Emerging roles of apolipoprotein e and apolipoprotein A-I in the pathogenesis and treatment of lung disease

American Journal of Respiratory Cell and Molecular Biology

Volumn 55, Issue 2, 2016, Pages 159-169

  Yao, Xianglan ^a   Gordon, Elizabeth M ^a   Figueroa, Debbie M ^a   Barochia, Amisha V ^a   Levine, Stewart J ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Apolipoprotein E; apolipoprotein A I; lipid transport; lung disease

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN E; PEPTIDOMIMETIC AGENT;

ACUTE LUNG INJURY; ASTHMA; CHLAMYDIA; HOST RESISTANCE; HUMAN; HYPERCHOLESTEROLEMIA; INFLUENZA; LUNG BLOOD VESSEL; LUNG CANCER; LUNG DISEASE; LUNG EMPHYSEMA; LUNG FIBROSIS; LUNG PARENCHYMA; MOLECULAR PATHOLOGY; MYCOBACTERIUM; NONHUMAN; PH; REVIEW; SEPSIS; ANIMAL; LUNG DISEASES; METABOLISM;

ANIMALS; APOLIPOPROTEIN A-I; APOLIPOPROTEINS E; HUMANS; LUNG DISEASES;

EID: 84988982940     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0060TR     Document Type: Review

References (98)

1. Mahley RW, Weisgraber KH, Huang Y. Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer?s disease to AIDS. J Lipid Res 2009;50:S183-S188.
2. Goldstein JL, Brown MS. The LDL receptor. Arterioscler Thromb Vasc Biol 2009;29:431-438.
3. Kingwell BA, Chapman MJ, Kontush A, Miller NE. HDL-targeted therapies: progress, failures and future. Nat Rev Drug Discov 2014;13:445-464.
4. Yao X, Fredriksson K, Yu ZX, Xu X, Raghavachari N, Keeran KJ, Zywicke GJ, Kwak M, Amar MJ, Remaley AT, et al. Apolipoprotein E negatively regulates house dust mite-induced asthma via a low-density lipoprotein receptor-mediated pathway. Am J Respir Crit Care Med 2010;182:1228-1238.
5. Lin CT, Xu YF, Wu JY, Chan L. Immunoreactive apolipoprotein E is a widely distributed cellular protein. Immunohistochemical localization of apolipoprotein E in baboon tissues. J Clin Invest 1986;78:947-958.
6. Voyno-Yasenetskaya TA, Dobbs LG, Erickson SK, Hamilton RL. Low density lipoprotein- and high density lipoprotein-mediated signal transduction and exocytosis in alveolar type II cells. Proc Natl Acad Sci USA 1993;90:4256-4260.
7. Hansmann G, de Jesus Perez VA, Alastalo TP, Alvira CM, Guignabert C, Bekker JM, Schellong S, Urashima T, Wang L, Morrell NW, et al. An antiproliferative BMP-2/PPARg/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J Clin Invest 2008;118: 1846-1857.
8. Takemura R, Werb Z. Modulation of apoprotein E secretion in response to receptor-mediated endocytosis in resident and inflammatory macrophages. J Exp Med 1984;159:167-178.
9. Chen J, Chen Z, Chintagari NR, Bhaskaran M, Jin N, Narasaraju T, Liu L. Alveolar type I cells protect rat lung epithelium from oxidative injury. J Physiol 2006;572:625-638.
10. Pendse AA, Arbones-Mainar JM, Johnson LA, Altenburg MK, Maeda N. Apolipoprotein E knock-out and knock-in mice: atherosclerosis, metabolic syndrome, and beyond. J Lipid Res 2009;50:S178-S182.
11. Massaro D, Massaro GD. Apoetm1Unc mice have impaired alveologenesis, low lung function, and rapid loss of lung function. Am J Physiol Lung Cell Mol Physiol 2008;294:L991-L997.
12. Massaro D, Massaro GD. Developmental alveologenesis: new roles for ApoE and LDL receptor. Pediatr Res 2011;70:458-461.
13. Ryan AJ, Medh JD, McCoy DM, Salome RG, Mallampalli RK. Maternal loading with very low-density lipoproteins stimulates fetal surfactant synthesis. Am J Physiol Lung Cell Mol Physiol 2002;283:L310-L318.
14. Goldklang M, Golovatch P, Zelonina T, Trischler J, Rabinowitz D, Lemaître V, D?Armiento J. Activation of the TLR4 signaling pathway and abnormal cholesterol efflux lead to emphysema in ApoE-deficient mice. Am J Physiol Lung Cell Mol Physiol 2012;302:L1200-L1208.
15. Ouyang Q, Huang Z, Lin H, Ni J, Lu H, Chen X, Wang Z, Lin L. Apolipoprotein E deficiency and high-fat diet cooperate to trigger lipidosis and inflammation in the lung via the toll-like receptor 4 pathway. Mol Med Rep 2015;12:2589-2597.
16. Samokhin AO, Bühling F, Theissig F, Brömme D. ApoE-deficient mice on cholate-containing high-fat diet reveal a pathology similar to lung sarcoidosis. Am J Pathol 2010;176:1148-1156.
17. Naura AS, Hans CP, Zerfaoui M, Errami Y, Ju J, Kim H, Matrougui K, Kim JG, Boulares AH. High-fat diet induces lung remodeling in ApoE-deficient mice: an association with an increase in circulatory and lung inflammatory factors. Lab Invest 2009;89:1243-1251.
18. Hansmann G, Wagner RA, Schellong S, Perez VA, Urashima T, Wang L, Sheikh AY, Suen RS, Stewart DJ, Rabinovitch M. Pulmonary arterial hypertension is linked to insulin resistance and reversed by peroxisome proliferator-activated receptor-g activation. Circulation 2007;115:1275-1284.
19. Lawrie A, Hameed AG, Chamberlain J, Arnold N, Kennerley A, Hopkinson K, Pickworth J, Kiely DG, Crossman DC, Francis SE. Paigen diet-fed apolipoprotein E knockout mice develop severe pulmonary hypertension in an interleukin-1-dependent manner. Am J Pathol 2011;179:1693-1705.
20. Christensen DJ, Ohkubo N, Oddo J, Van Kanegan MJ, Neil J, Li F, Colton CA, Vitek MP. Apolipoprotein E and peptide mimetics modulate inflammation by binding the SET protein and activating protein phosphatase 2A. J Immunol 2011;186:2535-2542.
21. Chen B, Moore TV, Li Z, Sperling AI, Zhang C, Andrade J, Rodriguez A, Bahroos N, Huang Y, Morrisey EE, et al. Gata5 deficiency causes airway constrictor hyperresponsiveness in mice. Am J Respir Cell Mol Biol 2014;50:787-795.
22. Yao X, Dai C, Fredriksson K, Lam J, Gao M, Keeran KJ, Nugent GZ, Qu X, Yu ZX, Jeffries N, et al. Human apolipoprotein E genotypes differentially modify house dust mite-induced airway disease in mice. Am J Physiol Lung Cell Mol Physiol 2012;302:L206-L215.
23. Jiang ZL, Li YF, Song JY,Guo YQ. Effects of b3-adrenoceptor activation on the interaction between adrenoceptors and angiotensin II receptors in apolipoprotein E knockout mouse lung. Eur J Pharmacol 2014;742:75-80.
24. Arunachalam G, Sundar IK, Hwang JW, Yao H, Rahman I. Emphysema is associated with increased inflammation in lungs of atherosclerosis-prone mice by cigarette smoke: implications in comorbidities of COPD. J Inflamm (Lond) 2010;7:34.
25. Yamashita CM, Fessler MB, Vasanthamohan L, Lac J, Madenspacher J, McCaig L, Yao L, Wang L, Puntorieri V, Mehta S, et al. Apolipoprotein E-deficient mice are susceptible to the development of acute lung injury. Respiration 2014;87:416-427.
26. Jacobsen NR, Møller P, Jensen KA, Vogel U, Ladefoged O, Loft S, Wallin H. Lung inflammation and genotoxicity following pulmonary exposure to nanoparticles in ApoE-/- mice. Part Fibre Toxicol 2009;6:2.
27. Venosa A, Malaviya R, Choi H, Gow AJ, Laskin JD, Laskin DL. Characterization of distinct macrophage subpopulations during nitrogen mustard-induced lung injury and fibrosis. Am J Respir Cell Mol Biol 2016;54:436-446.
28. Madenspacher JH, Azzam KM, Gong W, Gowdy KM, Vitek MP, Laskowitz DT, Remaley AT, Wang JM, Fessler MB. Apolipoproteins and apolipoprotein mimetic peptides modulate phagocyte trafficking through chemotactic activity. J Biol Chem 2012;287: 43730-43740.
29. Ni JQ, Ouyang Q, Lin L, Huang Z, Lu H, Chen X, Lin H, Wang Z, Xu D, Zhang Y. Role of Toll-like receptor 4 on lupus lung injury and atherosclerosis in LPS-challenge ApoE-/- mice. Clin Dev Immunol 2013;2013:476856.
30. Van Oosten M, Rensen PC, Van Amersfoort ES, Van Eck M, Van Dam AM, Breve JJ, Vogel T, Panet A, Van Berkel TJ, Kuiper J. Apolipoprotein E protects against bacterial lipopolysaccharide-induced lethality. A new therapeutic approach to treat gram-negative sepsis. J Biol Chem 2001; 276:8820-8824.
31. Rensen PC, Oosten M, Bilt E, Eck M, Kuiper J, Berkel TJ. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. J Clin Invest 1997;99:2438-2445.
32. Li L, Thompson PA, Kitchens RL. Infection induces a positive acute phase apolipoprotein E response from a negative acute phase gene: role of hepatic LDL receptors. J Lipid Res 2008;49: 1782-1793.
33. Read TE, Harris HW, Grunfeld C, Feingold KR, Calhoun MC, Kane JP, Rapp JH. Chylomicrons enhance endotoxin excretion in bile. Infect Immun 1993;61:3496-3502.
34. de Bont N, Netea MG, Demacker PN, Verschueren I, Kullberg BJ, van Dijk KW, van der Meer JW, Stalenhoef AF. Apolipoprotein E knock-out mice are highly susceptible to endotoxemia and Klebsiella pneumoniae infection. J Lipid Res 1999;40:680-685.
35. de Bont N, Netea MG, Demacker PN, Kullberg BJ, van der Meer JW, Stalenhoef AF. Apolipoprotein E-deficient mice have an impaired immune response to Klebsiella pneumoniae. Eur J Clin Invest 2000; 30:818-822.
36. Roselaar SE, Daugherty A. Apolipoprotein E-deficient mice have impaired innate immune responses to Listeria monocytogenes in vivo. J Lipid Res 1998;39:1740-1743.
37. Kattan OM, Kasravi FB, Elford EL, Schell MT, Harris HW. Apolipoprotein E-mediated immune regulation in sepsis. J Immunol 2008;181:1399-1408.
38. Chuang K, Elford EL, Tseng J, Leung B, Harris HW. An expanding role for apolipoprotein E in sepsis and inflammation. Am J Surg 2010; 200:391-397.
39. Lynch JR, Tang W, Wang H, Vitek MP, Bennett ER, Sullivan PM,Warner DS, Laskowitz DT. APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. J Biol Chem 2003;278:48529-48533.
40. Wang H, Christensen DJ, Vitek MP, Sullivan PM, Laskowitz DT. APOE genotype affects outcome in a murine model of sepsis: implications for a new treatment strategy. Anaesth Intensive Care 2009;37:38-45.
41. Gale SC, Gao L, Mikacenic C, Coyle SM, Rafaels N, Murray Dudenkov T, Madenspacher JH, Draper DW, Ge W, Aloor JJ, et al. APOe4 is associated with enhanced in vivo innate immune responses in human subjects. J Allergy Clin Immunol 2014;134:127-134.
42. Moretti EW, Morris RW, Podgoreanu M, Schwinn DA, Newman MF, Bennett E, Moulin VG, Mba UU, Laskowitz DT; Perioperative Genetics and Safety Outcomes Study (PEGASUS) Investigative Team. APOE polymorphism is associated with risk of severe sepsis in surgical patients. Crit Care Med 2005;33:2521-2526.
43. van den Elzen P, Garg S, León L, Brigl M, Leadbetter EA, Gumperz JE, Dascher CC, Cheng TY, Sacks FM, Illarionov PA, et al. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005;437:906-910.
44. Allan LL, Hoefl K, Zheng DJ, Chung BK, Kozak FK, Tan R, van den Elzen P. Apolipoprotein-mediated lipid antigen presentation in B cells provides a pathway for innate help by NKT cells. Blood 2009; 114:2411-2416.
45. Gérard HC, Fomicheva E, Whittum-Hudson JA, Hudson AP. Apolipoprotein E4 enhances attachment of Chlamydophila (Chlamydia) pneumoniae elementary bodies to host cells. Microb Pathog 2008;44:279-285.
46. Gérard HC, Wang GF, Balin BJ, Schumacher HR, Hudson AP. Frequency of apolipoprotein E (APOE) allele types in patients with Chlamydia-associated arthritis and other arthritides. Microb Pathog 1999;26:35-43.
47. Nazzal D, Therville N, Yacoub-Youssef H, Garcia V, Thomsen M, Levade T, Segui B, Benoist H. Apolipoprotein E-deficient mice develop an anti-Chlamydophila pneumoniae T helper 2 response and resist vascular infection. J Infect Dis 2010;202:782-790.
48. Fu P, Wang AM, He LY, Song JM, Xue JC, Wang CQ. Elevated serum ApoE levels are associated with bacterial infections in pediatric patients. J Microbiol Immunol Infect 2014;47:122-129.
49. Wang C, Wang Y, Wang A, Fu P, Yang Y. The diagnostic value of apolipoprotein E in pediatric patients with invasive bacterial infections. Clin Biochem 2012;45:215-218.
50. Rice SJ, Liu X, Miller B, Joshi M, Zhu J, Caruso C, Gilbert C, Toth J, Reed M, Rassaei N, et al. Proteomic profiling of human plasma identifies apolipoprotein E as being associated with smoking and a marker for squamous metaplasia of the lung. Proteomics 2015;15: 3267-3277.
51. Su WP, Chen YT, Lai WW, Lin CC, Yan JJ, Su WC. Apolipoprotein E expression promotes lung adenocarcinoma proliferation and migration and as a potential survival marker in lung cancer. Lung Cancer 2011;71:28-33.
52. Wang Y, Chen Z, Chen J, Pan J, Zhang W, Pan Q, Ding H, Lin X, Wen X, Li Y, et al. The diagnostic value of apolipoprotein E in malignant pleural effusion associated with non-small cell lung cancer. Clin Chim Acta 2013;421:230-235.
53. Gueddari N, Favre G, Hachem H, Marek E, Le Gaillard F, Soula G. Evidence for up-regulated low density lipoprotein receptor in human lung adenocarcinoma cell line A549. Biochimie 1993;75:811-819.
54. Leman LJ, Maryanoff BE, Ghadiri MR. Molecules that mimic apolipoprotein A-I: potential agents for treating atherosclerosis. J Med Chem 2014;57:2169-2196.
55. Rader DJ, Hovingh GK. HDL and cardiovascular disease. Lancet 2014; 384:618-625.
56. Provost PR, Boucher E, Tremblay Y. Apolipoprotein A-I, A-II, C-II, and H expression in the developing lung and sex difference in surfactant lipids. J Endocrinol 2009;200:321-330.
57. Dai C, Yao X, Keeran KJ, Zywicke GJ, Qu X, Yu ZX, Dagur PK, McCoy JP, Remaley AT, Levine SJ. Apolipoprotein A-I attenuates ovalbumin-induced neutrophilic airway inflammation via a granulocyte colony-stimulating factor-dependent mechanism. Am J Respir Cell Mol Biol 2012;47:186-195.
58. Kim TH, Lee YH, Kim KH, Lee SH, Cha JY, Shin EK, Jung S, Jang AS, Park SW, Uh ST, et al. Role of lung apolipoprotein A-I in idiopathic pulmonary fibrosis: antiinflammatory and antifibrotic effect on experimental lung injury and fibrosis. Am J Respir Crit Care Med 2010;182:633-642.
59. Dai C, Yao X, Vaisman B, Brenner T, Meyer KS, Gao M, Keeran KJ, Nugent GZ, Qu X, Yu ZX, et al. ATP-binding cassette transporter 1attenuates ovalbumin-induced neutrophilic airway inflammation. Am J Respir Cell Mol Biol 2014;51:626-636.
60. Bates SR, Tao JQ, Yu KJ, Borok Z, Crandall ED, Collins HL, Rothblat GH. Expression and biological activity of ABCA1 in alveolar epithelial cells. Am J Respir Cell Mol Biol 2008;38:283-292.
61. Bortnick AE, Favari E, Tao JQ, Francone OL, Reilly M, Zhang Y, Rothblat GH, Bates SR. Identification and characterization of rodent ABCA1 in isolated type II pneumocytes. Am J Physiol Lung Cell Mol Physiol 2003;285:L869-L878.
62. Delvecchio CJ, Bilan P, Nair P, Capone JP. LXR-induced reverse cholesterol transport in human airway smooth muscle is mediated exclusively by ABCA1. Am J Physiol Lung Cell Mol Physiol 2008;295:L949-L957.
63. Park SW, Lee EH, Lee EJ, Kim HJ, Bae DJ, Han S, Kim D, Jang AS, Uh ST, Kim YH, et al. Apolipoprotein A1 potentiates lipoxin A4 synthesis and recovery of allergen-induced disrupted tight junctions in the airway epithelium. Clin Exp Allergy 2013;43:914-927.
64. Wang W, Xu H, Shi Y, Nandedkar S, Zhang H, Gao H, Feroah T, Weihrauch D, Schulte ML, Jones DW, et al. Genetic deletion of apolipoprotein A-I increases airway hyperresponsiveness, inflammation, and collagen deposition in the lung. J Lipid Res 2010; 51:2560-2570.
65. McNeish J, Aiello RJ, Guyot D, Turi T, Gabel C, Aldinger C, Hoppe KL, Roach ML, Royer LJ, de Wet J, et al. High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc Natl Acad Sci USA 2000;97:4245-4250.
66. Bates SR, Tao JQ, Collins HL, Francone OL, Rothblat GH. Pulmonary abnormalities due to ABCA1 deficiency in mice. Am J Physiol Lung Cell Mol Physiol 2005;289:L980-L989.
67. Gauthier M, Ray A, Wenzel SE. Evolving concepts of asthma. Am J Respir Crit Care Med 2015;192:660-668.
68. Wang SH, Yuan SG, Peng DQ, Zhao SP. HDL and ApoA-I inhibit antigen presentation-mediated T cell activation by disrupting lipid rafts in antigen presenting cells. Atherosclerosis 2012;225:105-114.
69. Kim KD, Lim HY, Lee HG, Yoon DY, Choe YK, Choi I, Paik SG, Kim YS, Yang Y, Lim JS. Apolipoprotein A-I induces IL-10 and PGE2 production in human monocytes and inhibits dendritic cell differentiation and maturation. Biochem Biophys Res Commun 2005;338:1126-1136.
70. Tiniakou I, Drakos E, Sinatkas V, Van Eck M, Zannis VI, Boumpas D, Verginis P, Kardassis D. High-density lipoprotein attenuates Th1 and th17 autoimmune responses by modulating dendritic cell maturation and function. J Immunol 2015;194:4676-4687.
71. Yao X, Dai C, Fredriksson K, Dagur PK, McCoy JP, Qu X, Yu ZX, Keeran KJ, Zywicke GJ, Amar MJ, et al. 5A, an apolipoprotein A-I mimetic peptide, attenuates the induction of house dust mite-induced asthma. J Immunol 2011;186:576-583.
72. Nandedkar SD, Weihrauch D, Xu H, Shi Y, Feroah T, Hutchins W, Rickaby DA, Duzgunes N, Hillery CA, Konduri KS, et al. D-4F, an apoA-1 mimetic, decreases airway hyperresponsiveness, inflammation, and oxidative stress in a murine model of asthma. J Lipid Res 2011;52:499-508.
73. Barochia AV, Kaler M, Cuento RA, Gordon EM, Weir NA, Sampson M, Fontana JR, MacDonald S, Moss J, Manganiello V, et al. Serum apolipoprotein A-I and large high-density lipoprotein particles are positively correlated with FEV1 in atopic asthma. Am J Respir Crit Care Med 2015;191:990-1000.
74. Cirillo DJ, Agrawal Y, Cassano PA. Lipids and pulmonary function in the Third National Health and Nutrition Examination Survey. Am J Epidemiol 2002;155:842-848.
75. Nicholas BL, Skipp P, Barton S, Singh D, Bagmane D, Mould R, Angco G, Ward J, Guha-Niyogi B, Wilson S, et al. Identification of lipocalin and apolipoprotein A1 as biomarkers of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2010;181:1049-1060.
76. Kim C, Lee JM, Park SW, Kim KS, Lee MW, Paik S, Jang AS, Kim J, Uh S, Kim Y, et al. Attenuation of cigarette smoke-induced emphysema in mice by apolipoprotein A-1 overexpression. Am J Respir Cell Mol Biol 2016;54:91-102.
77. Yan YJ, Li Y, Lou B,WuMP. Beneficial effects of ApoA-I on LPS-induced acute lung injury and endotoxemia in mice. Life Sci 2006;79:210-215.
78. Ma J, Liao XL, Lou B, Wu MP. Role of apolipoprotein A-I in protecting against endotoxin toxicity. Acta Biochim Biophys Sin (Shanghai) 2004;36:419-424.
79. Jiao YL, Wu MP. Apolipoprotein A-I diminishes acute lung injury and sepsis in mice induced by lipoteichoic acid. Cytokine 2008;43:83-87.
80. Van Linthout S, Spillmann F, Graiani G, Miteva K, Peng J, Van Craeyveld E, Meloni M, Tölle M, Escher F, Subasigüller A, et al. Down-regulation of endothelial TLR4 signalling after apo A-I gene transfer contributes to improved survival in an experimental model of lipopolysaccharide-induced inflammation. J Mol Med (Berl) 2011;89: 151-160.
81. Li Y, Dong JB, Wu MP. Human ApoA-I overexpression diminishes LPSinduced systemic inflammation and multiple organ damage in mice. Eur J Pharmacol 2008;590:417-422.
82. Sharifov OF, Xu X, Gaggar A, Grizzle WE, Mishra VK, Honavar J, Litovsky SH, Palgunachari MN, White CR, Anantharamaiah GM, et al. Anti-inflammatory mechanisms of apolipoprotein A-I mimetic peptide in acute respiratory distress syndrome secondary to sepsis. PLoS One 2013;8:e64486.
83. Kwon WY, Suh GJ, Kim KS, Kwak YH, Kim K. 4F, apolipoprotein AI mimetic peptide, attenuates acute lung injury and improves survival in endotoxemic rats. J Trauma Acute Care Surg 2012;72:1576-1583.
84. Tu J, Zhang B, Chen Y, Liang B, Liang D, Liu G, He F. Association of apolipoprotein A1 -75 G/A polymorphism with susceptibility to the development of acute lung injury after cardiopulmonary bypass surgery. Lipids Health Dis 2013;12:172.
85. Emancipator K, Csako G, Elin RJ. In vitro inactivation of bacterial endotoxin by human lipoproteins and apolipoproteins. Infect Immun 1992;60:596-601.
86. Henning MF, Herlax V, Bakás L. Contribution of the C-terminal end of apolipoprotein AI to neutralization of lipopolysaccharide endotoxic effect. Innate Immun 2011;17:327-337.
87. Wurfel MM, Kunitake ST, Lichenstein H, Kane JP, Wright SD. Lipopolysaccharide (LPS)-binding protein is carried on lipoproteins and acts as a cofactor in the neutralization of LPS. J Exp Med 1994; 180:1025-1035.
88. Van Lenten BJ, Wagner AC, Anantharamaiah GM, Garber DW, Fishbein MC, Adhikary L, Nayak DP, Hama S, Navab M, Fogelman AM. Influenza infection promotes macrophage traffic into arteries of mice that is prevented by D-4F, an apolipoprotein A-I mimetic peptide. Circulation 2002;106:1127-1132.
89. Van Lenten BJ, Wagner AC, Navab M, Anantharamaiah GM, Hui EK, Nayak DP, Fogelman AM. D-4F, an apolipoprotein A-I mimetic peptide, inhibits the inflammatory response induced by influenza A infection of human type II pneumocytes. Circulation 2004;110:3252-3258.
90. Zamanian-Daryoush M, Lindner D, Tallant TC, Wang Z, Buffa J, Klipfell E, Parker Y, Hatala D, Parsons-Wingerter P, Rayman P, et al. The cardioprotective protein apolipoprotein A1 promotes potent antitumorigenic effects. J Biol Chem 2013;288:21237-21252.
91. Cheng T, Dai X, Zhou DL, Lv Y, Miao LY. Correlation of apolipoprotein A-I kinetics with survival and response to first-line platinum-based chemotherapy in advanced non-small cell lung cancer. Med Oncol 2015;32:407.
92. Marchi N, Mazzone P, Fazio V, Mekhail T, Masaryk T, Janigro D. ProApolipoprotein A1: a serum marker of brain metastases in lung cancer patients. Cancer 2008;112:1313-1324.
93. Sharma S, Umar S, Potus F, Iorga A, Wong G, Meriwether D, Breuils-Bonnet S, Mai D, Navab K, Ross D, et al. Apolipoprotein A-I mimetic peptide 4F rescues pulmonary hypertension by inducing microRNA-193-3p. Circulation 2014;130:776-785.
94. Lee Eh, Lee EJ, Kim Hj, Jang As, Koh Es, Uh ST, Kim Yh, Park SW, Park CS. Overexpression of apolipoprotein A1 in the lung abrogates fibrosis in experimental silicosis. PLoS One 2013;8:e55827.
95. Bloedon LT, Dunbar R, Duffy D, Pinell-Salles P, Norris R, DeGroot BJ, Movva R, Navab M, Fogelman AM, Rader DJ. Safety, pharmacokinetics, and pharmacodynamics of oral apoA-I mimetic peptide D-4F in high-risk cardiovascular patients. J Lipid Res 2008;49: 1344-1352.
96. Watson CE, Weissbach N, Kjems L, Ayalasomayajula S, Zhang Y, Chang I, Navab M, Hama S, Hough G, Reddy ST, et al. Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function. J Lipid Res 2011; 52:361-373.
97. Dunbar RL, Bloedon LT, Duffy D, Norris RB, Movva R, Navab M, Fogelman AM, Rader DJ. Daily oral administration of the apolipoprotein A-I mimetic peptide D-4F in patients with heart disease or equivalent risk improves high-density lipoprotein antiinflammatory function [abstract]. J Am Coll Cardiol 2007;49:366A.
98. Navab M, Reddy ST, Anantharamaiah GM, Imaizumi S, Hough G, Hama S, Fogelman AM. Intestine may be a major site of action for the apoA-I mimetic peptide 4F whether administered subcutaneously or orally. J Lipid Res 2011;52:1200-1210.