Atherosclerosis
Volume 194, Issue 1 , Pages 125-133 , September 2007

Angiotensin II induces IL-6 expression and the Jak-STAT3 pathway in aortic adventitia of LDL receptor-deficient mice

  • Adrian Recinos III

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
    • Corresponding Author InformationCorresponding author at: Division of Endocrinology, MRB 8.138, University of Texas Medical Branch, Galveston, 301 University Blvd., Galveston, TX 77555-1060, USA. Tel.: +1 409 772 2824; fax: +1 409 772 8709.
  • ,
  • Wanda S. LeJeune

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Hong Sun

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Chang Y. Lee

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Brian C. Tieu

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Muping Lu

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Tieying Hou

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Istvan Boldogh

      Affiliations

    • Department Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Ronald G. Tilton

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
    • Stark Diabetes Center, University of Texas Medical Branch, Galveston, TX 77555, USA
  • ,
  • Allan R. Brasier

      Affiliations

    • Department of Medicine, University of Texas Medical Branch, Galveston, TX 77555, USA
    • Sealy Center for Molecular Science, University of Texas Medical Branch, Galveston, TX 77555, USA

Received 10 March 2006 ,Revised 25 September 2006 ,Accepted 6 October 2006.

References 

  1. Daugherty A, Cassis L. Angiotensin II-mediated development of vascular diseases. Trends Cardiovasc Med. 2004;14:117–120
  2. Kon V, Jabs K. Angiotensin in atherosclerosis. Curr Opin Nephrol Hypertens. 2004;13:291–297
  3. Brasier AR, Recinos A, Eledrisi MS. Vascular inflammation and the renin-angiotensin system. Arterioscler Thromb Vasc Biol. 2002;22:1257–1266
  4. Brasier AR, Jamaluddin M, Han Y, Patterson C, Runge MS. Angiotensin II induces gene transcription through cell-type-dependent effects on the nuclear factor-kappaB (NF-kappaB) transcription factor. Mol Cell Biochem. 2000;212:155–169
  5. Murphy TJ, Alexander RW, Griendling KK, Runge MS, Bernstein KE. Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature. 1991;351:233–236
  6. Griendling KK, Ushio-Fukai M, Lassegue B, Alexander RW. Angiotensin II signaling in vascular smooth muscle. Hypertension. 1997;29:366–373
  7. Morawietz H, Rueckschloss U, Niemann B, et al. Angiotensin II induces LOX, the human endothelial receptor of oxidized low-density lipoprotein. Circulation. 1999;100:899–902
  8. Harrison D, Griendling KK, Landmesser U, Alexander RW. Role of oxidative stress in atherosclerosis. Am J Cardiol. 2003;91:7A–11A
  9. Bursill CA, Channon KM, Greaves DR. The role of chemokines in atherosclerosis: recent evidence from experimental models and population genetics. Curr Opin Lipidol. 2004;15:145–149
  10. Sheikine Y, Hansson GK. Chemokines and atherosclerosis. Ann Med. 2004;36:98–118
  11. Boyle JJ. Macrophage activation in atherosclerosis: pathogenesis and pharmacology of plaque rupture. Curr Vasc Pharmacol. 2005;3:63–68
  12. Pueyo ME, Gonzalez W, Nicoletti A, et al. Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via NF-kB activation induced by intracellular oxidative stress. Arterioscler Thromb Vasc Biol. 2000;20:645–651
  13. Hedin U, Roy J, Tran PK. Control of smooth muscle cell proliferation in vascular disease. Curr Opin Lipidol. 2004;15:559–565
  14. Cheng ZJ, Vapaatalo H, Mervaala E. Angiotensin II and vascular inflammation. Med Sci Monit. 2005;11:RA194–RA205
  15. Springer T. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multiple paradigm. Cell. 1994;76:301
  16. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605–1612
  17. Weiss D, Kools JJ, Taylor WR. Angiotensin II-induced hypertension accelerates the development of atherosclerosis in apoE-deficient mice. Circulation. 2001;103:448–454
  18. Breslow JL. Mouse models of atherosclerosis. Science. 1996;272:685–688
  19. Recinos A, Carr BK, Bartos DB, et al. Liver gene expression associated with diet and lesion development in atherosclerosis-prone mice: induction of components of alternative complement pathway. Physiol Genomics. 2004;19:131–142
  20. Bush E, Maeda N, Kuziel WA, et al. CC chemokine receptor 2 is required for macrophage infiltration and vascular hypertrophy in angiotensin II-induced hypertension. Hypertension. 2000;36:360–363
  21. Ni WH, Kitamoto S, Ishibashi M, et al. Monocyte chemoattractant protein-1 is an essential inflammatory mediator in angiotensin II-induced progression of established atherosclerosis in hypercholesterolemic mice. Arterioscler Thrombosis Vasc Biol. 2004;24:534–539
  22. Bruemmer D, Collins AR, Noh G, et al. Angiotensin II-accelerated atherosclerosis and aneurysm formation is attenuated in osteopontin-deficient mice. J Clin Invest. 2003;112:1318–1331
  23. Sherman CT, Brasier AR. Role of signal transducers and activators of transcription-1 and -3 in inducible regulation of the human angiotensinogen gene by interleukin-6. Mol Endocrinol. 2001;15:441–457
  24. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994;14:133–140
  25. Wang YX, Martin-McNulty B, Freay AD, et al. Angiotensin II increases urokinase-type plasminogen activator expression and induces aneurysm in the abdominal aorta of apolipoprotein E-deficient mice. Am J Pathol. 2001;159:1455–1464
  26. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987;68:231–240
  27. Tangirala RK, Rubin EM, Palinski W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res. 1995;36:2320–2328
  28. Geisterfer AA, Peach MJ, Owens GK. Angiotensin II induces hypertrophy, not hyperplasia, of cultured rat aortic smooth muscle cells. Circ Res. 1988;62:749–756
  29. Zhang Y, Griendling KK, Dikalova A, Owens GK, Taylor WR. Vascular hypertrophy in angiotensin II-induced hypertension is mediated by vascular smooth muscle cell-derived H2O2. Hypertension. 2005;46:732–737
  30. Sartore S, Chiavegato A, Faggin E, et al. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling—from innocent bystander to active participant. Circ Res. 2001;89:1111–1121
  31. Austyn JM, Gordon S. F4/80, a monoclonal antibody directed specifically against mouse macrophage. Eur J Immunol. 1981;11:805–815
  32. Han Y, Runge MS, Brasier AR. Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. Circ Res. 1999;84:695–703
  33. Loppnow H, Libby P. Proliferating or interleukin 1-activated human vascular smooth muscle cells secrete copious interleukin 6. J Clin Invest. 1990;85:731–738
  34. Schieffer B, Schieffer E, Hilfiker-Kleiner D, et al. Expression of angiotensin II and interleukin 6 in human coronary atherosclerotic plaques: potential implications for inflammation and plaque instability. Circulation. 2000;101:1372–1378
  35. Powell DW, Mifflin RC, Valentich JD, et al. Paracrine cells important in health and disease. Am J Physiol. 1999;277:C1–C9
  36. Dongari-Bagtzoglou AI, Ebersole JL. Increased presence of interleukin-6 (IL-6) and IL-8 secreting fibroblast subpopulations in adult periodontitis. J Periodontol. 1998;69:899–910
  37. Yang XP, Irani K, Mattagajasingh S, et al. Signal transducer and activator of transcription 3alpha and specificity protein 1 interact to upregulate intercellular adhesion molecule-1 in ischemic-reperfused myocardium and vascular endothelium. Arterioscler Thromb Vasc Biol. 2005;25:1395–1400
  38. Watanabe S, Mu W, Kahn A, et al. Role of JAK/STAT pathway in IL-6-induced activation of vascular smooth muscle cells. Am J Nephrol. 2004;24:387–392
  39. Dauer DJ, Ferraro B, Song LX, et al. Stat3 regulates genes common to both wound healing and cancer. Oncogene. 2005;24:3397–3408
  40. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res. 1999;250:273–283
  41. Weber KT, Sun Y, Katwa LC. Myofibroblasts and local angiotensin II in rat cardiac tissue repair. Int J Biochem Cell Biol. 1997;29:31–42
  42. Sugiyama S, Okada Y, Sukhova GK, et al. Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes. Am J Pathol. 2001;158:879–891

PII: S0021-9150(06)00610-1

doi: 10.1016/j.atherosclerosis.2006.10.013

Atherosclerosis
Volume 194, Issue 1 , Pages 125-133 , September 2007