Platelet chemokines in health and disease

Ela Karshovska; Christian Weber; Philipp von Hundelshausen

doi:10.1160/TH13-04-0341

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2013; 110(05): 894-902
DOI: 10.1160/TH13-04-0341

Theme Issue Article

Schattauer GmbH

Platelet chemokines in health and disease

Ela Karshovska

¹Institute for Cardiovascular Prevention, Ludwig-Maximilians University (LMU) Munich, Germany

,

Christian Weber

¹Institute for Cardiovascular Prevention, Ludwig-Maximilians University (LMU) Munich, Germany

,

Philipp von Hundelshausen

¹Institute for Cardiovascular Prevention, Ludwig-Maximilians University (LMU) Munich, Germany

› Author Affiliations

Abstract

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.

Keywords

Platelet immunology - chemokines - atherosclerosis - inflammation - infectious diseases

Full Text

References

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.