Anti-inflammatory peptides grab on to the whiskers of atherogenic oxidized lipids

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 9, 2009, Pages 1967-1975

  Epand, Raquel F ^a   Mishra, Vinod K ^b   Palgunachari, Mayakonda N ^b   Anantharamaiah, G M ^b,c   Epand, Richard M ^a  

^a MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Amphipathic helix; Atherosclerosis; Fluorescence; Lipid oxidation product; Peptide lipid interaction

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; APOLIPOPROTEIN A1; LEUCINE; LIPID; LIPOPROTEIN; LIPOSOME; PEPTIDE 2F; PEPTIDE 4F; PEPTIDE DERIVATIVE; PHENYLALANINE; UNCLASSIFIED DRUG;

ARTICLE; ATHEROGENESIS; BINDING AFFINITY; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DRUG ACTIVITY; DRUG POTENCY; ISOTHERM; ISOTHERMAL TITRATION CALORIMETRY; LIPID OXIDATION; LIPID VESICLE; PRIORITY JOURNAL; SOLID PHASE EXTRACTION; SOLUBILIZATION;

ANTI-INFLAMMATORY AGENTS; ATHEROSCLEROSIS; CALORIMETRY, DIFFERENTIAL SCANNING; LIPID BILAYERS; LIPIDS; OXIDATION-REDUCTION; PEPTIDES; PHOSPHATIDYLCHOLINES; PHOSPHOLIPID ETHERS; PHOSPHORYLCHOLINE;

EID: 68749091024     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.06.015     Document Type: Article

References (66)

1. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340 (1999) 115-126
2. Madjid M., Awan I., Willerson J.T., and Casscells S.W. Leukocyte count and coronary heart disease: implications for risk assessment. J Am. Coll. Cardiol. 44 (2004) 1945-1956
3. Haskard D.O. Accelerated atherosclerosis in inflammatory rheumatic diseases. Scand. J. Rheumatol. 33 (2004) 281-292
4. Stocker R., and Keaney J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 84 (2004) 1381-1478
5. Paoletti R., Gotto Jr. A.M., and Hajjar D.P. Inflammation in atherosclerosis and implications for therapy. Circulation 109 (2004) III20-III26
6. Willerson J.T., and Ridker P.M. Inflammation as a cardiovascular risk factor. Circulation 109 (2004) II2-10
7. Jialal I., Devaraj S., and Venugopal S.K. C-reactive protein: risk marker or mediator in atherothrombosis?. Hypertension 44 (2004) 6-11
8. Linton M.F., and Fazio S. Cyclooxygenase-2 and inflammation in atherosclerosis. Curr. Opin. Pharmacol. 4 (2004) 116-123
9. Spieker L.E., Ruschitzka F., Luscher T.F., and Noll G. HDL and inflammation in atherosclerosis. Curr. Drug Targets. Immune. Endocr. Metabol. Disord. 4 (2004) 51-57
10. Meng C.Q. Inflammation in atherosclerosis: new opportunities for drug discovery. Mini. Rev. Med. Chem. 5 (2005) 33-40
11. Domingues M.R., Reis A., and Domingues P. Mass spectrometry analysis of oxidized phospholipids. Chem. Phys. Lipids 156 (2008) 1-12
12. Tyurin V.A., Tyurina Y.Y., Feng W., Mnuskin A., Jiang J., Tang M., Zhang X., Zhao Q., Kochanek P.M., Clark R.S., Bayir H., and Kagan V.E. Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis. J. Neurochem. 107 (2008) 1614-1633
13. Berliner J.A., and Gharavi N.M. Endothelial cell regulation by phospholipid oxidation products. Free Radic. Biol Med. 45 (2008) 119-123
14. Chen R., Yang L., and McIntyre T.M. Cytotoxic phospholipid oxidation products. Cell death from mitochondrial damage and the intrinsic caspase cascade. J. Biol. Chem. 282 (2007) 24842-24850
15. Podrez E.A., Poliakov E., Shen Z., Zhang R., Deng Y., Sun M., Finton P.J., Shan L., Gugiu B., Fox P.L., Hoff H.F., Salomon R.G., and Hazen S.L. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J. Biol. Chem. 277 (2002) 38503-38516
16. Hazen S.L. Oxidized phospholipids as endogenous pattern recognition ligands in innate immunity. J. Biol. Chem. 283 (2008) 15527-15531
17. Ashraf M.Z., Kar N.S., Chen X., Choi J., Salomon R.G., Febbraio M., and Podrez E.A. Specific oxidized phospholipids inhibit scavenger receptor BI-mediated selective uptake of cholesteryl esters. J. Biol. Chem. 283 (2008) 10408-10414
18. Bernal-Mizrachi C., Gates A.C., Weng S., Imamura T., Knutsen R.H., DeSantis P., Coleman T., Townsend R.R., Muglia L.J., and Semenkovich C.F. Vascular respiratory uncoupling increases blood pressure and atherosclerosis. Nature 435 (2005) 502-506
19. Le N.A. Reducing oxidized lipids to prevent cardiovascular disease. Curr. Treat. Options Cardiovasc. Med. 10 (2008) 263-272
20. Rader D.J., and Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature 451 (2008) 904-913
21. Greenberg M.E., Li X.M., Gugiu B.G., Gu X., Qin J., Salomon R.G., and Hazen S.L. The lipid whisker model of the structure of oxidized cell membranes. J. Biol. Chem. 283 (2008) 2385-2396
22. Khandelia H., and Mouritsen O.G. Lipid gymnastics: evidence of complete acyl chain reversal in oxidized phospholipids from molecular simulations. Biophys. J. 96 (2009) 2734-2743
23. Subbanagounder G., Leitinger N., Schwenke D.C., Wong J.W., Lee H., Rizza C., Watson A.D., Faull K.F., Fogelman A.M., and Berliner J.A. Determinants of bioactivity of oxidized phospholipids. Specific oxidized fatty acyl groups at the sn-2 position. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 2248-2254
24. Moumtzi A., Trenker M., Flicker K., Zenzmaier E., Saf R., and Hermetter A. Import and fate of fluorescent analogs of oxidized phospholipids in vascular smooth muscle cells. J. Lipid Res. 48 (2007) 565-582
25. Navab M., Ananthramaiah G.M., Reddy S.T., Van Lenten B.J., Ansell B., Fonarow G.C., Vahabzadeh K., Hama S., Hough G., Kamranpour N., Berliner J.A., Lusis A., and Fogelman A.M. The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J. Lipid Res. 45 (2004) 993-1007
26. Nicholls S.J., Zheng L., and Hazen S.L. Formation of dysfunctional high-density lipoprotein by myeloperoxidase. Trends Cardiovasc. Med. 15 (2005) 212-219
27. Wilson P.W. Recombinant apolipoprotein A-I Milano effects on coronary atherosclerosis. Curr. Cardiol. Rep. 6 (2004) 438
28. Brewer H.B. Focus on high-density lipoproteins in reducing cardiovascular risk. Am. Heart J. 148 (2004) S14-S18
29. Sirtori C.R. ApoA-1 Milano and regression of atherosclerosis. JAMA 291 (2004) 1319
30. Kim H., Jacobson E.L., Jacobson M.K., and Lacko A.G. ApoA-1 Milano and regression of atherosclerosis. JAMA 291 (2004) 1319
31. Davidson M.H. Biologic therapies for dyslipidemia. Curr. Atheroscler. Rep. 6 (2004) 69-72
32. Duffy D., and Rader D.J. Drugs in development: targeting high-density lipoprotein metabolism and reverse cholesterol transport. Curr. Opin. Cardiol. 20 (2005) 301-306
33. Futterman L.G., and Lemberg L. Apo a-I Milano. Am. J. Crit. Care 14 (2005) 244-247
34. Kaul S., Coin B., Hedayiti A., Yano J., Cercek B., Chyu K.Y., and Shah P.K. Rapid reversal of endothelial dysfunction in hypercholesterolemic apolipoprotein E-null mice by recombinant apolipoprotein A-I(Milano)-phospholipid complex. J. Am. Coll. Cardiol. 44 (2004) 1311-1319
35. Kazi D., and Farmer J.A. Raising high-density lipoprotein cholesterol: innovative strategies against an old adversary. Curr. Atheroscler. Rep. 7 (2005) 88-94
36. Zhu X., Wu G., Zeng W., Xue H., and Chen B. Cysteine mutants of human apolipoprotein A-I: a study of secondary structural and functional properties. J. Lipid. Res. 46 (2005) 1303-1311
37. Hortin G.L., Shen R.F., Martin B.M., and Remaley A.T. Diverse range of small peptides associated with high-density lipoprotein. Biochem. Biophys. Res. Commun. 340 (2006) 909-915
38. Handattu S.P., Garber D.W., Horn D.C., Hughes D.W., Berno B., Bain A.D., Mishra K., Palgunachari M.N., Datta G., Anantharamaiah G.M., and Epand R.M. ApoA-I mimetic peptides with differing ability to inhibit atherosclerosis also exhibit differences in their interactions with membrane bilayers. J. Biol. Chem. 282 (2007) 1980-1988
39. Wool G.D., Vaisar T., Reardon C.A., and Getz G.S. 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. (2009) M900151-MJLR200
40. Van Lenten B.J., Wagner A.C., Navab M., Anantharamaiah G.M., Hui E.K., Nayak D.P., and Fogelman A.M. D-4F, an apolipoprotein A-I mimetic peptide, inhibits the inflammatory response induced by influenza A infection of human type II pneumocytes. Circulation 110 (2004) 3252-3258
41. Navab M., Anantharamaiah G.M., Reddy S.T., Van Lenten B.J., Datta G., Garber D., and Fogelman A.M. Human apolipoprotein A-I and A-I mimetic peptides: potential for atherosclerosis reversal. Curr. Opin. Lipidol. 15 (2004) 645-649
42. Navab M., Anantharamaiah G.M., Reddy S.T., Hama S., Hough G., Grijalva V.R., Wagner A.C., Frank J.S., Datta G., Garber D., and Fogelman A.M. 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 (2004) 3215-3220
43. Navab M., Anantharamaiah G.M., Reddy S.T., Van Lenten B.J., Hough G., Wagner A., Nakamura K., Garber D.W., Datta G., Segrest J.P., Hama S., and Fogelman A.M. Human apolipoprotein AI mimetic peptides for the treatment of atherosclerosis. Curr. Opin. Investig. Drugs 4 (2003) 1100-1104
44. Navab M., Anantharamaiah G.M., Hama S., Garber D.W., Chaddha M., Hough G., Lallone R., and Fogelman A.M. 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 (2002) 290-292
45. Garber D.W., Datta G., Chaddha M., Palgunachari M.N., Hama S.Y., Navab M., Fogelman A.M., Segrest J.P., and Anantharamaiah G.M. A new synthetic class A amphipathic peptide analogue protects mice from diet-induced atherosclerosis. J. Lipid Res. 42 (2001) 545-552
46. Navab M., Anantharamaiah G.M., Reddy S.T., Hama S., Hough G., Grijalva V.R., Yu N., Ansell B.J., Datta G., Garber D.W., and Fogelman A.M. Apolipoprotein A-I mimetic peptides. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1325-1331
47. Getz G.S., Wool G.D., and Reardon C.A. Apoprotein A-I mimetic peptides and their potential anti-atherogenic mechanisms of action. Curr. Opin. Lipidol. 20 (2009) 171-175
48. Navab M., Anantharamaiah G.M., and Fogelman A.M. The effect of apolipoprotein mimetic peptides in inflammatory disorders other than atherosclerosis. Trends Cardiovasc. Med. 18 (2008) 61-66
49. Van Lenten B.J., Navab M., Anantharamaiah G.M., Buga G.M., Reddy S.T., and Fogelman A.M. Multiple indications for anti-inflammatory apolipoprotein mimetic peptides. Curr. Opin. Investig. Drugs 9 (2008) 1157-1162
50. Deigner H.P., and Hermetter A. Oxidized phospholipids: emerging lipid mediators in pathophysiology. Curr. Opin. Lipidol. 19 (2008) 289-294
51. N.D. Vaziri, H. Moradi, M.V. Pahl, A.M. Fogelman, M. Navab, In vitro stimulation of HDL anti-inflammatory activity and inhibition of LDL pro-inflammatory activity in the plasma of patients with end-stage renal disease by an apoA-1 mimetic peptide, Kidney Int. (in press), doi:10.1038/ki.2009.177.
52. Gupta H., Dai L., Datta G., Garber D.W., Grenett H., Li Y., Mishra V., Palgunachari M.N., Handattu S., Gianturco S.H., Bradley W.A., Anantharamaiah G.M., and White C.R. Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein AI mimetic peptide. Circ. Res. 97 (2005) 236-243
53. Navab M., Anantharamaiah G.M., Hama S., Hough G., Reddy S.T., Frank J.S., Garber D.W., Handattu S., and Fogelman A.M. 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. 25 (2005) 1426-1432
54. Kruger A.L., Peterson S., Turkseven S., Kaminski P.M., Zhang F.F., Quan S., Wolin M.S., and Abraham N.G. 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 (2005) 3126-3134
55. Peterson S.J., Husney D., Kruger A.L., Olszanecki R., Ricci F., Rodella L.F., Stacchiotti A., Rezzani R., McClung J.A., Aronow W.S., Ikehara S., and Abraham N.G. Long-term treatment with the apolipoprotein A1 mimetic peptide increases antioxidants and vascular repair in type I diabetic rats. J. Pharmacol. Exp. Ther. 322 (2007) 514-520
56. Van Lenten B.J., Wagner A.C., Jung C.L., Ruchala P., Waring A.J., Lehrer R.I., Watson A.D., Hama S., Navab M., Anantharamaiah G.M., and Fogelman A.M. Anti-inflammatory apoA-I-mimetic peptides bind oxidized lipids with much higher affinity than human apoA-I. J. Lipid Res. 49 (2008) 2302-2311
57. Epand R.M., Epand R.F., Sayer B.G., Datta G., Chaddha M., and Anantharamaiah G.M. Two homologous apolipoprotein AI mimetic peptides. Relationship between membrane interactions and biological activity. J. Biol. Chem. 279 (2004) 51404-51414
58. Mishra V.K., Palgunachari M.N., Krishna R., Glushka J., Segrest J.P., and Anantharamaiah G.M. Effect of leucine to phenylalanine substitution on the nonpolar face of a class A amphipathic helical peptide on its interaction with lipid: high resolution solution NMR studies of 4F-dimyristoylphosphatidylcholine discoidal complex. J. Biol. Chem. 283 (2008) 34393-34402
59. Navab M., Hama S.Y., Anantharamaiah G.M., Hassan K., Hough G.P., Watson A.D., Reddy S.T., Sevanian A., Fonarow G.C., and Fogelman A.M. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: steps 2 and 3. J Lipid Res. 41 (2000) 1495-1508
60. Navab M., Hama S.Y., Cooke C.J., Anantharamaiah G.M., Chaddha M., Jin L., Subbanagounder G., Faull K.F., Reddy S.T., Miller N.E., and Fogelman A.M. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1. J. Lipid Res. 41 (2000) 1481-1494
61. Datta G., Chaddha M., Hama S., Navab M., Fogelman A.M., Garber D.W., Mishra V.K., Epand R.M., Epand R.F., Lund-Katz S., Phillips M.C., Segrest J.P., and Anantharamaiah G.M. Effects of increasing hydrophobicity on the physical-chemical and biological properties of a class A amphipathic helical peptide. J. Lipid Res. 42 (2001) 1096-1104
62. Privalov G., Kavina V., Freire E., and Privalov P.L. Precise scanning calorimeter for studying thermal properties of biological macromolecules in dilute solution. Anal. Biochem. 232 (1995) 79-85
63. Ames B.N. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 8 (1966) 115-118
64. Datta G., Epand R.F., Epand R.M., Chaddha M., Kirksey M.A., Garber D.W., Lund-Katz S., Phillips M.C., Hama S., Navab M., Fogelman A.M., Palgunachari M.N., Segrest J.P., and Anantharamaiah G.M. Aromatic residue position on the nonpolar face of class A amphipathic helical peptides determines biological activity. J. Biol. Chem. 279 (2004) 26509-26517
65. Venkatachalapathi Y.V., Phillips M.C., Epand R.M., Epand R.F., Tytler E.M., Segrest J.P., and Anantharamaiah G.M. Effect of end group blockage on the properties of a class A amphipathic helical peptide. Proteins 15 (1993) 349-359
66. Anantharamaiah G.M., Mishra V.K., Garber D.W., Datta G., Handattu S.P., Palgunachari M.N., Chaddha M., Navab M., Reddy S.T., Segrest J.P., and Fogelman A.M. Structural requirements for antioxidative and anti-inflammatory properties of apolipoprotein A-I mimetic peptides. J. Lipid Res. 48 (2007) 1915-1923