Mast cells in vulnerable coronary plaques: Potential mechanisms linking mast cell activation to plaque erosion and rupture

Current Opinion in Lipidology

Volumn 15, Issue 5, 2004, Pages 567-573

  Lindstedt, Ken A ^a   Kovanen, Petri T ^a  

^a WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

Apoptosis; Atherosclerosis; Endothelium; Erosion; Mast cell; Pericellular matrix; Plaque rupture; Proteases; Smooth muscle cell

Indexed keywords

CHEMOTACTIC FACTOR; CHYMASE; COLLAGEN; CYTOKINE; FIBRONECTIN; GROWTH FACTOR; HEPARIN; HISTAMINE; METALLOPROTEINASE; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA; TRYPTASE; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTERY ENDOTHELIUM; ATHEROSCLEROTIC PLAQUE; CELL ACTIVATION; CELL ADHESION; CELL DEATH; CELL DISRUPTION; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN DEGRADATION; COLLAGEN SYNTHESIS; CORONARY ARTERY ATHEROSCLEROSIS; CYTOKINE RELEASE; DEGRANULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME SYNTHESIS; EROSION; EXTRACELLULAR MATRIX; FOCAL ADHESION; GLYCOPROTEIN SYNTHESIS; HUMAN; IN VITRO STUDY; INFLAMMATORY CELL; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; RUPTURE; SECRETORY CELL; SMOOTH MUSCLE FIBER;

ANIMALS; APOPTOSIS; ARTERIAL OCCLUSIVE DISEASES; ARTERIOSCLEROSIS; CELL PROLIFERATION; CHEMOTAXIS; COLLAGEN; CORONARY ARTERIOSCLEROSIS; HUMANS; INFLAMMATION; MAST CELLS; MATRIX METALLOPROTEINASES; MODELS, BIOLOGICAL;

EID: 5044221645     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-200410000-00011     Document Type: Review

References (71)

1. Fuster V, Badimon L, Badimon JJ, Chesebro JH. The pathogenesis of coronary artery disease and the acute coronary syndromes. N Engl J Med 1992; 326:242-250.
2. Falk E. Why do plaques rupture? Circulation 1992; 86 (Suppl. III):30-42.
3. Virmani R, Kolodgie FD, Burke AP, et al. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2000; 20:1262-1275.
4. Naghavi M, Libby P, Falk E, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. Circulation 2003; 108:1664-1672. This review nicely summarizes the new definition of a vulnerable plaque and its relationship with vulnerable patients.
5. Richardson PD, Davies MJ, Born GVR. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaque. Lancet 1989; 2:941-944.
6. Libby P. Inflammation in atherosclerosis. Nature 2002; 420:868-874.
7. Leskinen MJ, Kovanen PT, Lindstedt KA. Regulation of smooth muscle cell growth, function and death in vitro by activated mast cells - a potential mechanism for the weakening and rupture of atherosclerotic plaques. Biochem Pharmacol 2003; 66:1493-1498.
8. Lindstedt KA, Leskinen MJ, Kovanen PT. Proteolysis of the pericellular matrix - a novel element determining cell survival and death in the pathogenesis of plaque erosion and rupture. Arterioscler Thromb Vasc Biol 2004; Published online before print June 10.
9. Kockx MM, Herman AG. Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res 2000; 45:736-746.
10. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation 1995; 92:657-671.
11. Moreno PR, Falk E, Palacios IF, et al. Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture. Circulation 1994; 90:775-778.
12. van der Wal AC, Becker AE, van der Loos CM, Das PK. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 1994; 89:36-44.
13. Kovanen PT, Kaartinen M, Paavonen T. Infiltrates of activated mast cells at the site of coronary atheromatous erosion or rupture in myocardial infarction. Circulation 1995; 92:1084-1088.
14. Williams CM, Galli SJ. The diverse potential effector and immunoregulatory roles of mast cells in allergic disease. J Allergy Clin Immunol 2000; 105:847-859.
15. Galli SJ. New concepts about the mast cell. N Engl J Med 1993; 328:257-265.
16. Mekori YA, Metcalfe DD. Mast cells in innate immunity. Immunol Rev 2000; 173:131-140.
17. Okumura S, Kashiwakura Ji, Tomita H, et al. Identification of specific gene expression profiles in human mast cells mediated by Toll-like receptor 4 and FcepsilonRI. Blood 2003; 102:2547-2554.
18. Frossi B, De Carli M, Pucillo C. The mast cell: an antenna of the microenvironment that directs the immune response. J Leukoc Biol 2004; 75:579-585. An excellent review discussing recent results on the role of mast cells in triggering innate immunity and directing adaptive immunity
19. Varadaradjalou S, Feger F, Thieblemont N, et al. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human mast cells. Eur J Immunol 2004; 33:899-906.
20. Kaartinen M, Penttilä A, Kovanen PT. Accumulation of activated mast cells in the shoulder region of human coronary atheroma, the predilection site of atheromatous rupture. Circulation 1994; 90:1669-1678.
21. Kovanen PT. Role of mast cells in atherosclerosis. In: Marone GS, editor. Human basophils and mast cells: clinical aspects. Basel: Karger; 1995. pp. 132-170.
22. Kelley JL, Chi DS, Abou-Auda W, et al. The molecular role of mast cells in atherosclerotic cardiovascular disease. Mol Med Today 2000; 6:304-308.
23. Metcalfe DD, Kaliner M, Donlon MA. The mast cell. Crit Rev Immunol 1981; 3:23-74.
24. Kaartinen M, Penttilä A, Kovanen PT. Mast cells of two types differing in neutral protease composition in the human aortic intima. Demonstration of both tryptase- and chymase-containing mast cells in normal intimas, fatty streaks, and the shoulder region of atheromas. Arterioscler Thromb 1994; 14:966-972.
25. Ishizaka T, Ishizaka K. Activation of mast cells for mediator release through IgE receptors. Prog Allergy 1984; 34:188-235.
26. Sedgwick JD, Holt PG, Turner KJ. Production of a histamine-releasing lymphokine by antigen- or mitogen-stimulated human peripheral T cells. Clin Exp Immunol 1981; 45:409-418.
27. Liu MC, Proud D, Lichtenstein LM, et al. Human lung macrophage-derived histamine-releasing activity is due to IgE-dependent factors. J Immunol 1986; 136:2588-2595.
28. Dvorak AM. Basophils and mast cells: piecemeal degranulation in situ and ex vivo: a possible mechanism for cytokine-induced function in disease. Immunol Ser 1992; 57:169-271.
29. Rohlich P, Anderson P, Uvnäs B. Electron microscope observations on compounds 48-80-induced degranulation in rat mast cells. Evidence for sequential exocytosis of storage granules. J Cell Biol 1971; 51:465-483.
30. Kovanen PT. The mast cell - a potential link between inflammation and cellular cholesterol deposition in atherogenesis. Eur Heart J 1993; 14 (Suppl. K):105-117.
31. Kokkonen JO, Kovanen PT. Stimulation of mast cells leads to cholesterol accumulation in macrophages in vitro by a mast cell granule-mediated uptake of low density lipoprotein. Proc Natl Acad Sci U S A 1987; 84:2287-2291.
32. Wang Y, Lindstedt KA, Kovanen PT. Mast cell granule remnants carry LDL into smooth muscle cells of synthetic phenotype and induce their conversion into foam cells. Arterioscler Thromb Vasc Biol 1995; 15:801-810.
33. Dvorak AM, Schleimer RP, Schulman ES, Lichtenstein LM. Human mast cells use conservation and condensation mechanisms during recovery from degranulation. In vitro studies with mast cells purified from human lungs. Lab Invest 1986; 54:663-678.
34. Kaartinen M, Penttilä A, Kovanen PT. Mast cells accompany microvessels in human coronary atheromas: implications for intimal neovascularization and hemorrhage. Atherosclerosis 1996; 123:123-131.
35. Laine P, Pentikäinen MO, Wurzner R, et al. Evidence for complement activation in ruptured coronary plaques in acute myocardial infarction. Am J Cardiol 2002; 90:404-408.
36. Schwartz LB, Austen KF. Structure and function of the chemical mediators of mast cells. In: Ishizaka K, editor. Mast cell activation and mediator release. Basel: S. Karger; 1984. pp. 271-321.
37. Compton SJ, Cairns JA, Holgate ST, Walls AF. Human mast cell tryptase stimulates the release of an IL-8-dependent neutrophil chemotactic activity from human umbilical vein endothelial cells (HUVEC). Clin Exp Immunol 2000; 121:31-36.
38. Pober JS, Gimbrone MA Jr, Lapierre LA, et al. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol 1986; 137:1893-1896.
39. Burns AR, Bowden RA, Abe Y, et al. P-selectin mediates neutrophil adhesion to endothelial cell borders. J Leukocyte Biol 1999; 65:299-306.
40. Gordon JR. TGFbeta1 and TNFalpha secreted by mast cells stimulated via the FcepsilonRI activate fibroblasts for high-level production of monocyte chemoattractant protein-1 (MCP-1). Cell Immunol 2000; 201:42-49.
41. Kaartinen M, Penttilä A, Kovanen PT. Mast cells in rupture-prone areas of human coronary atheromas produce and store TNF-a. Circulation 1996; 94:2787-2792.
42. Saren P, Welgus HG, Kovanen PT. TNF-alpha and IL-1beta selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol 1996; 157:4159-4165.
43. Di Girolamo N, Wakefield D. In vitro and in vivo expression of interstitial collagenase/MMP-1 by human mast cells. Dev Immunol 2000; 7:131-142.
44. Baram D, Vaday GG, Salamon P, et al. Human mast cells release metalloproteinase-9 on contact with activated T cells: juxtacrine regulation by TNF-alpha. J Immunol 2001; 167:4008-4016.
45. Nikkari ST, O'Brien KD, Ferguson M, et al. Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation 1995; 92:1393-1398.
46. Birkedal-Hansen H, Moore WG, Bodden MK, et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993; 4:197-250.
47. 84 bond by mast cell chymase. J Biol Chem 1994; 269:18134-18140.
48. Gruber BL, Marchese MJ, Suzuki K, et al. Synovial procollagenase activation by human mast cell tryptase dependence upon matrix metalloproteinase 3 activation. J Clin Invest 1989; 84:1657-1662.
49. Johnson JL, Jackson CL, Angelini GD, George SJ. Activation of matrix-degrading metalloproteinases by mast cell proteases in atherosclerotic plaques. Arterioscler Thromb Vasc Biol 1998; 18:1707-1715.
50. Vartio T, Seppä H, Vaheri A. Susceptibility of soluble and matrix fibronectins to degradation by tissue proteinases, mast cell chymase and cathepsin G. J Biol Chem 1981; 256:471-477.
51. Lohi J, Harvima I, Keski-Oja J. Pericellular substrates of human mast cell tryptase: 72,000 dalton gelatinase and fibronectin. J Cell Biochem 1992; 50:337-349.
52. Wang Y, Kovanen PT. Heparin proteoglycans released from rat serosal mast cells inhibit proliferation of rat aortic smooth muscle cells in culture. Circ Res 1999; 84:74-83.
53. Kazi M, Lundmark K, Religa P, et al. Inhibition of rat smooth muscle cell adhesion and proliferation by non-anticoagulant heparins. J Cell Physiol 2002; 193:365-372.
54. Lindstedt KA, Wang Y, Shiota N, et al. Activation of paracrine TGF-beta1 signaling upon stimulation and degranulation of rat serosal mast cells: a novel function for chymase. FASEB J 2001; 15:1377-1388.
55. Wang Y, Shiota N, Leskinen MJ, et al. Mast cell chymase inhibits smooth muscle cell growth and collagen expression in vitro: transforming growth factor-beta1-dependent and -independent effects. Arterioscler Thromb Vasc Biol 2001; 21:1928-1933.
56. Kaartinen M, van der Wal AC, van der Loos CM, et al. Mast cell infiltration in acute coronary syndromes: implications for plaque rupture. J Am Coll Cardiol 1998; 32:606-612.
57. Leskinen M, Wang Y, Leszczynski D, et al. Mast cell chymase induces apoptosis of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2001; 21:516-522.
58. Lätti S, Leskinen M, Shiota N, et al. Mast cell-mediated apoptosis of endothelial cells in vitro: a paracrine mechanism involving TNF-alpha-mediated down-regulation of bcl-2 expression. J Cell Physiol 2003; 195:130-138. The first study to show that mast cells, by secreting proinflammatory cytokines and proteases, may induce endothelial cell apoptosis in vitro.
59. Wallach D. Cell death induction by TNF: a matter of self control. Trends Biochem Sci 1997; 22:107-109.
60. Hara M, Matsumori A, Ono K, et al. Mast cells cause apoptosis of cardiomyocytes and proliferation of other intramyocardial cells in vitro. Circulation 1999; 100:1443-1449.
61. Leskinen MJ, Lindstedt KA, Wang Y, Kovanen PT. Mast cell chymase induces smooth muscle cell apoptosis by a mechanism involving fibronectin degradation and disruption of focal adhesions. Arterioscler Thromb Vasc Biol 2003; 23:238-243. This report describes the molecular mechanisms by which chymase induces SMC apoptosis.
62. Lindstedt L, Lee M, Kovanen PT. Chymase bound to heparin is resistant to its natural inhibitors and capable of proteolyzing high density lipoproteins in aortic intimai fluid. Atherosclerosis 2001; 155:87-97.
63. Tchougounova E, Forsberg E, Angelborg G, et al. Altered processing of fibronectin in mice lacking heparin: a role for heparin-dependent mast cell chymase in fibronectin degradation. J Biol Chem 2001; 276:3772-3777.
64. Wu WB, Peng HC, Huang TF. Disintegrin causes proteolysis of beta-catenin and apoptosis of endothelial cells. Involvement of cell-cell and cell-ECM interactions in regulating cell viability. Exp Cell Res 2003; 286:115-127.
65. Farb A, Burke AP, Tang AL, et al. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation 1996; 93:1354-1363.
66. Kolodgie FD, Burke AP, Farb A, et al. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler Thromb Vasc Biol 2002; 22:1642-1648.
67. Polunovsky VA, Wendt CH, Ingbar DH, et al. Induction of endothelial cell apoptosis by TNF alpha: modulation by inhibitors of protein synthesis. Exp Cell Res 1994; 214:584-594.
68. Bach FH, Hancock WW, Ferran C. Protective genes expressed in endothelial cells: a regulatory response to injury. Immunol Today 1997; 18:483-486.
69. Urbich C, Walter DH, Zeiher AM, Dimmeler S. Laminar shear stress upregulates integrin expression: role in endothelial cell adhesion and apoptosis. Circ Res 2000; 87:683-689.
70. Pohlman TH, Harlan JM. Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell Immunol 1989; 119:41-52.
71. Karsan A, Yee E, Harlan JM. Endothelial cell death induced by tumor necrosis factor-alpha is inhibited by the Bcl-2 family member, A1. J Biol Chem 1996; 271:27201-27204.