The role of lecithin:cholesterol acyltransferase in the modulation of cardiometabolic risks - A clinical update and emerging insights from animal models

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 4, 2012, Pages 654-659

  Ng, Dominic S ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Atherosclerosis; Brown adipose tissue; ER stress; High density lipoproteins; Insulin resistance; Lecithin cholesterol acyltransferase (LCAT)

Indexed keywords

HIGH DENSITY LIPOPROTEIN; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; TRIACYLGLYCEROL;

ANIMAL MODEL; ATHEROGENESIS; ATHEROSCLEROSIS; CARDIOMETABOLIC RISK; CARDIOVASCULAR RISK; CHOLESTEROL ESTERIFICATION; CHOLESTEROL TRANSPORT; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; EXPERIMENTAL MODEL; GLUCOSE METABOLISM; HETEROZYGOTE; HUMAN; HYPOALPHALIPOPROTEINEMIA; INSULIN RESISTANCE; LECITHIN CHOLESTEROL ACYLTRANSFERASE DEFICIENCY; LIPID METABOLISM; LIPOPROTEIN METABOLISM; LOSS OF FUNCTION MUTATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION;

ANIMALS; ATHEROSCLEROSIS; CHOLESTEROL; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; HUMANS; INSULIN RESISTANCE; LECITHIN ACYLTRANSFERASE DEFICIENCY; LIPOPROTEINS, HDL; MICE; OBESITY; PHOSPHATIDYLCHOLINE-STEROL O-ACYLTRANSFERASE;

ANIMALIA;

EID: 84857662249     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2011.12.012     Document Type: Review

References (57)

1. J.A. Kuivenhoven, E.J. van Voorst tot Voorst, H. Wiebusch, S.M. Wiebusch, S.M. Marcovina, H. Funke, G. Assmann, and P.H. Pritchard A unique genetic and biochemical presentation of fish-eye disease J. Clin. Invest. 96 1995 2783 2791
2. J.A. Kuivenhoven, P. Pritchard, J. Hill, J. Frohlich, G. Assmann, and J. Kastelein The molecular pathology of lecithin:cholesterol acyltransferase (LCAT) deficiency syndromes J. Lipid Res. 38 1997 191 205 (Pubitemid 27118033)
3. J.A. Glomset, G. Assmann, E. Gjone, and K.R. Norum Lecithin:cholesterol acyltransferase deficiency and fish eye disease C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, The Metabolic and Molecular Bases of Inherited Disease 1995 McGraw-Hill New York 1933 1951
4. C.H. Chen, and J.J. Albers Distribution of lecithin-cholesterol acyltransferase (LCAT) in human plasma lipoprotein fractions. Evidence for the association of active LCAT with low density lipoproteins Biochem. Biophys. Res. Commun. 107 1982 1091 1096 (Pubitemid 13207691)
5. A. Jonas Lecithin cholesterol acyltransferase Biochim. Biophys. Acta 1529 2000 245 256
6. K. O, J.S. Hill, X. Wang, and P.H. Pritchard Recombinant lecithin:cholesterol acyltransferase containing a Thr123 - >Ile mutation esterifies cholesterol in low density lipoprotein but not in high density lipoprotein J. Lipid Res. 34 1993 81 88 (Pubitemid 23016623)
7. A. von Eckardstein, Y. Huang, S. Wu, H. Funke, G. Noseda, and G. Assmann Reverse cholesterol transport in plasma of patients with different forms of familial HDL deficiency Arterioscler. Thromb. Vasc. Biol. 15 1995 691 703
8. T. Forte, A. Nichols, J. Glomset, and K. Norum The ultrastructure of plasma lipoproteins in lecithin:cholesterol acyltransferase deficiency Scand. J. Clin. Lab. Invest. Suppl. 137 1974 121 132
9. D.S. Ng, O.L. Francone, T.M. Forte, J. Zhang, M. Haghpassand, and E.M. Rubin Disruption of the murine lecithin:cholesterol acyltransferase gene causes impairment of adrenal lipid delivery and up-regulation of scavenger receptor class B type I J. Biol. Chem. 272 1997 15777 15781 (Pubitemid 27265554)
10. S. Narayanan Biochemistry and clinical relevance of lipoprotein X Ann. Clin. Lab. Sci. 14 1984 371 374 (Pubitemid 14062983)
11. X. Zhu, A.M. Herzenberg, M. Eskandarian, G.F. Maguire, J.W. Scholey, P.W. Connelly, and D.S. Ng A novel in vivo lecithin-cholesterol acyltransferase (LCAT)-deficient mouse expressing predominantly LpX is associated with spontaneous glomerulopathy Am. J. Pathol. 165 2004 1269 1278 (Pubitemid 39297732)
12. S. Jimi, N. Uesugi, K. Saku, H. Itabe, B. Zhang, K. Arakawa, and S. Takebayashi Possible induction of renal dysfunction in patients with lecithin:cholesterol acyltransferase deficiency by oxidized phosphatidylcholine in glomeruli Arterioscler. Thromb. Vasc. Biol. 19 1999 794 801 (Pubitemid 29135186)
13. H. Itabe, R. Hosoya, K. Karasawa, S. Jimi, K. Saku, S. Takebayashi, T. Imanaka, and T. Takano Metabolism of oxidized phosphatidylcholines formed in oxidized low density lipoprotein by lecithin-cholesterol acyltransferase J. Biochem. 126 1999 153 161 (Pubitemid 29355405)
14. V.S. Subramanian, J. Goyal, M. Miwa, J. Sugatami, M. Akiyama, M. Liu, and P.V. Subbaiah Role of lecithin-cholesterol acyltransferase in the metabolism of oxidized phospholipids in plasma: studies with platelet-activating factor-acetyl hydrolase-deficient plasma Biochim. Biophys. Acta 1439 1999 95 109 (Pubitemid 29296867)
15. L.A. Carlson, and L. Holmquist Evidence for deficiency of high density lipoprotein lecithin:cholesterol acyltransferase activity (alpha-LCAT) in fish eye disease Acta Med. Scand. 218 1985 189 196 (Pubitemid 16240417)
16. A.F. Ayyobi, S.H. McGladdery, S. Chan, G.B. John Mancini, J.S. Hill, and J.J. Frohlich Lecithin: cholesterol acyltransferase (LCAT) deficiency and risk of vascular disease: 25 year follow-up Atherosclerosis 177 2004 361 366 (Pubitemid 39505269)
17. G.K. Hovingh, B.A. Hutten, A.G. Holleboom, W. Petersen, P. Rol, A. Stalenhoef, A.H. Zwinderman, E. de Groot, J.J. Kastelein, and J.A. Kuivenhoven Compromised LCAT function is associated with increased atherosclerosis Circulation 112 2005 879 884 (Pubitemid 41170075)
18. L. Calabresi, D. Baldassarre, S. Castelnuovo, P. Conca, L. Bocchi, C. Candini, B. Frigerio, M. Amato, C.R. Sirtori, P. Alessandrini, M. Arca, G. Boscutti, L. Cattin, L. Gesualdo, T.G. Sampietro, G. Vaudo, F. Veglia, S. Calandra, and G. Franceschini Functional lecithin: cholesterol acyltransferase is not required for efficient atheroprotection in humans Circulation 120 2009 628 635
19. R. Duivenvoorden, A.G. Holleboom, B. van den Bogaard, A.J. Nederveen, E. de Groot, B.A. Hutten, A.W. Schimmel, G.K. Hovingh, J.J. Kastelein, J.A. Kuivenhoven, and E.S. Stroes Carriers of lecithin.cholesterol acyltransferase gene mutations have accelerated atherogenesis as assessed by carotid 3.0-T magnetic resonance imaging carriers of lecithin J. Am. Coll. Cardiol. 58 2011 2481 2487
20. A.G. Holleboom, J.A. Kuivenhoven, M. Vergeer, G.K. Hovingh, J.N. van Miert, N.J. Wareham, J.J. Kastelein, K.T. Khaw, and S.M. Boekhold Plasma levels of lecithin:cholesterol acyltransferase and risk of future coronary artery disease in apparently healthy men and women: a prospective case-control analysis nested in the EPIC-Norfolk population study J. Lipid Res. 51 2010 416 421
21. R.P. Dullaart, F. Perton, W.J. Sluiter, R. de Vries, and A. van Tol Plasma lecithin: cholesterol acyltransferase activity is elevated in metabolic syndrome and is an independent marker of increased carotid artery intima media thickness J. Clin. Endocrinol. Metab. 93 2008 4860 4866
22. R.P. Dullaart, F. Perton, M.W. van der Klauw, H.L. Hillege, and W.J. Sluiter High plasma lecithin:cholesterol acyltransferase activity does not predict low incidence of cardiovascular events: possible attenuation of cardioprotection associated with high HDL cholesterol Atherosclerosis 208 2010 537 542
23. L. Calabresi, D. Baldassarre, S. Simonelli, M. Gomaraschi, M. Amato, S. Castelnuovo, B. Frigerio, A. Ravasi, D. Sansaro, J. Kauhanen, R. Rauramaa, U. de Faire, A. Hamsten, A.J. Smit, E. Mannarino, S.E. Humphries, P. Giral, F. Veglia, C.R. Sirtori, G. Franceschini, and E. Tremoli Plasma lecithin:cholesterol acyltransferase (LCAT) and carotid intima-media thickness in European individuals at high cardiovascular risk J. Lipid Res. 52 2011 1569 1574
24. J.M. Hoeg, S. Santamarina-Fojo, A.M. Bérard, J.F. Cornhill, E.E. Herderick, S.H. Feldman, C.C. Haudenschild, B.L. Vaisman, R.F. Hoyt Jr., S.J. Demosky Jr., R.D. Kauffman, C.M. Hazel, S.M. Marcovina, and H.B. Brewer Jr. Overexpression of lecithin:cholesterol acyltransferase in transgenic rabbits prevents diet-induced atherosclerosis Proc. Natl. Acad. Sci. U. S. A. 93 1996 11448 11453 (Pubitemid 26347141)
25. M.E. Brousseau, and J.M. Hoeg Transgenic rabbits as models for atherosclerosis research J. Lipid Res. 40 1999 365 375 (Pubitemid 29116139)
26. A.M. Bérard, B. Föger, A. Remaley, R. Shamburek, B.L. Vaisman, G. Talley, B. Paigen, R.F. Hoyt Jr., S. Marcovina, H.B. Brewer Jr., and S. Santamarina-Fojo High plasma HDL concentrations associated with enhanced atherosclerosis in transgenic mice overexpressing lecithin-cholesteryl acyltransferase Nat. Med. 3 3 1997 744 749 (Pubitemid 27298717)
27. B. Föger, M. Chase, M.J. Amar, B.L. Vaisman, R.D. Shamburek, B. Paigen, J. Fruchart-Najib, J.A. Paiz, C.A. Koch, R.F. Hoyt, H.B. Brewe Jr., and S. Santamarina-Fojo Cholesteryl ester transfer protein corrects dysfunctional high density lipoproteins and reduces aortic atherosclerosis in lecithin cholesterol acyltransferase transgenic mice J. Biol. Chem. 274 1999 36912 36920
28. A. Mehlum, M. Muri, T.A. Hagve, L.A. Solberg, and H. Prydz Mice overexpressing human lecithin:cholesterol acyltransferase are not protected against diet-induced atherosclerosis APMIS 105 1997 861 868 (Pubitemid 27483633)
29. J.W. Furbee Jr., and J.S. Parks Transgenic overexpression of human lecithin:cholesterol acyltransferase (LCAT) in mice does not increase aortic cholesterol deposition Atherosclerosis 165 2002 89 100 (Pubitemid 35229987)
30. N. Sakai, B.L. Vaisman, C.A. Koch, R.F. Hoyt Jr., S.M. Meyn, G.D. Talley, J.A. Paiz, H.B. Brewer Jr., and S. Santamarina-Fojo Targeted disruption of the mouse lecithin:cholesterol acyltransferase (LCAT) gene. Generation of a new animal model for human LCAT deficiency J. Biol. Chem. 272 1997 7506 7510 (Pubitemid 27166465)
31. G. Lambert, N. Sakai, B.L. Vaisman, E.B. Neufeld, B. Marteyn, C.C. Chan, B. Paigen, E. Lupia, A. Thomas, L.J. Striker, J. Blanchette-Mackie, G. Csako, J.N. Brady, R. Costello, G.E. Striker, A.T. Remaley, H.B. Brewer Jr., and S. Santamarina-Fojo Analysis of glomerulosclerosis and atherosclerosis in lecithin cholesterol acyltransferase-deficient mice J. Biol. Chem. 276 2001 15090 15098
32. D.S. Ng, G.F. Maguire, J. Wylie, A. Ravandi, W. Xuan, Z. Ahmed, M. Eskandarian, A. Kuksis, and P.W. Connelly Oxidative stress is markedly elevated in lecithin:cholesterol acyltransferase-deficient mice and is paradoxically reversed in the apolipoprotein E knockout background in association with a reduction in atherosclerosis J. Biol. Chem. 277 2002 1715 1720
33. D.M. Shih, Y.R. Xia, X.P. Wang, E. Miller, L.W. Castellani, G. Subbanagounder, H. Cheroutre, K.F. Faull, J.A. Berliner, J.L. Witztum, and A.J. Lusis Combined serum paraoxonase knockout/apolipoprotein E knockout mice exhibit increased lipoprotein oxidation and atherosclerosis J. Biol. Chem. 275 2000 17527 17535 (Pubitemid 30430794)
34. H. Tanigawa, J.T. Billheimer, J. Tohyama, I.V. Fuki, D.S. Ng, G.H. Rothblat, and D.J. Rader Lecithin:cholesterol acyltransferase expression has minimal effects on macrophage reverse cholesterol transport in vivo Circulation 120 2009 160 169
35. J.W. Furbee Jr., J.K. Sawyer, and J.S. Parks Lecithin:cholesterol acyltransferase deficiency increases atherosclerosis in the low density lipoprotein receptor and apolipoprotein E knockout mice J. Biol. Chem. 277 2002 3511 3519 (Pubitemid 34953221)
36. E. Thomàs-Moyà, M. Gianotti, A.M. Proenza, and I. Lladó Paraoxonase 1 response to a high-fat diet: gender differences in the factors involved Mol. Med. 13 2007 203 209 (Pubitemid 46944964)
37. X. Zhang, R. Strakovsky, D. Zhou, Y. Zhang, and Y.X. Pan A maternal high-fat diet represses the expression of antioxidant defense genes and induces the cellular senescence pathway in the liver of male offspring rats J. Nutr. 141 2011 1254 1259
38. X. Rousset, B. Vaisman, B. Auerbach, B.R. Krause, R. Homan, J. Stonik, G. Csako, R. Shamburek, and A.T. Remaley Effect of recombinant human lecithin cholesterol acyltransferase infusion on lipoprotein metabolism in mice J. Pharmacol. Exp. Ther. 335 2010 140 148
39. X. Rousset, R. Shamburek, B. Vaisman, M. Amar, and A.T. Remaley Lecithin cholesterol acyltransferase: an anti- or pro-atherogenic factor? Curr. Atheroscler. Rep. 13 2011 249 256
40. H. Gylling, and T.A. Miettinen Non-cholesterol sterols, absorption and synthesis of cholesterol and apolipoprotein A-I kinetics in a Finnish lecithin-cholesterol acyltransferase deficient family Atherosclerosis 95 1992 25 33
41. M. Nishiwaki, K. Ikewaki, G. Bader, H. Nazih, M. Hannuksela, A.T. Remaley, R.D. Shamburek, and H.B. Brewer Jr. Human lecithin:cholesterol acyltransferase deficiency: in vivo kinetics of low-density lipoprotein and lipoprotein-X. Arterioscler Thromb. Vasc. Biol. 26 2006 1370 1375 (Pubitemid 44305384)
42. L. Calabresi, L. Pisciotta, A. Costantin, I. Frigerio, I. Eberini, P. Alessandrini, M. Arca, G.B. Bon, G. Boscutti, G. Busnach, G. Frascà, L. Gesualdo, M. Gigante, G. Lupattelli, A. Montali, S. Pizzolitto, I. Rabbone, M. Rolleri, G. Ruotolo, T. Sampietro, A. Sessa, G. Vaudo, A. Cantafora, F. Veglia, S. Calandra, S. Bertolini, and G. Franceschini 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. 25 2005 1972 1978 (Pubitemid 41243471)
43. J.W. Furbee Jr., O. Francone, and J.S. Parks In vivo contribution of LCAT to apolipoprotein B lipoprotein cholesteryl esters in LDL receptor and apolipoprotein E knockout mice J. Lipid Res. 43 2002 428 437 (Pubitemid 34252273)
44. H. Song, L. Zhu, C.M. Picardo, G. Maguire, V. Leung, P.W. Connelly, and D.S. Ng Coordinated alteration of hepatic gene expression in fatty acid and triglyceride synthesis in LCAT-null mice is associated with altered PUFA metabolism Am. J. Physiol. Endocrinol. Metab. 290 2006 E17 E25
45. J. Frohlich, R. McLeod, P.H. Pritchard, J. Fesmire, and W. McConathy Plasma lipoprotein abnormalities in heterozygotes for familial lecithin:cholesterol acyltransferase deficiency Metabolism 37 1988 3 8 (Pubitemid 18057188)
46. D.S. Ng, C. Xie, G.F. Maguire, X. Zhu, F. Ugwu, E. Lam, and P.W. Connelly Hypertriglyceridemia in lecithin-cholesterol acyltransferase-deficient mice is associated with hepatic overproduction of triglycerides, increased lipogenesis, and improved glucose tolerance J. Biol. Chem. 279 2004 7636 7642 (Pubitemid 38294644)
47. L. Li, M. Naples, H. Song, R. Yuan, F. Ye, S. Shafi, K. Adeli, and D.S. Ng LCAT-null mice develop improved hepatic insulin sensitivity through altered regulation of transcription factors and suppressors of cytokine signaling Am. J. Physiol. Endocrinol. Metab. 293 2007 E587 E594
48. L. Li, M.A. Hossain, S. Sadat, L. Hager, L. Liu, L. Tam, S. Schroer, L. Huogen, I.G. Fantus, P.W. Connelly, M. Woo, and D.S. Ng Lecithin cholesterol acyltransferase null mice are protected from diet-induced obesity and insulin resistance in a gender-specific manner through multiple pathways J. Biol. Chem. 286 2011 17809 17820
49. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Görgün, L.H. Glimcher, and G.S. Hotamisligil Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461 (Pubitemid 39372439)
50. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140 (Pubitemid 44300242)
51. 2 +-ATPase 2b is a major regulator of endoplasmic reticulum stress and glucose homeostasis in obesity Proc. Natl. Acad. Sci. U. S. A. 107 2010 19320 19325
52. C.N. Bennett, S.E. Ross, K.A. Longo, L. Bajnok, N. Hemati, K.W. Johnson, S.D. Harrison, and O.A. MacDougald Regulation of Wnt signaling during adipogenesis J. Biol. Chem. 277 2002 30998 31004 (Pubitemid 34970803)
53. W.S. Wright, K.A. Longo, V.W. DolinskY, I. Gerin, S. Kang, C.N. Bennett, S.H. Chiang, T.C. Prestwich, C. Gress, C.F. Burant, V.S. Susulic, and O.A. MacDougald Wnt10b inhibits obesity in ob/ob and agouti mice Diabetes 56 2007 295 303
54. P. Seale, S. Kajimura, W. Yang, S. Chin, L.M. Rohas, M. Uldry, G. Tavernier, D. Langin, and B.M. Spiegelman Transcriptional control of brown fat determination by PRDM16 Cell Metab. 6 2007 38 54 (Pubitemid 47008902)
55. S. Kajimura, P. Seale, T. Tomaru, H. Erdjument-Bromage, M.P. Cooper, J.L. Ruas, S. Chin, P. Tempst, M.A. Lazar, and B.M. Spiegelman Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex Genes Dev. 22 2008 1397 1409 (Pubitemid 351717529)
56. S. Cinti Reversible physiological transdifferentiation in the adipose organ Proc. Nutr. Soc. 68 2009 340 349
57. K. Almind, M. Manieri, W.I. Sivitz, S. Cinti, and C.R. Kahn Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice Proc. Natl. Acad. Sci. U. S. A. 104 2007 2366 2371 (Pubitemid 46391403)