. 1987; 50(6):831-40. PMID: 3621347
2. Bass BL, Weintraub H. An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell. 1988; 55(6):1089-98. PMID: 3203381
3. Nakamuta M, Chang BH, Zsigmond E, Kobayashi K, Lei H, Ishida BY, et al. Complete phenotypic characterization of apobec-1 knockout mice with a wild-type genetic background and a human apolipoprotein B transgenic background, and restoration of apolipoprotein B mRNA editing by somatic gene transfer of Apobec-1. J Biol Chem. 1996; 271(42):25981-8. PMID: 8824235
4. Hartner JC, Walkley CR, Lu J, Orkin SH. ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling. Nat Immunol. 2009; 10(1):109-15. doi: 10.1038/ni.1680 PMID: 19060901
5. Hartner JC, Schmittwolf C, Kispert A, Muller AM, Higuchi M, Seeburg PH. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J Biol Chem. 2004; 279(6):4894-902. PMID: 14615479
6. Sharma PM, Bowman M, Madden SL, Rauscher FJ 3rd, Sukumar S. RNA editing in the Wilms' tumor susceptibility gene, WT1. Genes Dev. 1994; 8(6):720-31. PMID: 7926762
7. Grohmann M, Hammer P, Walther M, Paulmann N, Buttner A, Eisenmenger W, et al. Alternative splicing and extensive RNA editing of human TPH2 transcripts. PLoS One. 2010; 5(1):e8956. doi: 10.1371/journal.pone.0008956 PMID: 20126463
8. Klimek-Tomczak K, Mikula M, Dzwonek A, Paziewska A, Karczmarski J, Hennig E, et al. Editing of hnRNP K protein mRNA in colorectal adenocarcinoma and surrounding mucosa. Br J Cancer. 2006; 94(4):586-92. PMID: 16404425
9. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R, et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol. 2004; 22(8):1001-5. PMID: 15258596
10. Li M, Wang IX, Li Y, Bruzel A, Richards AL, Toung JM, et al. Widespread RNA and DNA Sequence Differences in the Human Transcriptome. Science. 2011; 333(6038):53-8. doi: 10.1126/science.1207018 PMID: 21596952
11. Ariyaratana S, Loeb DM. The role of the Wilms tumour gene (WT1) in normal and malignant haematopoiesis. Expert Rev Mol Med. 2007; 9(14):1-17. PMID: 17524167
12. Pelletier J, Bruening W, Kashtan CE, Mauer SM, Manivel JC, Striegel JE, et al. Germline mutations in the Wilms' tumor suppressor gene are associated with abnormal urogenital development in Denys-Drash syndrome. Cell. 1991; 67(2):437-47. PMID: 1655284
13. Virappane P, Gale R, Hills R, Kakkas I, Summers K, Stevens J, et al. Mutation of the Wilms' tumor 1 gene is a poor prognostic factor associated with chemotherapy resistance in normal karyotype acute myeloid leukemia: the United Kingdom Medical Research Council Adult Leukaemia Working Party. J Clin Oncol. 2008; 26(33):5429-35. doi: 10.1200/JCO.2008.16.0333 PMID: 18591546
14. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). International journal of cancer Journal international du cancer. 1980; 26(2):171-6. PMID: 6970727
15. Hirose M, Minato K, Tobinai K, Shimoyama M, Watanabe S, Abe T. A novel monocytoid cultured cell line, P31/Fujioka, derived from acute monoblastic leukemia. Gan. 1982; 73(5):735-41. PMID: 6962783
16. Gallagher R, Collins S, Trujillo J, McCredie K, Ahearn M, Tsai S, et al. Characterization of the continuous, differentiating myeloid cell line (HL-60) from a patient with acute promyelocytic leukemia. Blood. 1979; 54(3):713-33. PMID: 288488
17. Koeffler HP, Golde DW. Acute myelogenous leukemia: a human cell line responsive to colonystimulating activity. Science. 1978; 200(4346):1153-4. PMID: 306682
18. Drummond IA, Rupprecht HD, Rohwer-Nutter P, Lopez-Guisa JM, Madden SL, Rauscher FJ 3rd, et al. DNA recognition by splicing variants of the Wilms' tumor suppressor, WT1. Mol Cell Biol. 1994; 14(6):3800-9. PMID: 8196623
19. Zhu Y, Luo H, Zhang X, Song J, Sun C, Ji A, et al. Abundant and selective RNA-editing events in the medicinal mushroom Ganoderma lucidum. Genetics. 2014; 196(4):1047-57. doi: 10.1534/genetics.114.161414 PMID: 24496007
20. Castandet B, Araya A. RNA editing in plant organelles. Why make it easy? Biochemistry Biokhimiia. 2011; 76(8):924-31. doi: 10.1134/S0006297911080086 PMID: 22022966
21. Schrider DR, Gout JF, Hahn MW. Very few RNA and DNA sequence differences in the human transcriptome. PLoS One. 2011; 6(10):e25842. doi: 10.1371/journal.pone.0025842 PMID: 22022455
22. Lin W, Piskol R, Tan MH, Li JB. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome". Science. 2012; 335(6074):1302; author reply doi: 10.1126/science.1210624 PMID: 22422964
23. Kleinman CL, Majewski J. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome". Science. 2012; 335(6074):1302; author reply doi: 10.1126/science.1210624 PMID: 22422964
24. Ho PA, Kuhn J, Gerbing RB, Pollard JA, Zeng R, Miller KL, et al. WT1 synonymous single nucleotide polymorphism rs16754 correlates with higher mRNA expression and predicts significantly improved outcome in favorable-risk pediatric acute myeloid leukemia: a report from the children's oncology group. J Clin Oncol. 2011; 29(6):704-11. doi: 10.1200/JCO.2010.31.9327 PMID: 21189390
25. Harris RS, Petersen-Mahrt SK, Neuberger MS. RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell. 2002; 10(5):1247-53. PMID: 12453430
26. Conticello SG. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 2008; 9(6):229.1-10. doi: 10.1186/gb-2008-9-6-229 PMID: 18598372
27. Byeon IJ, Ahn J, Mitra M, Byeon CH, Hercik K, Hritz J, et al. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat Commun. 2013; 4:1890. doi: 10.1038/ncomms2883 PMID: 23695684
28. Melcher T, Maas S, Herb A, Sprengel R, Seeburg PH, Higuchi M. A mammalian RNA editing enzyme. Nature. 1996; 379(6564):460-4. PMID: 8559253
29. Mehta A, Kinter MT, Sherman NE, Driscoll DM. Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA. Mol Cell Biol. 2000; 20(5):1846-54. PMID: 10669759
30. Storck S, Aoufouchi S, Weill JC, Reynaud CA. AID and partners: for better and (not) for worse. Curr Opin Immunol. 2011; 23(3):337-44. doi: 10.1016/j.coi.2011.02.002 PMID: 21439803
31. Cheong C, Tinoco I Jr., Chollet A. Thermodynamic studies of base pairing involving 2,6-diaminopurine. Nucleic Acids Res. 1988; 16(11):5115-22. PMID: 3387218
32. Suspène R AM, Guétard D, Henry M, Eckhoff G, Marchio A, Pineau P, Dejean A, Vartanian JP, Wain-Hobson S. Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc Natl Acad Sci U S A. 2011; 108(12):4858-63. doi: 10.1073/pnas.1009687108 PMID: 21368204
33. Wijesinghe P, Bhagwat AS. Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G. Nucleic Acids Res. 2012; 40(18):9206-17. doi: 10.1093/nar/gks685 PMID: 22798497
34. Garcia GA, Kittendorf JD. Transglycosylation: a mechanism for RNA modification (and editing?). Bioorganic chemistry. 2005; 33(3):229-51. PMID: 15888313
35. Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol. 2010; 17(2):222-9. doi: 10.1038/nsmb.1744 PMID: 20062055
36. Refsland EW, Stenglein MD, Shindo K, Albin JS, Brown WL, Harris RS. Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res. 2010; 38(13):4274-84. doi: 10.1093/nar/gkq174 PMID: 20308164
37. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, et al. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics. 2002; 79(3):285-96. PMID: 11863358
38. Harris RS, Liddament MT. Retroviral restriction by APOBEC proteins. Nat Rev Immunol. 2004; 4(11):868-77. PMID: 15516966
39. Chiu YL, Greene WC. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol. 2008; 26:317-53. doi: 10.1146/annurev.immunol.26.021607.090350 PMID: 18304004
40. Bogerd HP,Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS,Moran JV, et al. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A. 2006; 103(23):8780-5. PMID: 16728505
41. Peng G, Greenwell-Wild T, Nares S, Jin W, Lei KJ, Rangel ZG, et al. Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood. 2007; 110(1):393-400. PMID: 17371941
42. Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res. 2006; 34(1):89-95. PMID: 16407327
43. Wijesinghe P, Bhagwat AS. Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G. Nucleic Acids Res. 2012.
44. Carpenter MA, Li M, Rathore A, Lackey L, Law EK, Land AM, et al. Methylcytosine and Normal Cytosine Deamination by the Foreign DNA Restriction Enzyme APOBEC3A. J Biol Chem. 2012; 287(41):34801-8. doi: 10.1074/jbc.M112.385161 PMID: 22896697
45. Landry S, Narvaiza I, Linfesty DC, Weitzman MD. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO reports. 2011; 12(5):444-50. doi: 10.1038/embor.2011.46 PMID: 21460793
46. Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P, et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet. 2013; 45(9):970-6. doi: 10.1038/ng.2702 PMID: 23852170
47. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature. 2013; 500(7463):415-21. doi: 10.1038/nature12477 PMID: 23945592
48. Taylor BJ, Nik-Zainal S, Wu YL, Stebbings LA, Raine K, Campbell PJ, et al. DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. Elife. 2013; 2:e00534. doi: 10.7554/eLife.00534 PMID: 23599896