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PMID: 21822774 Published · ppublish English Journal Article

AAV8-mediated long-term expression of human LCAT significantly improves lipid profiles in hCETP;Ldlr(+/-) mice.

Journal of cardiovascular translational research ·Vol. 4 ·No. 6 ·2011-12-00 ·Pages 801-10

Chen Z, Chu D, Castro-Perez JM, Ni W, Zhang A, Krsmanovic ML, Xie D, Shah V, Stout SJ, McLaren DG, Stefanni AC, Lee SH, Roddy TP, Plump AS, Hubbard BK, Vogt TF, Zhou HH

Abstract

Lecithin:cholesterol acyltransferase (LCAT) is the key circulating enzyme responsible for high-density lipoprotein (HDL) cholesterol esterification, HDL maturation, and potentially reverse cholesterol transport. To further explore LCAT's mechanism of action on lipoprotein metabolism, we employed adeno-associated viral vector (AAV) serotype 8 to achieve long-term (32-week) high level expression of human LCAT in hCETP;Ldlr(+/-) mice, and characterized the lipid profiles in detail. The mice had a marked increase in HDL cholesterol, HDL particle size, and significant reduction in low-density lipoprotein (LDL) cholesterol, plasma triglycerides, and plasma apoB. Plasma LCAT activity significantly increased with humanized substrate specificity. HDL cholesteryl esters increased in a fashion that fits human LCAT specificity. HDL phosphatidylcholines trended toward decrease, with no change observed for HDL lysophosphatidylcholines. Triglycerides reduction appeared to reside in all lipoprotein particles (very low-density lipoprotein (VLDL), LDL, and HDL), with HDL triglycerides composition highly reflective of VLDL, suggesting that changes in HDL triglycerides were primarily driven by the altered triglycerides metabolism in VLDL. In summary, in this human-like model for lipoprotein metabolism, AAV8-mediated overexpression of human LCAT resulted in profound changes in plasma lipid profiles. Detailed lipid analyses in the lipoprotein particles suggest that LCAT's beneficial effect on lipid metabolism includes not only enhanced HDL cholesterol esterification but also improved metabolism of apoB-containing particles and triglycerides. Our findings thus shed new light on LCAT's mechanism of action and lend support to its therapeutic potential in treating dyslipidemia.

MeSH Terms
Animals Cholesterol Ester Transfer Proteins/genetics,metabolism Dependovirus/genetics Disease Models, Animal Dyslipidemias/enzymology,genetics,therapy Gene Transfer Techniques Genetic Therapy Genetic Vectors Humans Lipids/blood Liver/enzymology Male Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Particle Size Phosphatidylcholine-Sterol O-Acyltransferase/genetics,metabolism Receptors, LDL/deficiency,genetics Time Factors
Chemicals
CETP protein, human Cholesterol Ester Transfer Proteins Lipids Receptors, LDL Phosphatidylcholine-Sterol O-Acyltransferase
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Chen Zhu
Atherosclerosis, Cardiovascular Diseases, Merck Research Laboratories, RY80T-A100, 126 E. Lincoln Ave, Rahway, NJ 07065, USA. [email protected]
Chu Donald
Castro-Perez Jose M
Ni Weihua
Zhang Aiwu
Krsmanovic Mihajlo L
Xie Dan
Shah Vinit
Stout Steven J
McLaren David G
Stefanni Alice C
Lee Sang Ho
Roddy Thomas P
Plump Andrew S
Hubbard Brian K
Vogt Thomas F
Zhou Heather H
References (42)
42 references, click to expand
  1. HDL cholesterol and other lipids in coronary heart disease. The cooperative lipoprotein phenotyping study.
    Circulation. 1977 May;55(5):767-72 PMID: 191215
  2. High plasma HDL concentrations associated with enhanced atherosclerosis in transgenic mice overexpressing lecithin-cholesteryl acyltransferase.
    Nat Med. 1997 Jul;3(7):744-9 PMID: 9212100
  3. Statins, high-density lipoprotein cholesterol, and regression of coronary atherosclerosis.
    JAMA. 2007 Feb 7;297(5):499-508 PMID: 17284700
  4. Tailoring the AAV vector capsid for gene therapy.
    Gene Ther. 2009 Mar;16(3):311-9 PMID: 19052631
  5. Lecithin:cholesterol acyltransferase (LCAT) mass; its relationship to LCAT activity and cholesterol esterification rate.
    J Lipid Res. 1981 Nov;22(8):1206-13 PMID: 7320631
  6. The molecular pathology of lecithin:cholesterol acyltransferase (LCAT) deficiency syndromes.
    J Lipid Res. 1997 Feb;38(2):191-205 PMID: 9162740
  7. Origin and disappearance of plasma lecithin: cholesterol acyltransferase.
    Am J Physiol. 1971 Mar;220(3):735-41 PMID: 5545684
  8. Lipases and lecithin: cholesterol acyltransferase in the control of lipoprotein metabolism.
    Curr Opin Lipidol. 1995 Jun;6(3):130-5 PMID: 7648001
  9. Cholesteryl ester transfer protein corrects dysfunctional high density lipoproteins and reduces aortic atherosclerosis in lecithin cholesterol acyltransferase transgenic mice.
    J Biol Chem. 1999 Dec 24;274(52):36912-20 PMID: 10601244
  10. A new enzyme-linked immunosorbent assay with two monoclonal antibodies to specific epitopes measures human lecithin-cholesterol acyltransferase.
    J Lipid Res. 2002 Feb;43(2):325-34 PMID: 11861675
  11. HDL cholesterol and protective factors in atherosclerosis.
    Circulation. 2004 Jun 15;109(23 Suppl 1):III8-14 PMID: 15198960
  12. The molecular basis of lecithin:cholesterol acyltransferase deficiency syndromes: a comprehensive study of molecular and biochemical findings in 13 unrelated Italian families.
    Arterioscler Thromb Vasc Biol. 2005 Sep;25(9):1972-8 PMID: 15994445
  13. Characterization of proteoliposomes containing apoprotein A-I: a new substrate for the measurement of lecithin: cholesterol acyltransferase activity.
    J Lipid Res. 1982 Jul;23(5):680-91 PMID: 6811681
  14. Compromised LCAT function is associated with increased atherosclerosis.
    Circulation. 2005 Aug 9;112(6):879-84 PMID: 16061733
  15. Advances in understanding of the role of lecithin cholesterol acyltransferase (LCAT) in cholesterol transport.
    Clin Chim Acta. 1999 Aug;286(1-2):257-71 PMID: 10511297
  16. Widespread and stable pancreatic gene transfer by adeno-associated virus vectors via different routes.
    Diabetes. 2006 Apr;55(4):875-84 PMID: 16567506
  17. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11854-9 PMID: 12192090
  18. Familial lecithin:cholesterol acyltransferase deficiency--a clinical survey.
    Scand J Clin Lab Invest Suppl. 1974;137:73-82 PMID: 4367606
  19. Overexpression of human lecithin:cholesterol acyltransferase in cholesterol-fed rabbits: LDL metabolism and HDL metabolism are affected in a gene dose-dependent manner.
    J Lipid Res. 1997 Dec;38(12):2537-47 PMID: 9458277
  20. Genetic and phenotypic heterogeneity in familial lecithin: cholesterol acyltransferase (LCAT) deficiency. Six newly identified defective alleles further contribute to the structural heterogeneity in this disease.
    J Clin Invest. 1993 Feb;91(2):677-83 PMID: 8432868
  21. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8.
    Mol Ther. 2006 Jul;14(1):45-53 PMID: 16713360
  22. Plasma phospholipid transfer protein, cholesteryl ester transfer protein and lecithin:cholesterol acyltransferase in end-stage renal disease (ESRD).
    Nephrol Dial Transplant. 2009 Aug;24(8):2541-6 PMID: 19297356
  23. Fractionation of egg and soybean phosphatidylcholines by silver resin chromatography.
    J Chromatogr. 1991 Feb 1;538(2):469-73 PMID: 2016389
  24. Molecular physiology of reverse cholesterol transport.
    J Lipid Res. 1995 Feb;36(2):211-28 PMID: 7751809
  25. Plasma lipoproteins in familial lecithin: cholesterol acyltransferase deficiency: physical and chemical studies of low and high density lipoproteins.
    J Clin Invest. 1971 May;50(5):1131-40 PMID: 5552410
  26. The mechanism of the plasma cholesterol esterification reaction: plasma fatty acid transferase.
    Biochim Biophys Acta. 1962 Nov 19;65:128-35 PMID: 13948499
  27. Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates.
    Mol Ther. 2006 Jan;13(1):77-87 PMID: 16219492
  28. The plasma lecithins:cholesterol acyltransferase reaction.
    J Lipid Res. 1968 Mar;9(2):155-67 PMID: 4868699
  29. Markedly accelerated catabolism of apolipoprotein A-II (ApoA-II) and high density lipoproteins containing ApoA-II in classic lecithin: cholesterol acyltransferase deficiency and fish-eye disease.
    J Clin Invest. 1994 Jan;93(1):321-30 PMID: 8282802
  30. Comparative specificity of plasma lecithin:cholesterol acyltransferase from ten animal species.
    Lipids. 1991 Jun;26(6):416-20 PMID: 1881237
  31. Specificity of lecithin:cholesterol acyltransferase and atherogenic risk: comparative studies on the plasma composition and in vitro synthesis of cholesteryl esters in 14 vertebrate species.
    J Lipid Res. 1995 Aug;36(8):1813-24 PMID: 7595102
  32. High-density lipoproteins, cholesterol transport and coronary heart disease.
    Circulation. 1979 Jul;60(1):1-3 PMID: 221132
  33. Analysis of glomerulosclerosis and atherosclerosis in lecithin cholesterol acyltransferase-deficient mice.
    J Biol Chem. 2001 May 4;276(18):15090-8 PMID: 11278414
  34. Overexpression of lecithin:cholesterol acyltransferase in transgenic rabbits prevents diet-induced atherosclerosis.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11448-53 PMID: 8876155
  35. Adenoviral expression of human lecithin-cholesterol acyltransferase in nonhuman primates leads to an antiatherogenic lipoprotein phenotype by increasing high-density lipoprotein and lowering low-density lipoprotein.
    Metabolism. 2009 Apr;58(4):568-75 PMID: 19303980
  36. Familial lecithin:cholesterol acyltransferase deficiency. Studies on lipid composition and morphology of tissues.
    Scand J Clin Lab Invest Suppl. 1974;137:93-100 PMID: 4367608
  37. LCAT modulates atherogenic plasma lipoproteins and the extent of atherosclerosis only in the presence of normal LDL receptors in transgenic rabbits.
    Arterioscler Thromb Vasc Biol. 2000 Feb;20(2):450-8 PMID: 10669643
  38. Increased plasma HDL cholesterol levels and biliary cholesterol excretion in hamster by LCAT overexpression.
    FEBS Lett. 2004 Jul 16;570(1-3):25-9 PMID: 15251433
  39. Determination of the complete structure of natural lecithins.
    Lipids. 1967 May;2(3):217-24 PMID: 17805770
  40. Marked atherosclerosis in a patient with familiar lecithin: cholesterol acyltransferase deficiency associated with end-stage renal disease and diabetes mellitus.
    Am J Nephrol. 2001 Sep-Oct;21(5):415-9 PMID: 11684807
  41. Distribution and functions of lecithin:cholesterol acyltransferase and cholesteryl ester transfer protein in plasma lipoproteins. Evidence for a functional unit containing these activities together with apolipoproteins A-I and D that catalyzes the esterification and transfer of cell-derived cholesterol.
    J Biol Chem. 1989 Apr 25;264(12):7066-72 PMID: 2496125
  42. Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice.
    J Virol. 2005 Jan;79(1):214-24 PMID: 15596817
Article Info
Journal
Journal of cardiovascular translational research
Abbr.
J Cardiovasc Transl Res
ISSN
1937-5395
Published
2011-12-00
Epub
2011-00-06
Pages
801-10
Language
English
Region
United States
NLM ID
101468585
Subset
IM
Analysis Services
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