Skip to main content
PMC home page
Indian Journal of Clinical Biochemistry logoLink to Indian Journal of Clinical Biochemistry
. 2009 Jul 9;24(2):179–183. doi: 10.1007/s12291-009-0032-z

Escherichia coli lipopolysaccharide administration alters antioxidant profile during hypercholesterolemia

Kallol Dutta 1, Biswadev Bishayi 1,2,✉
PMCID: PMC3453217  PMID: 23105829

Abstract

Pathogens, especially Gram-negative bacteria or bacterial endotoxin, along with other classical factors, may be involved in inflammatory response within the aortic endothelium during the progression of cardiovascular disease. Studies have shown that bacterial endotoxin activates various inflammatory processes in the body. Our study aims to establish a correlation between endotoxemia and vascular expression of antioxidant enzymes. Swiss albino mice (4 weeks old) were fed a high fat diet for 24 weeks and then were administered Escherichia coli endotoxin intraperitonealy, for 4 weeks. Tissue antioxidant enzymes, serum levels of IL-6 and TNF alpha were measured from the mice. We report that i.p. administration of endotoxin to hyperlipidemic mice resulted in elevation of superoxide dismutase and catalase enzymes, which was paralleled by a systemic reduction of serum cholesterol and LDL expression. Myeloperoxidase levels were also found to be elevated in aortic tissue, while an increase was also observed in the serum cytokine levels.

Key Words: Endotoxin, Hyperlipidemia, Aortic inflammation, Antioxidant enzymes

Full Text

The Full Text of this article is available as a PDF (61.8 KB).

References

  • 1.Stoll L.L., Denning G.M., Weintraub N.L. Potential role of endotoxin as a proinflammatory mediator of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2227–2236. doi: 10.1161/01.ATV.0000147534.69062.dc. [DOI] [PubMed] [Google Scholar]
  • 2.Paik H.D., Park J.S., Park E. Effects of Bacillus polyfermenticus SCD on lipid and antioxidant metabolism in rats fed a high fat and high cholesterol diet. Biol Pharm Bull. 2005;28:1270–1274. doi: 10.1248/bpb.28.1270. [DOI] [PubMed] [Google Scholar]
  • 3.Kerttuala Y., Vaara M., Pyhala L., Sariola H., Kostiainen E., Huttunen J.K. Effect of bacterial lipopolysaccharide on serum lipids and on the development of aortic atherosclerosis in rabbits. Atherosclerosis. 1986;59:307–312. doi: 10.1016/0021-9150(86)90126-7. [DOI] [PubMed] [Google Scholar]
  • 4.Yla-Herttluala S., Pesonen E., Kaprio E., Rapola J., Soveri T., Viikari J., Savilahti E., et al. Effect of repeated endotoxin treatment and hypercholesterolemia on preatherosclerotic lesions in weaned pigs. II. Lipid and glycosaminoglycan analysis of intima and inner media. Atherosclerosis. 1988;72:173–181. doi: 10.1016/0021-9150(88)90078-0. [DOI] [PubMed] [Google Scholar]
  • 5.Lehr H.A., Sagban T.A., Ihling C., Zähringer U., Hungerer K.D., Blumrich M., Reifenberg K., Bhakdi S. Immunopathogenesis of atherosclerosis: endotoxin accelerates atherosclerosis in rabbits on hypercholesterolemic diet. Circulation. 2001;104:914–920. doi: 10.1161/hc3401.093153. [DOI] [PubMed] [Google Scholar]
  • 6.Oosten V.M., Rensen P.C.N., Amersfoort E.S., Eck M., Van D., Brevé J.J.P., Vogel T., et al. Apolipoprotein E protects against bacterial LPS induced lethality. A new therapeutic approach to treat Gram-negative sepsis. J Biol Chem. 2001;276:8820–8824. doi: 10.1074/jbc.M009915200. [DOI] [PubMed] [Google Scholar]
  • 7.Wang F., Wang L.Y., Wright D., Parmely M.J. Redox imbalance differentially inhibits LPS induced macrophage activation in the mouse liver. Infect Immune. 1999;67:5409–5416. doi: 10.1128/iai.67.10.5409-5416.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Patel R.P., Moelering D., Murphy-Ullrich J., Jo H., Beckman J.S., Darley-Usmar V.M. Cell signaling by reactive nitrogen and oxygen species in atherosclerosis. Free Radical Biol Med. 2000;28:1780–1794. doi: 10.1016/S0891-5849(00)00235-5. [DOI] [PubMed] [Google Scholar]
  • 9.Cynshi O., Kawabe Y., Suzuki T., Takashima Y., Kaise H. Anti-atherogenic effects of the anti-oxidant BO-653 in three different animal models. Proc Natl Acad Sci. 1998;95:10123–10128. doi: 10.1073/pnas.95.17.10123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Devi G.S., Prasad M.H., Saraswati I., Raghu D. Free radicals and anti-oxidant enzymes and lipid peroxidations in different types of leukemias. Clin Chim Acta. 2000;293:53–62. doi: 10.1016/S0009-8981(99)00222-3. [DOI] [PubMed] [Google Scholar]
  • 11.Fukai T., Galis Z.S., Meng X., Parthasarathy S., Harrison D.G. Vascular expression of extracellular superoxide dismutase in atherosclerosis. J Clin Invest. 1998;101:2101–2111. doi: 10.1172/JCI2105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Wissler R.W. Theories and new horizons in the pathogenesis of atherosclerosis and the mechanisms of clinical effects. Arch Pathol Lab Med. 1992;116:1281–1291. [PubMed] [Google Scholar]
  • 13.Wassman S., Wassmann K., Nickenig G. Modulation of oxidant enzyme expression in vascular cells. Hypertension. 2004;44:381–386. doi: 10.1161/01.HYP.0000142232.29764.a7. [DOI] [PubMed] [Google Scholar]
  • 14.Blankenbug S., Rupprecht H.J., Bickel C., Torzewski M., Hafner G., Tiret L., Smieja M., et al. Glutathione peroxidase 1 activity and cardiovascular events in patients with coronary artery disease. N Eng J Med. 2003;349:1605–1613. doi: 10.1056/NEJMoa030535. [DOI] [PubMed] [Google Scholar]
  • 15.Brennan M.L., Penn M.S., Lente F., Nambi V., Shishehbor M.H., Aviles R.J. Prognostic value of myeloperoxidase in patients with chest pain. N Eng J Med. 2003;349:1595–1604. doi: 10.1056/NEJMoa035003. [DOI] [PubMed] [Google Scholar]
  • 16.Leopold J.A., Loscalzo J. Oxidative enzymopathies and vascular disease. Ath Thromb Vasc Biol. 2005;25:1332–1340. doi: 10.1161/01.ATV.0000163846.51473.09. [DOI] [PubMed] [Google Scholar]
  • 17.Guo Z.M., Remman H.V., Yang H., Chen X.L., Mele J., Vijg J., Epstein C.J., et al. Changes in expression of antioxidant enzymes affect cell-mediated LDL oxidation and oxidized LDL induced apoptosis in mouse aortic cells. Ath Thromb Vasc Biol. 2001;21:1131–1138. doi: 10.1161/hq0701.092092. [DOI] [PubMed] [Google Scholar]
  • 18.Mates J.M., Jimenez F.S. Anti-oxidant enzymes and their implication in pathophysiologic processes. Frontiers in Biosciences. 1999;4:339–345. doi: 10.2741/Mates. [DOI] [PubMed] [Google Scholar]
  • 19.Plump A.S., Smith J.D., Hayek T., Aalto-Setala K., Walsh A., Verstuyft J.G., Rubin E.M., Breslow J.L. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343–353. doi: 10.1016/0092-8674(92)90362-G. [DOI] [PubMed] [Google Scholar]
  • 20.Ogata M., Yoshida S., Kamochi M., Shigematsu A., Mizuguchi A. Enhancement of lipopolysaccharide-induced tumor necrosis factor production in mice by carrageenan pretreatment. Infect Immun. 1991;59:679–683. doi: 10.1128/iai.59.2.679-683.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Burtis C.A., Ashwood E.R., Bruns D.E., editors. Tietz textbook of clinical chemistry and molecular diagnostics. St. Louis, MO: Elsevier Saunders; 2006. p. 485. [Google Scholar]
  • 22.Aebi H. Methods in Enzymology, Volume 105. NY: Academic press; 1984. Catalase in vitro; p. 121. [DOI] [PubMed] [Google Scholar]
  • 23.Lee J.S., Bok S.H., Park Y.B., Lee M.K., Choi M.S. 4-hydroxycinnamate lowers plasma and hepatic lipids without changing anti-oxidant enzyme activities. Ann Nutr Metab. 2003;47:144–151. doi: 10.1159/000070037. [DOI] [PubMed] [Google Scholar]
  • 24.Benoit M., Frenette J., Cote C.H. Lengthening contractioninduced inflammation is linked to secondary damage but devoid of neutrophil invasion. J Appl Physiol. 2002;92:1995–2004. doi: 10.1063/1.1494845. [DOI] [PubMed] [Google Scholar]
  • 25.Bradford M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;7:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  • 26.Soop M., Duxbury H., Agwunobi A.O., Gibson J.M., Hopkins S.J., Childs C., Cooper R.G., et al. Euglycemic hyperinsulinemia augments the cytokine and endocrine responses to endotoxins in humans. Am J Physiol Endocrinol Metab. 2002;282:E1276–E1285. doi: 10.1152/ajpendo.00535.2001. [DOI] [PubMed] [Google Scholar]
  • 27.Lyke K.E., Burges R., Cissoko Y., Sangare M., Dao I., Diarra A., Kone R., et al. Serum Levels of the Proinflammatory Cytokines Interleukin-1 Beta (IL-1), IL-6, IL-8, IL-10, Tumor Necrosis Factor Alpha, and IL-12 (p70) in Malian Children with Severe Plasmodium falciparum Malaria and Matched Uncomplicated Malaria or Healthy Controls. Infect Immun. 2004;72:5630–5637. doi: 10.1128/IAI.72.10.5630-5637.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Steinberg D., Witzurn J.L. Is the oxidative modification hypothesis relevant to human atherosclerosis? Do the antioxidant trials conducted till date refutes the hypothesis? Circulation. 2002;105:2107–2111. doi: 10.1161/01.CIR.0000014762.06201.06. [DOI] [PubMed] [Google Scholar]
  • 29.Wang H.H., Hung T.M., Wei J., Chiang A.N. Fish oil increases anti-oxidant enzyme activities in macrophages and reduces atherosclerotic lesion in apo E knock out mice. Cardiovascular Res. 2004;61:169–176. doi: 10.1016/j.cardiores.2003.11.002. [DOI] [PubMed] [Google Scholar]
  • 30.Parmely M.J., Wang F., Wright D. Gamma interferon prevents inhibitory effects of oxidative stress on host responses to E.coli infection. Infect immune. 2001;64:2621–2629. doi: 10.1128/IAI.69.4.2621-2629.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Zamora Z.B., Borrego A., Lopez O.Y., Delgado R., Gonzalez R., Menendez S., Frank Hernandez F., Schulz S. Effects of ozone oxidative preconditioning on TNF-α release and antioxidant-prooxidant intracellular balance in mice during endotoxic shock. Mediators of Inflam. 2005;1:16–22. doi: 10.1155/MI.2005.16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Ferns G.A.A., Lamb D.J. What does lipoprotein oxidation phenomenon mean? Biochem Soc Transac. 2004;32:160–163. doi: 10.1042/BST0320160. [DOI] [PubMed] [Google Scholar]
  • 33.Garlund B., Sjolin J., Nilsson A., Roll M., Wickerts C., Wertlind B. Plasma levels of cytokines in primary septic shock in humans: correlation with disease severity. J Infect Dis. 1995;172:296–301. doi: 10.1093/infdis/172.1.296. [DOI] [PubMed] [Google Scholar]

Articles from Indian Journal of Clinical Biochemistry are provided here courtesy of Springer

RESOURCES