DOI QR코드

DOI QR Code

Biomedicinal implications of high-density lipoprotein: its composition, structure, functions, and clinical applications

  • Published : 2009.07.31

Abstract

High-density lipoprotein (HDL) is a proven biomarker for the monitoring of changes in antioxidant and anti-inflammation capability of body fluids. The beneficial virtues of HDL are highly dependent on its lipids and protein compositions, and their ratios. In normal state, the HDL particle is enriched with lipids and several HDL-associated enzymes, which are responsible for its antioxidant activity. Lower HDL-cholesterol levels (<40 mg/dL) have been recognized as an independent risk factor for coronary artery disease, as well as being a known component of metabolic syndrome. Functional and structural changes of HDL have been recognized as factors pivotal to the evaluation of HDL-quality. In this review, I have elected to focus on the functional and structural correlations of HDL and the roles of HDL-associated apolipoproteins and enzymes. Recent clinical applications of HDL have also been reviewed, particularly the therapeutic targeting of HDL metabolism and reconstituted HDL; these techniques represent promising emerging strategies for the treatment of cardiovascular disease, for drug or gene therapy.

Keywords

References

  1. Gordon, T., Castelli, W. P., Hjortland, M. C., Kannel, W. B. and Dawber, T. R. (1977) High density lipoprotein as a protective factor against coronary heart disease. Am. J. Med. 62, 707-714 https://doi.org/10.1016/0002-9343(77)90874-9
  2. Fielding, C. J. and Fielding, P. E. (1995) Molecular physiology of reverse cholesterol transport. J. Lipid. Res. 36, 211-228
  3. Ross, R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809 https://doi.org/10.1038/362801a0
  4. Glomset, J. A. (1968) The plasma lecithins: cholesterol acyltransferase reaction. J. Lipid. Res. 9, 155-167
  5. Lewis, G. F. and Rader, D. J. (2005) New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ. Res. 96, 1221-1232 https://doi.org/10.1161/01.RES.0000170946.56981.5c
  6. Miller, G. J. and Miller, N. E. (1975) Plasma-high-density- lipoprotein concentration and development of ischaemic heart-disease. Lancet 1, 16-19 https://doi.org/10.1016/S0140-6736(02)95332-8
  7. Zannis, V. I., Cole, F. S., Jackson, C. L., Kurnit, D. M. and Karathanasis, S. K. (1985) Distribution of apolipoprotein A-I, C-II, C-III, and E mRNA in fetal human tissues. Time-dependent induction of apolipoprotein E mRNA by cultures of human monocyte-macrophages. Biochemistry 24, 4450-4455 https://doi.org/10.1021/bi00337a028
  8. Brewer, H. B. (2004) High-density lipoproteins: a new potential therapeutic target for the prevention of cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 24, 387-391 https://doi.org/10.1161/01.ATV.0000121505.88326.d2
  9. Oram, J. F. (2003) HDL apolipoproteins and ABCA1: partners in the removal of excess cellular cholesterol. Arterioscler. Thromb. Vasc. Biol. 23, 720-727 https://doi.org/10.1161/01.ATV.0000054662.44688.9A
  10. Jonas, A. (1998) Regulation of lecithin cholesterol acyltransferase activity. Prog. Lipid. Res. 37, 209-234 https://doi.org/10.1016/S0163-7827(98)00007-1
  11. Yancey, P. G., Bortnick, A. E., Kellner-Weibel, G, de la Llera-Moya, M., Phillips, M. C. and Rothblat, G. H. (2003) Importance of different pathways of cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23, 712-719 https://doi.org/10.1161/01.ATV.0000057572.97137.DD
  12. Barter, P. J., Brewer, H. B., Jr., Chapman, M. J., Hennekens, C. H., Rader, D. J. and Tall, A. R. (2003) CETP a novel target for raising HDL and inhibiting atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23, 160-167 https://doi.org/10.1161/01.ATV.0000054658.91146.64
  13. Barter, P. J., Nicholls, S., Rye, K. A., Anantharamaiah, G. M., Naval, M. and Fogelman, A. M. (2004) Antiinflammatory properties of HDL. Circ. Res. 95, 764-772 https://doi.org/10.1161/01.RES.0000146094.59640.13
  14. Miller, N. E., Thelle, D. S., Forde, O. H. and Mjos, O. D. (1977) The Tromso heart-study. High-density lipoprotein and coronary heart-disease: a prospective case-control study. Lancet 309, 965-968 https://doi.org/10.1016/S0140-6736(77)92274-7
  15. Goldbourt, U. and Medalie, J. H. (1979) High density lipoprotein cholesterol and incidence of coronary heart disease the Israeli Ischemic Heart Disease Study. Am. J. Epidemiol. 109, 296-308
  16. Badimon, J. J., Fuster, V. and Badimon, L. (1992) Role of high density lipoproteins in the regression of atherosclerosis. Circulation 86, III86-94
  17. M., Chaddha, M., Jin, L., Subbanagounder, G., Faull, K. F., Reddy, S. T., Miller, N. E. and Fogelman, A. M. (2000) Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1. J. Lipid. Res. 41, 1481-1494
  18. Bielicki, J. K. and Oda, M. N. (2002) apoA-IMilano and apoA-IParis exhibit an antioxidant activity distinct from that of wild-type apoA-I. Biochemistry 41, 2089-2096 https://doi.org/10.1021/bi011716p
  19. Pownall, H. J. and Ehnholm, C. (2005) Enhancing reverse cholesterol transport: the case for phosphatidylcholine therapy. Curr. Opin. Lipidol. 16, 265-268 https://doi.org/10.1097/01.mol.0000169345.15450.4b
  20. Cho, K. H., Park, S. H., Han, J. M., Kim, H. C., Choi, Y. K. and Choi, I. (2006) ApoA-I mutants V156K and R173C promote anti-inflammatory function and antioxidant activities. Eur. J. Clin. Invest. 36, 875-882 https://doi.org/10.1111/j.1365-2362.2006.01737.x
  21. Ross, R. (1999) Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340, 115-126 https://doi.org/10.1056/NEJM199901143400207
  22. Cesari, M., Penninx, B. W., Newman, A. B., Kritchevsky, S. B., Nicklas, B. J., Sutton-Tyrrell, K., Rubin, S. M., Ding, J., Simonsick, E. M., Harris, T. B. and Pahor, M. (2003) Inflammatory markers and onset of cardiovascular events-results from the Health ABC study. Circulation 108, 2317-2322 https://doi.org/10.1161/01.CIR.0000097109.90783.FC
  23. Tzoulaki, I., Murray, G. D., Lee, A. J., Rumley, A., Lowe, G. D. and Fowkes, F. G. (2005) C-reactive protein, interleukin- 6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population. Circulation 112, 976-983 https://doi.org/10.1161/CIRCULATIONAHA.104.513085
  24. Ramirez, M. J., Ibanez, A., Navasa, M., Casals, E., Morales- Ruiz, M. and Jimenez, W. (2004) High-density lipoproteins reduce the effect of endotoxin on cytokine production and systemic hemodynamics in cirrhotic rats with ascites. J. Hepatol. 40, 424-430 https://doi.org/10.1016/j.jhep.2003.11.017
  25. S., Mota-Filipe, H., Hinds, C. J., Miller, N. E. and Thiemermann, C. (2003) Reconstituted high-density lipoprotein attenuates organ injury and adhesion molecule expression in a rodent model of endotoxic shock. Shock 20, 551-557 https://doi.org/10.1097/01.shk.0000097249.97298.a3
  26. Borhani, D. W., Rogers, D. P., Engler, J. A. and Brouillette, C. G. (1997) Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl. Acad. Sci. U.S.A. 94, 12291-12296 https://doi.org/10.1073/pnas.94.23.12291
  27. Palgunachari, M. N., Mishra, V. K., Lund-Katz, S., Phillips, M. C., Adeyeye, S. O., Alluri, S., Anantharamaiah, G. M. and Segrest, J. P. (1996) Only the two end helixes of eight tandem amphipathic helical domains of human apo A-I have significant lipid affinity. Implications for HDL assembly. Arterioscler. Thromb. Vasc. Biol. 16, 328-338 https://doi.org/10.1161/01.ATV.16.2.328
  28. Mishra, V. K., Palgunachari, M. N., Segrest, J. P. and Anantharamaiah, G. M. (1994) Interactions of synthetic peptide analogs of the class A amphipathic helix with lipids. Evidence for the snorkel hypothesis. J. Biol. Chem. 269, 7185-7191
  29. Gordon, J. I., Sims, H. F., Lentz, S. R., Edelstein, C., Scanu, A. M. and Strauss, A. W. (1982) Proteolytic processing of human preproapolipoprotein A-I. J. Biol. Chem. 257, 4978-4986
  30. Boguski, M. S., Freeman, M., Elshourbagy, N. A., Taylor, J. M. and Gordon, J. I. (1986) On computer-assisted analysis of biological sequences: proline punctuation, consensus sequences, and apolipoprotein repeats. J. Lipid. Res. 27, 1011-1034
  31. Brewer, H. B., Jr., Lux, S. E., Ronan, R. and John, K. M. (1972) Amino acid sequence of human apoLp-Gln-II (apoA-II), an apolipoprotein isolated from the high-density lipoprotein complex. Proc. Natl. Acad. Sci. U.S.A. 69, 1304-1308 https://doi.org/10.1073/pnas.69.5.1304
  32. Blanco-Vaca, F., Escola-Gil, J. C., Martin-Campos, J. M. and Julve, J. (2001) Role of apoA-II in lipid metabolism and atherosclerosis: advances in the study of an enigmatic protein. J. Lipid. Res. 42, 1727-1739
  33. Ribas, V., Sanchez-Quesada, J. L., Anton, R., Camacho, M., Julve, J., Escola-Gil, J. C., Vila, L., Ordonez-Llanos, J. and Blanco-Vaca, F. (2004) 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. 95, 789-797 https://doi.org/10.1161/01.RES.0000146031.94850.5f
  34. Park, S. H., Kim, J. R., Park, J. E. and Cho, K. H. (2007) A Caucasian male with very low blood cholesterol and low apoA-II without evidence of atherosclerosis. Eur. J. Clin. Invest. 37, 249-256 https://doi.org/10.1111/j.1365-2362.2007.01768.x
  35. Jong, M. C., Hofker, M. H. and Havekes, L. M. (1999) Role of ApoCs in lipoprotein metabolism: functional differences between ApoC1, ApoC2, and ApoC3. Arterioscler. Thromb. Vasc. Biol. 19, 472-484 https://doi.org/10.1161/01.ATV.19.3.472
  36. Shachter, N. S. (2001) Apolipoproteins C-I and C-III as important modulators of lipoprotein metabolism. Curr. Opin. Lipidol. 12, 297-304 https://doi.org/10.1097/00041433-200106000-00009
  37. Alsayed, N. and Rebourcet, R. (1991) Abnormal concentrations of CII, CIII, and E apolipoproteins among apolipoprotein B-containing, B-free, and A-I-containing lipoprotein particles in hemodialysis patients. Clin. Chem. 37, 387-393
  38. Cho, K. H., Park, S. H., Park, J. E., Kim, Y. O., Choi, I., Kim, J. J. and Kim, J. R. (2008) The function, composition, and particle size of high-density lipoprotein were severely impaired in an oliguric phase of hemorrhagic fever with renal syndrome. Clin. Biochem. 41, 56-64 https://doi.org/10.1016/j.clinbiochem.2007.10.007
  39. Cho, K. H. (2009) Synthesis of reconstituted high-density lipoprotein (rHDL) containing apoA-I and apoC-III: the functional role of apoC-III in rHDL. Mol. Cells 27, 291-297 https://doi.org/10.1007/s10059-009-0037-8
  40. Jonas, A. (1991) Lecithin-cholesterol acyltransferase in the metabolism of high-density lipoproteins. Biochim. Biophys. Acta 1084, 205-220 https://doi.org/10.1016/0005-2760(91)90062-M
  41. Lagrost, L., Dengremont, C., Athias, A., de Geitere, C., Fruchart, J. C., Lallemant, C., Gambert, P. and Castro, G. (1995) Modulation of cholesterol efflux from Fu5AH hepatoma cells by the apolipoprotein content of high density lipoprotein particles. Particles containing various proportions of apolipoproteins A-I and A-II. J. Biol. Chem. 270, 13004-13009 https://doi.org/10.1074/jbc.270.22.13004
  42. Fournier, N., Cogny, A., Atger, V., Pastier, D., Goudouneche, D., Nicoletti, A., Moatti, N., Chambaz, J., Paul, J. L. and Kalopissis, A. D. (2002) Opposite effects of plasma from human apolipoprotein A-II transgenic mice on cholesterol efflux from J774 macrophages and Fu5AH hepatoma cells. Arterioscler. Thromb. Vasc. Biol. 22, 638-643 https://doi.org/10.1161/01.ATV.0000013023.11297.B2
  43. Kuivenhoven, J. A., Pritchard, H., Hill, J., Frohlich, J., Assmann, G. and Kastelein, J. (1997) The molecular pathology of lecithin: cholesterol acyltransferase (LCAT) deficiency syndromes. J. Lipid. Res. 38, 191-205
  44. Morton, R. E. (1999) Cholesteryl ester transfer protein and its plasma regulator: lipid transfer inhibitor protein. Curr. Opin. Lipidol. 10, 321-327 https://doi.org/10.1097/00041433-199908000-00006
  45. Jarnagin, A. S., Kohr, W. and Fielding, C. (1987) Isolation and specificity of a Mr 74,000 cholesteryl ester transfer protein from human plasma. Proc. Natl. Acad. Sci. U.S.A. 84, 1854-1857 https://doi.org/10.1073/pnas.84.7.1854
  46. Brown, M. L., Inazu, A., Hesler, C. B., Agellon, L. B., Mann, C., Whitlock, M. E., Marcel, Y. L., Milne, R. W., Koizumi, J. and Mabuchi, H. (1989) Molecular basis of lipid transfer protein deficiency in a family with increased high-density lipoproteins. Nature 342, 448-451 https://doi.org/10.1038/342448a0
  47. Brousseau, M. E. (2005) Emerging role of high-density lipoprotein in the prevention of cardiovascular disease. Drug Discov. Today 10, 1095-1101 https://doi.org/10.1016/S1359-6446(05)03514-2
  48. Eckerson, H. W., Wyte, C. M. and La Du, B. N. (1983) The human serum paraoxonase/arylesterase polymorphism. Am. J. Hum. Genet. 35, 1126-1138
  49. Yla-Herttuala, S., Palinski, W., Rosenfeld, M. E., Parthasarathy, S., Carew, T. E., Butler, S., Witztum, J. L. and Steinberg, D. (1989) Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84, 1086-1095 https://doi.org/10.1172/JCI114271
  50. Mackness, M. I., Walker, C. H. and Carlson, L. A. (1987) Low A-esterase activity in serum of patients with fish-eye disease. Clin. Chem. 33, 587-588
  51. Mackness, M. I., Peuchant, E., Dumon, M. F., Walker, C. H. and Clerc, M. (1989) Absence of 'A'-esterase activity in the serum of a patient with Tangier disease. Clin. Biochem. 22, 475-478 https://doi.org/10.1016/S0009-9120(89)80101-8
  52. Gur, M., Aslan, M., Yildiz, A., Demirbag, R., Yilmaz, R., Selek, S., Erel, O. and Ozdogru, I. (2006) Paraoxonase and arylesterase activities in coronary artery disease. Eur. J. Clin. Invest. 36, 779-787 https://doi.org/10.1111/j.1365-2362.2006.01727.x
  53. Erlich, P. M., Lunetta, K. L., Cupples, L. A., Huyck, M., Green, R. C., Baldwin, C. T. and Farrer, L. A. (2006) Polymorphisms in the PON gene cluster are associated with Alzheimer disease. Hum. Mol. Genet. 15, 77-85 https://doi.org/10.1093/hmg/ddi428
  54. Karasawa, K. (2006) Clinical aspects of plasma plateletactivating factor-acetylhydrolase. Biochim. Biophys. Acta. 1761, 1359-1372 https://doi.org/10.1016/j.bbalip.2006.06.017
  55. Six, D. A. and Dennis, E. A. (2000) The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim. Biophys. Acta. 1488, 1-19 https://doi.org/10.1016/S1388-1981(00)00105-0
  56. Watson, A. D., Navab, M., Hama, S. Y., Sevanian, A., Prescott, S. M., Stafforini, D. M., McIntyre, T. M., Du, B. N., Fogelman, A. M. and Berliner, J. A. (1995) Effect of platelet activating factor-acetylhydrolase on the formation and action of minimally oxidized low density lipoprotein. J. Clin. Invest. 95, 774-782 https://doi.org/10.1172/JCI117726
  57. Evangelou, A. M. (1994) Platelet-activating factor (PAF): implications for coronary heart and vascular diseases. Prostaglandins Leukot. Essent. Fatty. Acids. 50, 1-28 https://doi.org/10.1016/0952-3278(94)90101-5
  58. Navab, M., Anantharamaiah, G. M., Reddy, S. T., Van Lenten, B. J., Datta, G., Garber, D. and Fogelman, A. M. (2004) Human apolipoprotein A-I and A-I mimetic peptides: potential for atherosclerosis reversal. Curr. Opin. Lipidol. 15, 645-649 https://doi.org/10.1097/00041433-200412000-00004
  59. Lerch, P. G., Fortsch, V., Hodler, G. and Bolli, R. (1996) Production and characterization of a reconstituted high density lipoproteins for therapeutic applications. Vox. Sang. 71, 155-164 https://doi.org/10.1046/j.1423-0410.1996.7130155.x
  60. Tardif, J. C., Gregoire, J., L'Allier, P. L., Ibrahim, R., Lesperance, J., Heinonen, T. M., Kouz, S., Berry, C., Basser, R., Lavoie, M. A., Guertin, M. C. and Rodes-Cabau, J. (2007) Effects of reconstituted high-density lipoprotein infusions on coronary atherosclerosis. J. Am. Med. Assoc. 297, 1675-1682 https://doi.org/10.1001/jama.297.15.jpc70004
  61. Franceschini, G., Sirtori, C. R., Capurso, A., 2nd, Weisgraber, K. H. and Mahley, R. W. (1980) A-IMilano apoprotein. Decreased high density lipoprotein cholesterol levels with significant lipoprotein modifications and without clinical atherosclerosis in an Italian family. J. Clin. Invest. 66, 892-900 https://doi.org/10.1172/JCI109956
  62. Tardif, J. C., Heinonen, T. and Noble, S. (2009) High-density lipoprotein/apolipoprotein A-I infusion therapy. Curr. Atheroscler. Rep. 11, 58-63 https://doi.org/10.1007/s11883-009-0009-7
  63. Han, J. M., Jeong, T. S., Lee, W. S., Choi, I. and Cho, K. H. (2005) Structural and functional properties of V156K and A158E mutants of apolipoprotein A-I in the lipid-free and lipid-bound states. J. Lipid. Res. 46, 589-596 https://doi.org/10.1194/jlr.M400468-JLR200
  64. Cho, K. H., Park, S. H., Han, J. M., Kim, H. C., Chung, Y. J., Choi, I. and Kim, J. R. (2007) A point mutant of apolipoprotein A-I, V156K, exhibited potent anti-oxidant and antiatherosclerotic activity in hypercholesterolemic C57BL/6 mice. Exp. Mol. Med. 39, 160-169 https://doi.org/10.1038/emm.2007.18
  65. Cho, K. H. and Kim, J. R. (2009). A reconstituted high-density lipoprotein containing V156K or R173C apoA-I exhibited anti-inflammatory activity in apo-E deficient mice and showed resistance to myeloperoxidase-mediated oxidation. Exp. Mol. Med. 41, 417-428 https://doi.org/10.3858/emm.2009.41.6.047
  66. Lacko, A. G., Nair, M., Paranjape, S., Johnson, S., McConathy, W. J. (2002) High density lipoprotein complexes as delivery vehicles for anticancer drugs. Anticancer Res. 22, 2045-2049
  67. Oda, M. N., Hargreaves, P. L., Beckstead, J. A., Redmond, K. A., van Antwerpen, R. and Ryan, R. O. (2006) Reconstituted high density lipoprotein enriched with the polyene antibiotic amphotericin B. J. Lipid. Res. 47, 260-267 https://doi.org/10.1194/jlr.D500033-JLR200
  68. Bijsterbosch, M. K., van de Bilt, H. and van Berkel, T. J. (1996) Specific targeting of a lipophilic prodrug of iododeoxyuridine to parenchymal liver cells using lactosylated reconstituted high density lipoprotein particles. Biochem. Pharmacol. 52, 113-121 https://doi.org/10.1016/0006-2952(96)00170-0
  69. Koudinov, A. R., Berezov, T. T., Kumar, A. and Koudiniva, N. V. (1998) Alzheimer's amyloid $\beta$ interaction with normal human plasma high density lipoprotein: association with apolipoprotein and lipids. Clinina. Chimica. Acta 270, 75-84 https://doi.org/10.1016/S0009-8981(97)00207-6
  70. Paterno, R., Ruocco, A., Postiglione, A., Hubsch, A., Andresen, I. and Lang, M. G. (2004) Reconstituted High-density lipoprotein exhibits neuroprotection in two rat models of stroke. Cerebrovasc. Dis. 17, 204-211 https://doi.org/10.1159/000075792

Cited by

  1. Statins and hemoperfusion improve 28-day survival in septic shock patients vol.7, pp.4, 2012, https://doi.org/10.2478/s11536-011-0169-z
  2. Localization of Native High-Density Lipoprotein and Its Relation to Plaque Morphology in Human Coronary Artery vol.54, pp.6, 2013, https://doi.org/10.1536/ihj.54.348
  3. High-dose consumption of NaCl resulted in severe degradation of lipoproteins associated with hyperlipidemia, hyperglycemia, and infertility via impairment of testicular spermatogenesis vol.5, pp.2, 2016, https://doi.org/10.1039/C5TX00059A
  4. Grape Polyphenols Increase the Activity of HDL Enzymes in Old and Obese Rats vol.2013, 2013, https://doi.org/10.1155/2013/593761
  5. High Consumption of Iron Exacerbates Hyperlipidemia, Atherosclerosis, and Female Sterility in Zebrafish via Acceleration of Glycation and Degradation of Serum Lipoproteins vol.9, pp.7, 2017, https://doi.org/10.3390/nu9070690
  6. Relation of atrial fibrillation (AF) and change of lipoproteins: Male patients with AF exhibited severe pro-inflammatory and pro-atherogenic properties in lipoproteins vol.47, pp.10-11, 2014, https://doi.org/10.1016/j.clinbiochem.2013.10.026
  7. Activation of lipoprotein lipase increases serum high density lipoprotein 2 cholesterol and enlarges high density lipoprotein 2 particles in rats vol.668, pp.1-2, 2011, https://doi.org/10.1016/j.ejphar.2011.06.040
  8. Enhancement of High-Density Lipoprotein Cholesterol Functions by Encapsulation of Policosanol Exerts Anti-Senescence and Tissue Regeneration Effects Via Improvement of Anti-Glycation, Anti-Apoptosis, and Cholesteryl Ester Transfer Inhibition vol.19, pp.1, 2016, https://doi.org/10.1089/rej.2015.1712
  9. Application of Polydimethylsiloxane/Glass Microchips for Fast Electrophoretic Separation of Serum High-density Lipoprotein Subclasses vol.40, pp.2, 2012, https://doi.org/10.1016/S1872-2040(11)60531-8
  10. Effects of the Particulate Matter2.5 (PM2.5) on Lipoprotein Metabolism, Uptake and Degradation, and Embryo Toxicity vol.38, pp.12, 2015, https://doi.org/10.14348/molcells.2015.0194
  11. Analysis of apolipoprotein A-I as a substrate for matrix metalloproteinase-14 vol.409, pp.1, 2011, https://doi.org/10.1016/j.bbrc.2011.04.105
  12. Dysfunctional Lipoproteins from Young Smokers Exacerbate Cellular Senescence and Atherogenesis with Smaller Particle Size and Severe Oxidation and Glycation vol.140, pp.1, 2014, https://doi.org/10.1093/toxsci/kfu076
  13. Modified Lipoproteins by Acrylamide Showed More Atherogenic Properties and Exposure of Acrylamide Induces Acute Hyperlipidemia and Fatty Liver Changes in Zebrafish vol.15, pp.4, 2015, https://doi.org/10.1007/s12012-014-9294-7
  14. Cold-water extract of Korean Red Ginseng exhibits potent inhibitory effects against cholesteryl ester transfer protein activity and fructose-mediated glycation along with lipid-lowering activity in hyperlipidemic zebrafish 2017, https://doi.org/10.1016/j.jgr.2017.01.005
  15. Association between ApoA-II -265T/C polymorphism and oxidative stress in patients with type 2 diabetes mellitus vol.29, pp.7, 2015, https://doi.org/10.1016/j.jdiacomp.2015.05.024
  16. Pericoronary Adipose Tissue as Storage and Supply Site for Oxidized Low-Density Lipoprotein in Human Coronary Plaques vol.11, pp.3, 2016, https://doi.org/10.1371/journal.pone.0150862
  17. Modified apolipoprotein (apo) A-I by artificial sweetener causes severe premature cellular senescence and atherosclerosis with impairment of functional and structural properties of apoA-I in lipid-free and lipid-bound state vol.31, pp.5, 2011, https://doi.org/10.1007/s10059-011-1009-3
  18. Lipid signaling in the endothelium vol.319, pp.9, 2013, https://doi.org/10.1016/j.yexcr.2013.01.009
  19. ω-6 (18:2) and ω-3 (18:3) fatty acids in reconstituted high-density lipoproteins show different functionality of anti-atherosclerotic properties and embryo toxicity vol.26, pp.12, 2015, https://doi.org/10.1016/j.jnutbio.2015.08.008
  20. Reconstituted High-Density Lipoprotein Containing Human Growth Hormone-1 Shows Potent Tissue Regeneration Activity with Enhancement of Anti-Oxidant and Anti-Atherosclerotic Activities vol.18, pp.3, 2015, https://doi.org/10.1089/rej.2014.1644
  21. A proteoliposome containing apolipoprotein A-I mutant (V156K) enhances rapid tumor regression activity of human origin oncolytic adenovirus in tumor-bearing zebrafish and mice vol.34, pp.2, 2012, https://doi.org/10.1007/s10059-012-2291-4
  22. Impaired Antioxidant Ability of HDL and More Oxidized LDL are associated with Male Patients with Atrial Fibrillation vol.5, pp.2, 2016, https://doi.org/10.12997/jla.2016.5.2.145
  23. A novel modified paclitaxel-loaded discoidal recombinant high-density lipoproteins: Preparation, characterizations and in vivo evaluation vol.8, pp.1, 2013, https://doi.org/10.1016/j.ajps.2013.07.002
  24. Abnormalities in lipoprotein kinetics in Type 2 diabetes vol.5, pp.2, 2010, https://doi.org/10.2217/clp.10.2
  25. Association of paraoxonase-1 activity and major depressive disorder in patients with metabolic syndrome vol.35, pp.S2, 2015, https://doi.org/10.1007/s13410-015-0385-1
  26. Aspartame-fed zebrafish exhibit acute deaths with swimming defects and saccharin-fed zebrafish have elevation of cholesteryl ester transfer protein activity in hypercholesterolemia vol.49, pp.11, 2011, https://doi.org/10.1016/j.fct.2011.08.001
  27. 1,8-cineole protected human lipoproteins from modification by oxidation and glycation and exhibited serum lipid-lowering and anti-inflammatory activity in zebrafish vol.45, pp.10, 2012, https://doi.org/10.5483/BMBRep.2012.45.10.044
  28. Human pericoronary adipose tissue as storage and possible supply site for oxidized low-density lipoprotein and high-density lipoprotein in coronary artery vol.69, pp.1, 2017, https://doi.org/10.1016/j.jjcc.2016.03.015
  29. A Point Mutant of Apolipoprotein A-I (V156K) Showed Enhancement of Cellular Insulin Secretion and Potent Activity of Facultative Regeneration in Zebrafish vol.15, pp.3, 2012, https://doi.org/10.1089/rej.2011.1246
  30. Lycopene intervention reduces inflammation and improves HDL functionality in moderately overweight middle-aged individuals vol.24, pp.1, 2013, https://doi.org/10.1016/j.jnutbio.2012.03.015
  31. Modified High-Density Lipoproteins by Artificial Sweetener, Aspartame, and Saccharin, Showed Loss of Anti-atherosclerotic Activity and Toxicity in Zebrafish vol.15, pp.1, 2015, https://doi.org/10.1007/s12012-014-9273-z
  32. Consumption of high-dose vitamin C (1250 mg per day) enhances functional and structural properties of serum lipoprotein to improve anti-oxidant, anti-atherosclerotic, and anti-aging effects via regulation of anti-inflammatory microRNA vol.6, pp.11, 2015, https://doi.org/10.1039/C5FO00738K
  33. Incorporation of Human Growth Hormone-2 into Proteoliposome Enhances Tissue Regeneration with Anti-Oxidant and Anti-Senescence Activities vol.18, pp.1, 2015, https://doi.org/10.1089/rej.2014.1594
  34. Different Functional and Structural Characteristics between ApoA-I and ApoA-4 in Lipid-Free and Reconstituted HDL State: ApoA-4 Showed Less Anti-Atherogenic Activity vol.38, pp.6, 2015, https://doi.org/10.14348/molcells.2015.0052
  35. Anti-Aging and Tissue Regeneration Ability of Policosanol Along with Lipid-Lowering Effect in Hyperlipidemic Zebrafish via Enhancement of High-Density Lipoprotein Functionality vol.19, pp.2, 2016, https://doi.org/10.1089/rej.2015.1745
  36. High-density lipoprotein subfractions display proatherogenic properties in overweight and obese children vol.74, pp.3, 2013, https://doi.org/10.1038/pr.2013.93
  37. Preparation, Characterizations, and In Vitro Metabolic Processes of Paclitaxel-Loaded Discoidal Recombinant High-Density Lipoproteins vol.101, pp.8, 2012, https://doi.org/10.1002/jps.23210
  38. Bovine apolipoprotein (apo)A-I displays more enhanced antioxidant and anti-atherosclerotic activity in lipid-free and lipid-bound states than human and porcine apoA-I vol.32, pp.4, 2013, https://doi.org/10.3892/ijmm.2013.1473
  39. Propiedades antioxidantes y antiinflamatorias de las lipoproteínas de alta densidad vol.22, 2010, https://doi.org/10.1016/S0214-9168(10)70014-0
  40. Imaging of Native High-Density Lipoprotein in Human Coronary Plaques by Color Fluorescent Angioscopy vol.78, pp.7, 2014, https://doi.org/10.1253/circj.CJ-13-1585
  41. Breast Milk from Frequent Trans Fatty Acid Consumers Shows High Triglyceride and Glucose Levels, but Low Cholesterol and Apolipoprotein A-I levels, with Resulting Impaired In Vitro Zebrafish Embryo Growth and Survival vol.11, pp.5, 2016, https://doi.org/10.1089/bfm.2015.0181
  42. Fetal HDL/apoE: a novel regulator of gene expression in human placental endothelial cells vol.43, pp.22, 2011, https://doi.org/10.1152/physiolgenomics.00109.2011
  43. Whole Food versus Supplement: Comparing the Clinical Evidence of Tomato Intake and Lycopene Supplementation on Cardiovascular Risk Factors vol.5, pp.5, 2014, https://doi.org/10.3945/an.114.005231
  44. Consumption of Cuban Policosanol Improves Blood Pressure and Lipid Profile via Enhancement of HDL Functionality in Healthy Women Subjects: Randomized, Double-Blinded, and Placebo-Controlled Study vol.2018, pp.1942-0994, 2018, https://doi.org/10.1155/2018/4809525