APOBEC3A cytidine deaminase induces RNA editing in monocytes and macrophages

Nature Communications

Volumn 6, Issue , 2015, Pages

  Sharma, Shraddha ^a   Patnaik, Santosh K ^a   Thomas Taggart, R ^a   Kannisto, Eric D ^a   Enriquez, Sally M ^b   Gollnick, Paul ^b   Baysal, Bora E ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3A; CYTIDINE DEAMINASE; INTERFERON; RNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; ALPHA INTERFERON; APOBEC3A PROTEIN, HUMAN; OXYGEN; PROTEIN; SMALL INTERFERING RNA;

AMINO ACID; GENE EXPRESSION; MAMMAL; POLARIZATION; RNA; VIRAL DISEASE;

AMINO ACID SEQUENCE; ARTICLE; DEAMINATION; EMBRYO; HUMAN; HUMAN CELL; HYPOXIA; MACROPHAGE; MONOCYTE; POLARIZATION; RETROPOSON; RNA EDITING; VIRUS INFECTION; VIRUS PATHOGENESIS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

MAMMALIA;

CYTIDINE DEAMINASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; INTERFERON-ALPHA; MACROPHAGES; MONOCYTES; OXYGEN; PROTEINS; RNA; RNA EDITING; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84928378277     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7881     Document Type: Article

References (61)

1. Tang, W., Fei, Y. & Page, M. Biological significance of RNA editing in cells. Mol. Biotechnol. 52, 91-100 (2012).
2. Ramaswami, G. et al. Accurate identification of human Alu and non-Alu RNA editing sites. Nat. Methods 9, 579-581 (2012).
3. Peng, Z. et al. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat. Biotechnol. 30, 253-260 (2012).
4. Li, J. B. et al. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324, 1210-1213 (2009).
5. Slotkin, W. & Nishikura, K. Adenosine-to-inosine RNA editing and human disease. Genome Med. 5, 105 (2013).
6. Bransteitter, R., Prochnow, C. & Chen, X. S. The current structural and functional understanding of APOBEC deaminases. Cell. Mol. Life Sci. 66, 3137-3147 (2009).
7. Fritz, E. L. et al. A comprehensive analysis of the effects of the deaminase AID on the transcriptome and methylome of activated B cells. Nat. Immunol. 14, 749-755 (2013).
8. Prohaska, K. M., Bennett, R. P., Salter, J. D. & Smith, H. C. The multifaceted roles of RNA binding in APOBEC cytidine deaminase functions. Wiley Interdiscip. Rev. RNA 5, 493-508 (2014).
9. Teng, B., Burant, C. F. & Davidson, N. O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260, 1816-1819 (1993).
10. Takenaka, M., Zehrmann, A., Verbitskiy, D., Hartel, B. & Brennicke, A. RNA editing in plants and its evolution. Annu. Rev. Genet. 47, 335-352 (2013).
11. Baysal, B. E. A recurrent stop-codon mutation in succinate dehydrogenase subunit B gene in normal peripheral blood and childhood T-cell acute leukemia. PLoS One 2, e436 (2007).
12. Baysal, B. E. et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848-851 (2000).
13. Guzy, R. D., Sharma, B., Bell, E., Chandel, N. S. & Schumacker, P. T. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen speciesdependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell. Biol. 28, 718-731 (2008).
14. Dahia, P. L. Pheochromocytoma and paraganglioma pathogenesis: learning from genetic heterogeneity. Nat. Rev. Cancer 14, 108-119 (2014).
15. Hoekstra, A. S. & Bayley, J. P. The role of complex II in disease. Biochim. Biophys. Acta 1827, 543-551 (2013).
16. Baysal, B. E. et al. Hypoxia-inducible C-to-U coding RNA editing downregulates SDHB in monocytes. PeerJ 1, e152 (2013).
17. Peng, G., Lei, K. J., Jin, W., Greenwell-Wild, T. & Wahl, S. M. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferoninduced anti-HIV-1 activity. J. Exp. Med. 203, 41-46 (2006).
18. Beyer, M. et al. High-resolution transcriptome of human macrophages. PLoS One 7, e45466 (2012).
19. Pham, T. V. & Jimenez, C. R. An accurate paired sample test for count data. Bioinformatics 28, i596-i602 (2012).
20. Lorenz, R. et al. ViennaRNA Package 2.0. Algorithms Mol. Biol. 6, 26 (2011).
21. Koning, F. A. et al. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J. Virol. 83, 9474-9485 (2009).
22. Hudson, T. J. et al. International network of cancer genome projects. Nature 464, 993-998 (2010).
23. Blanc, V. & Davidson, N. O. C-to-U RNA editing: mechanisms leading to genetic diversity. J. Biol. Chem. 278, 1395-1398 (2003).
24. Holtz, C. M., Sadler, H. A. & Mansky, L. M. APOBEC3G cytosine deamination hotspots are defined by both sequence context and single-stranded DNA secondary structure. Nucleic Acids Res. 41, 6139-6148 (2013).
25. Chen, H. et al. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16, 480-485 (2006).
26. Mitra, M. et al. Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res. 42, 1095-1110 (2014).
27. Byeon, I. J. et al. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun. 4, 1890 (2013).
28. Ooms, M., Krikoni, A., Kress, A. K., Simon, V. & Munk, C. APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J. Virol. 86, 6097-6108 (2012).
29. Arias, J. F., Koyama, T., Kinomoto, M. & Tokunaga, K. Retroelements versus APOBEC3 family members: no great escape from the magnificent seven. Front. Microbiol. 3, 275 (2012).
30. Wiegand, H. L. & Cullen, B. R. Inhibition of alpharetrovirus replication by a range of human APOBEC3 proteins. J. Virol. 81, 13694-13699 (2007).
31. Berger, G. et al. APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog. 7, e1002221 (2011).
32. Muckenfuss, H. et al. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281, 22161-22172 (2006).
33. Bogerd, H. P. et al. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc. Natl Acad. Sci. USA 103, 8780-8785 (2006).
34. Narvaiza, I. et al. Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog. 5, e1000439 (2009).
35. Kinomoto, M. et al. All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res. 35, 2955-2964 (2007).
36. Bogerd, H. P., Wiegand, H. L., Doehle, B. P., Lueders, K. K. & Cullen, B. R. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res. 34, 89-95 (2006).
37. Stavrou, S. et al. Different modes of retrovirus restriction by human APOBEC3A and APOBEC3G in vivo. PLoS Pathog. 10, e1004145 (2014).
38. Wang, Y. et al. Ankrd17 positively regulates RIG-I-like receptor (RLR)- mediated immune signaling. Eur. J. Immunol. 42, 1304-1315 (2012).
39. Buchberg, A. M., Bedigian, H. G., Jenkins, N. A. & Copeland, N. G. Evi-2, a common integration site involved in murine myeloid leukemogenesis. Mol. Cell. Biol. 10, 4658-4666 (1990).
40. Pos, W., Sethi, D. K. & Wucherpfennig, K. W. Mechanisms of peptide repertoire selection by HLA-DM. Trends Immunol. 34, 495-501 (2013).
41. Winograd-Katz, S. E., Fassler, R., Geiger, B. & Legate, K. R. The integrin adhesome: from genes and proteins to human disease. Nat. Rev. Mol. Cell. Biol. 15, 273-288 (2014).
42. Burr, M. L. et al. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc. Natl Acad. Sci. USA 108, 2034-2039 (2011).
43. Du, N. et al. Cell surface vimentin is an attachment receptor for enterovirus 71.
44. Engelman, A. & Cherepanov, P. The structural biology of HIV-1: mechanistic and therapeutic insights. Nat. Rev. Microbiol. 10, 279-290 (2012).
45. Garrison, A. R. et al. Crimean-Congo hemorrhagic fever virus utilizes a clathrin- and early endosome-dependent entry pathway. Virology 444, 45-54 (2013).
46. Sorin, M. et al. Recruitment of a SAP18-HDAC1 complex into HIV-1 virions and its requirement for viral replication. PLoS Pathog. 5, e1000463 (2009).
47. Stenglein, M. D., Burns, M. B., Li, M., Lengyel, J. & Harris, R. S. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat. Struct. Mol. Biol. 17, 222-229 (2010).
48. Strehl, C. et al. Hypoxia: how does the monocyte-macrophage system respond to changes in oxygen availability? J. Leukoc. Biol. 95, 233-241 (2014).
49. Wynn, T. A., Chawla, A. & Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 496, 445-455 (2013).
50. Tian, Y., Chang, J. C., Fan, E. Y., Flajolet, M. & Greengard, P. Adaptor complex AP2/PICALM, through interaction with LC3, targets Alzheimer's APP-CTF for terminal degradation via autophagy. Proc. Natl Acad. Sci. USA 110, 17071-17076 (2013).
51. Liang, B., Duan, B. Y., Zhou, X. P., Gong, J. X. & Luo, Z. G. Calpain activation promotes BACE1 expression, amyloid precursor protein processing, and amyloid plaque formation in a transgenic mouse model of Alzheimer disease. J. Biol. Chem. 285, 27737-27744 (2010).
52. Brodeur, J. et al. LDLR-related protein 10 (LRP10) regulates amyloid precursor protein (APP) trafficking and processing: evidence for a role in Alzheimer's disease. Mol. Neurodegener. 7, 31 (2012).
53. Treusch, S. et al. Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 334, 1241-1245 (2011).
54. Goate, A. et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706 (1991).
55. Bradshaw, E. M. et al. CD33 Alzheimer's disease locus: altered monocyte function and amyloid biology. Nat. Neurosci. 16, 848-850 (2013).
56. Mentzer, S. J., Guyre, P. M., Burakoff, S. J. & Faller, D. V. Spontaneous aggregation as a mechanism for human monocyte purification. Cell. Immunol. 101, 312-319 (1986).
57. Seager Danciger, J. et al. Method for large scale isolation, culture and cryopreservation of human monocytes suitable for chemotaxis, cellular adhesion assays, macrophage and dendritic cell differentiation. J. Immunol. Methods 288, 123-134 (2004).
58. Liao, Y., Smyth, G. K. & Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41, e108 (2013).
59. Wang, L., Wang, S. & Li, W. RSeQC: quality control of RNA-seq experiments. Bioinformatics 28, 2184-2185 (2012).
60. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
61. Kreuzer, K. A. et al. Highly sensitive and specific fluorescence reverse transcription-PCR assay for the pseudogene-free detection of beta-actin transcripts as quantitative reference. Clin. Chem. 45, 297-300 (1999).