Home LiteratureArticle Details
PMID: 12374571 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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.

The Biochemical journal ·Vol. 369 ·No. Pt 2 ·2003-01-15 ·Pages 255-62

Hersberger M, Patarroyo-White S, Qian X, Arnold KS, Rohrer L, Balestra ME, Innerarity TL

Abstract

Apolipoprotein (apo) B mRNA editing is the deamination of C(6666) to uridine, which results in translation of the apoB-48 protein instead of the genomically encoded apoB-100. ApoB-48-containing lipoproteins are cleared more rapidly from plasma and are less atherogenic than apoB-100-containing low-density lipoproteins (LDLs). In humans, the intestine predominantly produces apoB-48 whereas the liver secretes apoB-100 only. To evaluate a potential therapeutic use for liver-induced apoB mRNA editing in humans, we investigated the efficiency and safety of transgenic expression of apoB mRNA-editing enzyme catalytic polypeptide 1 (APOBEC-1) in the absence of endogenous editing in the mouse model. Here we show that regulatable tetO-mediated APOBEC-1 expression in the livers of gene-targeted mice lacking endogenous APOBEC-1 results in 30% apoB mRNA editing. In a time-course experiment, the expression of tetO-APOBEC-1 mRNA was suppressed within 2 days after mice were fed doxycycline and apoB mRNA editing and apoB-48 formation were suppressed within 4 days. However, tetO-APOBEC-1 expression resulted in regulatable aberrant hyperediting of several cytidines downstream of C(6666) in apoB mRNA and in novel APOBEC-1 target 1 (NAT1) mRNA. Several of the cytidines in apoB mRNA were hyperedited to a level similar to that of C(6666), although editing at C(6666) was lower than that in wild-type mice. These results demonstrate that even moderate APOBEC-1 expression can lead to hyperediting, limiting the single-gene approach for gene therapy with APOBEC-1.

MeSH Terms
APOBEC-1 Deaminase Animals Apolipoproteins B/genetics,metabolism Cholesterol, LDL/blood Cytidine Deaminase/genetics,metabolism Down-Regulation/physiology Gene Expression Regulation, Enzymologic Humans Liver/physiology Mice Mice, Transgenic RNA Editing Rabbits Transgenes Triglycerides/blood
Chemicals
Apolipoproteins B Cholesterol, LDL Triglycerides APOBEC-1 Deaminase APOBEC1 protein, human Apobec1 protein, mouse Cytidine Deaminase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hersberger Martin
Gladstone Institute of Cardiovascular Disease, University of California, Building 40, Third Floor, P.O. Box 419100, 2550 23rd Street, San Francisco, CA 94141-9100, U.S.A. hmr@kc.unizh.ch
Patarroyo-White Susannah
Qian Xiaobing
Arnold Kay S
Rohrer Lucia
Balestra Maureen E
Innerarity Thomas L
References (55)
55 references, click to expand
  1. Site-specific creation of uridine from cytidine in apolipoprotein B mRNA editing.
    Nucleic Acids Res. 1991 Mar 25;19(6):1197-201 PMID: 2030940
  2. 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 Feb 1;11(3):321-33 PMID: 9030685
  3. The functional characteristics of a human apolipoprotein E variant (cysteine at residue 142) may explain its association with dominant expression of type III hyperlipoproteinemia.
    J Biol Chem. 1992 Jan 25;267(3):1962-8 PMID: 1730728
  4. In vitro apolipoprotein B mRNA editing activity can be modulated by fasting and refeeding rats with a high carbohydrate diet.
    Biochem Biophys Res Commun. 1992 Mar 16;183(2):899-903 PMID: 1550595
  5. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5547-51 PMID: 1319065
  6. Phylogenetic analysis of the apolipoprotein B mRNA-editing region. Evidence for a secondary structure between the mooring sequence and the 3' efficiency element.
    J Biol Chem. 1999 Dec 3;274(49):34590-7 PMID: 10574922
  7. Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA.
    Mol Cell Biol. 2000 Mar;20(5):1846-54 PMID: 10669759
  8. Purification and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex.
    J Biol Chem. 2000 Jun 30;275(26):19848-56 PMID: 10781591
  9. Induction of cytidine to uridine editing on cytoplasmic apolipoprotein B mRNA by overexpressing APOBEC-1.
    J Biol Chem. 2000 Jul 28;275(30):22663-9 PMID: 10833526
  10. The effect of tetracycline on the hepatic secretion of triglyceride.
    Biochim Biophys Acta. 1972 May 23;270(1):74-80 PMID: 4338742
  11. Enhanced binding by cultured human fibroblasts of apo-E-containing lipoproteins as compared with low density lipoproteins.
    Biochemistry. 1978 Apr 18;17(8):1440-7 PMID: 206278
  12. Cell surface receptor binding of phospholipid . protein complexes containing different ratios of receptor-active and -inactive E apoprotein.
    J Biol Chem. 1980 Jun 10;255(11):5454-60 PMID: 7372644
  13. Role of sex and age in the tetracycline-induced hepatic steatosis. I. Comparative study on the effect of rolitetracycline on some parameters of hepatic lipid metabolism in male and female mice.
    Toxicol Appl Pharmacol. 1980 Jul;54(3):508-13 PMID: 7394802
  14. Comparative evaluation of the effects of tetracycline and doxycycline on blood and liver lipids on male and female mice.
    Arzneimittelforschung. 1981;31(12):2118-20 PMID: 7199310
  15. Apolipoprotein B synthesis by human liver and intestine in vitro.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5296-300 PMID: 3460091
  16. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine.
    Cell. 1987 Sep 11;50(6):831-40 PMID: 3621347
  17. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon.
    Science. 1987 Oct 16;238(4825):363-6 PMID: 3659919
  18. Apolipoprotein gene expression in the rat is regulated in a tissue-specific manner by thyroid hormone.
    J Lipid Res. 1988 Nov;29(11):1511-22 PMID: 3149287
  19. Apolipoprotein B messenger RNA editing in the rat liver. Modulation by fasting and refeeding a high carbohydrate diet.
    J Biol Chem. 1990 Nov 5;265(31):19263-70 PMID: 2229075
  20. Fasting decreases apolipoprotein B mRNA editing and the secretion of small molecular weight apoB by rat hepatocytes: evidence that the total amount of apoB secreted is regulated post-transcriptionally.
    J Lipid Res. 1990 Sep;31(9):1663-8 PMID: 1701004
  21. Apolipoprotein B mRNA editing. Direct determination of the edited base and occurrence in non-apolipoprotein B-producing cell lines.
    J Biol Chem. 1990 Dec 25;265(36):22446-52 PMID: 2266136
  22. Apolipoprotein B mRNA editing is associated with UV crosslinking of proteins to the editing site.
    Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):222-6 PMID: 8419928
  23. Molecular cloning of an apolipoprotein B messenger RNA editing protein.
    Science. 1993 Jun 18;260(5115):1816-9 PMID: 8511591
  24. The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase.
    J Biol Chem. 1993 Oct 5;268(28):20709-12 PMID: 8407891
  25. The mechanism for apo-B mRNA editing is deamination.
    Biochem Biophys Res Commun. 1993 Sep 30;195(3):1204-10 PMID: 8216250
  26. Cloning and mutagenesis of the rabbit ApoB mRNA editing protein. A zinc motif is essential for catalytic activity, and noncatalytic auxiliary factor(s) of the editing complex are widely distributed.
    J Biol Chem. 1994 Aug 26;269(34):21725-34 PMID: 8063816
  27. Overexpression of hepatic lipase in transgenic rabbits leads to a marked reduction of plasma high density lipoproteins and intermediate density lipoproteins.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8724-8 PMID: 8078949
  28. Adenovirus-mediated gene transfer of rat apolipoprotein B mRNA-editing protein in mice virtually eliminates apolipoprotein B-100 and normal low density lipoprotein production.
    J Biol Chem. 1994 Nov 25;269(47):29395-404 PMID: 7961918
  29. Transcriptional activation by tetracyclines in mammalian cells.
    Science. 1995 Jun 23;268(5218):1766-9 PMID: 7792603
  30. Apolipoprotein B mRNA-editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8483-7 PMID: 7667315
  31. Proposed nomenclature for the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme: APOBEC-1.
    RNA. 1995 Mar;1(1):3 PMID: 7489485
  32. Ethanol modulates apolipoprotein B mRNA editing in the rat.
    J Lipid Res. 1995 Oct;36(10):2069-78 PMID: 8576634
  33. Biosynthesis of apolipoprotein B48-containing lipoproteins. Regulation by novel post-transcriptional mechanisms.
    J Biol Chem. 1996 Feb 2;271(5):2353-6 PMID: 8576187
  34. An auxiliary factor containing a 240-kDa protein complex is involved in apolipoprotein B RNA editing.
    Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1097-102 PMID: 8577721
  35. 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 May 10;271(19):11506-10 PMID: 8626710
  36. Apobec-1 and apolipoprotein B mRNA editing.
    Biochim Biophys Acta. 1997 Mar 10;1345(1):11-26 PMID: 9084497
  37. Effective lowering of plasma, LDL, and esterified cholesterol in LDL receptor-knockout mice by adenovirus-mediated gene delivery of ApoB mRNA editing enzyme (Apobec1).
    Arterioscler Thromb Vasc Biol. 1997 May;17(5):889-97 PMID: 9157952
  38. Partial characterization of the auxiliary factors involved in apolipoprotein B mRNA editing through APOBEC-1 affinity chromatography.
    J Biol Chem. 1997 Oct 31;272(44):27700-6 PMID: 9346911
  39. Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100.
    J Clin Invest. 1998 Mar 1;101(5):1084-93 PMID: 9486979
  40. 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 Apr 1;26(7):1644-52 PMID: 9512534
  41. Two efficiency elements flanking the editing site of cytidine 6666 in the apolipoprotein B mRNA support mooring-dependent editing.
    J Biol Chem. 1998 Apr 17;273(16):9435-42 PMID: 9545269
  42. Low expression of the apolipoprotein B mRNA-editing transgene in mice reduces LDL levels but does not cause liver dysplasia or tumors.
    Arterioscler Thromb Vasc Biol. 1998 Jun;18(6):1013-20 PMID: 9633945
  43. Inhibition of the apolipoprotein B mRNA editing enzyme-complex by hnRNP C1 protein and 40S hnRNP complexes.
    Biol Chem. 1998 Aug-Sep;379(8-9):1063-73 PMID: 9792439
  44. Lipoprotein clearance mechanisms in LDL receptor-deficient "Apo-B48-only" and "Apo-B100-only" mice.
    J Clin Invest. 1998 Oct 15;102(8):1559-68 PMID: 9788969
  45. Secondary structure for the apolipoprotein B mRNA editing site. Au-binding proteins interact with a stem loop.
    J Biol Chem. 1998 Nov 27;273(48):31707-17 PMID: 9822632
  46. Disproportionate relationship between APOBEC-1 expression and apolipoprotein B mRNA editing activity.
    Exp Cell Res. 1999 Oct 10;252(1):154-64 PMID: 10502408
  47. Targeted disruption of the mouse apobec-1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48.
    J Biol Chem. 1996 Apr 26;271(17):9887-90 PMID: 8626621
  48. Overexpression of APOBEC-1 results in mooring sequence-dependent promiscuous RNA editing.
    J Biol Chem. 1996 Feb 9;271(6):3011-7 PMID: 8621694
  49. A novel function for apolipoprotein B: lipoprotein synthesis in the yolk sac is critical for maternal-fetal lipid transport in mice.
    J Lipid Res. 1996 Feb;37(2):347-60 PMID: 9026532
  50. Hepatic expression of the catalytic subunit of the apolipoprotein B mRNA editing enzyme (apobec-1) ameliorates hypercholesterolemia in LDL receptor-deficient rabbits.
    Hum Gene Ther. 1996 May 20;7(8):943-57 PMID: 8727508
  51. Gene transfer of cytidine deaminase apoBEC-1 lowers lipoprotein(a) in transgenic mice and induces apolipoprotein B editing in rabbits.
    Hum Gene Ther. 1996 Jan;7(1):39-49 PMID: 8825867
  52. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10933-8 PMID: 8855286
  53. A plasmid rescue to investigate mutagenesis in transgenic D. melanogaster.
    Mutat Res. 1996 Dec 12;361(2-3):165-72 PMID: 8980702
  54. Cloning of an Apobec-1-binding protein that also interacts with apolipoprotein B mRNA and evidence for its involvement in RNA editing.
    J Biol Chem. 1997 Jan 17;272(3):1452-5 PMID: 8999813
  55. Apolipoprotein B mRNA editing is an intranuclear event that occurs posttranscriptionally coincident with splicing and polyadenylation.
    J Biol Chem. 1991 Oct 25;266(30):20550-4 PMID: 1939106
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2003-01-15
Pages
255-62
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1223090
Subset
IM
Grants
NHLBI NIH HHS · HL 47660 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com