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01-08-2012

Lipopolysaccharide-Induced Proliferation of the Vasa Vasorum in a Rabbit Model of Atherosclerosis as Evaluated by Contrast-Enhanced Ultrasound Imaging and Histology

Authors: Jinwei Tian, Sining Hu, Xue Han, Nana Dong, Huai Yu, Yanli Sun, Bo Yu

Published in: Inflammation | Issue 4/2012

Abstract

Whether lipopolysaccharide (LPS) can promote vasa vasorum (VV) proliferation for atherosclerosis in vivo is unclear. Eighteen rabbits with atherosclerosis were randomly assigned into one of three groups of six. Group A received biweekly injections of 10 mL saline after 2 weeks of balloon injury. Groups B and C received biweekly intravenous injections of 3.0 μg LPS in 10 mL saline at weeks 10 and 4, respectively, until study termination. LPS significantly increased the levels of triglycerides and C-reactive protein and decreased the level of high-density lipoprotein cholesterol. Group C had significant larger plaques and more macrophages than group A (p = 0.01 and p < 0.001, respectively). Contrast enhancement ultrasound imaging and histological detection demonstrated that plaques in group C had a significantly higher VV density than that in group A (p = 0.009 and p = 0.002, respectively). In summary, VV proliferation for plaque destabilization can be accelerated by LPS-induced systemic inflammation and changes in lipid profiles.

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Raetz, C.R., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annual Review of Biochemistry 71: 635–700.PubMedCrossRef

Wiedermann, C.J., S. Kiechl, S. Dunzendorfer, P. Schratzberger, G. Egger, F. Oberhollenzer, and J. Willeit. 1999. Association of endotoxemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck study. Journal of the American College of Cardiology 34: 1975–1981.PubMedCrossRef

Lehr, H.A., T.A. Sagban, C. Ihling, U. Zahringer, K.D. Hungerer, M. Blumrich, K. Reifenberg, and S. Bhakdi. 2001. Immunopathogenesis of atherosclerosis: endotoxin accelerates atherosclerosis in rabbits on hypercholesterolemic diet. Circulation 104: 914–920.PubMedCrossRef

Engelmann, M.G., C.V. Redl, and S. Nikol. 2004. Recurrent perivascular inflammation induced by lipopolysaccharide (endotoxin) results in the formation of atheromatous lesions in vivo. Laboratory Investigation 84: 425–432.PubMedCrossRef

Kim, S.J., J.H. Park, K.H. Kim, W.R. Lee, S. Lee, O.C. Kwon, K.S. Kim, and K.K. Park. 2010. Effect of NF-κB decoy oligodeoxynucleotide on LPS/high-fat diet-induced atherosclerosis in an animal model. Basic & Clinical Pharmacology & Toxicology 107: 925–930.CrossRef

Sluimer, J.C., F.D. Kolodgie, A.P. Bijnens, K. Maxfield, E. Pacheco, B. Kutys, H. Duimel, P.M. Frederik, V.W. van Hinsbergh, R. Virmani, and M.J. Daemen. 2009. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. Journal of the American College of Cardiology 53: 1517–1527.PubMedCrossRef

Koo, T.H., H.O. Jun, S.K. Bae, S.R. Kim, C.P. Moon, S.K. Jeong, W.S. Kim, G.C. Kim, H.O. Jang, I. Yun, K.W. Kim, and M.K. Bae. 2007. Porphyromonas gingivalis, periodontal pathogen, lipopolysaccharide induces angiogenesis via extracellular signal-regulated kinase 1/2 activation in human vascular endothelial cells. Archives of Pharmacal Research 30: 34–42.PubMedCrossRef

Staub, D., M.B. Patel, A. Tibrewala, D. Ludden, M. Johnson, P. Espinosa, B. Coll, K.A. Jaeger, and S.B. Feinstein. 2010. Vasa vasorum and plaque neovascularization on contrast-enhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events. Stroke 41: 41–47.PubMedCrossRef

Moguillansky, D., X. Leng, A. Carson, L. Lavery, A. Schwartz, X. Chen, and F.S. Villanueva. 2011. Quantification of plaque neovascularization using contrast ultrasound: a histologic validation. European Heart Journal 32: 646–653.PubMedCrossRef

10.

Meng, L., B. Lv, S. Zhang, and B. Yv. 2008. in vivo optical coherence tomography of experimental thrombosis in a rabbit carotid model. Heart 94: 777–780.PubMedCrossRef

11.

Mattsby-Baltzer, I., A. Jakobsson, J. Sorbo, and K. Norrby. 1994. Endotoxin is angiogenic. International Journal of Experimental Pathology 75: 191–196.PubMed

12.

Harmey, J.H., C.D. Bucana, W. Lu, A.M. Byrne, S. McDonnell, C. Lynch, D. Bouchier-Hayes, and Z. Dong. 2002. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. International Journal of Cancer 101: 415–422.CrossRef

13.

Kolodgie, F.D., H.K. Gold, A.P. Burke, D.R. Fowler, H.S. Kruth, D.K. Weber, A. Farb, L.J. Guerrero, M. Hayase, R. Kutys, J. Narula, A.V. Finn, and R. Virmani. 2003. Intraplaque hemorrhage and progression of coronary atheroma. The New England Journal of Medicine 349: 2316–2325.PubMedCrossRef

14.

Leibovich, S.J., J.F. Chen, G. Pinhal-Enfield, P.C. Belem, G. Elson, A. Rosania, M. Ramanathan, C. Montesinos, M. Jacobson, M.A. Schwarzschild, J.S. Fink, and B. Cronstein. 2002. Synergistic up-regulation of vascular endothelial growth factor expression in murine macrophages by adenosine A (2A) receptor agonists and endotoxin. American Journal of Pathology 160: 2231–2244.PubMedCrossRef

15.

Ramanathan, M., G. Pinhal-Enfield, I. Hao, and S.J. Leibovich. 2007. Synergistic up-regulation of vascular endothelial growth factor (VEGF) expression in macrophages by adenosine A2A receptor agonists and endotoxin involves transcriptional regulation via the hypoxia response element in the VEGF promoter. Molecular Biology of the Cell 18: 14–23.PubMedCrossRef

16.

Kiriakidis, S., E. Andreakos, C. Monaco, B. Foxwell, M. Feldmann, and E. Paleolog. 2003. VEGF expression in human macrophages is NF-kappaB-dependent: studies using adenoviruses expressing the endogenous NF-kappaB inhibitor IkappaBalpha and a kinase-defective form of the IkappaB kinase 2. Journal of Cell Science 116: 665–674.PubMedCrossRef

17.

Ramanathan, M., A. Giladi, and S.J. Leibovich. 2003. Regulation of vascular endothelial growth factor gene expression in murine macrophages by nitric oxide and hypoxia. Experimental Biology and Medicine (Maywood) 228: 697–705.

18.

Shi, Q., L.A. Cox, J. Glenn, M.E. Tejero, V. Hondara, J.L. Vandeberg, and X.L. Wang. 2010. Molecular pathways mediating differential responses to lipopolysaccharide between human and baboon arterial endothelial cells. Clinical and Experimental Pharmacology and Physiology 37: 178–184.PubMedCrossRef

19.

Liu, H.T., W.M. Li, X.Y. Li, Q.S. Xu, Q.S. Liu, X.F. Bai, C. Yu, and Y.G. Du. 2010. Chitosan oligosaccharides inhibit the expression of interleukin-6 in lipopolysaccharide-induced human umbilical vein endothelial cells through p38 and ERK1/2 protein kinases. Basic & Clinical Pharmacology & Toxicology 106: 362–371.

20.

Lin, C.M., H. Chang, Y.H. Chen, S.Y. Li, I.H. Wu, and J.H. Chiu. 2006. Protective role of wogonin against lipopolysaccharide-induced angiogenesis via VEGFR-2, not VEGFR-1. International Immunopharmacology 6: 1690–1698.PubMedCrossRef

21.

Lin, C.M., H. Chang, S.Y. Li, I.H. Wu, and J.H. Chiu. 2006. Chrysin inhibits lipopolysaccharide-induced angiogenesis via down-regulation of VEGF/VEGFR-2(KDR) and IL-6/IL-6R pathways. Planta Medica 72: 708–714.PubMedCrossRef

22.

Chen, Y., N. Lu, Y. Ling, Y. Gao, L. Wang, Y. Sun, Q. Qi, F. Feng, W. Liu, Q. You, and Q. Guo. 2009. Wogonoside inhibits lipopolysaccharide-induced angiogenesis in vitro and in vivo via toll-like receptor 4 signal transduction. Toxicology 259: 10–17.PubMedCrossRef

23.

Li, H., M.W. Freeman, and P. Libby. 1995. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. Journal of Clinical Investigation 95: 122–133.PubMedCrossRef

24.

Ostos, M.A., D. Recalde, M.M. Zakin, and D. Scott-Algara. 2002. Implication of natural killer T cells in atherosclerosis development during a LPS-induced chronic inflammation. FEBS Letters 519: 23–29.PubMedCrossRef

25.

Westerterp, M., J.F. Berbee, N.M. Pires, G.J. van Mierlo, R. Kleemann, J.A. Romijn, L.M. Havekes, and P.C. Rensen. 2007. Apolipoprotein C-I is crucially involved in lipopolysaccharide-induced atherosclerosis development in apolipoprotein E-knockout mice. Circulation 116: 2173–2181.PubMedCrossRef

26.

Lin, F.Y., Y.H. Chen, Y.W. Lin, J.S. Tsai, J.W. Chen, H.J. Wang, Y.L. Chen, C.Y. Li, and S.J. Lin. 2006. The role of human antigen R, an RNA-binding protein, in mediating the stabilization of toll-like receptor 4 mRNA induced by endotoxin: a novel mechanism involved in vascular inflammation. Arteriosclerosis, Thrombosis, and Vascular Biology 26: 2622–2629.PubMedCrossRef

27.

Feng, X., Y. Zhang, R. Xu, X. Xie, L. Tao, H. Gao, Y. Gao, Z. He, and H. Wang. 2010. Lipopolysaccharide up-regulates the expression of Fcalpha/mu receptor and promotes the binding of oxidized low-density lipoprotein and its IgM antibody complex to activated human macrophages. Atherosclerosis 208: 396–405.PubMedCrossRef

28.

Goteiner, D., R.G. Craig, R. Ashmen, M.N. Janal, B. Eskin, and N. Lehrman. 2008. Endotoxin levels are associated with high-density lipoprotein, triglycerides, and troponin in patients with acute coronary syndrome and angina: possible contributions from periodontal sources. Journal of Periodontology 79: 2331–2339.PubMedCrossRef

29.

Cue, J.I., J.T. DiPiro, L.J. Brunner, J.E. Doran, M.E. Blankenship, A.R. Mansberger, and M.L. Hawkins. 1994. Reconstituted high density lipoprotein inhibits physiologic and tumor necrosis factor alpha responses to lipopolysaccharide in rabbits. Archives of Surgery 129: 193–197.PubMedCrossRef

30.

Skyba, D.M., A.R. Jayaweera, N.C. Goodman, S. Ismail, G. Camarano, and S. Kaul. 1994. Quantification of myocardial perfusion with myocardial contrast echocardiography during left atrial injection of contrast. Implications for venous injection. Circulation 90: 1513–1521.PubMedCrossRef

31.

Staub, D., A.F. Schinkel, B. Coll, S. Coli, A.F. van der Steen, J.D. Reed, C. Krueger, K.E. Thomenius, D. Adam, E.J. Sijbrands, F.J. ten Cate, and S.B. Feinstein. 2010. Contrast-enhanced ultrasound imaging of the vasa vasorum: from early atherosclerosis to the identification of unstable plaques. JACC. Cardiovascular Imaging 3: 761–771.PubMedCrossRef

32.

Feinstein, S.B. 2006. Contrast ultrasound imaging of the carotid artery vasa vasorum and atherosclerotic plaque neovascularization. Journal of the American College of Cardiology 48: 236–243.PubMedCrossRef

Title: Lipopolysaccharide-Induced Proliferation of the Vasa Vasorum in a Rabbit Model of Atherosclerosis as Evaluated by Contrast-Enhanced Ultrasound Imaging and Histology
Authors: Jinwei Tian
Sining Hu
Xue Han
Nana Dong
Huai Yu
Yanli Sun
Bo Yu
Publication date: 01-08-2012
Publisher: Springer US
Published in: Inflammation / Issue 4/2012
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI: https://doi.org/10.1007/s10753-012-9468-z

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