Inflammation and Thrombosis
2001; Lippincott Williams & Wilkins; Volume: 103; Issue: 13 Linguagem: Inglês
10.1161/01.cir.103.13.1718
ISSN1524-4539
Autores Tópico(s)Immune Response and Inflammation
ResumoHomeCirculationVol. 103, No. 13Inflammation and Thrombosis Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUBInflammation and Thrombosis The Clot Thickens Peter Libby and Daniel I. Simon Peter LibbyPeter Libby From the Brigham and Women's Hospital, Boston, Mass. and Daniel I. SimonDaniel I. Simon From the Brigham and Women's Hospital, Boston, Mass. Originally published3 Apr 2001https://doi.org/10.1161/01.CIR.103.13.1718Circulation. 2001;103:1718–1720Textbooks often portray thrombosis as a bland protective mechanism critical for stanching blood loss after injury: the prick of a lancet, the wound of a scalpel, or the predator's fangs neatly trigger a proteolytic cascade culminating in fibrin formation and cross-linking. However, in diseases such as atherosclerosis, the picture differs substantially from this simplistic model. In the natural history of atherosclerosis, thrombosis involves an inciting injury more subtle than a wound. In such pathological states, the importance of an intricate interface between inflammation and thrombosis becomes apparent.Septic Shock: An Extreme Example of Inflammatory Activation of the EndotheliumConsider the case of septic shock, a dramatic example of the link between inflammation and thrombosis. When Gram-negative bacteria release their endotoxin into the bloodstream, the lipopolysaccharide can change endothelial lining of blood vessels from an anticoagulant, profibrinolytic surface into one that promotes thrombosis. Bacterial endotoxin potently stimulates expression of the gene encoding tissue factor, a procoagulant molecule that multiplies manyfold the activity of coagulation factors VIIa and Xa. Endotoxin also can augment endothelial cell production of fibrinolytic inhibitor plasminogen activator inhibitor-1 (PAI-1). These alterations in endothelial function lead to the frequent clinical scenario of disseminated intravascular coagulation, a common concomitant of Gram-negative sepsis.Less-global endothelial activation may contribute to thrombosis in situ in more-chronic diseases such as atherosclerosis. Many inflammatory mediators found in human atherosclerotic plaques can augment tissue factor gene expression by endothelial cells. For example, interleukin-1 (IL-1) or tumor necrosis factor not only augment tissue factor gene expression but also PAI-1 production by human endothelial cells. Bacterial endotoxins within atheroma conceivably could derive from local Chlamydia pneumonia or other microbial infection. Endotoxin-induced expression of tissue factor and PAI-1 by endothelium thus may provide a stimulus that promotes thrombotic complication of "active" atherosclerotic plaques. In this manner, endogenous or bacterial inflammatory mediators can critically mediate functions of endothelial cells that promote systemic or local thrombosis in disease.Inflammatory Leukocytes as a Source of Thrombogenic StimuliIn the atheromatous plaque, macrophages often localize under the endothelial layer. A subpopulation of foamy macrophages in human atheroma express tissue factor.1 When plaques rupture, allowing contact of the blood with these tissue factor–bearing macrophages, thrombosis can ensue. Blood monocytes and resting tissue macrophages do not express tissue factor. However, when stimulated by certain inflammatory mediators, these mononuclear phagocytes transcribe the tissue factor gene. Bacterial endotoxin potently stimulates tissue factor gene expression in human mononuclear phagocytes.2 But what nonmicrobial stimuli might elicit tissue factor gene expression in atherosclerotic plaques? Unlike human endothelial cells, human mononuclear phagocytes do not augment tissue factor gene expression appreciably in response to soluble mediators such as IL-1 or tumor necrosis factor. Recent work has identified a cell surface–based signaling system, CD154 (CD40 ligand), binding to its receptor CD40 on the leukocyte, that can induce tissue factor expression.3 Because several cell types in atheroma bear CD154, this novel pathway probably contributes to macrophage tissue factor expression in the human atheroma.4Smooth Muscle Cells: Source of Procoagulants and Amplifier of Inflammatory Responses During ThrombosisThe smooth muscle cell is not commonly implicated in clotting. However, smooth muscle cells, like endothelial cells and macrophages, can express tissue factor procoagulant.5 Indeed, in superficial arterial erosion accounting for some fatal coronary thrombi, tissue factor expressed by smooth muscle cells uncovered by the endothelial erosion may contribute to thrombogenesis. Like the macrophage, for smooth muscle cells, CD154 may represent an important pathway of procoagulant activation of relevance to atherosclerosis.6The smooth muscle cell not only produces procoagulant but also can undergo inflammatory activation when exposed to thrombin and products of thrombosis. For example, thrombin stimulation causes smooth muscle cells to produce IL-6 abundantly.7 Platelet-derived growth factor, released from platelet alpha granules during thrombosis, can also markedly augment IL-6 production by smooth muscle cells.8 IL-6, in turn, can induce the acute phase response. Altering the pattern of hepatic protein synthesis from everyday "housekeeping" to the proteins in acute-phase response, IL-6 can increase plasma concentrations of fibrinogen, PAI-1, and the inflammatory marker C-reactive protein. Thus, local thrombotic stimulation of smooth muscle cells in the artery wall can amplify inflammatory response and promote a systemic procoagulant effect due to increased fibrinogen and PAI-1 levels in the circulation.New Roles for the Platelet in InflammationAlthough physicians readily acknowledge the key function of platelets in arterial thrombosis, most relegate platelets to a limited role as a responder to thrombotic stimuli. Platelets are nonnucleated and incapable of protein synthesis, and few researchers have accorded a regulatory role to these cell fragments. We now increasingly appreciate that the lowly platelet can take its rightful place beside its nucleated brethren as a source of inflammatory mediators (Table). For example, platelet factor 4, long recognized to be a platelet product, belongs to the CXC chemokine family of inflammatory mediators. Curiously, one particular chemokine (stromal cell–derived factor-1) can potently stimulate platelet aggregation; thus, platelets can both produce and respond to chemoattractant cytokines.9 Recent work has established that platelets can express CD154, the very molecule that regulates tissue factor gene expression in the macrophage and smooth muscle cell.10 von Hundelshausen et al,11 in this issue of Circulation, indicate that the T-cell cytokine "regulated on activation, normal T expressed and secreted" (RANTES), can participate in macrophage adhesion to endothelial cell by functioning as a bridge. Precedent for this kind of function for chemokines bound to the surface of endothelial cells and leukocyte adhesion exists in the cases of other chemokines, including macrophage chemoattractant protein-1 and IL-8.12 The new observations of von Hundelshausen and colleagues extend our appreciation of the links between thrombosis and inflammatory mediators.In injured arteries, recruitment of inflammatory leukocytes also can involve thrombosis. Platelets colocalize with leukocytes at sites of hemorrhage, within atherosclerotic and postangioplasty restenotic lesions, and in areas of ischemia-reperfusion injury. This heterotypic interaction between platelets and leukocytes links hemostatic/thrombotic and inflammatory responses. Just as adhesion of leukocytes to the inflamed endothelium involves rolling (mediated by selectins) followed by a tighter integrin-mediated adhesion, leukocyte attachment to and transmigration across a carpet of platelets adherent to the injured intima may occur in similar sequential steps.13 Initial tethering and rolling of leukocytes on platelet P-selectin precedes their firm adhesion and transplatelet migration, processes that depend on the leukocyte integrin Mac-1 and platelet glycoprotein Ibα.14 In addition to promoting accumulation of leukocytes at sites of platelet coverage within the vasculature, binding of platelets to neutrophils influences key cellular effector responses by inducing leukocyte activation; augmenting cell-adhesion molecule expression; and generating signals that promote integrin activation, chemokine synthesis, and the respiratory burst. Interestingly, both neutrophil-platelet and monocyte-platelet aggregates circulate in the peripheral blood of patients with coronary artery disease and may correlate with disease activity.1516Inflammation and Thrombosis: Intertwined in Vascular PathologyThe examples above illustrate how major cell types involved in vascular diseases express multiple functions at the interface of thrombosis and inflammation. Inflammation can beget local thrombosis, and thrombosis can amplify inflammation. Thus, we can regard anti-inflammatory therapies as potentially antithrombotic, obvious in the case of aspirin but a useful framework for rethinking mechanisms of benefit of other strategies (Figure 1). In addition, antithrombotic treatment may suppress inflammation and help break the vicious cycle of the acute coronary syndromes by limiting the local and systemic amplification loops described above. The biology of the diseases that preoccupy us in the clinic guide us in adjustment of our classic textbook categorizations of cells and their functions.The opinions expressed in this editorial are not necessarily those of the editors or of the American Heart Association.Download figureDownload PowerPoint Figure 1. Accumulating data linking inflammation and thrombosis support the hypothesis illustrated here that anti-inflammatory therapies may limit thrombosis and that antithrombotic therapies may reduce vascular inflammation. Table 1. Examples of Inflammatory Modulators Produced by PlateletsPlatelet-derived growth factorPlatelet factor 4CD 154 (CD40 ligand)RANTESThrombospondinTransforming growth factor-βNitric oxideThis work was supported in part by grants from the National Institutes of Health (HL-57506 and DK-55656 to D.I.S. and HL-34636 to P.L.).FootnotesCorrespondence to Peter Libby, MD, Brigham and Women's Hospital, 221 Longwood Ave, LMRC 307, Boston, MA 02115. 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