Metabolic regulation of APOBEC-1 Complementation Factor trafficking in mouse models of obesity and its positive correlation with the expression of ApoB protein in hepatocytes

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1802, Issue 11, 2010, Pages 976-985

  Galloway, Chad A ^a   Ashton, John ^a   Sparks, Janet D ^a   Mooney, Robert A ^a   Smith, Harold C ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

APOBEC 1 Complementation Factor; Apolipoprotein B; Diabetes; Insulin resistance; MRNA editing

Indexed keywords

APOBEC 1 COMPLEMENTATION FACTOR; APOLIPOPROTEIN B; LEPTIN; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DYSLIPIDEMIA; ENDOSOME; HYPERINSULINEMIA; INSULIN RESISTANCE; LIPOPROTEIN SECRETION; LIVER CELL; MALE; METABOLIC REGULATION; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA INTERFERENCE;

ANIMALS; APOLIPOPROTEINS B; BLOTTING, WESTERN; CELLS, CULTURED; CYTIDINE DEAMINASE; CYTOPLASM; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HEPATOCYTES; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; OBESITY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA EDITING; RNA INTERFERENCE; RNA, MESSENGER;

ANIMALIA; MUS;

EID: 77956648554     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.06.003     Document Type: Article

References (59)

1. Burd C.G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science 1994, 265:615-621.
2. Brennan C.M., Steitz J.A. HuR and mRNA stability. Cell. Mol. Life Sci. 2001, 58:266-277.
3. 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.
4. Backus J.W., Smith H.C. Three distinct RNA sequence elements are required for efficient apolipoprotein B (apoB) RNA editing in vitro. Nucleic Acids Res. 1992, 20:6007-6014.
5. Backus J.W., Smith H.C. Specific 3' sequences flanking a minimal apolipoprotein B (apoB) mRNA editing 'cassette' are critical for efficient editing in vitro. Biochim. Biophys. Acta 1994, 1217:65-73.
6. Mehta A., Banerjee S., Driscoll D.M. Apobec-1 interacts with a 65-kDa complementing protein to edit apolipoprotein-B mRNA in vitro. J. Biol. Chem. 1996, 271:28294-28299.
7. Lellek H., Kirsten R., Diehl I., Apostel F., Buck F., Greeve J. Purification and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex. J. Biol. Chem. 2000, 275:19848-19856.
8. Teng B., Burant C.F., Davidson N.O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 1993, 260:1816-1819.
9. 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 1987, 238:363-366.
10. 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.
11. Funahashi T.F., Giannoni A.M., DePaoli S.F., Skarosi, 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. 1995, 36:414-428.
12. Mukhopadhyay D., Plateroti M., Anant S., Nassir F., Samarut J., Davidson N.O. Thyroid hormone regulates hepatic triglyceride mobilization and apolipoprotein B messenger ribonucleic acid editing in a murine model of congenital hypothyroidism. Endocrinology 2003, 144:711-719.
13. Chen Z., Eggerman T.L., Potosky D., Arborati M., Patterson A.P. Calcium increases apolipoprotein B mRNA editing. Biochem. Biophys. Res. Commun. 2000, 277:221-227.
14. Van Mater D., Sowden M.P., Cianci J., Sparks J.D., Sparks C.E., Ballatori N., Smith H.C. Ethanol increases apolipoprotein B mRNA editing in rat primary hepatocytes and McArdle cells. Biochem. Biophys. Res. Commun. 1998, 252:334-339.
15. von Wronski M.A., Hirano K.I., Cagen L.M., Wilcox H.G., Raghow R., Thorngate F.E., Heimberg M., Davidson N.O., Elam M.B. Insulin increases expression of apobec-1, the catalytic subunit of the apolipoprotein B mRNA editing complex in rat hepatocytes. Metabolism 1998, 47:869-873.
16. Lau P.P., Cahill D.J., Zhu H.J., Chan L. Ethanol modulates apolipoprotein B mRNA editing in the rat. J. Lipid Res. 1995, 36:2069-2078.
17. 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.
18. Baum C.L., Teng B.B., Davidson N.O. Apolipoprotein B messenger RNA editing in the rat liver. Modulation by fasting and refeeding a high carbohydrate diet. J. Biol. Chem. 1990, 265:19263-19270.
19. 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.
20. Blanc V., Henderson J.O., Newberry E.P., Kennedy S., Luo J., Davidson N.O. Targeted deletion of the murine apobec-1 complementation factor (acf) gene results in embryonic lethality. Mol. Cell. Biol. 2005, 25:7260-7269.
21. Farese R.V., Ruland S.L., Flynn L.M., Stokowski R.P., Young S.G. Knockout of the mouse apolipoprotein B gene results in embryonic lethality in homozygotes and protection against diet-induced hypercholesterolemia in heterozygotes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1774-1778.
22. Fine-Tuning of RNA Functions by Modification and Editing 2005, Springer-Verlag, Heidelberg. H. Grosjean (Ed.).
23. 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.
24. 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.
25. 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.
26. Blanc V., Kennedy S., 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. 2003, 278:41198-41204.
27. 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.
28. 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.
29. Chester A., Somasekaram A., Tzimina M., Jarmuz A., Gisbourne J., O'Keefe R., Scott J., Navaratnam N. The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay. EMBO J. 2003, 22:3971-3982.
30. Smith H.C. Analysis of protein complexes assembled on apolipoprotein B mRNA for mooring sequence-dependent RNA editing. Methods 1998, 15:27-39.
31. Phung T.L., Roncone A., Jensen K.L., Sparks C.E., Sparks J.D. Phosphoinositide 3-kinase activity is necessary for insulin-dependent inhibition of apolipoprotein B secretion by rat hepatocytes and localizes to the endoplasmic reticulum. J. Biol. Chem. 1997, 272:30693-30702.
32. Sparks J.D., Bolognino M., Trax P.A., Sparks C.E. The production and utility of monoclonal antibodies to rat apolipoprotein B lipoproteins. Atherosclerosis 1986, 61:205-211.
33. Backus J.W., Eagleton M.J., Harris S.G., Sparks C.E., Sparks J.D., Smith H.C. Quantitation of endogenous liver apolipoprotein B mRNA editing. Biochem. Biophys. Res. Commun. 1990, 170:513-518.
34. Gomez-Lechon M.J., Donato M.T., Martinez-Romero A., Jimenez N., Castell J.V., O'Connor J.E. A human hepatocellular in vitro model to investigate steatosis. Chem. Biol. Interact. 2007, 165:106-116.
35. Paddison P.J., Caudy A.A., Sachidanandam R., Hannon G.J. Short hairpin activated gene silencing in mammalian cells. Methods Mol. Biol. 2004, 265:85-100.
36. Ro S., Hwang S.J., Ordog T., Sanders K.M. Adenovirus-based short hairpin RNA vectors containing an EGFP marker and mouse U6, human H1, or human U6 promoter. Biotechniques 2005, 38:625-627.
37. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.
38. Anant S., Henderson J.O., Mukhopadhyay D., Navaratnam N., Kennedy S., Min J., Davidson N.O. Novel role for RNA-binding protein CUGBP2 in mammalian RNA editing. J. Biol. Chem. 2001, 276:47338-47351.
39. Lau P.P., Chang B.H., Chan L. Two-hybrid cloning identifies an RNA-binding protein, GRY-RBP, as a component of apobec-1 editosome. Biochem. Biophys. Res. Commun. 2001, 282:977-983.
40. Blanc V., Navaratnam N., Henderson J.O., Anant S., Kennedy S., Jarmuz A., Scott J., Davidson N.O. 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. 2001, 276:10272-10283.
41. Tilg H., Moschen A.R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 2006, 6:772-783.
42. Uygun A., Kadayifci A., Yesilova Z., Erdil A., Yaman H., Saka M., Deveci M.S., Bagci S., Gulsen M., Karaeren N., Dagalp K. Serum leptin levels in patients with nonalcoholic steatohepatitis. Am. J. Gastroenterol. 2000, 95:3584-3589.
43. Yagmur E., Trautwein C., Gressner A.M., Tacke F. Resistin serum levels are associated with insulin resistance, disease severity, clinical complications, and prognosis in patients with chronic liver diseases. Am. J. Gastroenterol. 2006, 101:1244-1252.
44. Araya J., Rodrigo R., Videla L.A., Thielemann L., Orellana M., Pettinelli P., Poniachik J. Increase in long-chain polyunsaturated fatty acid n-6/n-3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin. Sci. (Lond.) 2004, 106:635-643.
45. Chen H., Charlat O., Tartaglia L.A., Woolf E.A., Weng X., Ellis S.J., Lakey N.D., Culpepper J., Moore K.J., Breitbart R.E., Duyk G.M., Tepper R.I., Morgenstern J.P. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996, 84:491-495.
46. Sahai A., Malladi P., Pan X., Paul R., Melin-Aldana H., Green R.M., Whitington P.F. Obese and diabetic db/db mice develop marked liver fibrosis in a model of nonalcoholic steatohepatitis: role of short-form leptin receptors and osteopontin. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G1035-G1043.
47. Thorngate F.E., Raghow R., Wilcox H.G., Werner C.S., Heimberg M., Elam M.B. Insulin promotes the biosynthesis and secretion of apolipoprotein B-48 by altering apolipoprotein B mRNA editing. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:5392-5396.
48. Baetens D., Stefan Y., Ravazzola M., Malaisse-Lagae F., Coleman D.L., Orci L. Alteration of islet cell populations in spontaneously diabetic mice. Diabetes 1978, 27:1-7.
49. Greeve J., Altkemper I., Dieterich J.H., Greten H., 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. 1993, 34:1367-1383.
50. 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.
51. Gibbons G.F., Wiggins D., Brown A.M., Hebbachi A.M. Synthesis and function of hepatic very-low-density lipoprotein. Biochem. Soc. Trans. 2004, 32:59-64.
52. Fu T., Mukhopadhyay D., Davidson N.O., Borensztajn J. The peroxisome proliferator-activated receptor alpha (PPARalpha) agonist ciprofibrate inhibits apolipoprotein B mRNA editing in low density lipoprotein receptor-deficient mice: effects on plasma lipoproteins and the development of atherosclerotic lesions. J. Biol. Chem. 2004, 279:28662-28669.
53. Lee G.H., Proenca R., Montez J.M., Carroll K.M., Darvishzadeh J.G., Lee J.I., Friedman J.M. Abnormal splicing of the leptin receptor in diabetic mice. Nature 1996, 379:632-635.
54. Tartaglia L.A., Dembski M., Weng X., Deng N., Culpepper J., Devos R., Richards G.J., Campfield L.A., Clark F.T., Deeds J., Muir C., Sanker S., Moriarty A., Moore K.J., Smutko J.S., Mays G.G., Wool E.A., Monroe C.A., Tepper R.I. Identification and expression cloning of a leptin receptor, OB-R. Cell 1995, 83:1263-1271.
55. Yamashita T., Murakami T., Otani S., Kuwajima M., Shima K. Leptin receptor signal transduction: OBRa and OBRb of fa type. Biochem. Biophys. Res. Commun. 1998, 246:752-759.
56. Murakami T., Yamashita T., Iida M., Kuwajima M., Shima K. A short form of leptin receptor performs signal transduction. Biochem. Biophys. Res. Commun. 1997, 231:26-29.
57. Allister E.M., Borradaile N.M., Edwards J.Y., Huff M.W. Inhibition of microsomal triglyceride transfer protein expression and apolipoprotein b100 secretion by the citrus flavonoid naringenin and by insulin involves activation of the mitogen-activated protein kinase pathway in hepatocytes. Diabetes 2005, 54:1676-1683.
58. Liao W., Hui T.Y., Young S.G., Davis R.A. Blocking microsomal triglyceride transfer protein interferes with apoB secretion without causing retention or stress in the ER. J. Lipid Res. 2003, 44:978-985.
59. Graham J.M. Fractionation of a microsomal fraction from rat liver or cultured cells. Methods Mol. Biol. 1993, 19:51-57.