Functional characterization of APOBEC-1 complementation factor phosphorylation sites

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 3, 2007, Pages 408-418

  Lehmann, David M ^a,b   Galloway, Chad A ^a   MacElrevey, Celeste ^a   Sowden, Mark P ^a   Wedekind, Joseph E ^a   Smith, Harold C ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

apoB; APOBEC 1 Complementation factor; Phosphorylation; Regulation; RNA editing

Indexed keywords

APOBEC 1 COMPLEMENTATION FACTOR; APOLIPOPROTEIN B; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; COMPLEMENTARY DNA; CYCLIC AMP DEPENDENT PROTEIN KINASE; MESSENGER RNA; PHOSPHOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN KINASE C; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; LIVER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RNA EDITING; RNA SYNTHESIS; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANIMALS; APOLIPOPROTEINS B; CELLS, CULTURED; ENZYME ACTIVATION; HEPATOCYTES; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEQUENCE ALIGNMENT;

RATTUS;

EID: 33847066346     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.11.019     Document Type: Article

References (59)

1. Johnson D.F., Poksay K.S., and Innerarity T.L. The mechanism for apo-B mRNA editing is deamination. Biochem. Biophys. Res. Commun. 195 (1993) 1204-1210
2. Powell L.M., Wallis S.C., Pease R.J., Edwards Y.H., Knott T.J., and Scott J. A novel form of tissue-specific RNA processing produces apolipoprotein- B48 in intestine. Cell 50 (1987) 831-840
3. Chen S.H., Habib G., Yang C.Y., Gu Z.W., Lee B.R., Weng S.A., Silberman S.R., Cai S.J., Deslypere J.P., Rosseneu M., et al. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 238 (1987) 363-366
4. Lau P.P., Zhu H.-J., Baldini H.A., Charnsangavej C., and Chan L. Dimeric structure of a human apo B mRNA editing protein and cloning and chromosomal localization of its gene. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8522-8526
5. Teng B., Burant C.F., and Davidson N.O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260 (1993) 1816-1819
6. Mehta A., Kinter M.T., Sherman N.E., and 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. 20 (2000) 1846-1854
7. Greeve J., Altkemper I., Dieterich J.H., Greten H., and Windler E. Apolipoprotein B mRNA editing in 12 different mammalian species: hepatic expression is reflected in low concentrations of apoB-containing plasma lipoproteins. J. Lipid Res. 34 (1993) 1367-1383
8. Backus J.W., Eagleton M.J., Harris S.G., Sparks C.E., Sparks J.D., and Smith H.C. Quantitation of endogenous liver apolipoprotein B mRNA editing. Biochem. Biophys. Res. Commun. 170 (1990) 513-518
9. Lau P.P., Xiong W., Zhu H.-J., Chen S.-H., and Chan L. Apo B mRNA editing is an intranuclear event that occurs posttranscriptionally coincident with splicing and polyadenylation. J. Biol. Chem. 266 (1991) 20550-20554
10. Sowden M., Hamm J.K., Spinelli S., and Smith H.C. Determinants involved in regulating the proportion of edited apolipoprotein B RNAs. RNA 2 (1996) 274-288
11. Smith H.C., Kuo S.R., Backus J.W., Harris S.G., Sparks C.E., and Sparks J.D. In vitro apolipoprotein B mRNA editing: identification of a 27S editing complex. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 1489-1493
12. Smith H.C. Analysis of protein complexes assembled on apolipoprotein B mRNA for mooring sequence-dependent RNA editing. Methods 15 (1998) 27-39
13. Harris S.G., Sabio I., Mayer E., Steinberg M.F., Backus J.W., Sparks J.D., Sparks C.E., and Smith H.C. Extract-specific heterogeneity in high-order complexes containing apolipoprotein B mRNA editing activity and RNA-binding proteins. J. Biol. Chem. 268 (1993) 7382-7392
14. Sowden M.P., Ballatori N., De Mesy Jensen K.L., Hamilton Reed L., and 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. 115 (2002) 1027-1039
15. Yang Y., and 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. U. S. A. 94 (1997) 13075-13080
16. Blanc V., Henderson J.O., Kennedy S., and 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. 276 (2001) 46386-46393
17. Chester A., Somasekaram A., Tzimina M., Jarmuz A., Gisbourne J., O'keefe R., Scott J., and Navaratnam N. The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay. EMBO J. 22 (2003) 3971-3982
18. Funahashi T.F., Giannoni A.M., Depaoli S.F., Skarosi, and Davidson N.O. Tissue-specific, developmental and nutritional regulation of the gene encoding the catalytic subunit of the rat apoB mRNA editing enzyme: functional role in the modulation of apoB mRNA editing. J. Lipid Res. 36 (1995) 414-428
19. Demmer L.A., Levin M.S., Elovson J., Reuben M.A., Lusis A.J., and Gordon J.I. Tissue-specific expression and developmental regulation of the rat apolipoprotein B gene. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 8102-8106
20. Patterson A.P., Tennyson G.E., Hoeg J.M., Sviridov D.D., and Brewer Jr. H.B. Ontogenetic regulation of apolipoprotein B mRNA editing during human and rat development in vivo. Arterioscler. Thromb. 12 (1992) 468-473
21. Wu J.H., Semenkovish C.F., Chen S.-H., Li W.-H., and Chan L. Apolipoprotein B mRNA editing: validation of a sensitive assay and developmental biology of RNA editing in the rat. J. Biol. Chem. 265 (1990) 12312-12316
22. Huguchi K., Kitagawa K., Kogishi K., and Takeda T. Developmental and age-related changes in apoB mRNA editing in mice. J. Lipid Res. 33 (1992) 1753-1764
23. Jiao S., Moberly J.B., and Schonfeld G. Editing of apolipoprotein B messenger RNA in differentiated Caco-2 cells. J. Lipid Res. 31 (1990) 695-700
24. Von Wronski M.A., Hirano K.I., Cagen L.M., Wilcox H.G., Raghow R., Thorngate F.E., Heimberg M., Davidson N.O., and Elam M.B. Insulin increases expression of apobec-1, the catalytic subunit of the apolipoprotein B mRNA editing complex in rat hepatocytes. Metabolism 47 (1998) 869-873
25. Giangreco A., Sowden M.P., Mikityansky I., and Smith H.C. Ethanol stimulates apolipoprotein B mRNA editing in the absence of de novo RNA or protein synthesis. Biochem. Biophys. Res. Commun. 289 (2001) 1162-1167
26. Lehmann D.M., Galloway C.A., Sowden M.P., and Smith H.C. Metabolic regulation of apoB mRNA editing is associated with phosphorylation of APOBEC-1 complementation factor. Nucleic Acids Res. 34 (2006) 3299-3308
27. C.A. Galloway, M.P. Sowden, H.C. Smith, Increasing the yield of soluble recombinant protein expressed in E. coli by induction during late log phase, Biotechniques 34 (2003) 524-6, 528, 530.
28. Nakagawa Y., Irie K., Ohigashi H., Hayashi H., and Wender P.A. Synthesis and PKC isozyme surrogate binding of indothiolactam-V, a new thioamide analogue of tumor promoting indolactam-V. Bioorg. Med. Chem. Lett. 10 (2000) 2087-2090
29. Higashi K., Hoshino M., Nomura T., Saso K., Ito M., and Hoek J.B. Interaction of protein phosphatases and ethanol on phospholipase C-mediated intracellular signal transduction processes in rat hepatocytes: role of protein kinase A. Alcohol Clin. Exp. Res. 20 (1996) 320A-324A
30. Bouscarel B., Matsuzaki Y., Le M., Gettys T.W., and Fromm H. Changes in G protein expression account for impaired modulation of hepatic cAMP formation after BDL. Am. J. Physiol. 274 (1998) G1151-G1159
31. Liu H.X., Zhang M., and Krainer A.R. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev. 12 (1998) 1998-2012
32. Mehta A., and Driscoll D.M. Identification of domains in APOBEC-1 complementation factor required for RNA binding and apolipoprotein B mRNA editing. RNA 8 (2002) 69-82
33. Blanc V., Kennedy S., and Davidson N.O. A novel nuclear localization signal in the auxiliary domain of apobec-1 complementation factor regulates nucleocytoplasmic import and shuttling. J. Biol. Chem. 278 (2003) 41198-41204
34. Yang X., and Gabuzda D. Mitogen-activated protein kinase phosphorylates and regulates the HIV-1 Vif protein. J. Biol. Chem. 273 (1998) 29879-29887
35. Wang X., and Tanaka Hall T.M. Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat. Struct. Biol. 8 (2001) 141-145
36. Selenko P., Gregorovic G., Sprangers R., Stier G., Rhani Z., Kramer A., and Sattler M. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol. Cell 11 (2003) 965-976
37. Deo R.C., Bonanno J.B., Sonenberg N., and Burley S.K. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 98 (1999) 835-845
38. Handa N., Nureki O., Kurimoto K., Kim I., Sakamoto H., Shimura Y., Muto Y., and Yokoyama S. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398 (1999) 579-585
39. Backus J.W., and Smith H.C. Three distinct RNA sequence elements are required for efficient apolipoprotein B (apoB) RNA editing in vitro. Nucleic Acids Res. 20 (1992) 6007-6014
40. Mehta A., and Driscoll D.M. A sequence-specific RNA-binding protein complements apobec-1 To edit apolipoprotein B mRNA. Mol. Cell. Biol. 18 (1998) 4426-4432
41. Van Mater D., Sowden M.P., Cianci J., Sparks J.D., Sparks C.E., Ballatori N., and Smith H.C. Ethanol increases apolipoprotein B mRNA editing in rat primary hepatocytes and McArdle cells. Biochem. Biophys. Res. Commun. 252 (1998) 334-339
42. Lau P.P., Cahill D.J., Zhu H.J., and Chan L. Ethanol modulates apolipoprotein B mRNA editing in the rat. J. Lipid Res. 36 (1995) 2069-2078
43. Chen Z., Eggerman T.L., and Patterson A.P. Phosphorylation is a regulatory mechanism in apolipoprotein B mRNA editing. Biochem. J. 357 (2001) 661-672
44. Osada S., Mizuno K., Saido T.C., Suzuki K., Kuroki T., and Ohno S. A new member of the protein kinase C family, nPKC theta, predominantly expressed in skeletal muscle. Mol. Cell. Biol. 12 (1992) 3930-3938
45. Hoek J.B., and Kholodenko B.N. The intracellular signaling network as a target for ethanol. Alcohol Clin. Exp. Res. 22 (1998) 224S-230S
46. Newton A.C. Protein kinase C: structure, function, and regulation. J. Biol. Chem. 270 (1995) 28495-28498
47. Varani G., and Nagai K. RNA recognition by RNP proteins during RNA processing. Annu. Rev. Biophys. Biomol. Struct. 27 (1998) 407-445
48. Kielkopf C.L., Rodionova N.A., Green M.R., and Burley S.K. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell 106 (2001) 595-605
49. Price S.R., Evans P.R., and Nagai K. Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394 (1998) 645-650
50. Fribourg S., Gatfield D., Izaurralde E., and Conti E. A novel mode of RBD-protein recognition in the Y14-Mago complex. Nat. Struct. Biol. 10 (2003) 433-439
51. Kadlec J., Izaurralde E., and Cusack S. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nat. Struct. Mol. Biol. 11 (2004) 330-337
52. Tacke R., Chen Y., and Manley J.L. Sequence-specific RNA binding by an SR protein requires RS domain phosphorylation: creation of an SRp40-specific splicing enhancer. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 1148-1153
53. Xu Y. Regulation of p53 responses by post-translational modifications. Cell Death Differ. 10 (2003) 400-403
54. Radhakrishnan I., Perez-Alvarado G.C., Parker D., Dyson H.J., Montminy M.R., and Wright P.E. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell 91 (1997) 741-752
55. Keene J.D., and Tenenbaum S.A. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9 (2002) 1161-1167
56. Basu U., Si K., Deng H., and Maitra U. Phosphorylation of mammalian eukaryotic translation initiation factor 6 and its Saccharomyces cerevisiae homologue Tif6p: evidence that phosphorylation of Tif6p regulates its nucleocytoplasmic distribution and is required for yeast cell growth. Mol. Cell. Biol. 23 (2003) 6187-6199
57. Yun C.Y., Velazquez-Dones A.L., Lyman S.K., and Fu X.D. Phosphorylation-dependent and -independent nuclear import of RS domain-containing splicing factors and regulators. J. Biol. Chem. 278 (2003) 18050-18055
58. Jans D.A. The regulation of protein transport to the nucleus by phosphorylation. Biochem. J. 311 Pt 3 (1995) 705-716
59. W.L. Delano. DeLano Scientific LLC, San Carlos, CA, USA.