Enhancement by LDL of transfer of L-4F and oxidized lipids to HDL in C57BL/6J mice and human plasma

Journal of Lipid Research

Volumn 52, Issue 10, 2011, Pages 1795-1809

  Meriwether, David ^a   Imaizumi, Satoshi ^a   Grijalva, Victor ^a   Hough, Greg ^a   Vakili, Ladan ^a   Anantharamaiah, G M ^b   Farias Eisner, Robin ^a   Navab, Mohamad ^a   Fogelman, Alan M ^a   Reddy, Srinivasa T ^a   Shechter, Ishaiahu ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Apolipoprotein A I; Apolipoprotein A I mimetic peptides; Atherosclerosis; High density lipoprotein; Lipoproteins; Low density lipoprotein

Indexed keywords

15 HYDROPEROXYARACHIDONIC ACID; APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; PROTEIN L 4F; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CIRCULATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFLAMMATORY AGENTS; APOLIPOPROTEIN A-I; ATHEROSCLEROSIS; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MICE; MICE, INBRED C57BL; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; PEPTIDES;

EID: 80053205338     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M016741     Document Type: Article

References (55)

1. Anantharamaiah, G. M., J. L. Jones, C. G. Brouillette, C. F. Schmidt, B. H. Chung, T. A. Hughes, A. S. Bhown, and J. P. Segrest. 1985. Studies of synthetic peptide analogs of the amphipathic helix. Structure of complexes with dimyristoyl phosphatidylcholine. J. Biol. Chem. 260:10248-10255. (Pubitemid 16246560)
2. Anantharamaiah, G. M. 1986. Synthetic peptide analogs of apolipoproteins. Methods Enzymol. 128:627-647. (Pubitemid 16100920)
3. Segrest, J. P., R. L. Jackson, J. D. Morrisett, and A. M. Gotto, Jr. 1974. A molecular theory of lipid-protein interactions in the plasma lipoproteins. FEBS Lett. 38:247-258.
4. Segrest, J. P., M. K. Jones, H. De Loof, C. G. Brouillette, Y. V. Venkatachalapathi, and G. M. Anantharamaiah. 1992. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J. Lipid Res. 33:141-166.
5. Anantharamaiah, G. M., V. K. Mishra, D. W. Garber, G. Datta, S. P. Handattu, M. N. Palgunachari, M. Chaddha, M. Navab, S. T. Reddy, J. P. Segrest, et al. 2007. Structural requirements for antioxidative and anti-inflammatory properties of apolipoprotein A-I mimetic peptides. J. Lipid Res. 48:1915-1923. (Pubitemid 47360611)
6. Datta, G., M. Chaddha, S. Hama, M. Navab, A. M. Fogelman, D. W. Garber, V. K. Mishra, R. M. Epand, R. F. Epand, S. Lund-Katz, et al. 2001. Effects of increasing hydrophobicity on the physical-chemical and biological properties of a class A amphipathic helical peptide. J. Lipid Res. 42:1096-1104. (Pubitemid 32645791)
7. Plump, A. S., C. J. Scott, and J. L. Breslow. 1994. Human apolipoprotein A-I gene expression increases high density lipoprotein and suppresses atherosclerosis in the apolipoprotein E-deficient mouse. Proc. Natl. Acad. Sci. USA. 91:9607-9611. (Pubitemid 24297964)
8. Chiesa, G., and C. R. Sirtori. 2002. Use of recombinant apolipoproteins in vascular diseases: the case of apoA-I. Curr. Opin. Investig. Drugs. 3:420-426. (Pubitemid 34456061)
9. Nissen, S. E., T. Tsunoda, E. M. Tuzcu, P. Schoenhagen, C. J. Cooper, M. Yasin, G. M. Eaton, M. A. Lauer, W. S. Sheldon, C. L. Grines, et al. 2003. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA. 290:2292-2300. (Pubitemid 37430562)
10. Barter, P. J., S. Nicholls, K-A. Rye, G. M. Anantharamaiah, M. Navab, and A. M. Fogelman. 2004. Antiinflammatory properties of HDL. Circ. Res. 95:764-772. (Pubitemid 39390578)
11. Navab, M., S. Y. Hama, C. J. Cooke, G. M. Anantharamaiah, M. Chaddha, L. Jin, G. Subbanagounder, K. F. Faull, S. T. Reddy, N. E. Miller, et al. 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.
12. Navab, M., S. Y. Hama, G. M. Anantharamaiah, K. Hassan, G. P. Hough, A. D. Watson, S. T. Reddy, A. Sevanian, G. C. Fonarow, and A. M. Fogelman. 2000. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: steps 2 and 3. J. Lipid Res. 41:1495-1508.
13. 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. (Pubitemid 32366997)
14. Navab, M., G. M. Anantharamaiah, S. T. Reddy, S. Hama, G. Hough, V. R. Grijalva, N. Yu, B. J. Ansell, G. Datta, D. W. Garber, et al. 2005. Apolipoprotein A-I mimetic peptides. Arterioscler. Thromb. Vasc. Biol. 25:1325-1331.
15. Venkatachalapathi, Y. V., M. C. Phillips, R. M. Epand, R. F. Epand, E. M. Tytler, J. P. Segrest, and G. M. Anantharamaiah. 1993. Effect of end group blockage on the properties of a class A amphipathic helical peptide. Proteins. 15:349-359. (Pubitemid 23107033)
16. Getz, G. S., G. D. Wool, and C. A. Reardon. 2009. Apoprotein A-I mimetic peptides and their potential anti-atherogenic mechanisms of action. Curr. Opin. Lipidol. 20:171-175.
17. van Lenten, B. J., A. C. Wagner, M. Navab, G. M. Anantharamaiah, S. Hama, S. T. Reddy, and A. M. Fogelman. 2007. Lipoprotein inflammatory properties and serum amyloid A levels but not cholesterol levels predict lesion area in cholesterol-fed rabbits. J. Lipid Res. 48:2344-2353. (Pubitemid 350058746)
18. Navab, M., G. M. Anantharamaiah, S. Hama, D. W. Garber, M. Chaddha, G. Hough, R. Lallone, and A. M. Fogelman. 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. (Pubitemid 34106174)
19. Navab, M., I. Shechter, G. M. Anantharamaiah, S. T. Reddy, B. J. van Lenten, and A. M. Fogelman. 2010. Structure and function of HDL mimetics. Arterioscler. Thromb. Vasc. Biol. 30:164-168.
20. 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.
21. Navab, M., G. M. Anantharamaiah, and A. M. Fogelman. 2008. The effect of apolipoprotein mimetic peptides in inflammatory disorders other than atherosclerosis. Trends Cardiovasc. Med. 18:61-66. (Pubitemid 351282495)
22. Charles-Schoeman, C., M. L. Banquerigo, S. Hama, M. Navab, G. S. Park, B. J. van Lenten, A. C. Wagner, A. M. Fogelman, and E. Brahn. 2008. Treatment with an apolipoprotein A-1 mimetic peptide in combination with pravastatin inhibits collagen-induced arthritis. Clin. Immunol. 127:234-244.
23. Buga, G. M., J. S. Frank, G. A. Mottino, A. Hakhamian, A. Narasimha, A. D. Watson, B. Yekta, M. Navab, S. T. Reddy, G. M. Anantharamaiah, et al. 2008. D-4F reduces EO6 immunoreactivity, SREBP-1c mRNA levels, and renal inflammation in LDL receptornull mice fed a Western diet. J. Lipid Res. 49:192-205.
24. van Lenten, B. J., A. C. Wagner, G. M. Anantharamaiah, D. W. Garber, M. C. Fishbein, L. Adhikary, D. P. Nayak, S. Hama, M. Navab, and A. M. Fogelman. 2002. Influenza infection promotes macrophage traffic into arteries of mice that is prevented by D-4F, an apolipoprotein A-I mimetic peptide. Circulation. 106:1127-1132 (Pubitemid 34970855)
25. Buga, G. M., J. S. Frank, G. A. Mottino, M. Hendizadeh, A. Hakhamian, J. H. Tillisch, S. T. Reddy, M. Navab, G. M. Anantharamaiah, L. J. Ignarro, et al. 2006. D-4F decreases brain arteriole inflammation and improves cognitive performance in LDL receptor-null mice on a Western diet. J. Lipid Res. 47:2148-2160. (Pubitemid 44936125)
26. Handattu, S. P., D. W. Garber, C. E. Monroe, T. van Groen, I. Kadish, G. Nayyar, D. Cao, M. N. Palgunachari, L. Li, and G. M. Anantharamaiah. 2009. Oral apolipoprotein A-I mimetic peptide improves cognitive function and reduces amyloid burden in a mouse model of Alzheimer's disease. Neurobiol. Dis. 34:525-534.
27. 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.
28. Navab, M., S. T. Reddy, G. M. Anantharamaiah, S. Imaizumi, G. Hough, S. Hama, and A. M. Fogelman. 2011. Intestine maybe a major site of action for the ApoA-I mimetic peptide 4F whether the peptide is administered subcutaneously or orally. J Lipid Res. 52: 1200-1210.
29. Navab, M., G. M. Anantharamaiah, S. T. Reddy, S. Hama, G. Hough, V. R. Grijalva, A. C. Wagner, J. S. Frank, G. Datta, D. Garber, et al. 2004. 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. 109:3215-3220.
30. Troutt, J. S., W. E. Alborn, M. K. Mosior, J. Dai, A. T. Murphy, T. P. Beyer, Y. Zhang, G. Cao, and R. J. Konrad. 2008. An apolipoprotein A-I mimetic dose-dependently increases the formation of prebeta1 HDL in human plasma. J. Lipid Res. 49:581-587.
31. Fielding, C. J., and P. E. Fielding. 2001. Cellular cholesterol efflux. Biochim. Biophys. Acta. 1533:175-189. (Pubitemid 33127270)
32. 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.
33. Berliner, J. A., and A. D. Watson. 2005. A role for oxidized phospholipids in atherosclerosis. N. Engl. J. Med. 353:9-11. (Pubitemid 41007802)
34. Natarajan, R., and J. L. Nadler. 2004. Lipid inflammatory mediators in diabetic vascular disease. Arterioscler. Thromb. Vasc. Biol. 24:1542-1548. (Pubitemid 39180875)
35. Epand, R. F., V. K. Mishra, M. N. Palgunachari, G. M. Anantharamaiah, and R. M. Epand. 2009. Anti-inflammatory peptides grab on to the whiskers of atherogenic oxidized lipids. Biochim. Biophys. Acta. 1788:1967-1975.
36. Leitinger, N. 2008. The role of phospholipid oxidation products in inflammatory and autoimmune diseases: evidence from animal models and in humans. Subcell. Biochem. 49:325-350.
37. Ferguson, L. R. 2010. Chronic inflammation and mutagenesis. Mutat. Res. 690:3-11.
38. Moreno, J. J. 2009. New aspects of the role of hydroxyeicosatetraenoic acids in cell growth and cancer development. Biochem. Pharmacol. 77:1-10.
39. Morgantini, C., S. Imaizumi, V. Grijalva, M. Navab, A. M. Fogelman, and S. T. Reddy. 2010. Apolipoprotein A-I mimetic peptides prevent atherosclerosis development and reduce plaque inflammation in a murine model of diabetes. Diabetes. 59:3223-3228.
40. Imaizumi, S., V. Grijalva, M. Navab, B. J. van Lenten, A. C. Wagner, G. M. Anantharamiah, A. M. Fogelman, and S. T. Reddy. 2010. L-4F differentially alters plasma levels of oxidized fatty acids resulting in more anti-inflammatory HDL in mice. Drug Metab. Lett. 4:139-148.
41. 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.
42. Jones, M. K., G. M. Anantharamaiah, and J. P. Segrest. 1992. Computer programs to identify and classify amphipathic alpha helical domains. J. Lipid Res. 33:287-296.
43. Palgunachari, M. N., V. K. Mishra, S. Lund-Katz, M. C. Phillips, S. O. Adeyeye, S. Alluri, G. M. Anantharamaiah, and J. P. Segrest. 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. (Pubitemid 26056254)
44. Handattu, S. P., D. W. Garber, D. C. Horn, D. W. Hughes, B. Berno, A. D. Bain, V. K. Mishra, M. N. Palgunachari, G. Datta, G. M. Anantharamaiah, et al. 2007. ApoA-I mimetic peptides with differing ability to inhibit atherosclerosis also exhibit differences in their interactions with membrane bilayers. J. Biol. Chem. 282:1980-1988. (Pubitemid 47076708)
45. Havel, R. J., H. A. Eder, and J. H. Bragdon. 1955. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34:1345-1353.
46. Eisenberg, S. 1991. Plasma lipoproteins: structure, composition, classification, and metabolism. In Primary Hyperlipoproteinemias. G. Steiner and E. Shafrir, editors. McGraw-Hill, New York, Health Professions Division. pp. 23-41.
47. Garber, D. W., Y. V. Venkatachalapathi, K. B. Gupta, J. Ibdah, M. C. Phillips, J. B. Hazelrig, J. P. Segrest, and G. M. Anantharamaiah. 1992. Turnover of synthetic class A amphipathic peptide analogues of exchangeable apolipoproteins in rats. Correlation with physical properties. Arterioscler. Thromb. 12:886-894.
48. Morton, R. E., and D. J. Greene. 1994. Regulation of lipid transfer between lipoproteins by an endogenous plasma protein: selective inhibition among lipoprotein classes. J. Lipid Res. 35:836-847. (Pubitemid 24157235)
49. Christison, J. K., K. A. Rye, and R. Stocker. 1995. Exchange of oxidized cholesteryl linoleate between LDL and HDL mediated by cholesteryl ester transfer protein. J. Lipid Res. 36:2017-2026.
50. Asztalos, B. F., K. V. Horvath, K. Kajinami, C. Nartsupha, C. E. Cox, M. Batista, E. J. Schaefer, A. Inazu, and H. Mabuchi. 2004. Apolipoprotein composition of HDL in cholesteryl ester transfer protein deficiency. J. Lipid Res. 45:448-455. (Pubitemid 38337991)
51. Tall, A. 1995. Plasma lipid transfer proteins. Annu. Rev. Biochem. 64:235-257.
52. Watson, C. E., N. Weissbach, L. Kjems, S. Ayalasomayajula, Y. Zhang, I. Chang, M. Navab, S. Hama, G. Hough, S. T. Reddy, et al. 2011. Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function. J. Lipid Res. 52:361-373.
53. Windmueller, H. G., and A. L. Wu. 1981. Biosynthesis of plasma apolipoproteins by rat small intestine without dietary or biliary fat. J. Biol. Chem. 256:3012-3016. (Pubitemid 11067299)
54. Brunham, L. R., J. K. Kruit, J. Iqbal, C. Fievet, J. M. Timmins, T. D. Pape, B. A. Coburn, N. Bissada, B. Staels, A. K. Groen, et al. 2006. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 116:1052-1062.
55. Bisgaier, C. L., and R. M. Glickman. 1983. Intestinal synthesis, secretion, and transport of lipoproteins. Annu. Rev. Physiol. 45:625-636.