Infection induces a positive acute phase apolipoprotein E response from a negative acute phase gene: Role of hepatic LDL receptors

Journal of Lipid Research

Volumn 49, Issue 8, 2008, Pages 1782-1793

  Li, Li ^a   Thompson, Patricia A ^a   Kitchens, Richard L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Acute inflammation; High density lipoprotein; Lipopolysaccharide; Low density lipoprotein; Sepsis

Indexed keywords

ACUTE PHASE PROTEIN; APOLIPOPROTEIN E; BACTERIUM LIPOPOLYSACCHARIDE; HIGH DENSITY LIPOPROTEIN; LIPID; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; APOLIPOPROTEIN C1; LIPOPOLYSACCHARIDE;

ACUTE PHASE RESPONSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL INFECTION; CLINICAL ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; HOST RESISTANCE; HUMAN; INFECTION RESISTANCE; KLEBSIELLA PNEUMONIAE; LIPID TRANSPORT; LIPOPROTEIN SYNTHESIS; MACROPHAGE; MOUSE; NONHUMAN; PLASMA CLEARANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; BLOOD; ENTEROBACTER INFECTION; INFLAMMATION; LIVER; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SEPSIS;

ACUTE-PHASE REACTION; ANIMALS; APOLIPOPROTEIN C-I; APOLIPOPROTEINS E; HUMANS; INFLAMMATION; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES; MICE; RECEPTORS, LDL; RNA, MESSENGER; SEPSIS;

EID: 48349148598     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800172-JLR200     Document Type: Article

References (51)

1. Mahley, R. W., and S. C. Rall, Jr. 2000. Apolipoprotein E: far more than a lipid transport protein. Annu. Rev. Genomics Hum. Genet. 1: 507-537.
2. Mahley, R. W., K. H. Weisgraber, and Y. Huang. 2006. Inaugural article. Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 103: 5644-5651.
3. Liberopoulos, E., K. Siamopoulos, and M. Elisaf. 2004. Apolipoprotein E and renal disease. Am. J. Kidney Dis. 43: 223-233.
4. Moore, R. J., R. M. Chamberlain, and F. R. Khuri. 2004. Apolipoprotein E and the risk of breast cancer in African-American and non-Hispanic white women. Oncology. 66: 79-93.
5. De Bont, N., M. G. Netea, P. N. Demacker, I. Verschueren, B. J. Kullberg, K. W. Van Dijk, J. W. van der Meer, and A. F. Stalenhoef. 1999. Apolipoprotein E knock-out mice are highly susceptible to endotoxemia and Klebsiella pneumoniae infection. J. Lipid Res. 40: 60-685.
6. de Bont, N., M. G. Netea, P. N. Demacker, B. J. Kullberg, J. W. van der Meer, and A. F. Stalenhoef. 2000. Apolipoprotein E-deficient mice have an impaired immune response to Klebsiella pneumoniae. Eur. J. Clin. Invest. 30: 818-822.
7. Roselaar, S. E., and A. Daugherty. 1998. Apolipoprotein E-deficient mice have impaired innate immune responses to Listeria monocytogenes in vivo. J. Lipid Res. 39: 1740-1743.
8. Sinnis, P., T. E. Willnow, M. R. S. Briones, J. Herz, and V. Nussenzweig. 1996. Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J. Exp. Med. 184: 945-954.
9. Van Oosten, M. V., P. C. N. Rensen, E. S. Van Amersfoort, M. Van Eck, A. M. Van Dam, J. J. P. Brevé, T. Vogel, A. Panet, T. J. C. Van Berkel, and J. Kuiper. 2001. Apolipoprotein E protects against-bacterial lipopolysaccharide-induced lethality - a new therapeutic approach to treat Gram-negative sepsis. J. Biol. Chem. 276: 8820-8824.
10. Rensen, P. C. N., M. Van Oosten, E. Van de Bilt, M. Van Eck, J. Kuiper, and T. J. C. Van Berkel. 1997. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. J. Clin. Invest. 99: 2438-2445.
11. Laskowitz, D. T., D. M. Lee, D. Schmechel, and H. F. Staats. 2000. Altered immune responses in apolipoprotein E-deficient mice. J. Lipid Res. 41: 613-620.
12. Ali, K., M. Middleton, E. Pure, and D. J. Rader. 2005. Apolipoprotein E suppresses the type I inflammatory response in vivo. Circ. Res. 97: 922-927.
13. Grainger, D. J., J. Reckless, and E. McKilligin. 2004. Apolipoprotein E modulates clearance of apoptotic bodies in vitro and in vivo, resulting in a systemic proinflammatory state in apolipoprotein Edeficient mice. J. Immunol. 173: 6366-6375.
14. van den Elzen, P., S. Garg, L. Leon, M. Brigl, E. A. Leadbetter, J. E. Gumperz, C. C. Dascher, T. Y. Cheng, F. M. Sacks, P. A. Illarionov, et al. 2005. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature. 437: 906-910.
15. Moretti, E. W., R. W. Morris, M. Podgoreanu, D. A. Schwinn, M. F. Newman, E. Bennett, V. G. Moulin, U. U. Mba, and D. T. Laskowitz. 2005. APOE polymorphism is associated with risk of severe sepsis in surgical patients. Crit. Care Med. 33: 2521-2526.
16. Allan, C. M., S. Taylor, and J. M. Taylor. 1997. Two hepatic enhancers, HCR.1 and HCR.2, coordinate the liver expression of the entire human apolipoprotein E/C-I/C-IV/C-II gene cluster. J. Biol. Chem. 272: 29113-29119.
17. Shih, S. J., C. Allan, S. Grehan, E. Tse, C. Moran, and J. M. Taylor. 2000. Duplicated downstream enhancers control expression of the human apolipoprotein E gene in macrophages and adipose tissue. J. Biol. Chem. 275: 31567-31572.
18. Hashimoto, S., T. Suzuki, H. Y. Dong, N. Yamazaki, and K. Matsushima. 1999. Serial analysis of gene expression in human monocytes and macrophages. Blood. 94: 837-844.
19. Zannis, V. I., S. Cole, C. L. Jackson, D. M. Kurnit, and S. K. Karathanasis. 1985. Distribution of apolipoprotein A-I, C-II, C-III, and E mRNA in fetal human tissues. Time-dependent induction of apolipoprotein E mRNA by cultures of human monocytemacrophages. Biochemistry. 24: 4450-4455.
20. Jong, M. C., M. H. Hofker, and L. M. Havekes. 1999. Role of apoCs in lipoprotein metabolism: functional differences between apoC1, apoC2, and apoC3. Arterioscler. Thromb. Vasc. Biol. 19: 472-484.
21. Kraft, H. G., H. J. Menzel, F. Hoppichler, W. Vogel, and G. Utermann. 1989. Changes of genetic apolipoprotein phenotypes caused by liver transplantation: implications for apolipoprotein synthesis. J. Clin. Invest. 83: 137-142.
22. Linton, M. F., J. B. Atkinson, and S. Fazio. 1995. Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science. 267: 1034-1037.
23. Fazio, S., V. R. Babaev, A. B. Murray, A. H. Hasty, K. J. Carter, L. A. Gleaves, J. B. Atkinson, and M. F. Linton. 1997. Increased atherosclerosis in mice reconstituted with apolipoprotein E null macrophages. Proc. Natl. Acad. Sci. USA. 94: 4647-4652.
24. Cheung, M. C., and J. J. Albers. 1984. Characterization of lipoprotein particles isolated by immunoaffinity chromatography. Particles containing A-I and A-II and particles containing A-I but no A-II. J. Biol. Chem. 259: 12201-12209.
25. Jones, C., R. Garuti, P. Michaely, W. P. Li, N. Maeda, J. C. Cohen, J. Herz, and H. H. Hobbs. 2007. Disruption of LDL but not VLDL clearance in autosomal recessive hypercholesterolemia. J. Clin. Invest. 117: 165-174.
26. MacArthur, J. M., J. R. Bishop, K. I. Stanford, L. Wang, A. Bensadoun, J. L. Witztum, and J. D. Esko. 2007. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J. Clin. Invest. 117: 153-164.
27. Arai, T., F. Rinninger, L. Varban, V. Fairchild-Huntress, C. P. Liang, W. Chen, T. Seo, R. Deckelbaum, D. Huszar, and A. R. Tall. 1999. Decreased selective uptake of high density lipoprotein cholesteryl esters in apolipoprotein E knock-out mice. Proc. Natl. Acad. Sci. USA. 96: 12050-12055.
28. Gabay, C., and I. Kushner. 1999. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340: 448-454.
29. Aldred, A. R., and G. Schreiber. 1993. The negative acute phase proteins. In Acute Phase Proteins. A. Mackiewicz, I. Kushner, and H. Baumann, editors. CRC Press, Boca Raton, FL, 21-37.
30. Werb, Z., and J. R. Chin. 1983. Endotoxin suppresses expression of apoprotein E by mouse macrophages in vivo and in culture. J. Biol. Chem. 258: 10642-10648.
31. Hardardottir, I., J. Sipe, A. H. Moser, C. J. Fielding, K. R. Feingold, and C. Grunfeld. 1997. LPS and cytokines regulate extra hepatic mRNA levels of apolipoproteins during the acute phase response in Syrian hamsters. Biochim. Biophys. Acta. 1344: 210-220.
32. Tripp, R. J., A. Tabares, H. Wang, and S. Lanza-Jacoby. 1993. Altered hepatic production of apolipoproteins B and E in the fasted septic rat: factors in the development of hypertriglyceridemia. J. Surg. Res. 55: 465-472.
33. Khovidhunkit, W., M. S. Kim, R. A. Memon, J. K. Shigenaga, A. H. Moser, K. R. Feingold, and C. Grunfeld. 2004. Effects of infection and inflammation on lipid and lipoprotein metabolism mechanisms and consequences to the host. J. Lipid Res. 45: 1169-1196.
34. Kushner, I., and A. Mackiewicz. 1993. The acute phase response: an overview. In Acute Phase Proteins. A. Mackiewicz, I. Kushner, and H. Baumann, editors. CRC Press, Boca Raton, FL, 4-19.
35. Kitchens, R. L., G. Wolfbauer, J. J. Albers, and R. S. Munford. 1999. Plasma lipoproteins promote the release of bacterial lipopolysaccharide from the monocyte cell surface. J. Biol. Chem. 274: 34116-34122.
36. Engelking, L. J., H. Kuriyama, R. E. Hammer, J. D. Horton, M. S. Brown, J. L. Goldstein, and G. Liang. 2004. Overexpression of Insig-1 in the livers of transgenic mice inhibits SREBP processing and reduces insulin-stimulated lipogenesis. J. Clin. Invest. 113: 1168-1175.
37. Westerterp, M., W. de Haan, J. F. P. Berbee, L. M. Havekes, and P. C. N. Rensen. 2006. Endogenous apoC-I increases hyperlipidemia in apoE-knockout mice by stimulating VLDL production and inhibiting LPL. J. Lipid Res. 47: 1203-1211.
38. Kitchens, R. L., P. A. Thompson, R. S. Munford, and G. E. O'Keefe. 2003. Acute inflammation and infection maintain circulating phospholipid levels and enhance lipopolysaccharide binding to plasma lipoproteins. J. Lipid Res. 44: 2339-2348.
39. Liao, W., M. Rudling, and B. Angelin. 1999. Endotoxin suppresses mouse hepatic low-density lipoprotein-receptor expression via a pathway independent of the Toll-like receptor 4. Hepatology. 30: 1252-1256.
40. Netea, M. G., P. N. M. Demacker, B. J. Kullberg, O. C. Boerman, I. Verschueren, A. F. H. Stalenhoef, and J. W. M. van der Meer. 1996. Low-density lipoprotein receptor-deficient mice are protected against lethal endotoxemia and severe Gram-negative infections. J. Clin. Invest. 97: 1366-1372.
41. Barlage, S., D. Fröhlich, A. Böttcher, M. Jauhiainen, H. P. Müller, F. Noetzel, G. Rothe, C. Schütt, R. P. Linke, K. J. Lackner, et al. 2001. ApoE-containing high density lipoproteins and phospholipid transfer protein activity increase in patients with a systemic inflammatory response. J. Lipid Res. 42: 281-290.
42. Knouff, C., O. Briand, S. Lestavel, V. Clavey, M. Altenburg, and N. Maeda. 2004. Defective VLDL metabolism and severe atherosclerosis in mice expressing human apolipoprotein E isoforms but lacking the LDL receptor. Biochim. Biophys. Acta. 1684: 8-17.
43. Corsini, A., M. Mazzotti, A. Villa, F. M. Maggi, F. Bernini, L. Romano, C. Romano, R. Fumagalli, and A. L. Catapano. 1992. Ability of the LDL receptor from several animal species to recognize the human apoB binding domain: studies with LDL from familial defective apoB-100. Atherosclerosis. 93: 95-103.
44. Osono, Y., L. A. Woollett, J. Herz, and J. M. Dietschy. 1995. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J. Clin. Invest. 95: 1124-1132.
45. Böttcher, A., J. Schlosser, F. Kronenberg, H. Dieplinger, G. Knipping, K. J. Lackner, and G. Schmitz. 2000. Preparative free-solution isotachophoresis for separation of human plasma lipoproteins: apolipoprotein and lipid composition of HDL subfractions. J. Lipid Res. 41: 905-915.
46. Feingold, K. R., I. Staprans, R. A. Memon, A. H. Moser, J. K. Shigenaga, W. T. Doerrler, C. A. Dinarello, and C. Grunfeld. 1992. Endotoxin rapidly induces changes in lipid metabolism that produce hypertriglyceridemia: low doses stimulate hepatic triglyceride production while high doses inhibit clearance. J. Lipid Res. 33: 1765-1776.
47. Feingold, K. R., M. Marshall, R. Gulli, A. H. Moser, and C. Grunfeld. 1994. Effect of endotoxin and cytokines on lipoprotein lipase activity in mice. Arterioscler. Thromb. 14: 1866-1872.
48. Rensen, P. C. N., M. C. Jong, L. C. van Vark, H. van der Boom, W. L. Hendriks, T. J. C. Van Berkel, E. A. L. Biessen, and L. M. Havekes. 2000. Apolipoprotein E is resistant to intracellular degradation in vitro and in vivo: evidence for retroendocytosis. J. Biol. Chem. 275: 8564-8571.
49. Lucic, D., Z. H. Huang, D. S. Gu, M. K. Altenburg, N. Maeda, and T. Mazzone. 2007. Regulation of macrophage apoE secretion and sterol efflux by the LDL receptor. J. Lipid Res. 48: 366-372.
50. Liao, W., and C. H. Florén. 1992. Both the polysaccharide and lipid A parts of endotoxins are needed for the inhibitory effects of endotoxins on cellular LDL uptake. Scand. J. Clin. Lab. Invest. 52: 183-188.
51. Horton, J. D., J. C. Cohen, and H. H. Hobbs. 2007. Molecular biology of PCSK9: its role in LDL metabolism. Trends Biochem. Sci. 32: 71-77.