Atherosclerosis
Volume 206, Issue 2 , Pages 321-327 , October 2009

In vivo macrophage-specific RCT and antioxidant and antiinflammatory HDL activity measurements: New tools for predicting HDL atheroprotection

  • Joan Carles Escolà-Gil

      Affiliations

    • Institut de Recerca de l’Hospital de la Santa Creu i Sant Pau, Servei de Bioquímica, Hospital de la Santa Creu i Sant Pau, Barcelona 08025, Spain
    • CIBER de Diabetes y Enfermedades Metabólicas Asociadas, CIBERDEM, Barcelona 08036, Spain
    • Corresponding Author InformationCorresponding author at: Institut de Recerca de l’Hospital de la Santa Creu i Sant Pau, Servei de Bioquímica, Hospital de la Santa Creu i Sant Pau, Barcelona 08025, Spain.
    • ,
  • Noemí Rotllan

      Affiliations

    • Institut de Recerca de l’Hospital de la Santa Creu i Sant Pau, Servei de Bioquímica, Hospital de la Santa Creu i Sant Pau, Barcelona 08025, Spain
    • ,
  • Josep Julve

      Affiliations

    • CIBER de Diabetes y Enfermedades Metabólicas Asociadas, CIBERDEM, Barcelona 08036, Spain
    • ,
  • Francisco Blanco-Vaca

      Affiliations

    • Institut de Recerca de l’Hospital de la Santa Creu i Sant Pau, Servei de Bioquímica, Hospital de la Santa Creu i Sant Pau, Barcelona 08025, Spain
    • CIBER de Diabetes y Enfermedades Metabólicas Asociadas, CIBERDEM, Barcelona 08036, Spain
    • Departament de Bioquímica i Biologia Molecular, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain

Received 14 July 2008 ,Revised 1 December 2008 ,Accepted 8 December 2008.

References 

  1. Rader DJ. Molecular regulation of HDL metabolism and function: implications for novel therapies. J Clin Invest. 2006;116:3090–3100
  2. Chiesa G, Sirtori CR. Apolipoprotein A-I(Milano): current perspectives. Curr Opin Lipidol. 2003;14:159–163
  3. Navab M, Anantharamaiah GM, Reddy ST, et al. Mechanisms of disease: proatherogenic HDL—an evolving field. Nat Clin Pract Endocrinol Metab. 2006;2:504–511
  4. deGoma EM, deGoma RL, Rader DJ. Beyond high-density lipoprotein cholesterol levels evaluating high-density lipoprotein function as influenced by novel therapeutic approaches. J Am Coll Cardiol. 2008;51:2199–2211
  5. Escola-Gil JC, Calpe-Berdiel L, Palomer X, et al. Antiatherogenic role of high-density lipoproteins: insights from genetically engineered-mice. Front Biosci. 2006;11:1328–1348
  6. Cuchel M, Rader DJ. Macrophage reverse cholesterol transport: key to the regression of atherosclerosis?. Circulation. 2006;113:2548–2555
  7. Norata GD, Callegari E, Marchesi M, et al. High-density lipoproteins induce transforming growth factor-beta2 expression in endothelial cells. Circulation. 2005;111:2805–2811
  8. Ferretti G, Bacchetti T, Negre-Salvayre A, et al. Structural modifications of HDL and functional consequences. Atherosclerosis. 2006;184:1–7
  9. Norata GD, Pirillo A, Catapano AL. Modified HDL: biological and physiopathological consequences. Nutr Metab Cardiovasc Dis. 2006;16:371–386
  10. Navab M, Ananthramaiah GM, Reddy ST, et al. The double jeopardy of HDL. Ann Med. 2005;37:173–178
  11. Calpe-Berdiel L, Rotllan N, Palomer X, et al. Direct evidence in vivo of impaired macrophage-specific reverse cholesterol transport in ATP-binding cassette transporter A1-deficient mice. Biochim Biophys Acta. 2005;1738:6–9
  12. Wang MD, Franklin V, Marcel YL. In vivo reverse cholesterol transport from macrophages lacking ABCA1 expression is impaired. Arterioscler Thromb Vasc Biol. 2007;27:1837–1842
  13. Wang X, Collins HL, Ranalletta M, et al. Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J Clin Invest. 2007;117:2216–2224
  14. Mukhamedova N, Escher G, D'Souza W, et al. Enhancing apolipoprotein A-I-dependent cholesterol efflux elevates cholesterol export from macrophages in vivo. J Lipid Res. 2008;49:2312–2322
  15. Pennings M, Meurs I, Ye D, et al. Regulation of cholesterol homeostasis in macrophages and consequences for atherosclerotic lesion development. FEBS Lett. 2006;580:5588–5596
  16. Out R, Hoekstra M, Hildebrand RB, et al. Macrophage ABCG1 deletion disrupts lipid homeostasis in alveolar macrophages and moderately influences atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2006;26:2295–2300
  17. Ranalletta M, Wang N, Han S, et al. Decreased atherosclerosis in low-density lipoprotein receptor knockout mice transplanted with Abcg1−/− bone marrow. Arterioscler Thromb Vasc Biol. 2006;26:2308–2315
  18. Baldan A, Pei L, Lee R, et al. Impaired development of atherosclerosis in hyperlipidemic Ldlr−/− and ApoE−/− mice transplanted with Abcg1−/− bone marrow. Arterioscler Thromb Vasc Biol. 2006;26:2301–2307
  19. Out R, Jessup W, Le Goff W, et al. Coexistence of foam cells and hypocholesterolemia in mice lacking the ABC transporters A1 and G1. Circ Res. 2008;102:113–120
  20. Yvan-Charvet L, Ranalletta M, Wang N, et al. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest. 2007;117:3900–3908
  21. Out R, Hoekstra M, Habets K, et al. Combined deletion of macrophage ABCA1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels. Arterioscler Thromb Vasc Biol. 2008;28:258–264
  22. Huby T, Doucet C, Dachet C, et al. Knockdown expression and hepatic deficiency reveal an atheroprotective role for SR-BI in liver and peripheral tissues. J Clin Invest. 2006;116:2767–2776
  23. Van Eck M, Hoekstra M, Hildebrand RB, et al. Increased oxidative stress in scavenger receptor BI knockout mice with dysfunctional HDL. Arterioscler Thromb Vasc Biol. 2007;27:2413–2419
  24. Zhao B, Song J, Chow WN, et al. Macrophage-specific transgenic expression of cholesteryl ester hydrolase significantly reduces atherosclerosis and lesion necrosis in Ldlr mice. J Clin Invest. 2007;117:2983–2992
  25. Moore RE, Navab M, Millar JS, et al. Increased atherosclerosis in mice lacking apolipoprotein A-I attributable to both impaired reverse cholesterol transport and increased inflammation. Circ Res. 2005;97:763–771
  26. Castellani LW, Navab M, Van Lenten BJ, et al. Overexpression of apolipoprotein AII in transgenic mice converts high density lipoproteins to proinflammatory particles. J Clin Invest. 1997;100:464–474
  27. Ribas V, Sanchez-Quesada JL, Anton R, et al. Human apolipoprotein A-II enrichment displaces paraoxonase from HDL and impairs its antioxidant properties: a new mechanism linking HDL protein composition and antiatherogenic potential. Circ Res. 2004;95:789–797
  28. Blanco-Vaca F, Escola-Gil JC, Martin-Campos JM, et al. Role of apoA-II in lipid metabolism and atherosclerosis: advances in the study of an enigmatic protein. J Lipid Res. 2001;42:1727–1739
  29. Rotllan N, Ribas V, Calpe-Berdiel L, et al. Overexpression of human apolipoprotein A-II in transgenic mice does not impair macrophage-specific reverse cholesterol transport in vivo. Arterioscler Thromb Vasc Biol. 2005;25:e128–132
  30. Escola-Gil JC, Julve J, Martin-Campos JM, et al. Apolipoprotein A-II. In:  Fielding CJ editors. High-density lipoproteins: from basic biology to clinical aspects. Wiley-VCH; 2007;p. 25–41
  31. Nofer JR, Assmann G. Atheroprotective effects of high-density lipoprotein-associated lysosphingolipids. Trends Cardiovasc Med. 2005;15:265–271
  32. Nofer JR, Bot M, Brodde M, et al. FTY720, a synthetic sphingosine 1 phosphate analogue, inhibits development of atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation. 2007;115:501–508
  33. Getz GS, Reardon CA. Paraoxonase, a cardioprotective enzyme: continuing issues. Curr Opin Lipidol. 2004;15:261–267
  34. Ng CJ, Hama SY, Bourquard N, et al. Adenovirus mediated expression of human paraoxonase 2 protects against the development of atherosclerosis in apolipoprotein E-deficient mice. Mol Genet Metab. 2006;89:368–373
  35. Ng CJ, Bourquard N, Grijalva V, et al. Paraoxonase-2 deficiency aggravates atherosclerosis in mice despite lower apolipoprotein-B-containing lipoproteins: anti-atherogenic role for paraoxonase-2. J Biol Chem. 2006;281:29491–29500
  36. Ng CJ, Bourquard N, Hama SY, et al. Adenovirus-mediated expression of human paraoxonase 3 protects against the progression of atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2007;27:1368–1374
  37. Noto H, Hara M, Karasawa K, et al. Human plasma platelet-activating factor acetylhydrolase binds to all the murine lipoproteins, conferring protection against oxidative stress. Arterioscler Thromb Vasc Biol. 2003;23:829–835
  38. Quarck R, De Geest B, Stengel D, et al. Adenovirus-mediated gene transfer of human platelet-activating factor-acetylhydrolase prevents injury-induced neointima formation and reduces spontaneous atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2001;103:2495–2500
  39. Chen CH. Platelet-activating factor acetylhydrolase: is it good or bad for you?. Curr Opin Lipidol. 2004;15:337–341
  40. Asztalos BF, Schaefer EJ, Horvath KV, et al. Role of LCAT in HDL remodeling: investigation of LCAT deficiency states. J Lipid Res. 2007;48:592–599
  41. Stein O, Stein Y. Lipid transfer proteins (LTP) and atherosclerosis. Atherosclerosis. 2005;178:217–230
  42. Leitinger N, Watson AD, Hama SY, et al. Role of group II secretory phospholipase A2 in atherosclerosis: 2 Potential involvement of biologically active oxidized phospholipids. Arterioscler Thromb Vasc Biol. 1999;19:1291–1298
  43. Wolfrum C, Poy MN, Stoffel M. Apolipoprotein M is required for prebeta-HDL formation and cholesterol efflux to HDL and protects against atherosclerosis. Nat Med. 2005;11:418–422
  44. Christoffersen C, Jauhiainen M, Moser M, et al. Effect of apolipoprotein M on high density lipoprotein metabolism and atherosclerosis in low density lipoprotein receptor knock-out mice. J Biol Chem. 2008;283:1839–1847
  45. Harada LM, Amigo L, Cazita PM, et al. CETP expression enhances liver HDL-cholesteryl ester uptake but does not alter VLDL and biliary lipid secretion. Atherosclerosis. 2007;191:313–318
  46. Tanigawa H, Billheimer JT, Tohyama J, et al. Expression of cholesteryl ester transfer protein in mice promotes macrophage reverse cholesterol transport. Circulation. 2007;116:1267–1273
  47. Rotllan N, Calpe-Berdiel L, Guillaumet-Adkins A, et al. CETP activity variation in mice does not affect two major HDL antiatherogenic properties: macrophage-specific reverse cholesterol transport and LDL antioxidant protection. Atherosclerosis. 2008;196:505–513
  48. Cazita PM, Berti JA, Aoki C, et al. Cholesteryl ester transfer protein expression attenuates atherosclerosis in ovariectomized mice. J Lipid Res. 2003;44:33–40
  49. Westerterp M, van der Hoogt CC, de Haan W, et al. Cholesteryl ester transfer protein decreases high-density lipoprotein and severely aggravates atherosclerosis in APOE*3-Leiden mice. Arterioscler Thromb Vasc Biol. 2006;26:2552–2559
  50. Lie J, de Crom R, van Gent T, et al. Elevation of plasma phospholipid transfer protein increases the risk of atherosclerosis despite lower apolipoprotein B-containing lipoproteins. J Lipid Res. 2004;45:805–811
  51. Ishida T, Choi SY, Kundu RK, et al. Endothelial lipase modulates susceptibility to atherosclerosis in apolipoprotein-E-deficient mice. J Biol Chem. 2004;279:45085–45092
  52. Ko KW, Paul A, Ma K, et al. Endothelial lipase modulates HDL but has no effect on atherosclerosis development in apoE−/− and LDLR−/− mice. J Lipid Res. 2005;46:2586–2594
  53. Jin W, Wang X, Millar JS, et al. Hepatic proprotein convertases modulate HDL metabolism. Cell Metab. 2007;6:129–136
  54. Trigatti BL, Krieger M, Rigotti A. Influence of the HDL receptor SR-BI on lipoprotein metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol. 2003;23:1732–1738
  55. Zhang Y, Da Silva JR, Reilly M, et al. Hepatic expression of scavenger receptor class B type I (SR-BI) is a positive regulator of macrophage reverse cholesterol transport in vivo. J Clin Invest. 2005;115:2870–2874
  56. Yu L, Hammer RE, Li-Hawkins J, et al. Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc Natl Acad Sci U S A. 2002;99:16237–16242
  57. Calpe-Berdiel L, Rotllan N, Fievet C, et al. Liver X receptor-mediated activation of reverse cholesterol transport from macrophages to feces in vivo requires ABCG5/G8. J Lipid Res. 2008;49:1904–1911
  58. Wilund KR, Yu L, Xu F, et al. No association between plasma levels of plant sterols and atherosclerosis in mice and men. Arterioscler Thromb Vasc Biol. 2004;24:2326–2332
  59. Salen G, Shefer S, Nguyen L, et al. Sitosterolemia. J Lipid Res. 1992;33:945–955
  60. Temel RE, Tang W, Ma Y, et al. Hepatic Niemann-Pick C1-like 1 regulates biliary cholesterol concentration and is a target of ezetimibe. J Clin Invest. 2007;117:1968–1978
  61. Navab M, Anantharamaiah GM, Reddy ST, et al. Apolipoprotein A-I mimetic peptides and their role in atherosclerosis prevention. Nat Clin Pract Cardiovasc Med. 2006;3:540–547
  62. Singh IM, Shishehbor MH, Ansell BJ. High-density lipoprotein as a therapeutic target: a systematic review. JAMA. 2007;298:786–798
  63. Nissen SE, Tsunoda T, Tuzcu EM, et al. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA. 2003;290:2292–2300
  64. Tardif JC, Gregoire J, L’Allier PL, et al. Effects of reconstituted high-density lipoprotein infusions on coronary atherosclerosis: a randomized controlled trial. JAMA. 2007;297:1675–1682
  65. Schaefer EJ, Asztalos BF. Increasing high-density lipoprotein cholesterol, inhibition of cholesteryl ester transfer protein, and heart disease risk reduction. Am J Cardiol. 2007;100:n25–31
  66. Navab M, Anantharamaiah GM, Reddy ST, et al. Oral D-4F causes formation of pre-beta high-density lipoprotein and improves high-density lipoprotein-mediated cholesterol efflux and reverse cholesterol transport from macrophages in apolipoprotein E-null mice. Circulation. 2004;109:3215–3220
  67. Navab M, Anantharamaiah GM, Hama S, et al. D-4F and statins synergize to render HDL antiinflammatory in mice and monkeys and cause lesion regression in old apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol. 2005;25:1426–1432
  68. Bloedon LT, Dunbar RL, Duffy D, et al. Oral administration of the apolipoprotein A-1 mimetic peptide D-4F in humans with CHD improves HDL anti-inflammatory function after a single dose. Circulation. 2006;114:288
  69. Naik SU, Wang X, Da Silva JS, et al. Pharmacological activation of liver X receptors promotes reverse cholesterol transport in vivo. Circulation. 2006;113:90–97
  70. Zanotti I, Poti F, Pedrelli M, et al. The LXR agonist T0901317 promotes the reverse cholesterol transport from macrophages by increasing plasma efflux potential. J Lipid Res. 2008;49:954–960

PII: S0021-9150(09)00215-9

doi: 10.1016/j.atherosclerosis.2008.12.044

Atherosclerosis
Volume 206, Issue 2 , Pages 321-327 , October 2009

Article Tools