Subscribe to RSS
Please copy the URL and add it into your RSS Feed Reader.
https://www.thieme-connect.de/rss/thieme/en/10.1055-s-00035024.xml
Thromb Haemost 2013; 110(05): 894-902
DOI: 10.1160/TH13-04-0341
DOI: 10.1160/TH13-04-0341
Theme Issue Article
Platelet chemokines in health and disease
Further Information
Publication History
Received: 25 April 2013
Accepted after major revision: 17 May 2013
Publication Date:
01 December 2017 (online)
Summary
In recent years, it has become clear that platelets and platelet-derived chemokines, beyond their role in thrombosis and haemostasis, are important mediators affecting a broad spectrum of (patho)physiological conditions. These biologically active proteins are released from α-granules upon platelet activation, most probably even during physiological conditions. In this review, we give a concise overview and an update on the current understanding of platelet-derived chemokines in a context of health and disease.
Note: The review process for this manuscript was fully handled by G. Y. H. Lip, Editor in Chief.
-
References
- 1 Junt T, Schulze H, Chen Z. et al. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007; 317: 1767-1770.
- 2 Lievens D, von Hundelshausen P. Platelets in atherosclerosis. Thromb Haemost 2011; 106: 827-838.
- 3 Flad HD, Brandt E. Platelet-derived chemokines: pathophysiology and therapeutic aspects. Cell Mol Life Sci 2010; 67: 2363-2386.
- 4 Gleissner CA. Platelet-derived chemokines in atherogenesis: what's new?. Curr Vasc Pharmacol 2012; 10: 563-569.
- 5 Brandt E, Ludwig A, Petersen F. et al. Platelet-derived CXC chemokines: old players in new games. Immunol Rev 2000; 177: 204-216.
- 6 Projahn D, Koenen RR. Platelets: key players in vascular inflammation. J Leukoc Biol 2012; 92: 1167-1175.
- 7 van Nispen tot Pannerden H, de Haas F, Geerts W. et al. The platelet interior revisited: electron tomography reveals tubular alpha-granule subtypes. Blood 2010; 116: 1147-1156.
- 8 Cervi D, Yip TT, Bhattacharya N. et al. Platelet-associated PF-4 as a biomarker of early tumor growth. Blood 2008; 111: 1201-1207.
- 9 Italiano Jr. JE, Richardson JL, Patel-Hett S. et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008; 111: 1227-1233.
- 10 Sehgal S, Storrie B. Evidence that differential packaging of the major platelet granule proteins von Willebrand factor and fibrinogen can support their differential release. J Thromb Haemost 2007; 5: 2009-2016.
- 11 Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000; 18: 217-242.
- 12 Blanchet X, Langer M, Weber C. et al. Touch of chemokines. Frontiers Immunol 2012; 3: 175
- 13 Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 2000; 12: 121-127.
- 14 Struyf S, Burdick MD, Proost P. et al. Platelets release CXCL4L1, a nonallelic variant of the chemokine platelet factor-4/CXCL4 and potent inhibitor of angiogenesis. Circ Res 2004; 95: 855-857.
- 15 Burkhart JM, Vaudel M, Gambaryan S. et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 2012; 120: e73-82.
- 16 Rowley JW, Oler AJ, Tolley ND. et al. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 2011; 118: e101-111.
- 17 Massberg S, Konrad I, Schurzinger K. et al. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med 2006; 203: 1221-1233.
- 18 Stellos K, Langer H, Daub K. et al. Platelet-derived stromal cell-derived factor-1 regulates adhesion and promotes differentiation of human CD34+ cells to endothelial progenitor cells. Circulation 2008; 117: 206-215.
- 19 Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol 2007; 28: 299-307.
- 20 Kamykowski J, Carlton P, Sehgal S. et al. Quantitative immunofluorescence mapping reveals little functional coclustering of proteins within platelet alpha-granules. Blood 2011; 118: 1370-1373.
- 21 Chatterjee M, Huang Z, Zhang W. et al. Distinct platelet packaging, release, and surface expression of proangiogenic and antiangiogenic factors on different platelet stimuli. Blood 2011; 117: 3907-3911.
- 22 Maione TE, Gray GS, Petro J. et al. Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science 1990; 247: 77-79.
- 23 Brill A, Elinav H, Varon D. Differential role of platelet granular mediators in angiogenesis. Cardiovasc Res 2004; 63: 226-235.
- 24 Gengrinovitch S, Greenberg SM, Cohen T. et al. Platelet factor-4 inhibits the mitogenic activity of VEGF121 and VEGF165 using several concurrent mechanisms. J Biol Chem 1995; 270: 15059-15065.
- 25 Green CJ, Charles RS, Edwards BF. et al. Identification and characterization of PF4varl, a human gene variant of platelet factor 4. Mol Cell Biol 1989; 9: 1445-1451.
- 26 Kuo JH, Chen YP, Liu JS. et al. Alternative C-Terminal Helix Orientation Alters Chemokine Function: Structure of the Anti-angiogenic Chemokine, CXCL4L1. J Biol Chem. 2013 Epub ahead of print
- 27 Sarabi A, Kramp BK, Drechsler M. et al. CXCL4L1 inhibits angiogenesis and induces undirected endothelial cell migration without affecting endothelial cell proliferation and monocyte recruitment. J Thromb Haemost 2011; 9: 209-219.
- 28 Lasagni L, Francalanci M, Annunziato F. et al. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med 2003; 197: 1537-1549.
- 29 Struyf S, Salogni L, Burdick MD. et al. Angiostatic and chemotactic activities of the CXC chemokine CXCL4L1 (platelet factor-4 variant) are mediated by CXCR3. Blood 2011; 117: 480-488.
- 30 Balkwill FR. The chemokine system and cancer. J Pathol 2012; 226: 148-157.
- 31 Wiesner T, Bugl S, Mayer F. et al. Differential changes in platelet VEGF, Tsp, CXCL12, and CXCL4 in patients with metastatic cancer. Clin Exp Metastasis 2010; 27: 141-149.
- 32 Buergy D, Wenz F, Groden C. et al. Tumor-platelet interaction in solid tumors. Int J Cancer 2012; 130: 2747-2760.
- 33 Fiedler GM, Leichtle AB, Kase J. et al. Serum peptidome profiling revealed platelet factor 4 as a potential discriminating Peptide associated with pancreatic cancer. Clin Cancer Res 2009; 15: 3812-3819.
- 34 Peterson JE, Zurakowski D, Italiano Jr. JE. et al. VEGF, PF4 and PDGF are elevated in platelets of colorectal cancer patients. Angiogenesis 2012; 15: 265-273.
- 35 Aivado M, Spentzos D, Germing U. et al. Serum proteome profiling detects myelodysplastic syndromes and identifies CXC chemokine ligands 4 and 7 as markers for advanced disease. Proc Natl Acad Sci USA 2007; 104: 1307-1312.
- 36 Yang L, Du J, Hou J. et al. Platelet factor-4 and its p17-70 peptide inhibit myeloma proliferation and angiogenesis in vivo. BMC Cancer 2011; 11: 261
- 37 Struyf S, Burdick MD, Peeters E. et al. Platelet factor-4 variant chemokine CXCL4L1 inhibits melanoma and lung carcinoma growth and metastasis by preventing angiogenesis. Cancer Res 2007; 67: 5940-5948.
- 38 Han ZC, Bellucci S, Walz A. et al. Negative regulation of human megakaryocytopoiesis by human platelet factor 4 (PF4) and connective tissue-activating peptide (CTAP-III). Int J Cell Cloning 1990; 8: 253-259.
- 39 Lambert MP, Wang Y, Bdeir KH. et al. Platelet factor 4 regulates megakaryopoiesis through low-density lipoprotein receptor-related protein 1 (LRP1) on megakaryocytes. Blood 2009; 114: 2290-2298.
- 40 Lambert MP, Rauova L, Bailey M. et al. Platelet factor 4 is a negative autocrine in vivo regulator of megakaryopoiesis: clinical and therapeutic implications. Blood 2007; 110: 1153-1160.
- 41 Dudek AZ, Nesmelova I, Mayo K. et al. Platelet factor 4 promotes adhesion of hematopoietic progenitor cells and binds IL-8: novel mechanisms for modulation of hematopoiesis. Blood 2003; 101: 4687-4694.
- 42 Emadi S, Clay D, Desterke C. et al. IL-8 and its CXCR1 and CXCR2 receptors participate in the control of megakaryocytic proliferation, differentiation, and ploidy in myeloid metaplasia with myelofibrosis. Blood 2005; 105: 464-473.
- 43 Hodohara K, Fujii N, Yamamoto N. et al. Stromal cell-derived factor-1 (SDF-1) acts together with thrombopoietin to enhance the development of megakaryocytic progenitor cells (CFU-MK). Blood 2000; 95: 769-775.
- 44 Hamada T, Mohle R, Hesselgesser J. et al. Transendothelial migration of megakaryocytes in response to stromal cell-derived factor 1 (SDF-1) enhances platelet formation. J Exp Med 1998; 188: 539-548.
- 45 Avecilla ST, Hattori K, Heissig B. et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 2004; 10: 64-71.
- 46 Davoren A, Aster RH. Heparin-induced thrombocytopenia and thrombosis. Am J Hematol 2006; 81: 36-44.
- 47 Greinacher A. Heparin-induced thrombocytopenia. J Thromb Haemost 2009; 7 (Suppl. 01) 9-12.
- 48 Sachais BS, Rux AH, Cines DB. et al. Rational design and characterization of platelet factor 4 antagonists for the study of heparin-induced thrombocytopenia. Blood 2012; 119: 5955-5962.
- 49 Lambert MP, Sachais BS, Kowalska MA. Chemokines and thrombogenicity. Thromb Haemost 2007; 97: 722-729.
- 50 Eslin DE, Zhang C, Samuels KJ. et al. Transgenic mice studies demonstrate a role for platelet factor 4 in thrombosis: dissociation between anticoagulant and antithrombotic effect of heparin. Blood 2004; 104: 3173-3180.
- 51 Preston RJ, Tran S, Johnson JA. et al. Platelet factor 4 impairs the anticoagulant activity of activated protein C. J Biol Chem 2009; 284: 5869-5875.
- 52 Kowalska MA, Mahmud SA, Lambert MP. et al. Endogenous platelet factor 4 stimulates activated protein C generation in vivo and improves survival after thrombin or lipopolysaccharide challenge. Blood 2007; 110: 1903-1905.
- 53 Yeaman MR, Yount NY, Waring AJ. et al. Modular determinants of antimicrobial activity in platelet factor-4 family kinocidins. Biochim Biophys Acta 2007; 1768: 609-619.
- 54 Krijgsveld J, Zaat SA, Meeldijk J. et al. Thrombocidins, microbicidal proteins from human blood platelets, are C-terminal deletion products of CXC chemokines. J Biol Chem 2000; 275: 20374-20381.
- 55 Tang YQ, Yeaman MR, Selsted ME. Antimicrobial peptides from human platelets. Infection Immunity 2002; 70: 6524-6533.
- 56 Dankert J, Krijgsveld J, van Der Werff J. et al. Platelet microbicidal activity is an important defense factor against viridans streptococcal endocarditis. J Infect Dis 2001; 184: 597-605.
- 57 Fitzgerald JR, Loughman A, Keane F. et al. Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgammaRIIa receptor. Mol Microbiol 2006; 59: 212-230.
- 58 Andonegui G, Kerfoot SM, McNagny K. et al. Platelets express functional Toll-like receptor-4. Blood 2005; 106: 2417-2423.
- 59 Clark SR, Ma AC, Tavener SA. et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nature Med 2007; 13: 463-469.
- 60 Caudrillier A, Kessenbrock K, Gilliss BM. et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122: 2661-2671.
- 61 Grommes J, Alard JE, Drechsler M. et al. Disruption of platelet-derived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med 2012; 185: 628-636.
- 62 Mei J, Liu Y, Dai N. et al. CXCL5 regulates chemokine scavenging and pulmonary host defense to bacterial infection. Immunity 2010; 33: 106-117.
- 63 Schofield L, Grau GE. Immunological processes in malaria pathogenesis. Nat Rev Immunol 2005; 5: 722-735.
- 64 McMorran BJ, Wieczorski L, Drysdale KE. et al. Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 2012; 338: 1348-1351.
- 65 Srivastava K, Cockburn IA, Swaim A. et al. Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell H Microbe 2008; 4: 179-187.
- 66 Aggrey AA, Srivastava K, Ture S. et al. Platelet Induction of the Acute-Phase Response Is Protective in Murine Experimental Cerebral Malaria. J Immunol. 2013 Epub ahead of print.
- 67 Flaujac C, Boukour S, Cramer-Borde E. Platelets and viruses: an ambivalent relationship. Cell Mol Life Sci 2010; 67: 545-556.
- 68 Zucker-Franklin D, Seremetis S, Zheng ZY. Internalization of human immunodeficiency virus type I and other retroviruses by megakaryocytes and platelets. Blood 1990; 75: 1920-1923.
- 69 Chaipan C, Soilleux EJ, Simpson P. et al. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol 2006; 80: 8951-8960.
- 70 Lusso P. HIV and the chemokine system: 10 years later. Embo J 2006; 25: 447-456.
- 71 Cocchi F, DeVico AL, Garzino-Demo A. et al. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 1995; 270: 1811-1815.
- 72 Roscic-Mrkic B, Fischer M, Leemann C. et al. RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 2003; 102: 1169-1177.
- 73 Holme PA, Muller F, Solum NO. et al. Enhanced activation of platelets with abnormal release of RANTES in human immunodeficiency virus type 1 infection. Faseb J 1998; 12: 79-89.
- 74 Auerbach DJ, Lin Y, Miao H. et al. Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc Natl Acad Sci USA 2012; 109: 9569-9574.
- 75 Weber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res 2005; 96: 612-616.
- 76 Karshovska E, Weber C. Atherosclerosis: cell biology and lipoproteins--new mechanistic links in atherosclerosis: chemokines mediating the effects of lipids, platelets and dendritic cells. Curr Opin Lipidol 2012; 23: 400-401.
- 77 Huo Y, Schober A, Forlow SB. et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003; 9: 61-67.
- 78 von Hundelshausen P, Weber KS, Huo Y. et al. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 2001; 103: 1772-1777.
- 79 Sachais BS, Turrentine T, Dawicki McKenna JM. et al. Elimination of platelet factor 4 (PF4) from platelets reduces atherosclerosis in C57Bl/6 and apoE-/- mice. Thromb Haemost 2007; 98: 1108-1113.
- 80 Koenen RR, von Hundelshausen P, Nesmelova IV. et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15: 97-103.
- 81 Gerdes N, Zhu L, Ersoy M. et al. Platelets regulate CD4(+) T-cell differentiation via multiple chemokines in humans. Thromb Haemost 2011; 106: 353-362.
- 82 Gleissner CA, Shaked I, Erbel C. et al. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ Res 2010; 106: 203-211.
- 83 Gleissner CA, Shaked I, Little KM. et al. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J Immunol 2010; 184: 4810-4818.
- 84 von Hundelshausen P, Koenen RR, Sack M. et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105: 924-930.
- 85 Scheuerer B, Ernst M, Durrbaum-Landmann I. et al. The CXC-chemokine platelet factor 4 promotes monocyte survival and induces monocyte differentiation into macrophages. Blood 2000; 95: 1158-1166.
- 86 Nassar T, Sachais BS, Akkawi S. et al. Platelet factor 4 enhances the binding of oxidized low-density lipoprotein to vascular wall cells. J Biol Chem 2003; 278: 6187-6193.
- 87 Montecucco F, Braunersreuther V, Lenglet S. et al. CC chemokine CCL5 plays a central role impacting infarct size and post-infarction heart failure in mice. Eur Heart J 2012; 33: 1964-1974.
- 88 Hristov M, Zernecke A, Bidzhekov K. et al. Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury. Circ Res 2007; 100: 590-597.
- 89 Smith C, Damas JK, Otterdal K. et al. Increased levels of neutrophil-activating peptide-2 in acute coronary syndromes: possible role of platelet-mediated vascular inflammation. J Am Coll Cardiol 2006; 48: 1591-1599.
- 90 Karshovska E, Zagorac D, Zernecke A. et al. A small molecule CXCR4 antagonist inhibits neointima formation and smooth muscle progenitor cell mobilization after arterial injury. J Thromb Haemost 2008; 6: 1812-1815.
- 91 Zernecke A, Schober A, Bot I. et al. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 2005; 96: 784-791.
- 92 Schober A, Knarren S, Lietz M. et al. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation 2003; 108: 2491-2497.
- 93 Jonnalagadda D, Izu LT, Whiteheart SW. Platelet secretion is kinetically heterogeneous in an agonist-responsive manner. Blood 2012; 120: 5209-5216.
- 94 Weber C, Kraemer S, Drechsler M. et al. Structural determinants of MIF functions in CXCR2-mediated inflammatory and atherogenic leukocyte recruitment. Proc Natl Acad Sci USA 2008; 105: 16278-16283.
- 95 Strüßmann T, Tillmann S, Wirtz T. et al. Platelets are a previously unrecognized source of MIF. Thromb Haemost 2013; 110: 1004-1013.