Functions and regulation of the APOBEC family of proteins

Seminars in Cell and Developmental Biology

Volumn 23, Issue 3, 2012, Pages 258-268

  Smith, Harold C ^a,c,d   Bennett, Ryan P ^a   Kizilyer, Ayse ^b   McDougall, William M ^a   Prohaska, Kimberly M ^a,d  

^a Department of Biochemistry and Biophysics ^*  (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c Cancer Center   (United States)

^d OyaGen Inc   (United States)

Author keywords

APOBEC; DNA deaminase; Mutation; Regulation; RNA editing

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; HYDROLASE; UNCLASSIFIED DRUG;

GENOTOXICITY; HUMAN; NONHUMAN; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REVIEW;

EID: 84860381586     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.10.004     Document Type: Review

References (150)

1. Smith H.C. The APOBEC1 paradigm for mammalian cytidine deaminases that edit DNA and RNA. Austin 2009, 181-202. Landes BioScience, Chapter 15. H. Grosjean (Ed.).
2. Smith H.C., Gott J.M., Hanson M.R. A guide to RNA editing. RNA 1997, 3:1105-1123.
3. Powell L.M., Wallis S.C., Pease R.J., Edwards Y.H., Knott T.J., Scott J. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell 1987, 50:831-840.
4. Chen S.H., Habib G., Yang C.Y., Gu Z.W., Lee B.R., Weng S.A., et al. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 1987, 238:363-366.
5. Teng B., Burant C.F., Davidson N.O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 1993, 260:1816-1819.
6. 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 1995, 270:14762-14767.
7. Navaratnam N., Fujino T., Bayliss J., Jarmuz A., How A., Richardson N., et al. Escherichia coli cytidine deaminase provides a molecular model for ApoB RNA editing and a mechanism for RNA substrate recognition. J Mol Biol 1998, 275:695-714.
8. Navaratnam N., Bhattacharya S., Fujino T., Patel D., Jarmuz A.L., Scott J. Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell 1995, 81:187-195.
9. 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 2000, 20:1846-1854.
10. Mehta A., Driscoll D.M. Identification of domains in APOBEC-1 complementation factor required for RNA binding and apolipoprotein B mRNA editing. RNA 2002, 8:69-82.
11. Blanc V., Henderson J.O., Kennedy S., Davidson N.O. Mutagenesis of apobec-1 complementation factor reveals distinct domains that modulate RNA binding, protein-protein interaction with apobec-1, and complementation of C to U RNA-editing activity. J Biol Chem 2001, 276:46386-46393.
12. Lau P.P., Zhu H.-J., Baldini H.A., Charnsangavej C., Chan L. Dimeric structure of a human apo B mRNA editing protein and cloning and chromosomal localization of its gene. Proc Natl Acad Sci USA 1994, 91:8522-8526.
13. Galloway C.A., Kumar A., Krucinska J., Smith H.C. APOBEC-1 complementation factor (ACF) forms RNA-dependent multimers. Biochem Biophys Res Commun 2010, 398:38-43.
14. Sowden M.P., Ballatori N., de Mesy Jensen K.L., Hamilton Reed L., Smith H.C. The editosome for cytidine to uridine mRNA editing has a native complexity of 27S: identification of intracellular domains containing active and inactive editing factors. J Cell Sci 2002, 115:1027-1039.
15. Smith H.C. Analysis of protein complexes assembled on apolipoprotein B mRNA for mooring sequence-dependent RNA editing. Methods 1998, 15:27-39.
16. Chester A., Somasekaram A., Tzimina M., Jarmuz A., Gisbourne J., O'Keefe R., et al. The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay. EMBO J 2003, 22:3971-3982.
17. Navaratnam N., Patel D., Shah R.R., Greeve J.C., Powell L.M., Knott T.J., Scott J. An additional editing site is present in apolipoprotein B mRNA. Nucleic Acids Res 1991, 19:1741-1744.
18. Backus J.W., Schock D., Smith H.C. Only cytidines 5' of the apolipoprotein B mRNA mooring sequence are edited. Biochim Biophys Acta 1994, 1219:1-14.
19. Skuse G.R., Cappione A.J., Sowden M., Metheny L.J., Smith H.C. The neurofibromatosis type I messenger RNA undergoes base-modification RNA editing. Nucleic Acids Res 1996, 24:478-485.
20. Sowden M., Hamm J.K., Spinelli S., Smith H.C. Determinants involved in regulating the proportion of edited apolipoprotein B RNAs. RNA 1996, 2:274-288.
21. Rosenberg B.R., Hamilton C.E., Mwangi M.M., Dewell S., Papavasiliou F.N. Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3' UTRs. Nat Struct Mol Biol 2011, 18:230-236.
22. Lehmann D.M., Galloway C.A., Macelrevey C., Sowden M.P., Wedekind J.E., Smith H.C. Functional characterization of APOBEC-1 complementation factor phosphorylation sites. Biochim Biophys Acta 2007, 1773:408-418.
23. Lehmann D.M., Galloway C.A., Sowden M.P., Smith H.C. Metabolic regulation of apoB mRNA editing is associated with phosphorylation of APOBEC-1 complementation factor. Nucleic Acids Res 2006, 34:3299-3308.
24. Sowden M.P., Smith H.C. Commitment of apolipoprotein B RNA to the splicing pathway regulates cytidine-to-uridine editing-site utilization. Biochem J 2001, 359:697-705.
25. Mukhopadhyay D., Anant S., Lee R.M., Kennedy S., Viskochil D., Davidson N.O. C→U editing of neurofibromatosis 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 2002, 70:38-50.
26. Smith H.C., Mark P., Kefang X., Wedekind J.E. Structure and Function of Mammalian Cytidine Deaminases that Mediate Expressed Sequence Diversification 2005, 1610-2145. Springer-Verlag, NY. H. Grosjean (Ed.).
27. Thompson J., Gopal S. Genetic algorithm learning as a robust approach to RNA editing site prediction. BMC Bioinformatics 2006, 7:145.
28. Paz-Yaacov N., Levanon E.Y., Nevo E., Kinar Y., Harmelin A., Jacob-Hirsch J., et al. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proc Natl Acad Sci USA 2010, 107:12174-12179.
29. Farajollahi S., Maas S. Molecular diversity through RNA editing: a balancing act. Trends Genet 2010, 26:221-230.
30. Hirano K., Young S.G., Farese R.V., Ng J., Sande E., Warburton C., et al. Targeted disruption of the mouse apobec-1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48. J Biol Chem 1996, 271:9887-9890.
31. Nakamuta M., Chang B.H.J., Zsigmond E., Kobayashi K., Lei H., Ishida B.Y., Oka K., Li E., Chan L. Complete phenotypic characterization of the 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, 271:25981-25988.
32. 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 1996, 271:11506-11510.
33. Yamanaka S., Poksay K.S., Arnold K.S., Innerarity T.L. A novel translational repressor mRNA is edited extensively in livers containing tumors caused by the transgene expression of the apoB mRNA-editing enzyme. Genes Dev 1997, 11:321-333.
34. Yamanaka S., Balestra M., Ferrell L., Fan J., Arnold K.S., Taylor S., Taylor J.M., Innerarity T.L. Apolipoprotein B mRNA editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals. Proc Natl Acad Sci USA 1995, 92:8483-8487.
35. Harris R.S., Petersen-Mahrt S.K., Neuberger M.S. RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell 2002, 10:1247-1253.
36. Petersen-Mahrt S.K., Neuberger M.S. In vitro deamination of cytosine to uracil in single-stranded DNA by apolipoprotein B editing complex catalytic subunit 1 (APOBEC1). J Biol Chem 2003, 278:19583-19586.
37. Gee P., Ando Y., Kitayama H., Yamamoto S.P., Kanemura Y., Ebina H., et al. APOBEC1-mediated editing and attenuation of HSV-1 DNA implicates an antiviral role in neurons during encephalitis. J Virol 2011, 85(19):9726-9736.
38. 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 1998, 26:1644-1652.
39. Hersberger M., Patarroyo-White S., Qian X., Arnold K.S., Rohrer L., Balestra M.E., et al. Regulatable liver expression of the rabbit apolipoprotein B mRNA-editing enzyme catalytic polypeptide 1 (APOBEC-1) in mice lacking endogenous APOBEC-1 leads to aberrant hyperediting. Biochem J 2003, 369:255-262.
40. Severi F., Chicca A., Conticello S.G. Analysis of reptilian APOBEC1 suggests that RNA editing may not be its ancestral function. Mol Biol Evol 2011, 28:1125-1129.
41. Dance G.S., Beemiller P., Yang Y., Mater D.V., Mian I.S., Smith H.C. Identification of the yeast cytidine deaminase CDD1 as an orphan C→U RNA editase. Nucleic Acids Res 2001, 29:1772-1780.
42. Xie K., Sowden M.P., Dance G.S., Torelli A.T., Smith H.C., Wedekind J.E. The structure of a yeast RNA-editing deaminase provides insight into the fold and function of activation-induced deaminase and APOBEC-1. Proc Natl Acad Sci USA 2004, 101:8114-8119.
43. Smith H.C. Measuring editing activity and identifying cytidine-to-uridine mRNA editing factors in cells and biochemical isolates. Methods Enzymol 2007, 424:389-416.
44. Wedekind J.E., Dance G.S., Sowden M.P., Smith H.C. Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends Genet 2003, 19:207-216.
45. Kracker s D.A. Insights into the B cell specific process of immunoglobulin class switch recombination. Immunol Lett 2011, 138:97-103.
46. Di Noia J.M.N.M. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 2007, 76:1-22.
47. Muramatsu M., Anant S.V., Sugai S., Kinoshita M., Davidson K., Honjo N.O.T. 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 1999, 274:18470-18476.
48. Martin A.S.M. Antibody alterations. Nature 2001, 412:870-871.
49. Papavasiliou F.N.S.D. Somatic hypermutation of immunoglobulin genes: merging mechanisms for genetic diversity. Cell 2002, 109:S35-S44.
50. Odegard Vh S.D. Targeting of somatic hypermutation. Nat Rev Immunol 2006, 6:573-583.
51. Arakawa H.H.J., Buerstedde J.M. Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 2001, 295:1301.
52. Fugmann S.D., Schatz D.G. Immunology. One AID to unite them all. Science 2002, 295:1244-1245.
53. Muto T., Taniwaki M.M., Kinoshita M., Honjo K., Isolation T. Tissue distribution, and chromosomal localization of the human activation-induced cytidine deaminase (AID) gene. Genomics 2000, 68:85-88.
54. Revy P.M.T., Levy Y., Geissmann F., Plebani A., Sanal O., Catalan N., Forveille M., Dufourcq-Lagelouse R., Gennery A., Tezcan I., Ersoy F., Kayserili H., Ugazio A.G., Brousse N., Muramatsu M., Notarangelo L.D., Kinoshita K., Honjo T., Fischer A., Durandy A. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 2000, 102:565-575.
55. Muramatsu M., Fagarasan K.K., Yamada S., Shinkai S., Honjo Y.T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
56. Okazaki I.M., Honjo K.A.T. Role of AID in tumorigenesis. Adv Immunol 2007, 94:245-273.
57. McCarthy H.W.W., Barron L.L., Cromwell C.C., Wang J., Coombes K.R., Rangel R., Elenitoba-Johnson K.S., Keating M.J., Abruzzo L.V. High expression of activation-induced cytidine deaminase (AID) and splice variants is a distinctive feature of poor-prognosis chronic lymphocytic leukemia. Blood 2003, 101:4903-4908.
58. Marantidou F., Stalika D.A., Korkolopoulou E., Saetta P., Anagnostopoulos A., Laoutaris A., Stamatopoulos N., Belessi K., Scouras C., Patsouris Z.E. Activation-induced cytidine deaminase splicing patterns in chronic lymphocytic leukemia. Blood Cells Mol Dis 2010, 44:262-267.
59. Albesiano E., Damle M.B., Allen R.N., Rai S.L., Chiorazzi K.R.N. Activation-induced cytidine deaminase in chronic lymphocytic leukemia B cells: expression as multiple forms in a dynamic, variably sized fraction of the clone. Blood 2003, 102:3333-3339.
60. Wu X.D.J., Chang S.K., Nowakowski G.S., Jelinek D.F. Alternative splicing regulates activation-induced cytidine deaminase (AID): implications for suppression of AID mutagenic activity in normal and malignant B cells. Blood 2008, 112:4675-4682.
61. van Maldegem F.J.R., van Dijk R., Bende R.J., van Noesel C.J. Activation-induced cytidine deaminase splice variants are defective because of the lack of structural support for the catalytic site. J Immunol 2010, 184:2487-2491.
62. Okazaki I.M., Kakazu H.H., Yamada N., Muramatsu S., Kinoshita M., Honjo K.T. Constitutive expression of AID leads to tumorigenesis. J Exp Med 2003, 197:1173-1181.
63. Endo Y., Marusawa H., Kinoshita K., Morisawa T., Sakurai T., Okazaki I.M., et al. Expression of activation-induced cytidine deaminase in human hepatocytes via NF-kappaB signaling. Oncogene 2007, 26:5587-5595.
64. Muto T., Yamada O.I., Tanaka S., Kinoshita Y., Muramatsu K., Nagaoka M., Honjo H.T. Negative regulation of activation-induced cytidine deaminase in B cells. Proc Natl Acad Sci USA 2006, 103:2752-2757.
65. Sayegh C.E.Q.M., Agata Y., Murre C. E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nat Immunol 2003, 4:586-593.
66. Jannek Hauser N.S., Wallenius A., Baradaran S., Saarikettu J., Grundström T. B-cell receptor activation inhibits AID expression through calmodulin inhibition of E-proteins. Proc Natl Acad Sci USA 2008, 105:1267-1272.
67. Ta V.T., Catalan N.H., Durandy N., Fischer A., Imai A., Nonoyama K., Tashiro S., Ikegawa J., Ito M., Kinoshita S., Muramatsu K., Honjo M.T. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat Immunol 2003, 4:843-848.
68. Okuyama S., Marusawa H., Matsumoto T., Ueda Y., Matsumoto Y., Endo Y., et al. Excessive activity of apolipoprotein B mRNA editing enzyme catalytic polypeptide 2 (APOBEC2) contributes to liver and lung tumorigenesis. Int J Cancer 2011, 10.1002/ijc.26114.
69. Prochnow C., Bransteitter R., Klein M.G., Goodman M.F., Chen X.S. The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 2007, 445:447-451.
70. Lada A.G., Krick C.F., Kozmin S.G., Mayorov V.I., Karpova T.S., Rogozin I.B., et al. Mutator effects and mutation signatures of editing deaminases produced in bacteria and yeast. Biochemistry (Mosc) 2011, 76:131-146.
71. Sato Y., Probst H.C., Tatsumi R., Ikeuchi Y., Neuberger M.S., Rada C. Deficiency in APOBEC2 leads to a shift in muscle fiber type, diminished body mass, and myopathy. J Biol Chem 2010, 285:7111-7118.
72. OhAinle M., Kerns J.A., Malik H.S., Emerman M. Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 2006, 80:3853-3862.
73. 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, 79:285-296.
74. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650.
75. Smith H.C. APOBEC3G: a double agent in defense. Trends Biochem Sci 2011, 36:239-244.
76. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 2003, 424:99-103.
77. Zhang H., Yang B., Pomerantz R.J., Zhang C., Arunachalam S.C., Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 2003, 424:94-98.
78. Hultquist J.F., Lengyel J.A., Refsland E.W., Larue R.S., Lackey L., Brown W.L., et al. Human and Rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J Virol 2011, 85(21):11220-11234.
79. Zielonka J., Bravo I.G., Marino D., Conrad E., Perkovic M., Battenberg M., et al. Restriction of equine infectious anemia virus by equine APOBEC3 cytidine deaminases. J Virol 2009, 83:7547-7559.
80. Dang Y., Wang X., Esselman W.J., Zheng Y.H. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J Virol 2006, 80:10522-10533.
81. Delebecque F., Suspene R., Calattini S., Casartelli N., Saib A., Froment A., et al. Restriction of foamy viruses by APOBEC cytidine deaminases. J Virol 2006, 80:605-614.
82. Liddament M.T., Brown W.L., Schumacher A.J., Harris R.S. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 2004, 14:1385-1391.
83. Thielen B.K., McNevin J.P., McElrath M.J., Hunt B.V., Klein K.C., Lingappa J.R. Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J Biol Chem 2010, 285:27753-27766.
84. Bulliard Y., Narvaiza I., Bertero A., Peddi S., Rohrig U.F., Ortiz M., et al. Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J Virol 2011, 85:1765-1776.
85. Bonvin M., Achermann F., Greeve I., Stroka D., Keogh A., Inderbitzin D., et al. Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 2006, 43:1364-1374.
86. Xu R., Zhang X., Zhang W., Fang Y., Zheng S., Yu X.F. Association of human APOBEC3 cytidine deaminases with the generation of hepatitis virus B×antigen mutants and hepatocellular carcinoma. Hepatology 2007, 46:1810-1820.
87. Chiu Y.L., Witkowska H.E., Hall S.C., Santiago M., Soros V.B., Esnault C., et al. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc Natl Acad Sci USA 2006, 103:15588-15593.
88. Schumann G.G. APOBEC3 proteins: major players in intracellular defence against LINE-1-mediated retrotransposition. Biochem Soc Trans 2007, 35:637-642.
89. Esnault C., Millet J., Schwartz O., Heidmann T. Dual inhibitory effects of APOBEC family proteins on retrotransposition of mammalian endogenous retroviruses. Nucleic Acids Res 2006, 34:1522-1531.
90. Schumacher A.J., Nissley D.V., Harris R.S. APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. Proc Natl Acad Sci USA 2005, 102:9854-9859.
91. Hulme A.E., Bogerd H.P., Cullen B.R., Moran J.V. Selective inhibition of Alu retrotransposition by APOBEC3G. Gene 2007, 390:199-205.
92. 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 2006, 34:89-95.
93. Chen H., Lilley C.E., Yu Q., Lee D.V., Chou J., Narvaiza I., et al. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr Biol 2006, 16:480-485.
94. Muckenfuss H., Hamdorf M., Held U., Perkovic M., Lower J., Cichutek K., et al. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 2006, 281:22161-22172.
95. Stenglein M.D., Harris R.S. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 2006, 281:16837-16841.
96. Kinomoto M., Kanno T., Shimura M., Ishizaka Y., Kojima A., Kurata T., et al. All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res 2007, 35:2955-2964.
97. Tan L., Sarkis P.T., Wang T., Tian C., Yu X.F. Sole copy of Z2-type human cytidine deaminase APOBEC3H has inhibitory activity against retrotransposons and HIV-1. FASEB J 2009, 23:279-287.
98. Wichroski M.J., Robb G.B., Rana T.M. Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog 2006, 2:e41.
99. Landry S., Narvaiza I., Linfesty D.C., Weitzman M.D. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 2011, 12:444-450.
100. Rogozin I.B., Basu M.K., Jordan I.K., Pavlov Y.I., Koonin E.V. APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 2005, 4:1281-1285.
101. Yang Y., Sowden M.P., Yang Y., Smith H.C. Intracellular trafficking determinants in APOBEC-1, the catalytic subunit for cytidine to uridine editing of apolipoprotein B mRNA. Exp Cell Res 2001, 267:153-164.
102. Yang Y., Smith H.C. Multiple protein domains determine the cell type-specific nuclear distribution of the catalytic subunit required for apolipoprotein B mRNA editing. Proc Natl Acad Sci USA 1997, 94:13075-13080.
103. Yang Y., Sowden M.P., Smith H.C. Induction of cytidine to uridine editing on cytoplasmic apolipoprotein B mRNA by overexpressing APOBEC-1. J Biol Chem 2000, 275:22663-22669.
104. Lau P.P., Xiong W., Zhu H.-J., Chen S.-H., Chan L. Apo B mRNA editing is an intranuclear event that occurs posttranscriptionally coincident with splicing and polyadenylation. J Biol Chem 1991, 266:20550-20554.
105. Smith H.C., Kuo S.R., Backus J.W., Harris S.G., Sparks C.E., Sparks J.D. In vitro apolipoprotein B mRNA editing: identification of a 27S editing complex. Proc Natl Acad Sci USA 1991, 88:1489-1493.
106. Yang Y., Kovalski K., Smith H.C. Partial characterization of the auxiliary factors involved in apolipoprotein B mRNA editing through APOBEC-1 affinity chromatography. J Biol Chem 1997, 272:27700-27706.
107. Blanc V., Kennedy S.M., Davidson N.O. A novel nuclear localization signal in the auxiliary domain of apobec-1 complementation factor (ACF) regulates nucleo-cytoplasmic import and shuttling. J Biol Chem 2003, 278:21148-21204.
108. Smith H.C., Wedekind J.E., Kefang X., Sowden M.P. Mammalian C to U editing. Top Curr Biol 2005, 12:365-400.
109. Galloway C.A., Sowden M.P., Smith HC Increasing the yield of soluble recombinant protein expressed in E. coli by induction during late log phase. Biotechniques 2003, 34. 524-526, 528, 530.
110. Dance G.S.C., Sowden M.P., Cartegni L., Cooper E., Krainer A.R., Smith H.C. Two proteins essential for apolipoprotein B mRNA editing are expressed from a single gene through alternative splicing. J Biol Chem 2002, 277:12703-12709.
111. Sowden M.P., Lehmann D.M., Lin X., Smith C.O., Smith H.C. Identification of novel alternative splice variants of APOBEC-1 complementation factor with different capacities to support ApoB mRNA editing. J Biol Chem 2004, 278:197-206.
112. Patenaude A.M., Di Noia J.M. The mechanisms regulating the subcellular localization of AID. Nucleus 2010, 1:325-331.
113. Stavnezer Complex regulation and function of activation-induced cytidine deaminase. Trends Immunol 2011, 32:194-201.
114. Basu U FA, and Alt FW, post-translational regulation of activation-induced cytidine deaminase. Philos Trans R Soc B 2009, 364:667-673.
115. Rada C., Jarvis J.M., Milstein C. AID-GFP chimeric protein increases hypermutation of Ig genes with no evidence of nuclear localization. Proc Natl Acad Sci USA 2002, 99:7003-7008.
116. Patenaude A.M.O.A., Hu Y., Campo V.H., Kavli B., Buschiazzo A., Di Noia J.M. Active nuclear import and cytoplasmic retention of activation-induced deaminase. Nat Struct Mol Biol 2009, 16:517-527.
117. McBride K.M., Barreto V.M., Ramiro A.R., Stavropoulos P., Nussenzweig M.C. Somatic hypermutation is limited by CRM1-dependent nuclear export of activation induced deaminase. J Exp Med 2004, 199:1235-1244.
118. Ito S. Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc Natl Acad Sci USA 2004, 101:1975-1980.
119. Ganesh K.A.S., Taylor B., Simpson P., Rada C., Neuberger M. CTNNBL1 is a novel nuclear localization sequence-binding protein that recognizes RNA-splicing factors CDC5L and Prp31. J Biol Chem 2011, 286:17091-17102.
120. Orthwein A.P.A., Affar E.B., Lamarre Y.J.A., Di Noia J.M. Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J Exp Med 2010, 207:2751-2765.
121. Said A., Faili F., Zober C., D' Orlando O., Weller S., Weill J.C., Reynaud C.A. Proteasomal degradation restricts the nuclear lifespan of AID. J Exp Med 2008, 205:1357-1368.
122. Bennett R.P., Presnyak V., Wedekind J.E., Smith H.C. Nuclear exclusion of the HIV-1 host defense factor APOBEC3G requires a novel cytoplasmic retention signal and is not dependent on RNA binding. J Biol Chem 2008, 283:7320-7327.
123. Huthoff H., Autore F., Gallois-Montbrun S., Fraternali F., Malim M.H. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog 2009, 5:e1000330.
124. Huthoff H., Malim M.H. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation. J Virol 2007, 81:3807-3815.
125. Henry M., Guetard D., Suspene R., Rusniok C., Wain-Hobson S., Vartanian J.P. Genetic editing of HBV DNA by monodomain human APOBEC3 cytidine deaminases and the recombinant nature of APOBEC3G. PLoS One 2009, 4:e4277.
126. Stopak K.S., Chiu Y.L., Kropp J., Grant R.M., Greene W.C. Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J Biol Chem 2007, 282:3539-3546.
127. Kreisberg J.F., Yonemoto W., Greene W.C. Endogenous factors enhance HIV infection of tissue naive CD4T cells by stimulating high molecular mass APOBEC3G complex formation. J Exp Med 2006, 203:865-870.
128. Goila-Gaur R., Khan M.A., Miyagi E., Kao S., Opi S., Takeuchi H., et al. HIV-1 Vif promotes the formation of high molecular mass APOBEC3G complexes. Virology 2008, 372:136-146.
129. Kozak S.L., Marin M., Rose K.M., Bystrom C., Kabat D. The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J Biol Chem 2006, 281:29105-29119.
130. Huang J., Liang Z., Yang B., Tian H., Ma J., Zhang H. 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 2007, 282:33632-33640.
131. Gallois-Montbrun S., Kramer B., Swanson C.M., Byers H., Lynham S., Ward M., et al. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol 2007, 81:2165-2178.
132. McDougall W.M., Smith H.C. Direct evidence that RNA inhibits APOBEC3G ssDNA cytidine deaminase activity. Biochem Biophys Res Commun 2011, 412(4):612-617.
133. Wedekind J.E., Gillilan R., Janda A., Krucinska J., Salter J.D., Bennett R.P., et al. Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J Biol Chem 2006, 281:38122-38126.
134. Soros V.B., Yonemoto W., Greene W.C. Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog 2007, 3:e15.
135. Khan M.A., Goila-Gaur R., Opi S., Miyagi E., Takeuchi H., Kao S., et al. Analysis of the contribution of cellular and viral RNA to the packaging of APOBEC3G into HIV-1 virions. Retrovirology 2007, 4:48.
136. Svarovskaia E.S., Xu H., Mbisa J.L., Barr R., Gorelick R.J., Ono A., et al. Human APOBEC3G is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 2004, 270:35822-35828.
137. Zhang W., Du J., Yu K., Wang T., Yong X., Yu X.F. Association of potent human antiviral cytidine deaminases with 7SL RNA and viral RNP in HIV-1 virions. J Virol 2010, 84:12903-12913.
138. Wang T., Tian C., Zhang W., Luo K., Sarkis P.T., Yu L., et al. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J Virol 2007, 81:13112-13124.
139. Wang T.T.C., Zhang W., Sarkis P.T., Yu X.F. Interaction with 7SL RNA but not with HIV-1 genomic RNA or P bodies is required for APOBEC3F virion packaging. J Mol Biol 2008, 375:1098-1112.
140. Alce T.M., Popik W. APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J Biol Chem 2004, 4:97-107.
141. Cen S., Guo F., Niu M., Saadatmand J., Deflassieux J., Kleiman L. The interaction between HIV-1 Gag and APOBEC3G. J Biol Chem 2004, 279:33177-33184.
142. Luo K., Liu B., Xiao Z., Yu Y., Yu X., Gorelick R., et al. Amino-terminal region of the human immunodeficiency virus type 1 nucleocapsid is required for human APOBEC3G packaging. J Virol 2004, 78:11841-11852.
143. Wang T., Zhang W., Tian C., Liu B., Yu Y., Ding L., et al. Distinct viral determinants for the packaging of human cytidine deaminases APOBEC3G and APOBEC3C. Virology 2008, 377:71-79.
144. Stauch B.H.H., Perkovic M., Weisel M., Kopietz F., Cichutek K., Münk C., Schneider G. Model structure of APOBEC3C reveals a binding pocket modulating ribonucleic acid interaction required for encapsidation. Proc Natl Acad Sci USA 2009, 106:12079-12084.
145. Nonaka T., Toyoshima D.T., Muramatsu T., Honjo M., Kinoshita T.K. Carboxy-terminal domain of AID required for its mRNA complex formation in vivo. Proc Natl Acad Sci USA 2009, 106:2747-2751.
146. Bransteitter R., Pham P., Scharff M.D., Goodman M.F. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc Natl Acad Sci USA 2003, 100:4102-4107.
147. Iwatani Y., Takeuchi H., Strebel K., Levin J.G. Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J Virol 2006, 80:5992-6002.
148. Navarro F., Bollman B., Chen H., Konig R., Yu Q., Chiles K., et al. Complementary function of the two catalytic domains of APOBEC3G. Virology 2005, 333:374-386.
149. McDougall W.M., Okany C., Smith H.C. Deaminase activity on ssDNA occurred in vitro when APOBEC3G forms homotetramers and higher-order complexes. J Biol Chem 2011, 286:30655-30661.
150. Chelico L., Prochnow C., Erie D.A., Chen X.S., Goodman M.F. Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J Biol Chem 2010, 285:16195-16205.