Platelet chemokines and chemokine receptors, linking hemostasis, inflammation, and host defense

GEAR, ADRIAN R.L.; CAMERINI, DAVID

doi:10.1038/sj.mn.7800198

Cited by 317Platelet Disorders and TreatmentsChemokine receptors and signalingBlood Coagulation and Thrombosis Mechanisms

Platelet chemokines and chemokine receptors, linking hemostasis, inflammation, and host defense

GEAR, ADRIAN R.L., CAMERINI, DAVID·2003·Microcirculation

DOI 10.1038/sj.mn.7800198

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Abstract

Blood platelets play critical roles in hemostasis, providing rapid essential protection against bleeding and catalyzing the important slower formation of stable blood clots via the coagulation cascade. They are also involved in protection from infection by phagocytosis of pathogens and by secreting chemokines that attract leukocytes. Platelet function usually is activated by primary agonists such as adenosine diphosphate (ADP), thrombin, and collagen, whereas secondary agonists like adrenalin do not induce aggregation on their own but become highly effective in the presence of low levels of primary agonists. Current research has revealed that chemokines represent an important additional class of agonists capable of causing significant activation of platelet function. Early work on platelet alpha-granule proteins suggested that platelet factor 4, now known as CXCL4, modulated aggregation and secretion induced by low agonist levels. Subsequent reports revealed the presence in platelets of messenger RNA for several additional chemokines and chemokine receptors. Three chemokines in particular, CXCL12 (SDF-1), CCL17 (TARC), and CCL22 (MDC), recently have been shown to be strong and rapid activators of platelet aggregation and adhesion after their binding to platelet CXCR4 or CCR4, when acting in combination with low levels of primary agonists. CXCL12 can be secreted by endothelial cells and is present in atherosclerotic plaques, whereas CCL17 and CCL22 are secreted by monocytes and macrophages. Platelet activation leads to the release of alpha-granule chemokines, including CCL3 (MIP-1alpha), CCL5 (RANTES), CCL7 (MCP-3), CCL17, CXCL1 (growth-regulated oncogene-alpha), CXCL5 (ENA-78), and CXCL8 (IL-8), which attract leukocytes and further activate other platelets. These findings help to provide a direct linkage between hemostasis, infection, and inflammation and the development of atherosclerosis.

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“Consequent to vascular damage, activated platelets can also release an array of cellular growth factors and angiogenic factors such as PDGF and VEGF, as well as inflammatory mediators such as IL-8 [79,80,81].”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [80]

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Autologous platelets as a source of proteins for healing and tissue regeneration
Anitua, E., Andı́a, I., Ardanza, B., Nurden, P., & Nurden, A. T. (2003) · Thrombosis and Haemostasis · doi:10.1160/th03-07-0440 · Cited by 1,496 · see citing works
Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell–mediated elimination of tumor cells
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Platelets as Immune Cells
von Hundelshausen, P., & Weber, C. (2007) · Circulation Research · doi:10.1161/01.res.0000252802.25497.b7 · Cited by 682 · see citing works
The multifaceted role of fibrinogen in tissue injury and inflammation
Luyendyk, J. P., Schoenecker, J. G., & Flick, M. J. (2018) · Blood · doi:10.1182/blood-2018-07-818211 · Cited by 560 · see citing works
Platelets and wound healing
Alan, T. N. (2008) · Frontiers in bioscience · doi:10.2741/2947 · Cited by 519 · see citing works
Platelet activation leads to activation and propagation of the complement system
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Platelet Microparticles
Mause, S. F., von Hundelshausen, P., Zernecke, A., Koenen, R. R., & Weber, C. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000170133.43608.37 · Cited by 387 · see citing works
Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium
von Hundelshausen, P., Koenen, R. R., Sack, M., Mause, S. F., Adriaens, W., Proudfoot, A. E. I., Hackeng, T. M., & Weber, C. (2005) · Blood · doi:10.1182/blood-2004-06-2475 · Cited by 373 · see citing works
Macrophage Phenotype Modulation by CXCL4 in Atherosclerosis
Gleissner, C. A. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00001 · Cited by 346 · see citing works
Platelet Chemokines in Vascular Disease
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Gene Transfer of Stromal Cell–Derived Factor-1α Enhances Ischemic Vasculogenesis and Angiogenesis via Vascular Endothelial Growth Factor/Endothelial Nitric Oxide Synthase–Related Pathway
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Platelets and Chemokines in Atherosclerosis
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Chemokines
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Role of Platelets in Leukocyte Recruitment and Resolution of Inflammation
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Tissue Factor, Blood Coagulation, and Beyond: An Overview
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Hypoxic mitophagy regulates mitochondrial quality and platelet activation and determines severity of I/R heart injury
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Platelet-vessel wall interactions in atherosclerotic disease
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Plasma Cytokine Concentrations Indicate That <i>In Vivo</i> Hormonal Regulation of Immunity Is Altered During Long-Duration Spaceflight
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Extracorporeal Membrane Oxygenation in the Adult
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Human bone marrow megakaryocytes and platelets express PPARγ, and PPARγ agonists blunt platelet release of CD40 ligand and thromboxanes
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Maternal extracellular vesicles and platelets promote preeclampsia via inflammasome activation in trophoblasts
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CXCL5 Regulates Chemokine Scavenging and Pulmonary Host Defense to Bacterial Infection
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Platelets: essential components of the immune system.
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Role of the platelet chemokine platelet factor 4 (PF4) in hemostasis and thrombosis
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Cytokine Expression Profile of Dengue Patients at Different Phases of Illness
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The role of the CXC chemokines platelet factor-4 (CXCL4/PF-4) and its variant (CXCL4L1/PF-4var) in inflammation, angiogenesis and cancer
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The emerging role of platelets in adaptive immunity
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The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
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Escherichia coli Shiga Toxin Mechanisms of Action in Renal Disease
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Platelet Function in Cardiovascular Disease: Activation of Molecules and Activation by Molecules
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ExperimentalModels of Cerebral Malaria
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Release of potential immunomodulatory factors during platelet storage
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Future innovations in anti‐platelet therapies
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Differential Involvement of the P2Y 1 and P2Y 12 Receptors in Platelet Procoagulant Activity
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Are Platelets Cells? And if Yes, are They Immune Cells?
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Haemolytic uraemic syndrome
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Platelets and Their Interactions with Other Immune Cells
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Platelets support pulmonary recruitment of neutrophils in abdominal sepsis*
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Platelets are an unindicted culprit in the development of endometriosis: clinical and experimental evidence
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Crucial Role of the CCL2/CCR2 Axis in Neointimal Hyperplasia After Arterial Injury in Hyperlipidemic Mice Involves Early Monocyte Recruitment and CCL2 Presentation on Platelets
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Ovarian cancer, the coagulation pathway, and inflammation
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Cytokine release and gastrointestinal symptoms after gluten challenge in celiac disease
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Targeting myeloid cells in the tumor sustaining microenvironment
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Moderation of the platelet releasate response by aspirin
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Platelet secretion in inflammatory and infectious diseases
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Platelet-Leukocyte Interplay in Cancer Development and Progression
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Platelets Are Not Just for Clots
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Serum cytokines associated with severity and complications of kala-azar
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P-selectin
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CXCL4-induced macrophages in human atherosclerosis
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The A2b adenosine receptor protects against vascular injury
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Fibrin(ogen)-α M β 2 Interactions Regulate Leukocyte Function and Innate Immunity In Vivo
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Dietary curcumin inhibits atherosclerosis by affecting the expression of genes involved in leukocyte adhesion and transendothelial migration
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IL-17A and TNF-α Exert Synergistic Effects on Expression of CXCL5 by Alveolar Type II Cells In Vivo and In Vitro
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Impact of brief exercise on circulating monocyte gene and microRNA expression: Implications for atherosclerotic vascular disease
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Platelets: key players in vascular inflammation
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Role of platelets in neuroinflammation: a wide-angle perspective
Horstman, L. L., Jy, W., Ahn, Y. S., Zivadinov, R., Maghzi, A. H., Etemadifar, M., Alexander, J. S., & Minagar, A. (2010) · Journal of Neuroinflammation · doi:10.1186/1742-2094-7-10 · Cited by 104 · see citing works
Recognition of Bacterial Signal Peptides by Mammalian Formyl Peptide Receptors
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Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor
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Elevated Platelet Activation in Patients with Atopic Dermatitis and Psoriasis: Increased Plasma Levels of β-Thromboglobulin and Platelet Factor 4
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Antiplatelet drugs and outcome in mixed admissions to an intensive care unit*
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Platelet–neutrophil interactions under thromboinflammatory conditions
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Platelets in leucocyte recruitment and function
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Treatment With Ezetimibe Plus Low-Dose Atorvastatin Compared With Higher-Dose Atorvastatin Alone
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Platelet-mediated tumor metastasis mechanism and the role of cell adhesion molecules
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Effect of cis-resveratrol on genes involved in nuclear factor kappa B signaling
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The influence of implant surface properties on cell adhesion and proliferation
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Blocking ion channel KCNN4 alleviates the symptoms of experimental autoimmune encephalomyelitis in mice
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CCN2 is necessary for the function of mouse embryonic fibroblasts
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Ability of Platelet-Derived Extracellular Vesicles to Promote Neutrophil-Endothelial Cell Interactions
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Post-translational control of chemokines: a role for decoy receptors?
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Regulated expression of platelet factor 4 in human monocytes—role of PARs as a quantitatively important monocyte activation pathway
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The Inflammatory Role of Platelets in Cystic Fibrosis
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Human platelets target dendritic cell differentiation and production of proinflammatory cytokines
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Conversion of platelets from a proaggregatory to a proinflammatory adhesive phenotype: role of PAF in spatially regulating neutrophil adhesion and spreading
Kulkarni, S., Woollard, K. J., Thomas, S., Oxley, D., & Jackson, S. P. (2007) · Blood · doi:10.1182/blood-2006-08-040980 · Cited by 77 · see citing works
Differential and additive effects of platelet-derived chemokines on monocyte arrest on inflamed endothelium under flow conditions
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Role of Platelets in Inflammation
Arman, M., Payne, H., Ponomaryov, T., & Brill, A. G. (2015) · InTech eBooks · doi:10.5772/60536 · Cited by 78 · see citing works
Platelets Influence Vascularized Organ Transplants from Start to Finish
Kirk, A. D., Morrell, C. N., & Baldwin, W. M. (2008) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2008.02473.x · Cited by 75 · see citing works
Humanization of an Anti-CCR4 Antibody That Kills Cutaneous T-Cell Lymphoma Cells and Abrogates Suppression by T-Regulatory Cells
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Shiga Toxin Pathogenesis: Kidney Complications and Renal Failure
Obrig, T. G., & Karpman, D. (2011) · Current topics in microbiology and immunology · doi:10.1007/82_2011_172 · Cited by 75 · see citing works
Immune functions of platelets
Bode, C., Ahrens, I., & Duerschmied, D. (2014) · Thrombosis and Haemostasis · doi:10.1160/th14-02-0146 · Cited by 75 · see citing works
Platelet‐Activation Mechanisms and Vascular Remodeling
Rubenstein, D. A., & Yin, W. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170049 · Cited by 75 · see citing works
Role of Platelet Cytokines in Dengue Virus Infection
Singh, A., Bisht, P., Bhattacharya, S., & Guchhait, P. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.561366 · Cited by 74 · see citing works
Association of prior antiplatelet agents with mortality in sepsis patients: a nationwide population-based cohort study
Tsai, M.-J., Ou, S., Shih, C.-J., Chao, P.-W., Wang, L.-F., Shih, Y.-N., Li, S., Kuo, S., Hsu, Y.-T., & Chen, Y. (2015) · Intensive Care Medicine · doi:10.1007/s00134-015-3760-y · Cited by 74 · see citing works
Association between statin therapy and outcomes in critically ill patients: a nested cohort study
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Cytokine accumulation in photochemically treated and gamma‐irradiated platelet concentrates during storage
Apelseth, T. O., Hervig, T. A., Wentzel‐Larsen, T., & Bruserud, Ø. (2006) · Transfusion · doi:10.1111/j.1537-2995.2006.00800.x · Cited by 72 · see citing works
Pathogenesis of Human Adenomyosis: Current Understanding and Its Association with Infertility
Khan, K. N., Fujishita, A., & Mori, T. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11144057 · Cited by 74 · see citing works
Low Plasma RANTES Levels Are an Independent Predictor of Cardiac Mortality in Patients Referred for Coronary Angiography
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A Champion of Host Defense: A Generic Large-Scale Cause for Platelet Dysfunction and Depletion in Infection
Page, M. J., & Pretorius, E. (2020) · Seminars in Thrombosis and Hemostasis · doi:10.1055/s-0040-1708827 · Cited by 71 · see citing works
Characterization of the cytokine profile of platelet rich plasma (PRP) and PRP-induced cell proliferation and migration: Upregulation of matrix metalloproteinase-1 and -9 in HaCaT cells
Park, H.-B., Yang, J.-H., & Chung, K.-H. (2011) · The Korean Journal of Hematology · doi:10.5045/kjh.2011.46.4.265 · Cited by 70 · see citing works
The Role of Platelets in Leukocyte Recruitment in Chronic Contact Hypersensitivity Induced by Repeated Elicitation
Tamagawa‐Mineoka, R., Katoh, N., Ueda, E., Takenaka, H., Kita, M., & Kishimoto, S. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060881 · Cited by 70 · see citing works
Platelet activation suppresses HIV-1 infection of T cells
Tsegaye, T. S., Gnirß, K., Rahe‐Meyer, N., Kiene, M., Krämer-Kühl, A., Behrens, G. M. N., Münch, J., & Pöhlmann, S. (2013) · Retrovirology · doi:10.1186/1742-4690-10-48 · Cited by 69 · see citing works
Platelet-Derived Chemokine CXCL7 Dimer Preferentially Exists in the Glycosaminoglycan-Bound Form: Implications for Neutrophil–Platelet Crosstalk
Brown, A. J., Sepuru, K. M., Sawant, K. V., & Rajarathnam, K. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01248 · Cited by 69 · see citing works
Role of Macrophages in Cardioprotection
Yap, J., Cabrera-Fuentes, H. A., Irei, J. S., Hausenloy, D. J., & Boisvert, W. A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102474 · Cited by 69 · see citing works
Multifaceted Roles of Chemokine C-X-C Motif Ligand 7 in Inflammatory Diseases and Cancer
Wu, Q., Tu, H., & Li, J. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.914730 · Cited by 68 · see citing works
Platelet function and HIV: a case–control study
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Antiplatelet Therapy Is Associated With Decreased Transfusion-Associated Risk of Lung Dysfunction, Multiple Organ Failure, and Mortality in Trauma Patients*
Harr, J. N., Moore, E. E., Johnson, J. L., Chin, T. L., Wohlauer, M. V., Maier, R. V., Cuschieri, J., Sperry, J. L., Banerjee, A. M., Silliman, C. C., et al. (2012) · Critical Care Medicine · doi:10.1097/ccm.0b013e31826ab38b · Cited by 66 · see citing works
CXCR4 blockade induces atherosclerosis by affecting neutrophil function
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Outcomes of Severe Sepsis and Septic Shock Patients on Chronic Antiplatelet Treatment: A Historical Cohort Study
Valerio-Rojas, J. C., Jaffer‐Sathick, I., Kor, D. J., Gajic, O., & Cartin‐Ceba, R. (2013) · Critical Care Research and Practice · doi:10.1155/2013/782573 · Cited by 65 · see citing works

Functional expression of CCR1, CCR3, CCR4, and CXCR4 chemokine receptors on human platelets
Clemetson, K. J., Clemetson, J. M., Proudfoot, A. E. I., Power, C., Baggiolini, M., & Wells, T. N. C. (2000) · Blood · doi:10.1182/blood.v96.13.4046 · Cited by 272 · see citing works
Stromal cell–derived factor-1 and macrophage-derived chemokine: 2 chemokines that activate platelets
Kowalska, M. A., Ratajczak, M. Z., Majka, M., Jin, J., Kunapuli, S. P., Brass, L. F., & Poncz, M. (2000) · Blood · doi:10.1182/blood.v96.1.50.013k40_50_57 · Cited by 128 · see citing works
Adenosine diphosphate strongly potentiates the ability of the chemokines MDC, TARC, and SDF-1 to stimulate platelet function
Gear, A. R. L., Suttitanamongkol, S., Viisoreanu, D., Polanowska‐Grabowska, R., Raha, S., & Camerini, D. (2001) · Blood · doi:10.1182/blood.v97.4.937 · Cited by 98 · see citing works
Self-citation
HEMOSTASIS, THROMBOSIS, AND VASCULAR BIOLOGY Adenosine diphosphate strongly potentiates the ability of the chemokines MDC, TARC, and SDF-1 to stimulate platelet function
Gear, A. R. L., Suttitanamongkol, S., Viisoreanu, D., Polanowska‐Grabowska, R., Raha, S., & Camerini, D. (2016)
Self-citation
Platelet Chemokines in Vascular Disease
Gleissner, C. A., von Hundelshausen, P., & Ley, K. F. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.169417 · Cited by 313 · see citing works

Authors: GEAR, A. R. L., & CAMERINI, D.
Affiliations: University of Virginia (US)
Corresponding author: GEAR, ADRIAN R.L.
ORCID: CAMERINI, DAVID
Venue: Microcirculation
Publisher: Wiley
Published: 2003-07
Volume: 10
Issue: 3-4
Pages: 335-350
ISSN: 1073-9688 (ISSN-L)
1549-8719
DOI: 10.1038/sj.mn.7800198
OpenAlex: W2001798594
Cited by: 317
References: 161
Citations by year: 2026: 4 · 2025: 4 · 2024: 10 · 2023: 4 · 2022: 10 · 2021: 13 · 2020: 13 · 2019: 7 · 2018: 10 · 2017: 13 · 2016: 17 · 2015: 28 · 2014: 18 · 2013: 6 · 2012: 21
FWCI: 2.80
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 2401 d)
Locations: Microcirculation (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (1r29ai039943-01a1)
National Institute of Allergy and Infectious Diseases (AI 39943)
National Institute of Diabetes and Digestive and Kidney Diseases (DK59004)
Topics: Health Sciences › Medicine › Hematology › Platelet Disorders and Treatments
Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
Health Sciences › Medicine › Hematology › Blood Coagulation and Thrombosis Mechanisms
Keywords: chemokine receptors, platelet activation, platelet aggregation, hemostasis, inflammation, host defense, CXCL12, CCL17, CCL22, CXCR4, CCR4, alpha-granule proteins, atherosclerosis, leukocyte recruitment, platelet factor 4, CCL3, RANTES, CCL7, interleukin-8
MeSH terms: Blood Platelets, Hemostasis, Humans, Immunity, Inflammation, Chemokines, Receptors, Chemokine

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Platelet chemokines and chemokine receptors, linking hemostasis, inflammation, and host defense

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