In vivo efficacy of HDL-like nanolipid particles containing multivalent peptide mimetics of apolipoprotein A-I

Journal of Lipid Research

Volumn 55, Issue 10, 2014, Pages 2053-2063

  Zhao, Yannan ^a   Black, Audrey S ^a   Bonnet, David J ^a   Maryanoff, Bruce E ^a   Curtiss, Linda K ^a   Leman, Luke J ^a   Ghadiri, M Reza ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Amphiphilic; Atherosclerosis; Cholesterol; Drug development; Nanoparticle; helix

Indexed keywords

15 HYDROXYICOSATETRAENOIC ACID; AGENTS AFFECTING LIPID METABOLISM; ALANINE AMINOTRANSFERASE; APOLIPOPROTEIN A1; ASPARTATE AMINOTRANSFERASE; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; MONOMERIC CYSTYLGLYCYLVALYLLEUCYLGLUTAMYLSERYLPHENYLALANYLLYSYLALANYLSERYLPHENYLALANYLLEUCYLSERYLALANYLLEUCYLGLUTAMYLGLUTAMYLTRYPTOPHYLTHREONYLLYSYLLYSYLLEUCYLGLUTAMINAMIDE; NANOPARTICLE; SERUM AMYLOID A; TRIACYLGLYCEROL; TRIMERIC CYSTYLGLYCYLVALYLLEUCYLGLUTAMYLSERYLPHENYLALANYLLYSYLALANYLSERYLPHENYLALANYLLEUCYLSERYLALANYLLEUCYLGLUTAMYLGLUTAMYLTRYPTOPHYLTHREONYLLYSYLLYSYLLEUCYLGLUTAMINAMIDE; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PEPTIDOMIMETIC AGENT;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AREA UNDER THE CURVE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; ENZYME ACTIVITY; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; TREATMENT DURATION; ANIMAL; CHEMISTRY; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; APOLIPOPROTEIN A-I; FEMALE; LIPOPROTEINS, HDL; MICE; MICE, KNOCKOUT; NANOPARTICLES; PEPTIDOMIMETICS; RECEPTORS, LDL;

EID: 84907539382     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M049262     Document Type: Article

References (74)

1. Spillmann, F., H-P. Schultheiss, C. Tschoepe, and S. Van Linthout. 2010. High-density lipoprotein-raising strategies: update 2010. Curr. Pharm. Des. 16: 1517-1530.
2. Murphy, A. J., A. T. Remaley, and D. Sviridov. 2010. HDL therapy: two kinds of right? Curr. Pharm. Des. 16: 4134-4147.
3. Tardif, J. C. 2010. Emerging high-density lipoprotein infusion therapies: fulfilling the promise of epidemiology? J. Clin. Lipidol. 4: 399-404.
4. Patel, S., B. A. Di Bartolo, S. Nakhla, A. K. Heather, T. W. Mitchell, W. Jessup, D. S. Celermajer, P. J. Barter, and K-A. Rye. 2010. Anti-inflammatory effects of apolipoprotein A-I in the rabbit. Atherosclerosis. 212: 392-397.
5. Valenta, D. T., J. J. Bulgrien, C. L. Banka, and L. K. Curtiss. 2006. Overexpression of human apoA-I transgene provides long-term atheroprotection in LDL receptor-deficient mice. Atherosclerosis. 189: 255-263.
6. Shah, P. K., J. Yano, O. Reyes, K-Y. Chyu, S. Kaul, C. L. Bisgaier, S. Drake, and B. Cercek. 2001. High-dose recombinant apolipoprotein A-I Milano mobilizes tissue cholesterol and rapidly reduces plaque lipid and macrophage content in apolipoprotein E-deficient mice. Potential implications for acute plaque stabilization. Circulation. 103: 3047-3050.
7. Miyazaki, A., S. Sakuma, W. Morikawa, T. Takiue, F. Miake, T. Terano, M. Sakai, H. Hakamata, Y. Sakamoto, M. Natio, et al. 1995. Intravenous injection of rabbit apolipoprotein A-I inhibits the progression of atherosclerosis in cholesterol-fed rabbits. Arterioscler. Thromb. Vasc. Biol. 15: 1882-1888.
8. Rubin, E. M., R. M. Krauss, E. A. Spangler, J. G. Verstuyft, and S. M. Clift. 1991. Inhibition of early atherogenesis in transgenic mice by human apolipoprotein A-I. Nature. 353: 265-267.
9. Smits, L. P., R. S. Kootte, and E. S. Stroes. 2014. Reversal of atherosclerosis with apolipoprotein A1: Back to basics. Atherosclerosis. 232: 217-219.
10. Tardif, J. C., C. M. Ballantyne, P. Barter, J. L. Dasseux, Z. A. Fayad, M. C. Guertin, J. J. P. Kastelein, C. Keyserling, H. Klepp, W. Koenig, et al. 2014. Effects of the high-density lipoprotein mimetic agent CER-001 on coronary atherosclerosis in patients with acute coronary syndromes: a randomized trial. Eur. Heart J. epub ahead of print. doi:10.1093/eurheartj/ehu171.
11. Nicholls, S. J. 2012. Is niacin ineffective? Or did AIM-HIGH miss its target? Cleve. Clin. J. Med. 79: 38-43.
12. Joy, T. R., and R. A. Hegele. 2008. The failure of torcetrapib: what have we learned? Br. J. Pharmacol. 154: 1379-1381.
13. Rader, D. J., and A. R. Tall. 2012. The not-so-simple HDL story: Is it time to revise the HDL cholesterol hypothesis? Nat. Med. 18: 1344-1346.
14. Voight, B. F., G. M. Peloso, M. Orho-Melander, R. Frikke-Schmidt, M. Barbalic, M. K. Jensen, G. Hindy, H. Hólm, E. L. Ding, T. Johnson, et al. 2012. Plasma HDL cholesterol and risk of myocardial infarction: a mendelian randomisation study. Lancet. 380: 572-580.
15. Soran, H., S. Hama, R. Yadav, and P. N. Durrington. 2012. HDL functionality. Curr. Opin. Lipidol. 23: 353-366.
16. Heinecke, J. W. 2012. A new era for quantifying HDL and cardiovascular risk? Nat. Med. 18: 1346-1347.
17. Besler, C., T. F. Luscher, and U. Landmesser. 2012. Molecular mechanisms of vascular effects of high-density lipoprotein: alterations in cardiovascular disease. EMBO Mol. Med. 4: 251-268.
18. Rothblat, G. H., and M. C. Phillips. 2010. High-density lipoprotein heterogeneity and function in reverse cholesterol transport. Curr. Opin. Lipidol. 21: 229-238.
19. Camont, L., M. J. Chapman, and A. Kontush. 2011. Biological activities of HDL subpopulations and their relevance to cardiovascular disease. Trends Mol. Med. 17: 594-603.
20. Redondo, S., J. Martinez-Gonzalez, C. Urraca, and T. Tejerina. 2011. Emerging therapeutic strategies to enhance HDL function. Lipids Health Dis. 10: 175.
21. Katsuura, G., S. Shinohara, H. Shintaku, M. Eigyo, and A. Matsushita. 1991. Protective effect of CCK-8 and ceruletide on glutamate-induced neuronal cell death in rat neuron cultures: possible involvement of CCK-B receptors. Neurosci. Lett. 132: 159-162.
22. Getz, G. S., G. D. Wool, and C. A. Reardon. 2010. Biological properties of apolipoprotein A-I mimetic peptides. Curr. Atheroscler. Rep. 12: 96-104.
23. Osei-Hwedieh, D. O., M. Amar, D. Sviridov, and A. T. Remaley. 2011. Apolipoprotein mimetic peptides: mechanisms of action as anti-atherogenic agents. Pharmacol. Ther. 130: 83-91.
24. Van Lenten, B. J., A. C. Wagner, G. M. Anantharamaiah, M. Navab, S. T. Reddy, G. M. Buga, and A. M. Fogelman. 2009. Apolipoprotein A-I mimetic peptides. Curr. Atheroscler. Rep. 11: 52-57.
25. Gordon, S. M., and W. S. Davidson. 2012. Apolipoprotein A-I mimetics and high-density lipoprotein function. Curr. Opin. Endocrinol. Diabetes Obes. 19: 109-114.
26. Hovingh, G. K., A. E. Bochem, and J. J. Kastelein. 2010. Apolipoprotein A-I mimetic peptides. Curr. Opin. Lipidol. 21: 481-486.
27. Joy, T. R. 2012. Novel HDL-based therapeutic agents. Pharmacol. Ther. 135: 18-30.
28. D'Souza, W., J. A. Stonik, A. Murphy, S. J. Demosky, A. A. Sethi, X. L. Moore, J. Chin-Dusting, A. T. Remaley, and D. Sviridov. 2010. Structure/function relationships of apolipoprotein A-I mimetic peptides: implications for antiatherogenic activities of high-density lipoprotein. Circ. Res. 107: 217-227.
29. Wool, G. D., T. Vaisar, C. A. Reardon, and G. S. Getz. 2009. An apoA-I mimetic peptide containing a proline residue has greater in vivo HDL binding and anti-inflammatory ability than the 4F peptide. J. Lipid Res. 50: 1889-1900.
30. Lu, S. C., L. Atangan, K. Won Kim, M. M. Chen, R. Komorowski, C. Chu, J. Han, S. Hu, W. Gu, M. Veniant, et al. 2012. An apoA-I mimetic peptibody generates HDL-like particles and increases alpha-1 HDL subfraction in mice. J. Lipid Res. 53: 643-652.
31. Zhao, Y., T. Imura, L. J. Leman, L. K. Curtiss, B. E. Maryanoff, and M. R. Ghadiri. 2013. Mimicry of high-density lipoprotein: functional peptide-lipid nanoparticles based on multivalent peptide constructs. J. Am. Chem. Soc. 135: 13414-13424.
32. Ou, J., J. Wang, H. Xu, Z. Ou, M. G. Sorci-Thomas, D. W. Jones, P. Signorino, J. C. Densmore, S. Kaul, K. T. Oldham, et al. 2005. Effects of D-4F on vasodilation and vessel wall thickness in hypercholesterolemic LDL receptor-null and LDL receptor/apolipoprotein A-I double-knockout mice on Western diet. Circ. Res. 97: 1190-1197.
33. Navab, M., G. M. Anantharamaiah, and A. M. Fogelman. 2005. An apolipoprotein A-I mimetic works best in the presence of apolipoprotein A-I. Circ. Res. 97: 1085-1086.
34. Navab, M. 2002. Oral administration of an apo A-I mimetic peptide synthesized from D-amino acids dramatically reduces atherosclerosis in mice independent of plasma cholesterol. Circulation. 105: 290-292.
35. Garber, D. W., G. Datta, M. Chaddha, M. N. Palgunachari, S. Y. Hama, M. Navab, A. M. Fogelman, J. P. Segrest, and G. M. Anantharamaiah. 2001. A new synthetic class A amphipathic peptide analogue protects mice from diet-induced atherosclerosis. J. Lipid Res. 42: 545-552.
36. Handattu, S. P., G. Nayyar, D. W. Garber, M. N. Palgunachari, C. E. Monroe, T. D. Keenum, V. K. Mishra, G. Datta, and G. M. Anantharamaiah. 2013. Two apolipoprotein E mimetic peptides with similar cholesterol reducing properties exhibit differential atheroprotective effects in LDL-R null mice. Atherosclerosis. 227: 58-64.
37. Navab, M., S. T. Reddy, B. J. Van Lenten, G. M. Buga, G. Hough, A. C. Wagner, and A. M. Fogelman. 2012. High-density lipoprotein and 4F peptide reduce systemic inflammation by modulating intestinal oxidized lipid metabolism: novel hypotheses and review of literature. Arterioscler. Thromb. Vasc. Biol. 32: 2553-2560.
38. Navab, M., S. T. Reddy, G. M. Anantharamaiah, S. Imaizumi, G. Hough, S. Hama, and A. M. Fogelman. 2011. Intestine may be a major site of action for the apoA-I mimetic peptide 4F whether administered subcutaneously or orally. J. Lipid Res. 52: 1200-1210.
39. Van Lenten, B. J., A. C. Wagner, C-L. Jung, P. Ruchala, A. J. Waring, R. I. Lehrer, A. D. Watson, S. Hama, M. Navab, G. M. Anantharamaiah, et al. 2008. Anti-inflammatory apoA-I-mimetic peptides bind oxidized lipids with much higher affinity than human apoA-I. J. Lipid Res. 49: 2302-2311.
40. Mullick, A. E., P. S. Tobias, and L. K. Curtiss. 2005. Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 115: 3149-3156.
41. Thompson, G. R., M. MacMahon, and P. Claes. 1970. Precipitation by neomycin compounds of fatty acid and cholesterol from mixed micellar solutions. Eur. J. Clin. Invest. 1: 40-47.
42. Miettinen, T. A. 1982. Effects of neomycin alone and in combination with cholestyramine on serum methyl sterols and conversion of acetate and mevalonate to cholesterol. Scand. J. Clin. Lab. Invest. 42: 189-196.
43. Bergen, S. S., T. B. Van Itallie, D. M. Tennent, and W. H. Sebrell. 1959. Effect of an anion exchange resin on serum cholesterol in man. Proc. Soc. Exp. Biol. Med. 102: 676-679.
44. Grundy, S. M. 1972. Treatment of hypercholesterolemia by interference with bile acid metabolism. Arch. Intern. Med. 130: 638-648.
45. Raederstorff, D. G., M. F. Schlachter, V. Elste, and P. Weber. 2003. Effect of EGCG on lipid absorption and plasma lipid levels in rats. J. Nutr. Biochem. 14: 326-332.
46. Kirana, C., P. F. Rogers, L. E. Bennett, M. Y. Abeywardena, and G. S. Patten. 2005. Naturally derived micelles for rapid in vitro screening of potential cholesterol-lowering bioactives. J. Agric. Food Chem. 53: 4623-4627.
47. Lamousé-Smith, E. S., A. Tzeng, and M. N. Starnbach. 2011. The intestinal flora is required to support antibody responses to systemic immunization in infant and germ free mice. PLoS ONE. 6: e27662.
48. Hu, X., T. Wang, W. Li, F. Jin, and L. Wang. 2013. Effects of NS lactobacillus strains on lipid metabolism of rats fed a high-cholesterol diet. Lipids Health Dis. 12: 67.
49. Guo, X., X. Xia, R. Tang, J. Zhou, H. Zhao, and K. Wang. 2008. Development of a real-time PCR method for Firmicutes and Bacteroidetes in feces and its application to quantify intestinal population of obese and lean pigs. Lett. Appl. Microbiol. 47: 367-373.
50. Van Craeyveld, E., S. C. Gordts, N. Singh, F. Jacobs, and B. De Geest. 2012. A critical reassessment of murine and rabbit models of atherosclerosis: focus on lesion progression and remodelling. Acta Cardiol. 67: 11-21.
51. Zadelaar, S., R. Kleemann, L. Verschuren, J. de Vries-Van der Weij, J. van der Hoorn, H. M. Princen, and T. Kooistra. 2007. Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler. Thromb. Vasc. Biol. 27: 1706-1721.
52. Chattopadhyay, A., M. Navab, G. Hough, F. Gao, D. Meriwether, V. Grijalva, J. R. Springstead, M. N. Palgnachari, R. Namiri-Kalantari, F. Su, et al. 2013. A novel approach to oral apoA-I mimetic therapy. J. Lipid Res. 54: 995-1010. [Erratum. 2013. J. Lipid Res. 54: 3220.]
53. Navab, M., G. Hough, G. M. Buga, F. Su, A. C. Wagner, D. Meriwether, A. Chattopadhyay, F. Gao, V. Grijalva, J. S. Danciger, et al. 2013. Transgenic 6F tomatoes act on the small intestine to prevent systemic inflammation and dyslipidemia caused by Western diet and intestinally derived lysophosphatidic acid. J. Lipid Res. 54: 3403-3418.
54. Bloedon, L. T., R. Dunbar, D. Duffy, P. Pinell-Salles, R. Norris, B. J. DeGroot, R. Movva, M. Navab, A. M. Fogelman, and D. J. Rader. 2008. Safety, pharmacokinetics, and pharmacodynamics of oral apoA-I mimetic peptide D-4F in high-risk cardiovascular patients. J. Lipid Res. 49: 1344-1352.
55. Bielicki, J. K., H. Zhang, Y. Cortez, Y. Zheng, V. Narayanaswami, A. Patel, J. Johansson, and S. Azhar. 2010. A new HDL mimetic peptide that stimulates cellular cholesterol efflux with high efficiency greatly reduces atherosclerosis in mice. J. Lipid Res. 51: 1496-1503.
56. Handattu, S. P., G. Datta, R. M. Epand, R. F. Epand, M. N. Palgunachari, V. K. Mishra, C. E. Monroe, T. D. Keenum, M. Chaddha, G. M. Anantharamaiah, et al. 2010. Oral administration of L-mR18L, a single domain cationic amphipathic helical peptide, inhibits lesion formation in ApoE null mice. J. Lipid Res. 51: 3491-3499.
57. Benoit, P., F. Emmanuel, J. M. Caillaud, L. Bassinet, G. Castro, P. Gallix, J-C. Fruchart, D. Branellec, P. Denefle, and N. Duverger. 1999. Somatic gene transfer of human apoA-I inhibits atherosclerosis progression in mouse models. Circulation. 99: 105-110.
58. Busseuil, D., Y. Shi, M. Mecteau, G. Brand, A. E. Kernaleguen, E. Thorin, J. G. Latour, E. Rheaume, and J. C. Tardif. 2008. Regression of aortic valve stenosis by ApoA-I mimetic peptide infusions in rabbits. Br. J. Pharmacol. 154: 765-773.
59. Navab, M., S. T. Reddy, G. M. Anantharamaiah, G. Hough, G. M. Buga, J. Danciger, and A. M. Fogelman. 2012. D-4F-mediated reduction in metabolites of arachidonic and linoleic acids in the small intestine is associated with decreased inflammation in low-density lipoprotein receptor-null mice. J. Lipid Res. 53: 437-445.
60. Navab, M., P. Ruchala, A. J. Waring, R. I. Lehrer, S. Hama, G. Hough, M. N. Palgunachari, G. M. Anantharamaiah, and A. M. Fogelman. 2009. A novel method for oral delivery of apolipoprotein mimetic peptides synthesized from all L-amino acids. J. Lipid Res. 50: 1538-1547.
61. Su, F., K. R. Kozak, S. Imaizumi, F. Gao, M. W. Amneus, V. Grijalva, C. Ng, A. Wagner, G. Hough, G. Farias-Eisner, et al. 2010. Apolipoprotein A-I (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc. Natl. Acad. Sci. USA. 107: 19997-20002.
62. Navab, M., S. Hama, G. Hough, and A. M. Fogelman. 2003. Oral synthetic phospholipid (DMPC) raises high-density lipoprotein cholesterol levels, improves high-density lipoprotein function, and markedly reduces atherosclerosis in apolipoprotein E-null mice. Circulation. 108: 1735-1739.
63. Cho, B. H., J. R. Park, M. T. Nakamura, B. M. Odintsov, M. A. Wallig, and B. H. Chung. 2010. Synthetic dimyristoylphosphatidylcholine liposomes assimilating into high-density lipoprotein promote regression of atherosclerotic lesions in cholesterol-fed rabbits. Exp. Biol. Med. (Maywood). 235: 1194-1203.
64. David, L. A., C. F. Maurice, R. N. Carmody, D. B. Gootenberg, J. E. Button, B. E. Wolfe, A. V. Ling, A. S. Devlin, Y. Varma, M. A. Fischbach, et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 505: 559-563.
65. Serino, M., E. Luche, S. Gres, A. Baylac, M. Berge, C. Cenac, A. Waget, P. Klopp, J. Iacovoni, C. Klopp, et al. 2012. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 61: 543-553.
66. Daniel, H., A. M. Gholami, D. Berry, C. Desmarchelier, H. Hahne, G. Loh, S. Mondot, P. Lepage, M. Rothballer, A. Walker, et al. 2014. High-fat diet alters gut microbiota physiology in mice. ISME J. 8: 295-308.
67. Turnbaugh, P. J., F. Backhed, L. Fulton, and J. I. Gordon. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 3: 213-223.
68. Hildebrandt, M. A., C. Hoffmann, S. A. Sherrill-Mix, S. A. Keilbaugh, M. Hamady, Y. Y. Chen, R. Knight, R. S. Ahima, F. Bushman, and G. D. Wu. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 137: 1716-1724.
69. Turnbaugh, P. J., V. K. Ridaura, J. J. Faith, F. E. Rey, R. Knight, and J. I. Gordon. 2009. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1: ra14.
70. Sonnenburg, J. L., and M. A. Fischbach. 2011. Community health care: therapeutic opportunities in the human microbiome. Sci. Transl. Med. 3: 78ps12.
71. Lemon, K. P., G. C. Armitage, D. A. Relman, and M. A. Fischbach. 2012. Microbiota-targeted therapies: an ecological perspective. Sci. Transl. Med. 4: rv5.
72. Wang, Z., E. Klipfell, B. J. Bennett, R. Koeth, B. S. Levison, B. DuGar, A. E. Feldstein, E. B. Britt, X. Fu, Y-M. Chung, et al. 2011. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 472: 57-63.
73. Tang, W. H. W., Z. Wang, B. S. Levison, R. A. Koeth, E. B. Britt, X. Fu, Y. Wu, and S. L. Hazen. 2013. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N. Engl. J. Med. 368: 1575-1584.
74. Wang, D. Q. H. 2007. Regulation of intestinal cholesterol absorption. Annu. Rev. Physiol. 69: 221-248.