High density lipoprotein protects against polymicrobe-induced sepsis in mice

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 17947-17953

  Guo, Ling ^a   Ai, Junting ^a   Zheng, Zhong ^a   Howatt, Deborah A ^a   Daugherty, Alan ^a   Huang, Bin ^a   Li, Xiang An ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

HIGH DENSITY LIPOPROTEIN; PROTECTIVE EFFECTS;

MAMMALS;

APOLIPOPROTEIN A1; CORTICOSTERONE; CYTOKINE; HIGH DENSITY LIPOPROTEIN; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEATH; HORMONAL REGULATION; INFECTION SENSITIVITY; KNOCKOUT MOUSE; LEUKOCYTE MIGRATION; LIPOPROTEIN BLOOD LEVEL; METABOLIC CLEARANCE RATE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; STAPHYLOCOCCAL BACTEREMIA; STEROIDOGENESIS; STRAIN DIFFERENCE; SURVIVAL RATE; TRANSGENIC MOUSE;

EID: 84880069808     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.442699     Document Type: Article

References (50)

1. Bone, R. C. (1991) The pathogenesis of sepsis. Ann. Intern. Med. 115, 457-469
2. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., and Pinsky, M. R. (2001) Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310 (Pubitemid 32641789)
3. 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 (Pubitemid 36437931)
4. Riedemann, N. C., Guo, R. F., and Ward, P. A. (2003) The enigma of sepsis. J. Clin. Invest. 112, 460-467 (Pubitemid 38056327)
5. 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 (Pubitemid 39313504)
6. 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
7. Tsai, M. H., Peng, Y. S., Chen, Y. C., Lien, J. M., Tian, Y. C., Fang, J. T., Weng, H. H., Chen, P. C., Yang, C. W., and Wu, C. S. (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
8. 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 (Pubitemid 36583844)
9. 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 (Pubitemid 46115466)
10. Munford, R. S. (2005) Detoxifying endotoxin: Time, place and person. J. Endotoxin Res. 11, 69-84 (Pubitemid 40711482)
11. Read, T. E., Harris, H. W., Grunfeld, C., Feingold, K. R., Calhoun, M. C., Kane, J. P., and Rapp, J. H. (1993) Chylomicrons enhance endotoxin excretion in bile. Infect. Immun. 61, 3496-3502 (Pubitemid 23223444)
12. 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 (Pubitemid 20327356)
13. Harris, H. W., Grunfeld, C., Feingold, K. R., Read, T. E., Kane, J. P., Jones, A. L., Eichbaum, E. B., Bland, G. F., and Rapp, J. H. (1993) Chylomicrons alter the fate of endotoxin, decreasing tumor necrosis factor release and preventing death. J. Clin. Invest. 91, 1028-1034 (Pubitemid 23095278)
14. 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
15. 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
16. 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 (Pubitemid 11142375)
17. Mineo, C., and Shaul, P. W. (2012) Novel biological functions of highdensity lipoprotein cholesterol. Circ. Res. 111, 1079-1090
18. Ji, A., Wroblewski, J. M., Cai, L., de Beer, M. C., Webb, N. R., and van der Westhuyzen, D. R. (2012) NascentHDLformation in hepatocytes and role of ABCA1, ABCG1, and SR-BI. J. Lipid Res. 53, 446-455
19. Eisenberg, S. (1984) High density lipoprotein metabolism. J. Lipid Res. 25, 1017-1058
20. Williamson, R., Lee, D., Hagaman, J., and Maeda, N. (1992) Marked reduction of high density lipoprotein cholesterol in mice genetically modified to lack apolipoprotein A-I. Proc. Natl. Acad. Sci. U.S.A. 89, 7134-7138
21. Pavlou, E., Makris, K., Palaiologou, A., Kaldis, B., Vrioni, G., Economou, E., Eforakopoulou, M., Zerva, L., Drakopoulos, I., and Ioannidou, E. (2008) Decreased apolipoprotein A1 levels correlate with sepsis and adverse outcome among ICU patients. Crit. Care 12, P201
22. Dai, L., Datta, G., Zhang, Z., Gupta, H., Patel, R., Honavar, J., Modi, S., Wyss, J. M., Palgunachari, M., Anantharamaiah, G. M., and White, C. R. (2010) The apolipoprotein A-I mimetic peptide 4F prevents defects in vascular function in endotoxemic rats. J. Lipid Res. 51, 2695-2705
23. Hubsch, A. P., Powell, F. S., Lerch, P. G., and Doran, J. E. (1993) A reconstituted, apolipoprotein A-I containing lipoprotein reduces tumor necrosis factor release and attenuates shock in endotoxemic rabbits. Circ. Shock 40, 14-23 (Pubitemid 23148545)
24. Cué, J. I., DiPiro, J. T., Brunner, L. J., Doran, J. E., Blankenship, M. E., Mansberger, A. R., and Hawkins, M. L. (1994) Reconstituted high density lipoprotein inhibits physiologic and tumor necrosis factor α responses to lipopolysaccharide in rabbits. Arch. Surg. 129, 193-197 (Pubitemid 24056075)
25. Wang, L., Chen, W.-Z., and Wu, M.-P. (2010) Apolipoprotein A-I inhibits chemotaxis, adhesion, activation of THP-1 cells and improves the plasma HDL inflammatory index. Cytokine 49, 194-200
26. Pajkrt, D., Doran, J. E., Koster, F., Lerch, P. G., Arnet, B., van der Poll, T., ten Cate, J. W., and van Deventer, S. J. (1996) Antiinflammatory effects of reconstituted high-density lipoprotein during human endotoxemia. J. Exp. Med. 184, 1601-1608 (Pubitemid 26404453)
27. Parker, T. S., Levine, D. M., Chang, J. C., Laxer, J., Coffin, C. C., and Rubin, A. L. (1995) Reconstituted high-density lipoprotein neutralizes Gramnegative bacterial lipopolysaccharides in human whole blood. Infect. Immun. 63, 253-258
28. 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 (Pubitemid 24008776)
29. Eskandari, M. K., Bolgos, G., Miller, C., Nguyen, D. T., DeForge, L. E., and Remick, D. G. (1992) Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia. J. Immunol. 148, 2724-2730
30. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282, 2085-2088 (Pubitemid 29001265)
31. Echtenacher, B., Freudenberg, M. A., Jack, R. S., and Männel, D. N. (2001) Differences in innate defense mechanisms in endotoxemia and polymicrobial septic peritonitis. Infect. Immun. 69, 7271-7276 (Pubitemid 33086548)
32. Vazquez-Torres, A., Vallance, B. A., Bergman, M. A., Finlay, B. B., Cookson, B. T., Jones-Carson, J., and Fang, F. C. (2004) Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: Importance of the Kupffer cell network. J. Immunol. 172, 6202-6208 (Pubitemid 38621226)
33. Zhang, Z., Datta, G., Zhang, Y., Miller, A. P., Mochon, P., Chen, Y. F., Chatham, J., Anantharamaiah, G. M., and White, C. R. (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
34. Rittirsch, D., Huber-Lang, M. S., Flierl, M. A., and Ward, P. A. (2009) Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4, 31-36
35. Quezado, Z. M., Natanson, C., Banks, S. M., Alling, D. W., Koev, C. A., Danner, R. L., Elin, R. J., Hosseini, J. M., Parker, T. S., and Levine, D. M. (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
36. Feng, H., Guo, L., Song, Z., Gao, H., Wang, D., Fu, W., Han, J., Li, Z., Huang, B., and Li, X. A. (2010) Caveolin-1 protects against sepsis by modulating inflammatory response, alleviating bacterial burden, and suppressing thymocyte apoptosis. J. Biol. Chem. 285, 25154-25160
37. Guo, L., Song, Z., Li, M., Wu, Q., Wang, D., Feng, H., Bernard, P., Daugherty, A., Huang, B., and Li, X. A. (2009) Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J. Biol. Chem. 284, 19826-19834
38. Ocuin, L. M., Bamboat, Z. M., Balachandran, V. P., Cavnar, M. J., Obaid, H., Plitas, G., and DeMatteo, R. P. (2011) Neutrophil IL-10 suppresses peritoneal inflammatory monocytes during polymicrobial sepsis. J. Leukoc. Biol. 89, 423-432
39. Yurdakul, P., Dalton, J., Beattie, L., Brown, N., Erguven, S., Maroof, A., and Kaye, P. M. (2011) Compartment-specific remodeling of splenic microarchitecture during experimental visceral leishmaniasis. Am. J. Pathol. 179, 23-29
40. Suzuki, M., Pritchard, D. K., Becker, L., Hoofnagle, A. N., Tanimura, N., Bammler, T. K., Beyer, R. P., Bumgarner, R., Vaisar, T., de Beer, M. C., de Beer, F. C., Miyake, K., Oram, J. F., and Heinecke, J. W. (2010) Highdensity lipoprotein suppresses the type I interferon response, a family of potent antiviral immunoregulators, in macrophages challenged with lipopolysaccharide. Circulation 122, 1919-1927
41. Sorci-Thomas, M. G., Zabalawi, M., Bharadwaj, M. S., Wilhelm, A. J., Owen, J. S., Asztalos, B. F., Bhat, S., and Thomas, M. J. (2012) Dysfunctional HDL containing L159R apoA-I leads to exacerbation of atherosclerosis in hyperlipidemic mice. Biochim. Biophys. Acta 1821, 502-512
42. Wilhelm, A. J., Zabalawi, M., Grayson, J. M., Weant, A. E., Major, A. S., Owen, J., Bharadwaj, M., Walzem, R., Chan, L., Oka, K., Thomas, M. J., and Sorci-Thomas, M. G. (2009) Apolipoprotein A-I and its role in lymphocyte cholesterol homeostasis and autoimmunity. Arterioscler. Thromb. Vasc. Biol. 29, 843-849
43. Vishnyakova, T. G., Bocharov, A. V., Baranova, I. N., Chen, Z., Remaley, A. T., Csako, G., Eggerman, T. L., and Patterson, A. P. (2003) Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1. J. Biol. Chem. 278, 22771-22780 (Pubitemid 36830338)
44. 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
45. Hoekstra,M., Meurs, I., Koenders, M., Out, R., Hildebrand, R. B., Kruijt, J. K., Van Eck, M., and Van Berkel, T. J. (2008) Absence of HDL cholesteryl ester uptake in mice via SR-BI impairs an adequate adrenal glucocorticoid- mediated stress response to fasting. J. Lipid Res. 49, 738-745
46. 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 (Pubitemid 39390578)
47. Rubin, E. M., Ishida, B. Y., Clift, S. M., and Krauss, R. M. (1991) Expression of human apolipoprotein A-I in transgenic mice results in reduced plasma levels of murine apolipoprotein A-I and the appearance of two new high density lipoprotein size subclasses. Proc. Natl. Acad. Sci. U.S.A. 88, 434-438 (Pubitemid 21915479)
48. Yvan-Charvet, L., Pagler, T., Gautier, E. L., Avagyan, S., Siry, R. L., Han, S., Welch, C. L., Wang, N., Randolph, G. J., Snoeck, H. W., and Tall, A. R. (2010) ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328, 1689-1693
49. Acton, S., Rigotti, A., Landschulz, K. T., Xu, S., Hobbs, H. H., and Krieger, M. (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271, 518-520
50. Plump, A. S., Erickson, S. K., Weng, W., Partin, J. S., Breslow, J. L., and Williams, D. L. (1996) Apolipoprotein A-I is required for cholesteryl ester accumulation in steroidogenic cells and for normal adrenal steroid production. J. Clin. Invest. 97, 2660-2671 (Pubitemid 26187354)