Intravascular leukocyte migration through platelet thrombi: directing leukocytes to sites of vascular injury

Mehran Ghasemzadeh; Ehteramolsadat Hosseini

doi:10.1160/TH14-08-0662

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2015; 113(06): 1224-1235
DOI: 10.1160/TH14-08-0662

Review Article

Schattauer GmbH

Intravascular leukocyte migration through platelet thrombi: directing leukocytes to sites of vascular injury

Autoren

Mehran Ghasemzadeh

¹Blood Transfusion Research Center, High Institute for Research and Education in Transfusion Medicine, Tehran, Iran

²Australian Centre for Blood Diseases, Monash University, Melbourne, Victoria, Australia
Ehteramolsadat Hosseini

¹Blood Transfusion Research Center, High Institute for Research and Education in Transfusion Medicine, Tehran, Iran

³Department of Immunology, Alfred Medical Research and Education Precinct, Monash University, Melbourne, Victoria, Australia

Abstract

Summary

Leukocytes recruitment to thrombi supports an intimate cellular interaction leading to the enhancement of pro-coagulant functions and pro-inflammatory responses at site of vascular injury. Recent observations of neutrophil extracellular traps (NETs) formation and its mutual reactions with platelet thrombi adds more clinical interest to the growing body of knowledge in the field of platelet-leukocyte crosstalk. However, having considered thrombus as a barrier between leukocytes and injured endothelium, the full inflammatory roles of these cells during thrombosis is still ill defined. The most recent observation of neutrophils migration into the thrombi is a phenomenon that highlights the inflammatory functions of leukocytes at the site of injury. It has been hypothesised that leukocytes migration might be associated with the conveyance of highly reactive pro-inflammatory and/or procoagulant mediators to sites of vascular injury. In addition, the evidence of neutrophils migration into arterial thrombi following traumatic and ischaemia-reperfusion injury highlights the already described role of these cells in atherosclerosis. Regardless of the mechanisms behind leukocyte migration, whether these migrated cells benefit normal homeostasis by their involvement in wound healing and vascular rebuilding or they increase unwilling inflammatory responses, could be of interest for future researches that provide new insight into biological importance of leukocyte recruitment to thrombi.

Keywords

Platelet-leukocyte crosstalk - NETs formation - intravascular leukocyte migration - neutrophil induced atherosclerosis

Volltext

Referenzen

References
1 Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nature Rev Immunol 2013; 13: 159-175.
2 Ghasemzadeh M. et al. The CXCR1/2 ligand NAP-2 promotes directed intravascular leukocyte migration through platelet thrombi. Blood 2013; 121: 4555-4566.
3 Kobayashi SD, DeLeo FR. Role of neutrophils in innate immunity: a systems biology- level approach. Wiley Interdis Rev 2009; 01: 309-333.
4 Amulic B. et al. Neutrophil function: from mechanisms to disease. Ann Rev Immunol 2012; 30: 459-489.
5 Soehnlein O, Lindbom L. Phagocyte partnership during the onset and resolution of inflammation. Nature Rev Immunol 2010; 10: 427-439.
6 Canturk NZ. et al. The relationship between neutrophils and incisional wound healing. Skin Pharmacol Appl Skin Physiol 2001; 14: 108-116.
7 Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol 2012; 05: 354-366.
8 Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nature Med 2011; 17: 1381-1390.
9 Rock KL. et al. The sterile inflammatory response. Ann Rev Immunol 2010; 28: 321-342.
10 Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nature Rev Immunol 2010; 10: 826-837.
11 Ghasemzadeh M, Hosseini E. Platelet-leukocyte crosstalk: Linking proinflammatory responses to procoagulant state. Thromb Res 2013; 131: 191-197.
12 Wang BG. et al. Two-photon microscopy of deep intravital tissues and its merits in clinical research. J Microsc 2010; 238: 1-20.
13 Niesner RA, Hauser AE. Recent advances in dynamic intravital multi-photon microscopy. Cytometry A 2011; 79: 789-798.
14 von Bruhl ML. et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209: 819-835.
15 Kreisel D. et al. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc Natl Acad Sci USA 2010; 107: 18073-18078.
16 Chevre R. et al. High-resolution imaging of intravascular atherogenic inflammation in live mice. Circulation Res 2014; 114: 770-779.
17 Kuijpers MJ, Heemskerk JW. Intravital imaging of thrombus formation in small and large mouse arteries: experimentally induced vascular damage and plaque rupture in vivo. Methods Mol Biol 2012; 788: 3-19.
18 Andrews RK. et al. Neutrophil extracellular traps (NETs) and the role of platelets in infection. Thromb Haemost 2014; 112: 659-665.
19 Fuchs TA. et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176: 231-241.
20 Fuchs TA. et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880-15885.
21 Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood 2014; 123 (18) 2768-76.
22 Ley K. et al. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nature Rev 2007; 07: 678-689.
23 Ryschich E. et al. Active leukocyte crawling in microvessels assessed by digital time-lapse intravital microscopy. J Surg Res 2006; 135: 291-296.
24 Bevilacqua MP. et al. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 1989; 243: 1160-1165.
25 Larsen E. et al. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell 1989; 59: 305-312.
26 Geng JG. et al. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature 1990; 343: 757-760.
27 Diacovo TG. et al. Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the beta 2-integrin CD11b/CD18. Blood 1996; 88: 146-157.
28 Eriksson EE. et al. Importance of primary capture and L-selectin-dependent secondary capture in leukocyte accumulation in inflammation and atherosclerosis in vivo. J Exp Med 2001; 194: 205-218.
29 Sugii Y. et al. In vivo PIV measurement of red blood cell velocity field in microvessels considering mesentery motion. Physiol Measurem 2002; 23: 403-416.
30 Gross PL. et al. Leukocyte-versus microparticle-mediated tissue factor transfer during arteriolar thrombus development. J Leukoc Biol 2005; 78: 1318-1326.
31 Lindbom L, Werr J. Integrin-dependent neutrophil migration in extravascular tissue. Semin Immunol 2002; 14: 115-121.
32 Berton G, Lowell CA. Integrin signalling in neutrophils and macrophages. Cell Signal 1999; 11: 621-635.
33 Kelly M. et al. Modulating leukocyte recruitment in inflammation. J Allergy Clin Immunol 2007; 120: 3-10.
34 Luo BH. et al. Structural basis of integrin regulation and signaling. Ann Rev Immunol 2007; 25: 619-647.
35 Ross GD. Regulation of the adhesion versus cytotoxic functions of the Mac- 1/CR3/alphaMbeta2-integrin glycoprotein. Crit Rev Immunol 2000; 20: 197-222.
36 Ehlers MR. CR3: a general purpose adhesion-recognition receptor essential for innate immunity. Microbes Infect 2000; 02: 289-294.
37 Mayadas TN, Cullere X. Neutrophil beta2 integrins: moderators of life or death decisions. Trends Immunol 2005; 26: 388-395.
38 Evangelista V. et al. Src family kinases mediate neutrophil adhesion to adherent platelets. Blood 2007; 109: 2461-2469.
39 Evangelista V. et al. Platelet/polymorphonuclear leukocyte interaction: P-selectin triggers protein-tyrosine phosphorylation-dependent CD11b/CD18 adhesion: role of PSGL-1 as a signaling molecule. Blood 1999; 93: 876-885.
40 Abbal C. et al. Lipid raft adhesion receptors and Syk regulate selectin-dependent rolling under flow conditions. Blood 2006; 108: 3352-3359.
41 Wang HB. et al. P-selectin primes leukocyte integrin activation during inflammation. Nature Immunol 2007; 08: 882-892.
42 Zarbock A. et al. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 2007; 26: 773-783.
43 Chesnutt BC. et al. Induction of LFA-1-dependent neutrophil rolling on ICAM-1 by engagement of E-selectin. Microcirculation 2006; 13: 99-109.
44 Zarbock A. et al. Galphai2 is required for chemokine-induced neutrophil arrest. Blood 2007; 110: 3773-3779.
45 Zarbock A. et al. Platelet-neutrophil-interactions: linking hemostasis and inflammation. Blood Rev 2007; 21: 99-111.
46 Proudfoot AE. et al. Glycosaminoglycan binding and oligomerisation are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci USA 2003; 100: 1885-1890.
47 Weber C, Springer TA. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J Clin Invest 1997; 100: 2085-2093.
48 Kulkarni S. et al. Conversion of platelets from a proaggregatory to a proinflammatory adhesive phenotype: role of PAF in spatially regulating neutrophil adhesion and spreading. Blood 2007; 110: 1879-1886.
49 Nojima S. Platelet-activating factor (PAF): an introduction. Lipids 1991; 26: 965-966.
50 Witko-Sarsat V. et al. Neutrophils: molecules, functions and pathophysiological aspects. Lab Invest 2000; 80: 617-653.
51 Marcus AJ. et al. Effects of acetyl glyceryl ether phosphorylcholine on human platelet function in vitro. Blood 1981; 58: 1027-1031.
52 Chao W, Olson MS. Platelet-activating factor: receptors and signal transduction. Biochem J 1993; 292: 617-629.
53 Prescott SM. et al. Platelet-activating factor and related lipid mediators. Ann Rev Biochem 2000; 69: 419-445.
54 Hosseini E, Ghasemzadeh M. Different stages of platelet adhesion to the site of vascular injury. Iran J Blood Cancer 2012; 04: 133-142.
55 Kulkarni S, Jackson SP. Platelet factor XIII and calpain negatively regulate integrin alphaIIbbeta3 adhesive function and thrombus growth. J Biol Chem 2004; 279: 30697-30706.
56 Pluskota E. et al. Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood 2008; 112: 2327-2335.
57 Pruenster M. et al. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nature Immunol 2009; 10: 101-108.
58 Zarbock A. et al. The Duffy antigen receptor for chemokines in acute renal failure: A facilitator of renal chemokine presentation. Crit Care Med 2007; 35: 2156-2163.
59 Kuschert GS. et al. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochem 1999; 38: 12959-12968.
60 Middleton J. et al. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 2002; 100: 3853-3860.
61 Johnson Z. et al. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytok Growth Factor Rev 2005; 16: 625-636.
62 Weingart C. et al. Dose dependent effects of platelet derived chondroitinsulfate A on the binding of CCL5 to endothelial cells. BMC Immunol 2008; 09: 72.
63 Stringer SE, Gallagher JT. Specific binding of the chemokine platelet factor 4 to heparan sulfate. J Biol Chem 1997; 272: 20508-20514.
64 von Hundelshausen P. et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105: 924-930.
65 Petersen F. et al. Platelet factor 4-induced neutrophil-endothelial cell interaction: involvement of mechanisms and functional consequences different from those elicited by interleukin-8. Blood 1999; 94: 4020-4028.
66 Kasper B. et al. Neutrophil adhesion to endothelial cells induced by platelet factor 4 requires sequential activation of Ras, Syk, and JNK MAP kinases. Blood 2006; 107: 1768-1775.
67 Ludwig A. et al. The CXC-chemokine neutrophil-activating peptide-2 induces two distinct optima of neutrophil chemotaxis by differential interaction with interleukin- 8 receptors CXCR-1 and CXCR-2. Blood 1997; 90: 4588-4597.
68 Brandt E. et al. Neutrophils can generate their activator neutrophil-activating peptide 2 by proteolytic cleavage of platelet-derived connective tissue-activating peptide III. Cytokine 1991; 03: 311-321.
69 Holt JC. et al. Isolation, characterisation, and immunological detection of neutrophil- activating peptide 2: a proteolytic degradation product of platelet basic protein. Proc Soc Exp Biol Med 1992; 199: 171-177.
70 Hamad OA. et al. Complement activation triggered by chondroitin sulfate released by thrombin receptor-activated platelets. J Thromb Haemost 2008; 06: 1413-1421.
71 Brinkmann V. et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
72 Zawrotniak M, Rapala-Kozik M. Neutrophil extracellular traps (NETs) - formation and implications. Acta Biochim Pol 2013; 60: 277-284.
73 Massberg S. et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nature Med 2010; 16: 887-896.
74 Clark SR. et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nature Med 2007; 13: 463-469.
75 Koupenova M. et al. Platelet-TLR7 mediates host survival and platelet count during viral infection in the absence of platelet-dependent thrombosis. Blood 2014; 124: 791-802.
76 Yipp BG, Kubes P. NETosis: how vital is it?. Blood 2013; 122: 2784-2794.
77 Neeli I. et al. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895-1902.
78 Pinsky DJ. et al. Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest 1996; 97: 493-500.
79 Wagner DD, Frenette PS. The vessel wall and its interactions. Blood 2008; 111: 5271-5281.
80 Karakurum M. et al. Hypoxic induction of interleukin-8 gene expression in human endothelial cells. J Clin Invest 1994; 93: 1564-1570.
81 Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol Rev 1999; 79: 609-634.
82 van Aken BE. et al. Interleukin 8 and venous thrombosis: evidence for a role of inflammation in thrombosis. Br J Haematol 2002; 116: 173-177.
83 McInturff AM. et al. Mammalian target of rapamycin regulates neutrophil extracellular trap formation via induction of hypoxia-inducible factor 1 alpha. Blood 2012; 120: 3118-3125.
84 Brill A. et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012; 10: 136-144.
85 Xu J. et al. Extracellular histones are major mediators of death in sepsis. Nature Med 2009; 15: 1318-1321.
86 Fuchs TA. et al. Histones induce rapid and profound thrombocytopenia in mice. Blood 2011; 118: 3708-3714.
87 Semeraro F. et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 2011; 118: 1952-1961.
88 Kannemeier C. et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci USA 2007; 104: 6388-6393.
89 Muller F. et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-1156.
90 Line BR. Pathophysiology and diagnosis of deep venous thrombosis. Semin Nucl Med 2001; 31: 90-101.
91 Fuchs TA. et al. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscl Thromb Vasc Biol 2012; 32: 1777-1783.
92 Wolberg AS. et al. Procoagulant activity in hemostasis and thrombosis: Virchow’s triad revisited. Anesth Analg 2012; 114: 275-285.
93 Si-Tahar M. et al. Human neutrophil elastase proteolytically activates the platelet integrin alphaIIbbeta3 through cleavage of the carboxyl terminus of the alphaIIb subunit heavy chain. Involvement in the potentiation of platelet aggregation. J Biol Chem 1997; 272: 11636-11647.
94 Xu J. et al. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187: 2626-2631.
95 Muller I. et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 2003; 17: 476-478.
96 Rauch U. et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96: 170-175.
97 Scholz T. et al. Transfer of tissue factor from platelets to monocytes: role of platelet- derived microvesicles and CD62P. Thromb Haemost 2002; 88: 1033-1038.
98 Falati S. et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003; 197: 1585-1598.
99 Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol 2013; 191: 2647-2656.
100 Soo KS. et al. Tissue plasminogen activator production by monocytes in venous thrombolysis. J Pathol 1996; 178: 190-194.
101 Kroll MH. et al. Platelets and shear stress. Blood 1996; 88: 1525-1541.
102 Cosemans JM. et al. The effects of arterial flow on platelet activation, thrombus growth, and stabilisation. Cardiovasc Res 2013; 99: 342-352.
103 Nesbitt WS. et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nature Med 2009; 15: 665-673.
104 Berndt MC. et al. Primary haemostasis: newer insights. Haemophilia 2014; 20 (Suppl. 04) 15-22.
105 Potter CM. et al. Role of shear stress in endothelial cell morphology and expression of cyclooxygenase isoforms. Arterioscl Thromb Vasc Biol 2011; 31: 384-391.
106 Nesbitt WS. et al. The impact of blood rheology on the molecular and cellular events underlying arterial thrombosis. J Mol Med 2006; 84: 989-995.
107 Savage B. et al. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on vwf rand factor. Cell 1996; 84: 289-297.
108 Goto S. et al. Effects of adenosine 5’-diphosphate (ADP) receptor blockade on platelet aggregation under flow. Blood 2002; 99: 4644-4645 author reply 465-466.
109 Mitchell MJ. et al. Fluid shear stress increases neutrophil activation via plateletactivating factor. Biophys J 2014; 106: 2243-2253.
110 Darbousset R. et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood 2012; 120: 2133-2143.
111 Firrell JC, Lipowsky HH. Leukocyte margination and deformation in mesenteric venules of rat. Am J Physiol 1989; 256: H1667-H1674.
112 Sundd P. et al. Biomechanics of leukocyte rolling. Biorheology 2011; 48: 1-35.
113 Sundd P. et al. ’Slings’ enable neutrophil rolling at high shear. Nature 2012; 488: 399-403.
114 Carvalho-Tavares J. et al. A role for platelets and endothelial selectins in tumor necrosis factor-alpha-induced leukocyte recruitment in the brain microvasculature. Circulation Res 2000; 87: 1141-1148.
115 Bernardo A. et al. Platelets adhered to endothelial cell-bound ultra-large von Willebrand factor strings support leukocyte tethering and rolling under high shear stress. J Thromb Haemost 2005; 03: 562-570.
116 Ostrovsky L. et al. A juxtacrine mechanism for neutrophil adhesion on platelets involves platelet-activating factor and a selectin-dependent activation process. Blood 1998; 91: 3028-3036.
117 Dubois C. et al. Glycoprotein VI-dependent and -independent pathways of thrombus formation in vivo. Blood 2006; 107: 3902-3906.
118 Deppermann C. et al. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. J Clin Invest 2013. please complete reference.
119 Darbousset R. et al. Involvement of neutrophils in thrombus formation in living mice. Pathol Biol 2014; 62: 1-9.
120 Yokoyama S. et al. Platelet P-selectin plays an important role in arterial thrombogenesis by forming large stable platelet-leukocyte aggregates. J Am Coll Cardiol 2005; 45: 1280-1286.
121 Sambrano GR. et al. Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature 2001; 413: 74-78.
122 Weiss EJ. et al. Protection against thrombosis in mice lacking PAR3. Blood 2002; 100: 3240-3244.
123 Jackson SP. Arterial thrombosis--insidious, unpredictable and deadly. Nature Med 2011; 17: 1423-1436.
124 Heemskerk JW. et al. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11: 2-16.
125 Reininger AJ. et al. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol 2010; 55: 1147-1158.
126 Cosemans JM. et al. Key role of glycoprotein Ib/V/IX and von Willebrand factor in platelet activation-dependent fibrin formation at low shear flow. Blood 2011; 117: 651-660.
127 Wang L. et al. Vascular smooth muscle-derived tissue factor is critical for arterial thrombosis after ferric chloride-induced injury. Blood 2009; 113: 705-713.
128 Mackman N. The many faces of tissue factor. J Thromb Haemost 2009; 07 (Suppl. 01) 136-139.
129 Kambas K. et al. The emerging role of neutrophils in thrombosis-the journey of TF through NETs. Frontiers Immunol 2012; 03: 385.
130 Rosen ED. et al. Laser-induced noninvasive vascular injury models in mice generate platelet- and coagulation-dependent thrombi. Am J Pathol 2001; 158: 1613-1622.
131 Atkinson BT. et al. Laser-induced endothelial cell activation supports fibrin formation. Blood 2010; 116: 4675-4683.
132 Vandendries ER. et al. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc Natl Acad Sci USA 2007; 104: 288-292.
133 Dubois C. et al. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J Clin Invest 2007; 117: 953-960.
134 Owens 3rd AP, Mackman N. Microparticles in hemostasis and thrombosis. Circulation Res 2011; 108: 1284-1297.
135 Phillipson M. et al. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J Exp Med 2006; 203: 2569-2575.
136 Issekutz AC, Issekutz TB. The contribution of LFA-1 (CD11a/CD18) and MAC-1 (CD11b/CD18) to the in vivo migration of polymorphonuclear leucocytes to inflammatory reactions in the rat. Immunology 1992; 76: 655-661.
137 Ding ZM. et al. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. J Immunol 1999; 163: 5029-5038.
138 Hentzen ER. et al. Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule- 1. Blood 2000; 95: 911-920.
139 Halai K. et al. ICAM-2 facilitates luminal interactions between neutrophils and endothelial cells in vivo. J Cell Sci 2014; 127: 620-629.
140 Sreeramkumar V. et al. Neutrophils scan for activated platelets to initiate inflammation. Science 2014; 346: 1234-1238.
141 Ono A. et al. Identification of a fibrin-independent platelet contractile mechanism regulating primary hemostasis and thrombus growth. Blood 2008; 112: 90-99.
142 Lawrence MB. et al. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood 1987; 70: 1284-1290.
143 Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 1991; 65: 859-873.
144 Moazzam F. et al. The leukocyte response to fluid stress. Proc Natl Acad Sci USA 1997; 94: 5338-5343.
145 Lawrence MB. et al. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L,P,E). J Cell Biol 1997; 136: 717-727.
146 Soehnlein O. Multiple roles for neutrophils in atherosclerosis. Circulation Res 2012; 110: 875-888.