Skip to main content

Advertisement

SpringerLink
Log in

Lipoproteins in inflammation and sepsis. I. Basic science

  • Mini series: Basic research-related topics in ICM
  • Published:
Intensive Care Medicine Aims and scope Submit manuscript

Abstract

Background

High-density lipoproteins (HDL) have been shown to bind and neutralize lipopolysaccharide (LPS) and are regarded as possible therapeutic agents for sepsis and conditions associated with local or systemic inflammation. However, in recent years, a multitude of possible immunomodulatory properties other than LPS neutralization have become evident.

Discussion

This review highlights the advances in the understanding of how HDL is protective in both in vitro and in vivo inflammatory settings, including the ability of HDL to modulate adhesion molecule expression, upregulate endothelial nitric oxide synthase and counteract oxidative stress. Also, the active components of HDL and the recent discovery of novel lipid modulators of inflammation are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Martin GS, Mannino DM, Eaton S, Moss M (2003) The Epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348:1546–1554

    Article  PubMed  Google Scholar 

  2. Hoyert DL, Kochanek KD, Murphy SL (1999) Deaths: final data for 1997. Natl Vital Stat Rep 47:1–104

    Google Scholar 

  3. Riedemann NC, Guo RF, Ward PA (2003) The enigma of sepsis. J Clin Invest 112:460–467

    Article  PubMed  CAS  Google Scholar 

  4. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303–1310

    Article  PubMed  CAS  Google Scholar 

  5. Smithies MN, Weaver CB (2004) Role of the tissue factor pathway in the pathogenesis and management of multiple organ failure. Blood Coagul Fibrinolysis 15 Suppl 1:S11–S20

    Google Scholar 

  6. Andrews P, Azoulay E, Antonelli M, Brochard L, Brun-Buisson C, Dobb G, Fagon JY, Gerlach H, Groeneveld J, Mancebo J, Metnitz P, Nava S, Pugin J, Pinsky M, Radermacher P, Richard C, Tasker R, Vallet B (2005) Year in review in intensive care medicine, 2004. III. Outcome, ICU organisation, scoring, quality of life, ethics, psychological problems and communication in the ICU, immunity and hemodynamics during sepsis, pediatric and neonatal critical care, experimental studies. Intensive Care Med 31:356–372

    Article  PubMed  Google Scholar 

  7. Andrews P, Azoulay E, Antonelli M, Brochard L, Brun-Buisson C, Dobb G, Fagon JY, Gerlach H, Groeneveld J, Mancebo J, Metnitz P, Nava S, Pugin J, Pinsky M, Radermacher P, Richard C, Tasker R, Vallet B (2005) Year in review in intensive care medicine, 2004. II. Brain injury, hemodynamic monitoring and treatment, pulmonary embolism, gastrointestinal tract, and renal failure. Intensive Care Med 31:177–188

    Article  PubMed  Google Scholar 

  8. Andrews P, Azoulay E, Antonelli M, Brochard L, Brun-Buisson C, Dobb G, Fagon JY, Gerlach H, Groeneveld J, Mancebo J, Metnitz P, Nava S, Pugin J, Pinsky M, Radermacher P, Richard C, Tasker R, Vallet B (2005) Year in review in intensive care medicine, 2004. I. Respiratory failure, infection, and sepsis. Intensive Care Med 31:28–40

    Article  PubMed  Google Scholar 

  9. Van Amersfoort ES, van Berkel TJ, Kuiper J (2003) Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin Microbiol Rev 16:379–414

    Article  PubMed  CAS  Google Scholar 

  10. Pinsky MR (2004) Dysregulation of the immune response in severe sepsis. Am J Med Sci 328:220–229

    Article  PubMed  Google Scholar 

  11. Cockerill GW, McDonald MC, Mota-Filipe H, Cuzzocrea S, Miller NE, Thiemermann C (2001) High density lipoproteins reduce organ injury and organ dysfunction in a rat model of hemorrhagic shock. FASEB J 15:1941–1952

    Article  PubMed  CAS  Google Scholar 

  12. Cuzzocrea S, Dugo L, Patel NS Di PR, Cockerill GW, Genovese T, Thiemermann C (2004) High-density lipoproteins reduce the intestinal damage associated with ischemia/reperfusion and colitis. Shock 21:342–351

    Article  PubMed  CAS  Google Scholar 

  13. McDonald MC, Dhadly P, Cockerill GW, Cuzzocrea S, Mota-Filipe H, Hinds CJ, Miller NE, Thiemermann C (2003) Reconstituted high-density lipoprotein attenuates organ injury and adhesion molecule expression in a rodent model of endotoxic shock. Shock 20:551–557

    Article  PubMed  CAS  Google Scholar 

  14. Thiemermann C, Patel NS, Kvale EO, Cockerill GW, Brown PA, Stewart KN, Cuzzocrea S, Britti D, Mota-Filipe H, Chatterjee PK (2003) High density lipoprotein (HDL) reduces renal ischemia/reperfusion injury. J Am Soc Nephrol 14:1833–1843

    Article  PubMed  CAS  Google Scholar 

  15. Cockerill GW, Reed S (1999) High-density lipoprotein: multipotent effects on cells of the vasculature. Int Rev Cytol 188:257–297

    PubMed  CAS  Google Scholar 

  16. Rye KA, Clay MA, Barter PJ (1999) Remodelling of high density lipoproteins by plasma factors. Atherosclerosis 145:227–238

    Article  PubMed  CAS  Google Scholar 

  17. Miller NE, Thelle DS, Forde OH, Mjos OD (1977) The Tromso heart-study. High-density lipoprotein and coronary heart-disease: a prospective case-control study. Lancet I:965–968

    Article  Google Scholar 

  18. Gordon T, Castelli WP, Hjortland MC, Kannel WB, Dawber TR (1977) High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. Am J Med 62:707–714

    Article  PubMed  CAS  Google Scholar 

  19. Reasner CA (2005) What is the most effective strategy for managing diabetic dyslipidaemia? Atheroscler Suppl 6:21–27

    Article  PubMed  CAS  Google Scholar 

  20. Eckardstein A von, Hersberger M, Rohrer L (2005) Current understanding of the metabolism and biological actions of HDL. Curr Opin Clin Nutr Metab Care 8:147–152

    Article  Google Scholar 

  21. Hudgins LC, Parker TS, Levine DM, Gordon BR, Saal SD, Jiang XC, Seidman CE, Tremaroli JD Lai J, Rubin AL (2003) A single intravenous dose of endotoxin rapidly alters serum lipoproteins and lipid transfer proteins in normal volunteers. J Lipid Res 44:1489–1498

    Article  PubMed  CAS  Google Scholar 

  22. Levels JH, Lemaire LC, van den Ende AE, van Deventer SJ, van Lanschot JJ (2003) Lipid composition and lipopolysaccharide binding capacity of lipoproteins in plasma and lymph of patients with systemic inflammatory response syndrome and multiple organ failure. Crit Care Med 31:1647–1653

    Article  PubMed  CAS  Google Scholar 

  23. Rohrer L, Hersberger, M von EA (2004) High density lipoproteins in the intersection of diabetes mellitus, inflammation and cardiovascular disease. Curr Opin Lipidol 15:269–278

    Article  PubMed  CAS  Google Scholar 

  24. Rall DP, Gaskins JR, Kelly MG (1957) Reduction of febrile response to bacterial polysaccharide following incubation with serum. Am J Physiol 188:559–562

    PubMed  CAS  Google Scholar 

  25. Ulevitch RJ, Johnston AR (1978) The modification of biophysical and endotoxic properties of bacterial lipopolysaccharides by serum. J Clin Invest 62:1313–1324

    PubMed  CAS  Google Scholar 

  26. Ulevitch RJ, Johnston AR, Weinstein DB (1979) New function for high density lipoproteins. Their participation in intravascular reactions of bacterial lipopolysaccharides. J Clin Invest 64:1516–1524

    PubMed  CAS  Google Scholar 

  27. Baumberger C, Ulevitch RJ, Dayer JM (1991) Modulation of endotoxic activity of lipopolysaccharide by high-density lipoprotein. Pathobiology 59:378–383

    Article  PubMed  CAS  Google Scholar 

  28. Grunfeld C, Marshall M, Shigenaga JK, Moser AH, Tobias P, Feingold KR (1999) Lipoproteins inhibit macrophage activation by lipoteichoic acid. J Lipid Res 40:245–252

    PubMed  CAS  Google Scholar 

  29. Tuin A, Huizinga-Van der Vlag A, van Loenen-Weemaes AM, Meijer DK, Poelstra K (2005) On the role and fate of LPS-dephosphorylating activity in the rat liver. Am J Physiol Gastrointest Liver Physiol 290:G377–385

    Article  PubMed  CAS  Google Scholar 

  30. Harris HW, Grunfeld C, Feingold KR, Read TE, Kane JP, Jones AL, Eichbaum EB, Bland GF, Rapp JH (1993) Chylomicrons alter the fate of endotoxin, decreasing tumor necrosis factor release and preventing death. J Clin Invest 91:1028–1034

    PubMed  CAS  Google Scholar 

  31. Rensen PC, Oosten M, Bilt E, Eck M, Kuiper J, Berkel TJ (1997) Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats In vivo. J Clin Invest 99:2438–2445

    PubMed  CAS  Google Scholar 

  32. Lamping N, Dettmer R, Schroder NW, Pfeil D, Hallatschek W, Burger R, Schumann RR (1998) LPS-binding protein protects mice from septic shock caused by LPS or gram-negative bacteria. J Clin Invest 101:2065–2071

    PubMed  CAS  Google Scholar 

  33. Vesy CJ, Kitchens RL, Wolfbauer G, Albers JJ, Munford RS (2000) Lipopolysaccharide-binding protein and phospholipid transfer protein release lipopolysaccharides from Gram-negative bacterial membranes. Infect Immun 68:2410–2417

    Article  PubMed  CAS  Google Scholar 

  34. Levels JHM, Marquart JA, Abraham PR, van den Ende AE, Molhuizen HOF, van Deventer SJH, Meijers JCM (2005) Lipopolysaccharide Is transferred from high-density to low-density lipoproteins by lipopolysaccharide-binding protein and phospholipid transfer protein. Infect Immun 73:2321–2326

    Article  PubMed  CAS  Google Scholar 

  35. Flegel WA, Wolpl A, Mannel DN, Northoff H (1989) Inhibition of endotoxin-induced activation of human monocytes by human lipoproteins. Infect Immun 57:2237–2245

    PubMed  CAS  Google Scholar 

  36. Cavaillon JM, Fitting C, Haeffner-Cavaillon N, Kirsch SJ, Warren HS (1990) Cytokine response by monocytes and macrophages to free and lipoprotein-bound lipopolysaccharide. Infect Immun 58:2375–2382

    PubMed  CAS  Google Scholar 

  37. Kitchens RL, Wolfbauer G, Albers JJ, Munford RS (1999) Plasma lipoproteins promote the release of bacterial lipopolysaccharide from the monocyte cell surface. J Biol Chem 274:34116–34122

    Article  PubMed  CAS  Google Scholar 

  38. Levine DM, Parker TS, Donnelly TM, Walsh A, Rubin AL (1993) In vivo protection against endotoxin by plasma high density lipoprotein. Proc Natl Acad Sci USA 90:12040–12044

    Article  PubMed  CAS  Google Scholar 

  39. Feingold KR, Funk JL, Moser AH, Shigenaga JK, Rapp JH, Grunfeld C (1995) Role for circulating lipoproteins in protection from endotoxin toxicity. Infect Immun 63:2041–2046

    PubMed  CAS  Google Scholar 

  40. Harris HW, Grunfeld C, Feingold KR, Rapp JH (1990) Human very low density lipoproteins and chylomicrons can protect against endotoxin-induced death in mice. J Clin Invest 86:696–702

    PubMed  CAS  Google Scholar 

  41. Hubsch AP, Casas AT, Doran JE (1995) Protective effects of reconstituted high-density lipoprotein in rabbit gram-negative bacteremia models. J Lab Clin Med 126:548–558

    PubMed  CAS  Google Scholar 

  42. Casas AT, Hubsch AP, Rogers BC, Doran JE (1995) Reconstituted high-density lipoprotein reduces LPS-stimulated TNF alpha. J Surg Res 59:544–552

    Article  PubMed  CAS  Google Scholar 

  43. Cockerill GW, Rye KA, Gamble JR, Vadas MA, Barter PJ (1995) High-density lipoproteins inhibit cytokine-induced expression of endothelial cell adhesion molecules. Arterioscler Thromb Vasc Biol 15:1987–1994

    PubMed  CAS  Google Scholar 

  44. Park SH, Park JH, Kang JS, Kang YH (2003) Involvement of transcription factors in plasma HDL protection against TNF-alpha-induced vascular cell adhesion molecule-1 expression. Int J Biochem Cell Biol 35:168–182

    Article  PubMed  CAS  Google Scholar 

  45. Yuhanna IS, Zhu Y, Cox BE, Hahner LD, Osborne-Lawrence S, Lu P, Marcel YL, Anderson RG, Mendelsohn ME, Hobbs HH, Shaul PW (2001) High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat Med 7:853–857

    Article  PubMed  CAS  Google Scholar 

  46. Wu CC, Ruetten H, Thiemermann C (1996) Comparison of the effects of aminoguanidine and N omega-nitro-L-arginine methyl ester on the multiple organ dysfunction caused by endotoxaemia in the rat. Eur J Pharmacol 300:99–104

    Article  PubMed  CAS  Google Scholar 

  47. Thiemermann C (1997) Nitric oxide and septic shock. Gen Pharmacol 29:159–166

    PubMed  CAS  Google Scholar 

  48. Wray GM, Millar CG, Hinds CJ, Thiemermann C (1998) Selective inhibition of the activity of inducible nitric oxide synthase prevents the circulatory failure, but not the organ injury/dysfunction, caused by endotoxin. Shock 9:329–335

    Article  PubMed  CAS  Google Scholar 

  49. Kaminski A, Pohl CB, Sponholz C, Ma N, Stamm C, Vollmar B, Steinhoff G (2004) Up-regulation of endothelial nitric oxide synthase inhibits pulmonary leukocyte migration following lung ischemia-reperfusion in mice. Am J Pathol 164:2241–2249

    PubMed  CAS  Google Scholar 

  50. Ferretti G, Bacchetti T, Moroni C, Savino S, Liuzzi A, Balzola F, Bicchiega V (2005) Paraoxonase activity in high-density lipoproteins: a comparison between healthy and obese females. J Clin Endocrinol Metab 90:1728–1733

    Article  PubMed  CAS  Google Scholar 

  51. Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M (1995) Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest 96:2882–2891

    Article  PubMed  CAS  Google Scholar 

  52. Chen G, Li J, Qiang X, Czura CJ, Ochani M, Ochani K, Ulloa L, Yang H, Tracey KJ, Wang P, Sama AE, Wang H (2005) Suppression of HMGB1 release by stearoyl lysophosphatidylcholine: an additional mechanism for its therapeutic effects in experimental sepsis. J Lipid Res 46:623–637

    Article  PubMed  CAS  Google Scholar 

  53. Yan JJ, Jung JS, Lee JE Lee J, Huh SO, Kim HS, Jung KC, Cho JY, Nam JS, Suh HW, Kim YH, Song DK (2004) Therapeutic effects of lysophosphatidylcholine in experimental sepsis. Nat Med 10:161–167

    Article  PubMed  CAS  Google Scholar 

  54. Stafforini DM, McIntyre TM, Carter ME, Prescott SM (1987) Human plasma platelet-activating factor acetylhydrolase. Association with lipoprotein particles and role in the degradation of platelet-activating factor. J Biol Chem 262:4215–4222

    PubMed  CAS  Google Scholar 

  55. Zimmerman GA, McIntyre TM, Prescott SM, Stafforini DM (2002) The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit Care Med 30:S294–S301

    Article  PubMed  CAS  Google Scholar 

  56. Opal S, Laterre PF, Abraham E, Francois B, Wittebole X, Lowry S, Dhainaut JF, Warren B, Dugernier T, Lopez A, Sanchez M, Demeyer I, Jauregui L, Lorente JA, McGee W, Reinhart K, Kljucar S, Souza S, Pribble J (2004) Recombinant human platelet-activating factor acetylhydrolase for treatment of severe sepsis: results of a phase III, multicenter, randomized, double-blind, placebo-controlled, clinical trial. Crit Care Med 32:332–341

    Article  PubMed  CAS  Google Scholar 

  57. Cue JI, DiPiro JT, Brunner LJ, Doran JE, Blankenship ME, Mansberger AR, Hawkins ML (1994) Reconstituted high density lipoprotein inhibits physiologic and tumor necrosis factor alpha responses to lipopolysaccharide in rabbits. Arch Surg 129:193–197

    PubMed  CAS  Google Scholar 

  58. Emancipator K, Csako G, Elin RJ (1992) In vitro inactivation of bacterial endotoxin by human lipoproteins and apolipoproteins. Infect Immun 60:596–601

    PubMed  CAS  Google Scholar 

  59. Flegel WA, Baumstark MW, Weinstock C, Berg A, Northoff H (1993) Prevention of endotoxin-induced monokine release by human low- and high-density lipoproteins and by apolipoprotein A-I. Infect Immun 61:5140–5146

    PubMed  CAS  Google Scholar 

  60. Van OM, Rensen PC, Van Amersfoort ES, Van EM, Van Dam AM, Breve JJ, Vogel T, Panet A, van Berkel TJ, Kuiper J (2001) Apolipoprotein E protects against bacterial lipopolysaccharide-induced lethality. A new therapeutic approach to treat gram-negative sepsis. J Biol Chem 276:8820–8824

    Article  Google Scholar 

  61. Goldfarb RD, Parker TS, Levine DM, Glock D, Akhter I, Alkhudari A, McCarthy RJ, David EM, Gordon BR, Saal SD, Rubin AL, Trenholme GM, Parrillo JE (2003) Protein-free phospholipid emulsion treatment improved cardiopulmonary function and survival in porcine sepsis. Am J Physiol Regul Integr Comp Physiol 284:R550–R557

    PubMed  Google Scholar 

  62. Winchell WW, Hardy J, Levine DM, Parker TS, Gordon BR, Saal SD (2002) Effect of administration of a phospholipid emulsion on the initial response of horses administered endotoxin. Am J Vet Res 63:1370–1378

    Article  PubMed  CAS  Google Scholar 

  63. Gordon BR, Parker TS, Levine DM, Feuerbach F, Saal SD, Sloan BJ Chu C, Stenzel KH, Parrillo JE, Rubin AL (2005) Neutralization of endotoxin by a phospholipid emulsion in healthy volunteers. J Infect Dis 191:1515–1522

    Article  PubMed  CAS  Google Scholar 

  64. Xia P, Vadas MA, Rye KA, Barter PJ, Gamble JR (1999) High density lipoproteins (HDL) interrupt the sphingosine kinase signaling pathway. A possible mechanism for protection against atherosclerosis by HDL. J Biol Chem 274:33143–33147

    Article  PubMed  CAS  Google Scholar 

  65. Bolick DT, Srinivasan S, Kim KW, Hatley ME, Clemens JJ, Whetzel A, Ferger N, Macdonald TL, Davis MD, Tsao PS, Lynch KR, Hedrick CC (2005) Sphingosine-1-phosphate prevents tumor necrosis factor-α-mediated monocyte adhesion to aortic endothelium in mice. Arterioscler Thromb Vasc Biol 25:976–981

    Article  PubMed  CAS  Google Scholar 

  66. Garg SK, Volpe E, Palmieri G, Mattei M, Galati D, Martino A, Piccioni MS, Valente E, De Bonanno E, Baldini PM, Spagnoli LG, Colizzi V, Fraziano M (2004) Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo. J Infect Dis 189:2129–2138

    Article  PubMed  CAS  Google Scholar 

  67. Nofer JR, Levkau B, Wolinska I, Junker R, Fobker M, von Eckardstein A, Seedorf U, Assmann G (2001) Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J Biol Chem 276:34480–34485

    Article  PubMed  CAS  Google Scholar 

  68. Wu A, Hinds CJ, Thiemermann C (2004) High-density lipoproteins in sepsis and septic shock: metabolism, actions, and therapeutic applications. Shock 21:210–221

    Article  PubMed  CAS  Google Scholar 

  69. Kimura T, Tomura H, Mogi C, Kuwabara A, Ishiwara M, Shibasawa K, Sato K, Ohwada, S Im DS, Kurose H (2006) Sphingosine 1-phosphate receptors mediate stimulatory and inhibitory signalings for expression of adhesion molecules in endothelial cells. Cell Signal (in press)

  70. Nofer JR, Geigenmuller S, Gopfert C, Assmann G, Buddecke E, Schmidt A (2003) High density lipoprotein-associated lysosphingolipids reduce E-selectin expression in human endothelial cells. Biochem Biophys Res Commun 310:98–103

    Article  PubMed  CAS  Google Scholar 

  71. Finigan JH, Dudek SM, Singleton PA, Chiang ET, Jacobson JR, Camp SM Ye SQ, Garcia JG (2005) Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 280:17286–17293

    Article  PubMed  CAS  Google Scholar 

  72. Singleton PA, Dudek SM, Chiang ET, Garcia JG (2005) Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J 19:1646–1656

    Article  PubMed  CAS  Google Scholar 

  73. Sunden-Cullberg J, Norrby-Teglund A, Rouhiainen A, Rauvala H, Herman G, Tracey KJ, Lee ML, Andersson J, Tokics L, Treutiger CJ (2005) Persistent elevation of high mobility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock. Crit Care Med 33:564–573

    Article  PubMed  CAS  Google Scholar 

  74. Drobnik W, Liebisch G, Audebert FX, Frohlich D, Gluck T, Vogel P, Rothe G, Schmitz G (2003) Plasma ceramide and lysophosphatidylcholine inversely correlate with mortality in sepsis patients. J Lipid Res 44:754–761

    Article  PubMed  CAS  Google Scholar 

  75. Ma Z, Li J, Yang L, Mu Y, Xie W, Pitt B, Li S (2004) Inhibition of LPS- and CpG DNA-induced TNF-α response by oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol 286:L808–L816

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. St. Bartholomew’s and The Royal London, School of Medicine and Dentistry, Queen Mary University of London, Centre for Experimental Medicine, Nephrology and Critical Care, William Harvey Research Institute, Charterhouse Square, EC1M 6BQ, London, UK

    Oliver Murch, Marika Collin, Charles J. Hinds & Christoph Thiemermann

Authors
  1. Oliver Murch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marika Collin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Charles J. Hinds
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christoph Thiemermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christoph Thiemermann.

Additional information

This work was supported by grants provided by the Medical Research Council and the William Harvey Research Foundation, UK.

This article is discussed in the editorial available at: http://dx.doi.org/10.1007/s00134-006-0434-9.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murch, O., Collin, M., Hinds, C.J. et al. Lipoproteins in inflammation and sepsis. I. Basic science. Intensive Care Med 33, 13–24 (2007). https://doi.org/10.1007/s00134-006-0432-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00134-006-0432-y

Keywords

Search

Navigation