Interaction of vascular smooth muscle cells and monocytes by soluble factors synergistically enhances IL-6 and MCP-1 production

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 296, Issue 4, 2009, Pages

  Chen, Li ^a   Frister, Adrian ^a   Wang, Song ^a   Ludwig, Andreas ^b   Behr, Hagen ^a   Pippig, Susanna ^a   Li, Beibei ^a   Simm, Andreas ^c   Hofmann, Britt ^c   Pilowski, Claudia ^a   Koch, Susanne ^a   Buerke, Michael ^a   Rose John, Stefan ^d   Werdan, Karl ^a   Loppnow, Harald ^a,c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^c MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

Chemokines; Cytokines; Inflammation; Interleukin 6; Lipo polysaccharide; Monocyte chemoattractant protein 1; Monocytes macrophages

Indexed keywords

CD14 ANTIGEN; GLYCOPROTEIN; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATHEROSCLEROSIS; CELL CULTURE; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MONOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ATHEROSCLEROSIS; CELL COMMUNICATION; CELLS, CULTURED; CHEMOKINE CCL2; COCULTURE TECHNIQUES; HUMANS; INTERLEUKIN-1; INTERLEUKIN-6; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; PHOSPHORYLATION; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 66249114365     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01158.2008     Document Type: Article

References (50)

1. Ancuta P, Wang J, Gabuzda D. CD16+ monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1- expressing endothelial cells. J Leukoc Biol 80: 1156-1164, 2006.
2. Bacon K, Gearing A, Camp R. Induction of in vitro human lymphocyte migration by interleukin-3, interleukin-4, and interleukin-6. Cytokine 2: 100-105, 1990.
3. Biswas P, Delfanti F, Bernasconi S, Mengozzi M, Cota M, Polentarutti N, Mantovani A, Lazzarin A, Sozzani S, Poli G. Interleukin-6 induces monocyte chemotactic protein-1 in peripheral blood mononuclear cells and in the U937 cell line. Blood 91: 258-265, 1998.
4. Chalaris A, Rabe B, Paliga K, Lange H, Laskay T, Fielding CA, Jones SA, Rose-John S, Scheller J. Apoptosis is a natural stimulus of IL-6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 110: 1748-1755, 2007.
5. Chomarat P, Banchereau J, Davoust J, Palucka AK. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 1: 510-514, 2000.
6. Dawson TC, Kuziel WA, Osahar TA, Maeda N. Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-defi- cient mice. Atherosclerosis 143: 205-211, 1999.
7. Elhage R, Clamens S, Besnard S, Mallat Z, Tedgui A, Arnal J, Maret A, Bayard F. Involvement of interleukin-6 in atherosclerosis but not in the prevention of fatty streak formation by 17beta-estradiol in apolipoprotein E-deficient mice. Atherosclerosis 156: 315-320, 2001.
8. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 2: 275-281, 1998.
9. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6: 508-519, 2006.
10. Hegde S, Pahne J, Smola-Hess S. Novel immunosuppressive properties of interleukin-6 in dendritic cells: inhibition of NF-κB binding activity and CCR7 expression. FASEB J 18: 1439-1441, 2004.
11. Hojo Y, Ikeda U, Maeda Y, Takahashi M, Takizawa T, Okada M, Funayama H, Shimada K. Interaction between human monocytes and vascular smooth muscle cells induces vascular endothelial growth factor expression. Atherosclerosis 150: 63-70, 2000.
12. Huber SA, Sakkinen P, Conze D, Hardin N, Tracy R. Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler Thromb Vasc Biol 19: 2364-2367, 1999.
13. Ichiki T, Jougasaki M, Setoguchi M, Imamura J, Nakashima H, Mat- suoka T, Sonoda M, Nakamura K, Minagoe S, Tei C. Cardiotrophin-1 stimulates intercellular adhesion molecule-1 and monocyte chemoattractant protein-1 in human aortic endothelial cells. Am J Physiol Heart Circ Physiol 294: H750-H763, 2008.
14. Jostock T, Müllberg J, Özbek S, Atreya R, Blinn G, Voltz N, Fischer M, Neurath MF, Rose-John S. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur J Biochem 268: 160-167, 2001.
15. Keidar S, Heinrich R, Kaplan M, Hayek T, Aviram M. Angiotensin II administration to atherosclerotic mice increases macrophage uptake of oxidized LDL: a possible role for interleukin-6. Arterioscler Thromb Vasc Biol 21: 1464-1469, 2001.
16. Kleemann R, Zadelaar S, Kooistra T. Cytokines and atherosclerosis: a comprehensive review of studies in mice. Cardiovasc Res 79: 360-376, 2008.
17. Klouche M, Bhakdi S, Hemmes M, Rose-John S. Novel path to activation of vascular smooth muscle cells: up-regulation of gp130 creates an autocrine activation loop by IL-6 and its soluble receptor. J Immunol 163: 4583-4589, 1999.
18. Loppnow H, Bil R, Hirt S, Schönbeck U, Herzberg M, Werdan K, Rietschel ET, Brandt E, Flad HD. Platelet-derived interleukin-1 induces cytokine production, but not proliferation of human vascular smooth muscle cells. Blood 91: 134-141, 1998.
19. Loppnow H, Libby P. Adult human vascular endothelial cells express the IL-6 gene differentially in response to LPS or IL-1. Cell Immunol 122: 493-503, 1989.
20. Loppnow H, Libby P. Comparative analysis of cytokine induction in human vascular endothelial and smooth muscle cells. Lymphokine Res 8: 293-299, 1989.
21. Loppnow H, Libby P. Functional significance of human vascular smooth muscle cell-derived interleukin-1 in paracrine and autocrine regulation pathways. Exp Cell Res 198: 283-290, 1992.
22. Loppnow H, Libby P. Proliferating or interleukin-1-activated human vascular smooth muscle cells secrete copious interleukin-6. J Clin Invest 85: 731-738, 1990.
23. Loppnow H, Werdan K, Buerke M. Vascular cells contribute to atherosclerosis by cytokine- and innate-immunity-related inflammatory mechanisms. Innate Immunity 14: 63-87, 2008.
24. Ludwig A, Weber C. Transmembrane chemokines: versatile "special agents" in vascular inflammation. Thromb Haemost 97: 694-703, 2007.
25. Lusis AJ. Atherosclerosis. Nature 407: 233-241, 2000.
26. Madan M, Bishayi B, Hoge M, Amar S. Atheroprotective role of interleukin-6 in diet- and/or pathogen-associated atherosclerosis using an ApoE heterozygote murine model. Atherosclerosis 197: 504 -514, 2008.
27. Morimoto H, Hirose M, Takahashi M, Kawaguchi M, Ise H, Kolat- tukudy PE, Yamada M, Ikeda U. MCP-1 induces cardioprotection against ischaemia/reperfusion injury: role of reactive oxygen species. Cardiovasc Res 78: 554-562, 2008.
28. Müllberg J, Dittrich E, Graeve L, Gerhartz C, Yasukawa K, Taga T, Kishimoto T, Heinrich PC, Rose-John S. Differential shedding of the two subunits of the interleukin-6 receptor. FEBS Lett 332: 174-178, 1993.
29. Müller-Newen G, Kuster A, Hemmann U, Keul R, Horsten U, Martens A, Graeve L, Wijdenes J, Heinrich PC. Soluble IL-6 receptor potentiates the antagonistic activity of soluble gp130 on IL-6 responses. J Immunol 161: 6347-6355, 1998.
30. Müller-Werdan U, Schumann H, Loppnow H, Fuchs R, Darmer D, Stadler J, Holtz J, Werdan K. Endotoxin and tumor necrosis factor-αexert a similar proinflammatory effect in neonatal rat cardiomyocytes, but have different cardiodepressant profiles. J Mol Cell Cardiol 30: 1027-1036, 1998.
31. Nabata T, Morimoto S, Koh E, Shiraishi T, Ogihara T. Interleukin-6 stimulates c-myc expression and proliferation of cultured vascular smooth muscle cells. Biochem Int 20: 445-453, 1990.
32. Parenti A, Bellik L, Brogelli L, Filippi S, Ledda F. Endogenous VEGF-A is responsible for mitogenic effects of MCP-1 on vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 286: H1978 - H1984, 2004.
33. Romano M, Sironi M, Toniatti C, Polentarutti N, Fruscella P, Ghezzi P, Faggioni R, Luini W, van Hinsbergh V, Sozzani S, Bussolino F, Poli V, Ciliberto G, Mantovani A. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6: 315-325, 1997.
34. Rose-John S, Heinrich PC. Soluble receptors for cytokines and growth factors: generation and biological function. Biochem J 300: 281-290, 1994.
35. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 80: 227-236, 2006.
36. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 340: c115-126, 1999.
37. Schieffer B, Selle T, Hilfiker A, Hilfiker-Kleiner D, Grote K, Tietge UJ, Trautwein C, Luchtefeld M, Schmittkamp C, Heeneman S, Dae- men MJ, Drexler H. Impact of interleukin-6 on plaque development and morphology in experimental atherosclerosis. Circulation 110: 3493-3500, 2004.
38. Schonbeck U, Herzberg M, Petersen A, Wohlenberg C, Gerdes J, Flad HD, Loppnow H. Human vascular smooth muscle cells express interleu- kin-1β-converting enzyme (ICE), but inhibit processing of the interleu- kin-1β precursor by ICE. J Exp Med 185: 1287-1294, 1997.
39. Schroers A, Hecht O, Kallen KJ, Pachta M, Rose-John S, Grötzinger J. Dynamics of the gp130 cytokine complex: a model for assembly on the cellular membrane. Protein Sci 14: 783-790, 2005.
40. Selzman CH, Miller SA, Zimmerman MA, Gamboni-Robertson F, Harken AH, Banerjee A. Monocyte chemotactic protein-1 directly induces human vascular smooth muscle proliferation. Am J Physiol Heart Circ Physiol 283: H1455-H1461, 2002.
41. Sun J, Sukhova GK, Wolters PJ, Yang M, Kitamoto S, Libby P, Macfarlane LA, Clair JM, Shi GP. Mast cells promote atherosclerosis by releasing proinflammatory cytokines. Nat Med 13: 719-724, 2007.
42. Takahashi M, Suzuki E, Takeda R, Oba S, Nishimatsu H, Kimura K, Nagano T, Nagai R, Hirata Y. Angiotensin II and tumor necrosis factor-αsynergistically promote monocyte chemoattractant protein-1 expression: roles of NF-κB, p38, and reactive oxygen species. Am J Physiol Heart Circ Physiol 294: H2879-H2888, 2008.
43. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86: 515-581, 2006.
44. 2-terminal amino acid sequence of a T-cell derived lymphokine with growth factor activity for B-cell hybridomas. Proc Natl Acad Sci USA 83: 9679-9683, 1986.
45. von Patay B, Loppnow H, Feindt J, Kurz B, Mentlein R. Cat- echolamines and lipopolysaccharide synergistically induce the release of interleukin-6 from thymic epithelial cells. J Neuroimmunol 86: 182-189, 1997.
46. Wang Z, Newman WH. Smooth muscle cell migration stimulated by interleukin-6 is associated with cytoskeletal reorganization. J Surg Res 111: 261-266, 2003.
47. Warner SJC, Libby P. Human vascular smooth muscle cells: target for and source of tumor necrosis factor. J Immunol 142: 100-109, 1989.
48. Watanabe S, Mu W, Kahn A, Jing N, Li JH, Lan HY, Nakagawa T, Ohashi R, Johnson RJ. Role of JAK/STAT pathway in IL-6-induced activation of vascular smooth muscle cells. Am J Nephrol 24: 387-392, 2004.
49. Westphal E, Chen L, Pilowski C, Koch K, Ebelt H, MUller-Werdan U, Werdan K, Loppnow H. Endotoxin-activated cultured neonatal rat cardiomyocytes express functional surface-associated interleukin-1α. J Endotoxin Res 13: 25-34, 2007.
50. Yu X, Dluz S, Graves DT, Zhang L, Antoniades HN, Hollander W, Prusty S, Valente AJ, Schwartz CJ, Sonenshein GE. Elevated expression of monocyte chemoattractant protein-1 by vascular smooth muscle cells in hypercholesterolemic primates. Proc Natl Acad Sci USA 89: 6953-6957, 1992.