The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay

EMBO Journal

Volumn 22, Issue 15, 2003, Pages 3971-3982

  Chester, Ann ^a   Somasekaram, Angelika ^a   Tzimina, Maria ^a   Jarmuz, Adam ^a   Gisbourne, Jane ^a   O'Keefe, Raymond ^b   Scott, James ^a   Navaratnam, Naveenan ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

ACF; APOBEC1; NMD; Nucleocytoplasmic shuttling

Indexed keywords

APOLIPOPROTEIN B; BIOLOGICAL FACTOR; COMPLEMENTING SPECIFICITY FACTOR; CYTIDINE DEAMINASE; HOLOENZYME; MESSENGER RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; ENZYME ACTIVITY; GENE FUNCTION; GENETIC ASSOCIATION; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RNA BINDING; RNA DEGRADATION; RNA EDITING; RNA TRANSLATION; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CELL NUCLEUS; CYTIDINE DEAMINASE; CYTOPLASM; HUMANS; NUCLEAR LOCALIZATION SIGNALS; RNA EDITING; RNA, MESSENGER; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 0041524056     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg369     Document Type: Article

References (51)

1. Blanc, V., Navaratnam, N., Henderson, J.O., Anant, S., Kennedy, S., Jarmuz, A., Scott, J. and Davidson, N.O. (2001a) Identification of GRY-RBP as an apolipoprotein B RNA-binding protein that interacts with both apobec-1 and apobec-1 complementation factor to modulate C to U editing. J. Biol. Chem., 276, 10272-10283.
2. Blanc, V., Henderson, J.O., Kennedy, S. and Davidson, N.O. (2001b) 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., 276, 46386-46393.
3. Chester, A., Scott, J., Anant, S. and Navaratnam, N. (2000) RNA editing: cytidine to uridine conversion in apolipoprotein B mRNA. Biochim. Biophys. Acta, 1494, 1-13.
4. Conti, E., Uy, M., Leighton, L., Blobel, G. and Kuriyan, J. (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell, 94, 193-204.
5. Dingwall, C. and Laskey, R. (1991) Nuclear targeting sequences - a consensus? Trends Biochem. Sci., 16, 478-481.
6. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W. and Luhrmann, R. (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell, 82, 475-483.
7. Flach, J., Bossie, M., Vogel, J., Corbett, A., Jinks, T., Willins, D.A. and Silver, P.A. (1994) A yeast RNA binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell. Biol., 14, 8399-8407.
8. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, 90, 1051-1060.
9. Fridell, R.A., Truant, R., Thorne, L., Benson, R.E. and Cullen, B.R. (1997) Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-β. J. Cell Sci., 110, 1325-1331.
10. Frischmeyer, P.A. and Dietz, H.C. (1999) Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet., 8, 1893-1900.
11. Fujino, T., Navaratnam, N., Jarmuz, A., von Haeseler, A. and Scott, J. (1999) C-U editing of apolipoprotein B mRNA in marsupials: identification and characterisation of APOBEC-1 from the American opossum Monodelphus domestica. Nucleic Acids Res., 27, 2662-2671.
12. Gerber, A.P. and Keller, W. (2001) RNA editing by base deamination: more enzymes, more targets, new mysteries. Trends Biochem. Sci., 26, 376-384.
13. Görlich, D. and Mattaj, I.W. (1996) Nucleocytoplasmic transport. Science, 271, 1513-1518.
14. Hentze, M.W. (2001) Protein synthesis. Believe it or not - translation in the nucleus. Science, 293, 1058-1059.
15. Hentze, M.W. and Kulozik, A.E. (1999) A perfect message: RNA surveillance and nonsense-mediated decay. Cell, 96, 307-310.
16. Hersberger, M. and Innerarity, T.L. (1998) Two efficiency elements flanking the editing site of cytidine 6666 in the apolipoprotein B mRNA support mooring-dependent editing. J. Biol. Chem., 273, 9435-9442.
17. Iborra, F.J., Jackson, D.A. and Cook, P.R. (2001) Coupled transcription and translation within nuclei of mammalian cells. Science, 293, 1139-1142.
18. Jarmuz, A., Chester, A., Bayliss, J., Gisbourne, J., Dunham, I., Scott, J. and Navaratnam, N. (2002) An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics, 79, 285-296.
19. La Casse, E.C. and Lefebvre, Y.A. (1995) Nuclear localization signals overlap DNA- or RNA-binding domains in nucleic acid-binding proteins. Nucleic Acids Res., 23, 1647-1656.
20. Lau, P.P., Xiong, W.J., Zhu, H.J., Chen, S.H. and Chan, L. (1991) Apolipoprotein B mRNA editing is an intranuclear event that occurs posttranscriptionally coincident with splicing and polyadenylation. J. Biol. Chem., 266, 20550-20554.
21. Le Hir, H., Izaurralde, E., Maquat, L.E. and Moore, M.J. (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J., 19, 6860-6869.
22. Lellek, H., Kirsten, R., Diehl, I., Apostel, F., Buck, F. and Greeve, J. (2000) Purification and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex. J. Biol. Chem., 275, 19848-19856.
23. Liao, W., Hong, S.-H., Chan, B.H.-J., Rudolph, F.B., Clark, S.C. and Chan, L. (1999) APOBEC-2, a cardiac- and skeletal muscle-specific member of the cytidine deaminase supergene family. Biochem. Biophys. Res. Commun., 260, 398-404.
24. Lykke-Andersen, J., Shu, M.D. and Steitz, J.A. (2000) Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell, 103, 1121-1131.
25. Madsen, P. et al. (1999) Psoriasis upregulated phorbolin-1 shares structural but not functional similarity to the mRNA-editing protein Apobec-1. J. Invest. Dermatol., 113, 162-169.
26. Maquat, L.E. (1996) Defects in RNA splicing and the consequence of shortened translational reading frames. Am. J. Hum. Genet., 59, 279-286.
27. Maquat, L.E. and Carmichael, G.G. (2001) Quality control of mRNA function. Cell, 104, 173-176.
28. Mehta, A. and Driscoll, D.M. (2002) Identification of domains in apobec-1 complementation factor required for RNA binding and apolipoprotein B mRNA editing. RNA, 8, 69-82.
29. Mehta, A., Kinter, M.T., Sherman, N.E. and Driscoll, D.M. (2000) Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA. Mol. Cell. Biol., 20, 1846-1854.
30. Muramatsu, M., Sankaranand, V.S., Anant, S., Susgai, M., Kinoshita, K., Davidson, N.O. and Honjo, T. (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, 18470-18476.
31. Nagy, E. and Maquat, L.E. (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci., 23, 198-199.
32. Navaratnam, N., Shah, R., Patel, D., Fay, V. and Scott, J. (1993a) Apolipoprotein B mRNA editing is associated with UV crosslinking of proteins to the editing site. Proc. Natl Acad. Sci. USA, 90, 222-226.
33. Navaratnam, N., Morrison, J.R., Bhattycharya, S., Patel, D., Funahashi, T., Giannoni, F., Teng, B.-B., Davidson, N.O. and Scott, J. (1993b) The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J. Biol. Chem., 268, 20709-20712.
34. Navaratnam, N., Bhattycharya, S., Fujino, T., Patel, D., Jarmuz, A.L. and Scott, J. (1995) Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell, 81, 187-195.
35. Navaratnam, N. et al. (1998) Escherichia coli cytidine deaminase provides a molecular model for apoB RNA editing and a mechanism for RNA substrate recognition. J. Mol. Biol., 275, 695-714.
36. Piñol-Roma, S. and Dreyfuss, G. (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature, 355, 730-732.
37. Piñol-Roma, S., Choi, Y.D., Matunis, M.J. and Dreyfuss, G. (1988) Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev., 2, 215-227.
38. Pollard, V.W. and Malim, M.H. (1998) The HIV-1 Rev protein. Annu. Rev. Microbiol., 52, 491-532.
39. Richardson, N., Navaratnam, N. and Scott, J. (1998) Secondary structure for the apolipoprotein B mRNA editing site: AU-binding proteins interact with a stem loop. J. Biol. Chem., 273, 31707-31717.
40. Schell, T., Kulozik, A.E. and Hentze, M.W. (2002) Integration of splicing, transport and translation to achieve mRNA quality control by the nonsense-mediated decay pathway. Genome Biol., 3, 1-6.
41. Scott, J. (1995) A place in the world for RNA editing. Cell, 81, 833-836.
42. Shah, R.R., Knott, T.J., LeGros, J.E., Navaratnam, N., Greeve, J.C. and Scott, J. (1991) Sequence requirements for the editing of apolipoprotein B mRNA. J. Biol. Chem., 266, 16301-16304.
43. Sheehy, A.M., Gaddis, N.C., Choi, J.D. and Malim, M.H. (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature, 418, 646-650.
44. Sowden, M.P., Ballatori, N., de Mesy Jensen, K.L., Hamilton Reed, L. and Smith, H.C. (2002) 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. 115, 1027-1039.
45. Sun, X., Perlick, H.A., Dietz, H.C. and Maquat, L.M. (1998) A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc. Natl Acad. Sci. USA, 95, 10009-10014.
46. Teng, B.-B., Burant, C.F. and Davidson, N.O. (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science, 260, 1816-1819.
47. Thermann, R., Neu-Yilik, G., Deters, A., Frede, U., Wehr, K., Hagemeier, C., Hentze, M.W. and Kulozik, A.E. (1998) Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J., 17, 3484-3494.
48. Wolff, B., Sanglier, J.-J. and Wang, Y. (1997) Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol., 4, 139-147.
49. Yamanaka, S., Poksay, K.S., Arnold, K.S. and Innerarity, T.L. (1997) 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., 11, 321-333.
50. Yang, Y., Yang, Y. and Smith, H.C. (1997) 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, 94, 13075-13080.
51. Yang, Y., Sowden, M.P., Yang, Y. and Smith, H.C. (2001) Intracellular trafficking determinants in APOBEC-1, the catalytic subunit for cytidine to uridine editing of apolipoprotein B mRNA. Exp. Cell Res., 267, 153-164.