Anti-inflammatory apoA-I-mimetic peptides bind oxidized lipids with much higher affinity than human apoA-I

Journal of Lipid Research

Volumn 49, Issue 11, 2008, Pages 2302-2311

  Van Lenten, Brian J ^a   Wagner, Alan C ^a   Jung, Chun Ling ^a   Ruchala, Piotr ^a   Waring, Alan J ^a   Lehrer, Robert I ^a   Watson, Andrew D ^a   Hama, Susan ^a   Navab, Mohamad ^a   Anantharamaiah, G M ^b   Fogelman, Alan M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Apolipoprotein A I; Atherosclerosis; Lipoproteins; Oxidized phospholipids

Indexed keywords

1 PALMITOYL 2 ARACHIDONOYLGLYCERO 3 PHOSPHATIDYLCHOLINE; ANALGESIC, ANTIINFLAMMATORY, ANTIRHEUMATIC AND ANTIGOUT AGENTS; ANTIINFLAMMATORY AGENT; APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDE 3F; PEPTIDE 3F 2; PEPTIDE 4F; PEPTIDE DERIVATIVE; PEPTIDE DEXTRO 4F; PHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG; APOA1 PROTEIN, HUMAN; AUTACOID; D 4F PEPTIDE; D-4F PEPTIDE; L 4F PEPTIDE; L-4F PEPTIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PEPTIDE; PHOSPHOLIPID;

ARTICLE; BINDING AFFINITY; BIOTINYLATION; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG BINDING; HUMAN; HUMAN CELL; ISOTHERM; LIPID OXIDATION; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN LIPID INTERACTION; SURFACE PLASMON RESONANCE; AMINO ACID SEQUENCE; CELL CULTURE; COMPARATIVE STUDY; LIPID PEROXIDATION; METABOLISM; MOLECULAR GENETICS; MOLECULAR MIMICRY; PHYSIOLOGY; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOLIPOPROTEIN A-I; CELLS, CULTURED; HUMANS; INFLAMMATION MEDIATORS; LIPID PEROXIDATION; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHOLIPIDS; PROTEIN BINDING;

EID: 57749104257     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800075-JLR200     Document Type: Article

References (40)

1. 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 class A amphipathic helical peptide. J. Lipid Res. 42: 1096-1104.
2. 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 apoA-I mimetic peptide synthesized from D-amino acids dramatically reduces atherosclerosis in mice independent of plasma cholesterol. Circulation. 105: 290-292.
3. 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.
4. Ou, Z., J. Ou, A. W. Ackerman, K. T. Oldham, and K. A. Pritchard, Jr. 2003. L-4F, an apolipoprotein A-1 mimetic, restores nitric oxide and superoxide anion balance in low-density lipoprotein-treated endothelial cells. Circulation. 107: 1520-1524.
5. Ou, J., Z. Ou, D. W. Jones, S. Holzhauer, O. A. Hatoum, A. W. Ackerman, D. W. Weihrauch, D. D. Gatterman, K. Guice, K. T. Oldham, et al. 2003. L-4F, an apolipoprotein A-I mimetic, dramatically improves vasodilation in hypercholesterolemia and sickle cell disease. Circulation. 107: 2337-2341.
6. Van Lenten, B. J., A. C. Wagner, M. Navab, G. M. Anantharamaiah, E. K. Hui, D. P. Nayak, and A. M. Fogelman. 2004. D-4F, an apolipoprotein A-I mimetic peptide, inhibits the inflammatory response induced by influenza A infection of human type II pneumocytes. Circulation. 110: 3252-3258.
7. 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, and A. M. Fogelman. 2004. Oral D-4F causes formation of pre-β 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.
8. Li, X., K-Y. Chyu, J. R. F. Neto, J. Yano, N. Nathwani, C. Ferreira, P. C. Dimayuga, B. Cercek, S. Kaul, and P. K. Shah. 2004. Differential effects of apolipoprotein A-I mimetic peptide on evolving and established atherosclerosis in apolipoprotein E-null mice. Circulation. 110: 1701-1705.
9. Epand, R. M., R. F. Epand, B. G. Sayer, G. Melacini, M. N. Palgunachari, J. P. Segrest, and G. M. Anantharamaiah. 2004. An apolipoprotein AI mimetic peptide: membrane interactions and the role of cholesterol. Biochemistry. 43: 5073-5083.
10. Datta, G., R. F. Epand, R. M. Epand, M. Chaddha, M. A. Kirksey, D. W. Garber, S. Lund-Katz, M. C. Phillips, S. Hama, M. Navab, et al. 2004. Aromatic residue position on the nonpolar face of class A amiphipathic helical peptides determines biological activity. J. Biol. Chem. 279: 26509-26517.
11. Navab, M., G. M. Anantharamaiah, S. Hama, G. Hough, S. T. Reddy, J. S. Frank, D. W. Garber, S. Handattu, and A. M. Fogelman. 2005. D-4F and statins synergize to render HDL anti-inflammatory in mice and monkeys and cause lesion regression in old apolipoprotein E-null mice. Arterioscler. Thromb. Vasc. Biol. 25: 1426-1432.
12. 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-knock out mice on Western diet. Circ. Res. 97: 1190-1197.
13. Kruger, A. L., S. Peterson, S. Turkseven, P. M. Kaminski, F. F. Zhang, S. Quan, M. S. Wolin, and N. G. Abraham. 2005. D-4F induces heme oxygenase-1 and extracellular superoxide dismutase, decreases endothelial cell sloughing, and improves vascular reactivity in rat model of diabetes. Circulation. 111: 3126-3134.
14. Gupta, H., L. Dai, G. Datta, D. W. Garber, H. Grenett, Y. Li, V. Mishra, M. N. PaIgunachari, S. Handattu, S. H. Gianturco, et al. 2005. Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein AI mimetic peptide. Circ. Res. 97: 236-243.
15. Tang, C., A. M. Wughan, G. M. Anantharamaiah, and J. F. Oram. 2006. Janus kinase 2 modulates the lipid-removing but not protein stabilizing interactions of amphipathic helices with ABCA1. J. Lipid Res. 47: 107-114.
16. Schnickel, G. T., G. R. Hsieh, E. L. Kachikwu, C. Garcia, A. Shefizadeh, M. G. Fishbein, and A. Ardehali. 2006. Cytoprotective gene HO-1 and chronic rejection in heart transplantation. Transplant. Proc. 38: 3259-3262.
17. 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.
18. Peterson, S. J., D. Husney, A. L. Kruger, R. Olszanecki, F. Ricci, L. F. Rodella, A. Stacchiotti, R. Rezzani, J. A. McClung, W. S. Aronow, et al. 2007. Long-term treatment with the apolipoprotein A1 mimetic peptide increases antioxidants and vascular repair in type I diabetic rats. J. Pharmacol, Exp. Ther. 322: 514-520.
19. Hsieh, G. R., G. T. Schnickel, C. Garcia, A. Shefizadeh, M. C. Fishbein, and A. Ardehali. 2007. Inflammation/oxidation in chronic rejection: apolipoprotein A-I mimetic peptide reduces chronic rejection of transplanted hearts. Transplantation. 84: 238-243.
20. Weihrauch, D., H. Xu, Y. Shi, J. Wang, J. Brien, D. W. Jones, S. Kaul, R. A. Komorowski, M. E. Csuka, K. T. Oldham, et al. 2007. Effects of D-4F on vasodilation, oxidative stress, angiostatin, myocardial inflammation, and angiogenic potential in tight-skin mice. Am. J. Physiol. Heart Circ. Physiol. 293: H1432-H1441.
21. 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.
22. 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 receptor-null mice fed a Western diet. J. Lipid Res. 49: 192-205.
23. Bloedon, L. T., R. L. 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.
24. 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.
25. 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.
26. Podrez, E. A., E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P. J. Finton, L. Shan, M. Febbraio, D. P. Hajjar, et al. 2002. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277: 38517-38523.
27. Gharavi, N. M., P. S. Gargalovic, I. Chang, J. A. Araujo, M. J. Clark, W. L. Szeto, A. D. Watson, A. J. Lusis, and J. A. Berliner. 2007. High-density lipoprotein modulates oxidized phospholipid signaling in human endothelial cells from proinflammatory to anti-inflammatory. Arterioscler. Thromb. Vasc. Biol. 27: 1346-1353.
28. Subbanagounder, G., J. W. Wong, H. Lee, K. F. Faull, E. Miller, J. L. Witztum, and J. A. Berliner. 2002. Epoxyisoprostane and epoxyclopentenne phospholipids regulate monocyte chemotactic protein-1 and interleukin-8 synthesis. Formation of these oxidized phospholipids in response to interleukin-1β. J. Biol. Chem. 277: 7271-7281.
29. Epand, R. M., R. F. Epand, B. G. Sayer, G. Datta, M. Chaddha, and G. M. Anantharamaiah. 2004. Two homologus apolipoprotein AI mimetic peptides. Relationship between membrane interactions and biological activity. J. Biol. Chem. 279: 51404-51414.
30. 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.
31. Fields, G. B., and R. L. Noble. 1990. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 35: 161-214.
32. Watson, A. D., N. Leitinger, M. Navab, K. F. Faull, H. Sohvi, J. L. Witztum, W. Palinski, D. Schwenke, R. G. Salomon, W. Sha, et al. 1997. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/ endothelial interactions and evidence for their presence in vivo. J. Biol. Chem. 272: 13597-13607.
33. Watson, A. D., G. Subbanagounder, K. F. Faull, M. Navab, M. E. Jung, A. M. Fogelman, and J. A. Berliner. 1999. Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein. J. Biol. Chem. 274: 24787-24798.
34. Gugiu, B. G., K. Mouillesseaux, V. Duong, T. Herzog, A. Hekimian, L. Koroniak, T. M. Vondriska, and A. D. Watson. 2008. Protein targets of oxidized phospholipids in endothelial cells. J. Lipid Res. 49: 510-520.
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. 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 anti-oxidative and anti-inflammatory properties of apolipoprotein A-I mimetic peptides. J. Lipid Res. 48: 1915-1923.
37. Wool, G. D., C. A. Reardon, and G. S. Getz. 2008. Apolipoprotein A-I mimetic peptide helix number and helix linker influence potentially anti-atherogenic properties. J. Lipid Res. 49: 1268-1283.
38. Forte, T. M., G. Subbanagounder, J. A. Berliner, P. J. Blanche, A. O. Clermont, Z. Jia, M. N. Oda, R. M. Krauss, and J. K. Bielicki. 2002. Altered activities of anti-atherogenic enzymes LCAT, paraoxonase, and platelet-activating factor acetylhydrolase in atherosclerosis-susceptible mice. J. Lipid Res. 43: 477-485.
39. Yeh, M., A. L. Cole, J. Choi, Y. Liu, D. Tulchinsky, J. H. Qiao, M. C. Fishbein, A. N. Dooley, T. Hovnanian, K. Mouilleseaux, et al. 2004. Role for sterol regulatory element-binding protein in activation of endothelial cells by phospholipid oxidation products. Circ. Res. 95: 780-788.
40. Gharavi, N. M., N. A. Baker, K. P. Mouillesseaux, W. Yeung, H. M. Honda, X. Hsieh, M. Yeh, E. J. Smart, and J. A. Berliner. 2006. Role of endothelial nitric oxide synthase in the regulation of SREBP activation by oxidized phospholipids. Circ. Res. 98: 768-776.