HDL in sepsis - risk factor and therapeutic approach

Frontiers in Pharmacology

Volumn 6, Issue OCT, 2015, Pages

  Morin, Emily E ^a   Guo, Ling ^b   Schwendeman, Anna ^a   Li, Xiang An ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Apolipoprotein A 1 (ApoA1); High density lipoprotein (HDL); Lipopolysaccharide (LPS); Sepsis; Sepsis therapy

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN A1 MILANO; ASPARTYLTRYPTOPHYLLEUCYLLYSYLALANYLPHENYLALANYLTYROSYLASPARTYLLYSYLVALYLALANYLGLUTAMYLLYSYLLEUCYLLYSYLGLUTAMYLALANYLPHENYLALANINE; ASPARTYLTRYPTOPHYLPHENYLALANYLLYSYLALANYLPHENYLALANYLTYROSYLASPARTYLLYSYLVALYLALANYLGLUTAMYLLYSYLPHENYLALANYLLYSYLGLUTAMYLALANYLPHENYLALANINE; CSL 111; ENDOTOXIN; HIGH DENSITY LIPOPROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; PEPTIDES AND PROTEINS; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CHOLESTEROL TRANSPORT; DETOXIFICATION; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; ENDOTOXEMIA; HORMONE SYNTHESIS; HUMAN; HYPOTENSION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; METABOLIC ACIDOSIS; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); RISK FACTOR; SALMONELLA;

EID: 84949669690     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00244     Document Type: Article

References (98)

1. Aird, W. C. (2003). The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 101, 3765-3777. doi: 10.1182/blood-2002-06-1887
2. Amar, M. J. A., D'Souza, W., Turner, S., Demosky, S., Sviridov, D., Stonik, J., et al. (2010). 5A apolipoprotein mimetic peptide promotes cholesterol e?ux and reduces atherosclerosis in mice. J. Pharmacol. Exp. Therapeut. 334, 634-641. doi: 10.1124/jpet.110.167890
3. Angus, D. C., and van der Poll, T. (2013). Severe sepsis and septic shock. N. Engl. J. Med. 369, 840-851. doi: 10.1056/NEJMra1208623
4. Argraves, K. M., and Argraves, W. S. (2007). HDL serves as a S1P signaling platform mediating a multitude of cardiovascular effects. J. Lipid Res. 48, 2325-2333. doi: 10.1194/jlr. R700011-JLR200
5. Barlage, S., Gnewuch, C., Liebisch, G., Wolf, Z., Audebert, F.-X., Glück, T., et al. (2009). Changes in HDL-associated apolipoproteins relate to mortality in human sepsis and correlate to monocyte and platelet activation. Intensive Care Med. 35, 1877-1885. doi: 10.1007/s00134-009-1609-y
6. Barter, P. J., Nicholls, S., Rye, K.-A., Anantharamaiah, G. M., Navab, M., and Fogelman, A. M. (2004). Antiinflammatory properties of HDL. Circ. Res. 95, 764-772. doi: 10.1161/01.res.0000146094.59640.13
7. Baumberger, C., Ulevitch, R. J., and Dayer, J. M. (1991). Modulation of endotoxic activity of lipopolysaccharide by high-density lipoprotein. Pathobiology 59, 378-383. doi: 10.1159/000163681
8. Cai, L., Ji, A., de Beer, F. C., Tannock, L. R., and van der Westhuyzen, D. R. (2008). SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J. Clin. Invest. 118, 364-375. doi: 10.1172/JCI31539
9. Carmody, R. J., and Chen, Y. H. (2007). Nuclear factor-kappaB: activation and regulation during toll-like receptor signaling. Cell. Mol. Immunol. 4, 31-41.
10. Casas, A. T., Hubsch, A. P., Rogers, B. C., and Doran, J. E. (1995). Reconstituted high-density lipoprotein reduces LPS-stimulated TNFa. J. Surg. Res. 59, 544-552. doi: 10.1006/jsre.1995.1204
11. Chen, X., Burton, C., Song, X., McNamara, L., Langella, A., Cianetti, S., et al. (2009). An apoA-I mimetic peptide increases LCAT activity in mice through increasing HDL concentration. Int. J. Biol. Sci. 5, 489-499. doi: 10.7150/ijbs.5.489
12. Chien, J. Y., Jerng, J. S., Yu, C. J., and Yang, P. C. (2005). Low serum level of high-density lipoprotein cholesterol is a poor prognostic factor for severe sepsis. Crit. Care Med. 33, 1688-1693. doi: 10.1097/01.CCM.0000171183.79525.6B
13. Cockerill, G. W., Rye, K.-A., Gamble, J. R., Vadas, M. A., and Barter, P. J. (1995). High-density lipoproteins inhibit cytokine-induced expression of endothelial cell adhesion molecules. Arterioscler. Thromb. Vasc. Biol. 15, 1987-1994. doi: 10.1161/01.atv.15.11.1987
14. Cockerill, G. W., Saklatvala, J., Ridley, S. H., Yarwood, H., Miller, N. E., Oral, B., et al. (1999). High-density lipoproteins differentially modulate cytokine-induced expression of e-selectin and cyclooxygenase-2. Arterioscler. Thromb. Vasc. Biol. 19, 910-917. doi: 10.1161/01.atv.19.4.910
15. Cohen, J. (1999). Adjunctive therapy in sepsis: a critical analysis of the clinical trial programme. Br. Med. Bull. 55, 212-225. doi: 10.1258/0007142991902222
16. Dai, L., Datta, G., Zhang, Z., Gupta, H., Patel, R., Honavar, J., et al. (2010). The apolipoprotein A-I mimetic peptide 4F prevents defects in vascular function in endotoxemic rats. J. Lipid Res. 51, 2695-2705. doi: 10.1194/jlr. M008086
17. De Nardo, D., Labzin, L. I., Kono, H., Seki, R., Schmidt, S. V., Beyer, M., et al. (2014). High-density lipoprotein mediates anti-inflammatory reprogramming of macrophages via the transcriptional regulator ATF3. Nat. Immunol. 15, 152-160. doi: 10.1038/ni.2784
18. Deanfield, J. E., Halcox, J. P., and Rabelink, T. J. (2007). Endothelial function and dysfunction: testing and clinical relevance. Circulation 115, 1285-1295. doi: 10.1161/circulationaha.106.652859
19. Dellinger, R. P., Levy, M. M., Rhodes, A., Annane, D., Gerlach, H., Opal, S. M., et al. (2013). Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit. Care Med. 41, 580-637. doi: 10.1097/CCM.0b013e31827e83af
20. DiPiro, J. T., Cue, J. I., Richards, C. S., Hawkins, M. L., Doran, J. E., and Mansberger, A. R. (1996). Pharmacokinetics of reconstituted human high-density lipoprotein in pigs after hemorrhagic shock with resuscitation. Crit. Care Med. 24, 440-444. doi: 10.1097/00003246-199603000-00013
21. Eggesbo, J. B., Lyberg, T., Aspelin, T., Hjermann, I., and Kierulf, P. (1996). Different binding of 125I-LPS to plasma proteins from persons with high or low HDL. Scand. J. Clin. Lab. Invest. 56, 533-543. doi: 10.3109/00365519609088809
22. Emancipator, K., Csako, G., and Elin, R. J. (1992). In vitro inactivation of bacterial endotoxin by human lipoproteins and apolipoproteins. Infect. Immun. 60, 596-601.
23. Fink, M. P., and Warren, H. S. (2014). Strategies to improve drug development for sepsis. Nat. Rev. Drug Discov. 13, 741-758. doi: 10.1038/nrd4368
24. Flegel, W. A., Wolpl, A., Mannel, D. N., and Northoff, H. (1989). Inhibition of endotoxin-induced activation of human monocytes by human lipoproteins. Infect. Immun. 57, 2237-2245.
25. Gong, M., Wilson, M., Kelly, T., Su, W., Dressman, J., Kincer, J., et al. (2003). HDL-associated estradiol stimulates endothelial NO synthase and vasodilation in an SR-BI-dependent manner. J. Clin. Invest. 111, 1579-1587. doi: 10.1172/JCI16777
26. Gordon, B. R. (2004). Poor outcomes associated with low lipid and lipoprotein levels*. Crit. Care Med. 32, 878-879. doi: 10.1097/01.CCM.0000117318.84442.9F
27. Grunfeld, C., Marshall, M., Shigenaga, J. K., Moser, A. H., Tobias, P., and Feingold, K. R. (1999). Lipoproteins inhibit macrophage activation by lipoteichoic acid. J. Lipid Res. 40, 245-252.
28. Guo, L., Ai, J., Zheng, Z., Howatt, D. A., Daugherty, A., Huang, B., et al. (2013). High density lipoprotein protects against polymicrobe-induced sepsis in mice. J. Biol. Chem. 288, 17947-17953. doi: 10.1074/jbc. M112.442699
29. Guo, L., Song, Z., Li, M., Wu, Q., Wang, D., Feng, H., et al. (2009). Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J. Biol. Chem. 284, 19826-19834. doi: 10.1074/jbc. M109.020933
30. Gupta, H., Dai, L., Datta, G., Garber, D. W., Grenett, H., Li, Y., et al. (2005). Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein ai mimetic peptide. Circ. Res. 97, 236-243. doi: 10.1161/01.res.0000176530.66400.48
31. Harris, H. W., Grunfeld, C., Feingold, K. R., and Rapp, J. H. (1990). Human very low density lipoproteins and chylomicrons can protect against endotoxin-induced death in mice. J. Clin. Invest. 86, 696-702. doi: 10.1172/JCI114765
32. Harris, H. W., Grunfeld, C., Feingold, K. R., Read, T. E., Kane, J. P., Jones, A. L., et al. (1993). Chylomicrons alter the fate of endotoxin, decreasing tumor necrosis factor release and preventing death. J. Clin. Invest. 91, 1028-1034. doi: 10.1172/JCI116259
33. Harris, H. W., Johnson, J. A., and Wigmore, S. J. (2002). Endogenous lipoproteins impact the response to endotoxin in humans. Crit. Care Med. 30, 23-31. doi: 10.1097/00003246-200201000-00004
34. Hewing, B., Moore, K. J., and Fisher, E. A. (2012). HDL and cardiovascular risk. Circ. Res. 111, 1117-1120. doi: 10.1161/circresaha.112.280958
35. Hubsch, A. P., Casas, A. T., and Doran, J. E. (1995). Protective effects of reconstituted high-density lipoprotein in rabbit gram-negative bacteremia models. J. Lab. Clin. Med. 126, 548-558.
36. Hubsch, A. P., Powell, F. S., Lerch, P. G., and Doran, J. E. (1993). A reconstituted, ApoA1 containing lipoprotein reduces tumor necrosis factor release and attenuates shock in endotoxemic rabbits. Circ. Shock 40, 14-23.
37. Imai, T., Fujita, T., and Yamazaki, Y. (2003). Beneficial effects of apolipoprotein A-I on endotoxemia. Surg. Today 33, 684-687. doi: 10.1007/s00595-003-2585-4
38. Krause, B. R., and Remaley, A. T. (2013). Reconstituted HDL for the acute treatment of acute coronary syndrome. Curr. Opin. Lipidol. 24, 480-486. doi: 10.1097/MOL.0000000000000020
39. Lagu, T., Rothberg, M. B., Shieh, M. S., Pekow, P. S., Steingrub, J. S., and Lindenauer, P. K. (2012). Hospitalizations, costs, and outcomes of severe sepsis in the United States 2003 to 2007. Crit. Care Med. 40, 754-761. doi: 10.1097/CCM.0b013e318232db65
40. Lee, R. P., Lin, N. T., Chao, Y. F., Lin, C. C., Harn, H. J., and Chen, H. I. (2007). High-density lipoprotein prevents organ damage in endotoxemia. Res. Nurs. Health 30, 250-260. doi: 10.1002/nur.20187
41. Levels, J. H. M., Abraham, P. R., van den Ende, A., and van Deventer, S. J. H. (2001). Distribution and kinetics of lipoprotein-bound endotoxin. Infect. Immun. 69, 2821-2828. doi: 10.1128/iai.69.5.2821-2828.2001
42. Levine, D. M., Parker, T. S., Donnelly, T. M., Walsh, A., and Rubin, A. L. (1993). In vivo protection against endotoxin by plasma high density lipoprotein. Proc. Natl. Acad. Sci. U.S.A. 90, 12040-12044. doi: 10.1073/pnas.90.24.12040
43. Lewis, G. F., and Rader, D. J. (2005). New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ. Res. 96, 1221-1232. doi: 10.1161/01.RES.0000170946.56981.5c
44. Li, X. A., Titlow, W. B., Jackson, B. A., Giltiay, N., Nikolova-Karakashian, M., Uittenbogaard, A., et al. (2002). High density lipoprotein binding to scavenger receptor, Class B, type I activates endothelial nitric-oxide synthase in a ceramide-dependent manner. J. Biol. Chem. 277, 11058-11063. doi: 10.1074/jbc. M110985200
45. Li, Y., Dong, J.-B., and Wu, M.-P. (2008). Human ApoA-I overexpression diminishes LPS-induced systemic inflammation and multiple organ damage in mice. Eur. J. Pharmacol. 590, 417-422. doi: 10.1016/j.ejphar.2008.06.047
46. Lüscher, T. F., Landmesser, U., von Eckardstein, A., and Fogelman, A. M. (2014). High-density lipoprotein: vascular protective effects, dysfunction, and potential as therapeutic target. Circ. Res. 114, 171-182. doi: 10.1161/circresaha.114.300935
47. Martin, G. S., Mannino, D. M., Eaton, S., and Moss, M. (2003). The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348, 1546-1554. doi: 10.1056/NEJMoa022139
48. Mendez, A. J., Lin, G., Wade, D. P., Lawn, R. M., and Oram, J. F. (2001). Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J. Biol. Chem. 276, 3158-3166. doi: 10.1074/jbc. M007717200
49. Mineo, C., Deguchi, H., Griffin, J. H., and Shaul, P. W. (2006). Endothelial and antithrombotic actions of HDL. Circ. Res. 98, 1352-1364. doi: 10.1161/01.res.0000225982.01988.93
50. Mineo, C., and Shaul, P. W. (2012). Novel biological functions of high-density lipoprotein cholesterol. Circ. Res. 111, 1079-1090. doi: 10.1161/circresaha.111.258673
51. Mineo, C., Yuhanna, I. S., Quon, M. J., and Shaul, P. W. (2003). High density lipoprotein-induced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J. Biol. Chem. 278, 9142-9149. doi: 10.1074/jbc. M211394200
52. Ming, X. F., Barandier, C., Viswambharan, H., Kwak, B. R., Mach, F., Mazzolai, L., et al. (2004). Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation 110, 3708-3714. doi: 10.1161/01.CIR.0000142867.26182.32
53. Moreira, R. S., Irigoyen, M., Sanches, T. R., Volpini, R. A., Camara, N. O. S., Malheiros, D. M., et al. (2014). Apolipoprotein A-I mimetic peptide 4F attenuates kidney injury, heart injury, and endothelial dysfunction in sepsis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R514-R524. doi: 10.1152/ajpregu.00445.2013
54. Munford, R. S. (2005). Detoxifying endotoxin: time, place and person. J. Endotoxin. Res. 11, 69-84. doi: 10.1179/096805105X35161
55. Munford, R. S., and Dietschy, J. M. (1985). Effects of specific antibodies, hormones, and lipoproteins on bacterial lipopolysaccharides injected into the rat. J. Infect. Dis. 152, 177-184. doi: 10.1093/infdis/152.1.177
56. Murch, O., Collin, M., Hinds, C. J., and Thiemermann, C. (2007). Lipoproteins in inflammation and sepsis. I. Basic science. Intensive Care Med. 33, 13-24. doi: 10.1007/s00134-006-0432-y
57. Navab, M., Anantharamaiah, G. M., Reddy, S. T., Hama, S., Hough, G., Grijalva, V. R., et al. (2005). Apolipoprotein A-I mimetic peptides. Arterioscler. Thromb. Vasc. Biol. 25, 1325-1331. doi: 10.1161/01.atv.0000165694.39518.95
58. Navab, M., Reddy, S. T., Van Lenten, B. J., and Fogelman, A. M. (2011). HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat. Rev. Cardiol. 8, 222-232. doi: 10.1038/nrcardio.2010.222
59. Nicholls, S. J., Uno, K., Kataoka, Y., and Nissen, S. E. (2011). ETC-216 for coronary artery disease. Expert Opin. Biol. Ther. 11, 387-394. doi: 10.1517/14712598.2011.557061
60. Nissen, S. E., Tsunoda, T., Tuzcu, E. M., Schoenhagen, P., Cooper, C. J., Yasin, M., 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. doi: 10.1001/jama.290.17.2292
61. Nofer, J.-R., Kehrel, B., Fobker, M., Levkau, B., Assmann, G., and Eckardstein, A. V. (2002). HDL and arteriosclerosis: beyond reverse cholesterol transport. Atherosclerosis 161, 1-16. doi: 10.1016/S0021-9150(01)00651-7
62. Ohashi, R., Mu, H., Wang, X., Yao, Q., and Chen, C. (2005). Reverse cholesterol transport and cholesterol efflux in atherosclerosis. QJM 98, 845-856. doi: 10.1093/qjmed/hci136
63. Pajkrt, D., Doran, J. E., Koster, F., Lerch, P. G., Arnet, B., van der Poll, T., et al. (1996). Antiinflammatory effects of reconstituted high-density lipoprotein during human endotoxemia. J. Exp. Med. 184, 1601-1608. doi: 10.1084/jem.184.5.1601
64. Patel, S., Drew, B. G., Nakhla, S., Duffy, S. J., Murphy, A. J., Barter, P. J., et al. (2009). Reconstituted high-density lipoprotein increases plasma high-density lipoprotein anti-inflammatory properties and cholesterol e?ux capacity in patients with type 2 diabetes. J. Am. Coll. Cardiol. 53, 962-971. doi: 10.1016/j.jacc.2008.12.008
65. Puff, N., Lamaziere, A., Seigneuret, M., Trugnan, G., and Angelova, M. I. (2005). HDLs induce raft domain vanishing in heterogeneous giant vesicles. Chem. Phys. Lipids 133, 195-202. doi: 10.1016/j.chemphyslip.2004.10.003
66. Quezado, Z. M., Natanson, C., Banks, S. M., Alling, D. W., Koev, C. A., Danner, R. L., et al. (1995). Therapeutic trial of reconstituted human high-density lipoprotein in a canine model of gram-negative septic shock. J. Pharmacol. Exp. Ther. 272, 604-611.
67. Raetz, C. R., and Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700. doi: 10.1146/annurev.biochem.71.110601.135414
68. Read, T. E., Harris, H. W., Grunfeld, C., Feingold, K. R., Calhoun, M. C., Kane, J. P., et al. (1993). Chylomicrons enhance endotoxin excretion in bile. Infect. Immun. 61, 3496-3502.
69. Remaley, A. T., Amar, M., and Sviridov, D. (2008). HDL-replacement therapy: mechanism of action, types of agents and potential clinical indications. Expert Rev. Cardiovasc. Ther. 6, 1203-1215. doi: 10.1586/14779072.6.9.1203
70. Riedemann, N. C., Guo, R. F., and Ward, P. A. (2003). The enigma of sepsis. J. Clin. Invest. 112, 460-467. doi: 10.1172/JCI200319523
71. Riwanto, M., and Landmesser, U. (2013). High density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J. Lipid Res. 54, 3227-3243. doi: 10.1194/jlr. R037762
72. Sessler, C. N., Perry, J. C., and Varney, K. L. (2004). Management of severe sepsis and septic shock. Curr. Opin. Crit. Care 10, 354-363. doi: 10.1097/01.ccx.0000139363.76068.7b
73. Sethi, A. A., Stonik, J. A., Thomas, F., Demosky, S. J., Amar, M., Neufeld, E., et al. (2008). Asymmetry in the lipid affinity of bihelical amphipathic peptides: a structural determinant for the specificity of ABCA1-dependent cholesterol e?ux by peptides. J. Biol. Chem. 283, 32273-32282. doi: 10.1074/jbc. M804461200
74. Shapiro, N. I., Schuetz, P., Yano, K., Sorasaki, M., Parikh, S. M., Jones, A. E., et al. (2010). The association of endothelial cell signaling, severity of illness, and organ dysfunction in sepsis. Crit. Care 14:R182. doi: 10.1186/cc9290
75. Singh, I. M., Shishehbor, M. H., and Ansell, B. J. (2007). High-density lipoprotein as a therapeutic target: a systematic review. JAMA 298, 786-798. doi: 10.1001/jama.298.7.786
76. Su, G. L. (2002). Lipopolysaccharides in liver injury: molecular mechanisms of Kupffer cell activation. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G256-G265. doi: 10.1152/ajpgi.00550.2001
77. Suzuki, M., Pritchard, D. K., Becker, L., Hoofnagle, A. N., Tanimura, N., Bammler, T. K., et al. (2010). High-density lipoprotein suppresses the type I interferon response, a family of potent antiviral immunoregulators, in macrophages challenged with lipopolysaccharide. Circulation 122, 1919-1927. doi: 10.1161/CIRCULATIONAHA.110.961193
78. Tardif, J. C., Grégoire, J., L'Allier, P. L., Ibrahim, R., Lespérance, J., Heinonen, T. M., et al. (2007). Effects of reconstituted high-density lipoprotein infusions on coronary atherosclerosis: a randomized controlled trial. JAMA 297, 1675-1682. doi: 10.1001/jama.297.15.jpc70004
79. Tsai, M. H., Peng, Y. S., Chen, Y. C., Lien, J. M., Tian, Y. C., Fang, J. T., et al. (2009). Low serum concentration of apolipoprotein A-I is an indicator of poor prognosis in cirrhotic patients with severe sepsis. J. Hepatol. 50, 906-915. doi: 10.1016/j.jhep.2008.12.024
80. Ulevitch, R. J., Johnston, A. R., and Weinstein, D. B. (1979). New function for high density lipoproteins. Their participation in intravascular reactions of bacterial lipopolysaccharides. J. Clin. Invest. 64, 1516-1524. doi: 10.1172/JCI109610
81. Ulevitch, R. J., Johnston, A. R., and Weinstein, D. B. (1981). New function for high density lipoproteins. Isolation and characterization of a bacterial lipopolysaccharide-high density lipoprotein complex formed in rabbit plasma. J. Clin. Invest. 67, 827-837. doi: 10.1172/JCI110100
82. Van Amersfoort, E. S., Van Berkel, T. J., and Kuiper, J. (2003). Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin. Microbiol. Rev. 16, 379-414. doi: 10.1128/CMR.16.3.379-414.2003
83. van Leeuwen, H. J., Heezius, E. C., Dallinga, G. M., van Strijp, J. A., Verhoef, J., and van Kessel, K. P. (2003). Lipoprotein metabolism in patients with severe sepsis. Crit. Care Med. 31, 1359-1366. doi: 10.1097/01.CCM.0000059724.08290.51
84. Van Lenten, B. J., Fogelman, A. M., Haberland, M. E., and Edwards, P. A. (1986). The role of lipoproteins and receptor-mediated endocytosis in the transport of bacterial lipopolysaccharide. Proc. Natl. Acad. Sci. U.S.A. 83, 2704-2708. doi: 10.1073/pnas.83.8.2704
85. Van Lenten, B. J., Wagner, A. C., Anantharamaiah, G. M., Garber, D. W., Fishbein, M. C., Adhikary, L., et al. (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. doi: 10.1161/01.cir.0000030182.35880.3e
86. Vickers, K. C., and Remaley, A. T. (2014). HDL and cholesterol: life after the divorce? J. Lipid Res. 55, 4-12. doi: 10.1194/jlr. R035964
87. Vincent, J. L., Rello, J., Marshall, J., Silva, E., Anzueto, A., Martin, C. D., et al. (2009). INternational study of the prevalence and outcomes of infection in intensive care units. JAMA 302, 2323-2329. doi: 10.1001/jama.2009.1754
88. Vishnyakova, T. G., Bocharov, A. V., Baranova, I. N., Chen, Z., Remaley, A. T., Csako, G., et al. (2003). Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1. J. Biol. Chem. 278, 22771-22780. doi: 10.1074/jbc. M211032200
89. Viswambharan, H., Ming, X. F., Zhu, S., Hubsch, A., Lerch, P., Vergeres, G., et al. (2004). Reconstituted high-density lipoprotein inhibits thrombin-induced endothelial tissue factor expression through inhibition of RhoA and stimulation of phosphatidylinositol 3-kinase but not Akt/endothelial nitric oxide synthase. Circ. Res. 94, 918-925. doi: 10.1161/01.RES.0000124302.20396.B7
90. von Eckardstein, A., Nofer, J.-R., and Assmann, G. (2001). High density lipoproteins and arteriosclerosis: role of cholesterol e?ux and reverse cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 21, 13-27. doi: 10.1161/01.atv.21.1.13
91. Warren, H. S., Amato, S. F., Fitting, C., Black, K. M., Loiselle, P. M., Pasternack, M. S., et al. (1993). Assessment of ability of murine and human anti-lipid A monoclonal antibodies to bind and neutralize lipopolysaccharide. J. Exp. Med. 177, 89-97. doi: 10.1084/jem.177.1.89
92. Yan, Y.-J., Li, Y., Lou, B., and Wu, M.-P. (2006). Beneficial effects of ApoA-I on LPS-induced acute lung injury and endotoxemia in mice. Life Sci. 79, 210-215. doi: 10.1016/j.lfs.2006.02.011
93. Yuhanna, I. S., Zhu, Y., Cox, B. E., Hahner, L. D., Osborne-Lawrence, S., Lu, P., et al. (2001). High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 7, 853-857. doi: 10.1038/89986
94. Yvan-Charvet, L., Welch, C., Pagler, T. A., Ranalletta, M., Lamkanfi, M., Han, S., et al. (2008). Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118, 1837-1847. doi: 10.1161/CIRCULATIONAHA.108.793869
95. Zhang, X., Wang, L., and Chen, B. (2015). Recombinant HDL (Milano) protects endotoxin-challenged rats from multiple organ injury and dysfunction. Biol. Chem. 396, 53-60. doi: 10.1515/hsz-2014-0188
96. Zhang, Z., Datta, G., Zhang, Y., Miller, A. P., Mochon, P., Chen, Y.-F., et al. (2009). Apolipoprotein A-I mimetic peptide treatment inhibits inflammatory responses and improves survival in septic rats. Am. J. Physiol. Heart Circ. Physiol. 297, H866-H873.
97. Zhu, X., Lee, J. Y., Timmins, J. M., Brown, J. M., Boudyguina, E., Mulya, A., et al. (2008). Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283, 22930-22941. doi: 10.1074/jbc. M801408200
98. Zhu, X., and Parks, J. S. (2012). New roles of HDL in inflammation and hematopoiesis. Annu. Rev. Nutr. 32, 161-182. doi: 10.1146/annurev-nutr-071811-150709