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Thromboinflammation: An Evolving Multifaceted Concept
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Thromboinflammation: An Evolving Multifaceted Concept

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Pathology, Diagnostics, and Therapeutics".

Deadline for manuscript submissions: closed (15 January 2023) | Viewed by 12963

Special Issue Editors

Dr. Gianni Francesco Guidetti

E-Mail Website
Guest Editor
Laboratory of Biochemistry, Department of Biology and Biotechnology “L. Spallanzani”, University of Pavia, 27100 Pavia, Italy
Interests: signal transduction; thrombosis; cancer researches; breast cancer cell
Dr. Silvia Stella Barbieri

E-Mail Website1 Website2
Guest Editor
Unit of Head of Brain-Heart Axis: Cellular and Molecular Mechanisms, Centro Cardiologico Monzino IRCCS, Via C. Parea, 4_20138 Milano, Italy
Interests: thrombosis; platelets; coagulation; extracellular vesicles; neurotrophins; oxidative stress; animal models; cellular models; behavioural and psychological factors; vascular biology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Thrombosis and inflammation have historically been investigated as separated processes in vascular biology. More recently, the complex picture embracing thrombus formation, coagulation activation, and innate and adaptive immunity is often indicated using terms such as thromboinflammation, immunothrombosis and immunohemostasis. These definitions aim to describe the vicious cycle in which inflammation triggers a pro-thrombotic state, while thrombosis in turn potentiates inflammation. Thromboinflammation is triggered by blood vessel injury, pathogen invasion, and inflammatory stimuli. From an evolutionary point of view, thromboinflammatory responses likely evolved to limit infections by capturing pathogens in clots, but when exaggerated they may cause disorders associated with high morbidity and mortality. Several pathological conditions, including stroke, deep vein thrombosis, myocardial infarction, bacteremia, and viremia, evolve in the context of thromboinflammation. Improving our knowledge on this process may lead to the development of novel therapeutic approaches. To understand thromboinflammation, it is vital to look deeply at the interactions between platelets, white blood cells, and endothelial cells, and between such host components and pathogens. Several classes of receptors and signal transduction pathways are likely involved in the generation of thromboinflammation, but the underlying molecular mechanisms are mostly unknown. This Special Issue will focus on most recent advances in the study of the molecular mechanisms supporting thromboinflammation. Both original research and review articles as well as short communications are strongly encouraged. Methodological studies focusing on new models and research techniques to study these aspects are also welcome.

Dr. Gianni Francesco Guidetti
Dr. Silvia Stella Barbieri
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • thromboinflammation
  • immunothrombosis
  • venous and arterial thrombosis
  • coagulation
  • inflammation
  • innate and adaptive immunity mood disorders
  • stroke
  • myocardial infarction
  • bacteremia
  • viremia
  • platelets
  • leukocytes
  • endothelial cells
  • signal transduction
  • cells receptors
  • extracellular vesicles

Published Papers (6 papers)

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Research

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10 pages, 804 KiB  
Article
Anticoagulation Monitoring with Activated Partial ThromboPlastin Time and Anti-Xa Activity in Intensive Care Unit Patients: Interest of Thrombin Generation Assay
by Paul Billoir, Thomas Elie, Jerrold H. Levy, Emmanuel Besnier, Bertrand Dureuil, Benoit Veber, Véronique Le Cam-Duchez and Thomas Clavier
Int. J. Mol. Sci. 2022, 23(19), 11219; https://doi.org/10.3390/ijms231911219 - 23 Sep 2022
Cited by 1 | Viewed by 2080
Abstract
Current guidelines recommend monitoring the anticoagulant effect of unfractionated heparin (UFH) by measuring anti-Xa activity rather than activated partial thromboplastin time (aPTT) in intensive care unit (ICU) patients. The primary objective of this study was to evaluate the correlation of aPTT, anti-Xa activity, [...] Read more.
Current guidelines recommend monitoring the anticoagulant effect of unfractionated heparin (UFH) by measuring anti-Xa activity rather than activated partial thromboplastin time (aPTT) in intensive care unit (ICU) patients. The primary objective of this study was to evaluate the correlation of aPTT, anti-Xa activity, and thrombin generation in UFH-treated ICU patients. A prospective observational pilot study was conducted in adult surgical ICU patients treated with UFH. aPTT and anti-Xa activity were monitored daily. The therapeutic target was aPTT between 50 s and 84 s, and/or anti-Xa between 0.3 and 0.7 U/mL. Correlation among aPTT, anti-Xa activity, and thrombin generation was determined by measuring endogenous thrombin potential (ETP), with the inflammatory response evaluated. C-reactive protein (CRP) was used as a marker of inflammatory response. The plasma of 107 samples from 30 ICU patients was analyzed. The correlation between aPTT and anti-Xa activity was 0.66, CI95% [0.54;0.76] (p < 0.0001). Although thrombin generation, aPTT, and anti-Xa were correlated with inflammatory responses, the correlation was higher with thrombin generation and anti-Xa activity compared to aPTT. When aPTT was in a therapeutic range, a low thrombin generation was observed but was 50% inhibited when anti-Xa was in a therapeutic range. Coagulation testing with aPTT, anti-Xa correlated with thrombin generation. A 50% decrease in thrombin generation was observed when anti-Xa was within a therapeutic range. Further work is needed to evaluate coagulation biomarker responses and clinical outcomes in specific ICU populations. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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Review

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26 pages, 3123 KiB  
Review
Crosstalk of Inflammation and Coagulation in Bothrops Snakebite Envenoming: Endogenous Signaling Pathways and Pathophysiology
by Joeliton S. Cavalcante, Denis Emanuel Garcia de Almeida, Norival A. Santos-Filho, Marco Aurélio Sartim, Amanda de Almeida Baldo, Lisele Brasileiro, Polianna L. Albuquerque, Sâmella S. Oliveira, Jacqueline Almeida Gonçalves Sachett, Wuelton Marcelo Monteiro and Rui Seabra Ferreira, Jr.
Int. J. Mol. Sci. 2023, 24(14), 11508; https://doi.org/10.3390/ijms241411508 - 15 Jul 2023
Cited by 4 | Viewed by 2250
Abstract
Snakebite envenoming represents a major health problem in tropical and subtropical countries. Considering the elevated number of accidents and high morbidity and mortality rates, the World Health Organization reclassified this disease to category A of neglected diseases. In Latin America, Bothrops genus snakes [...] Read more.
Snakebite envenoming represents a major health problem in tropical and subtropical countries. Considering the elevated number of accidents and high morbidity and mortality rates, the World Health Organization reclassified this disease to category A of neglected diseases. In Latin America, Bothrops genus snakes are mainly responsible for snakebites in humans, whose pathophysiology is characterized by local and systemic inflammatory and degradative processes, triggering prothrombotic and hemorrhagic events, which lead to various complications, organ damage, tissue loss, amputations, and death. The activation of the multicellular blood system, hemostatic alterations, and activation of the inflammatory response are all well-documented in Bothrops envenomings. However, the interface between inflammation and coagulation is still a neglected issue in the toxinology field. Thromboinflammatory pathways can play a significant role in some of the major complications of snakebite envenoming, such as stroke, venous thromboembolism, and acute kidney injury. In addition to exacerbating inflammation and cell interactions that trigger vaso-occlusion, ischemia–reperfusion processes, and, eventually, organic damage and necrosis. In this review, we discuss the role of inflammatory pathways in modulating coagulation and inducing platelet and leukocyte activation, as well as the inflammatory production mediators and induction of innate immune responses, among other mechanisms that are altered by Bothrops venoms. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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18 pages, 1632 KiB  
Review
Blood Platelets in Infection: The Multiple Roles of the Platelet Signalling Machinery
by Silvia M. G. Trivigno, Gianni Francesco Guidetti, Silvia Stella Barbieri and Marta Zarà
Int. J. Mol. Sci. 2023, 24(8), 7462; https://doi.org/10.3390/ijms24087462 - 18 Apr 2023
Cited by 6 | Viewed by 1947
Abstract
Platelets are classically recognized for their important role in hemostasis and thrombosis but they are also involved in many other physiological and pathophysiological processes, including infection. Platelets are among the first cells recruited to sites of inflammation and infection and they exert their [...] Read more.
Platelets are classically recognized for their important role in hemostasis and thrombosis but they are also involved in many other physiological and pathophysiological processes, including infection. Platelets are among the first cells recruited to sites of inflammation and infection and they exert their antimicrobial response actively cooperating with the immune system. This review aims to summarize the current knowledge on platelet receptor interaction with different types of pathogens and the consequent modulations of innate and adaptive immune responses. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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17 pages, 1816 KiB  
Review
Frail Silk: Is the Hughes-Stovin Syndrome a Behçet Syndrome Subtype with Aneurysm-Involved Gene Variants?
by Simona Manole, Raluca Rancea, Romana Vulturar, Siao-Pin Simon, Adrian Molnar and Laura Damian
Int. J. Mol. Sci. 2023, 24(4), 3160; https://doi.org/10.3390/ijms24043160 - 5 Feb 2023
Cited by 3 | Viewed by 2046
Abstract
Hughes-Stovin syndrome is a rare disease characterized by thrombophlebitis and multiple pulmonary and/or bronchial aneurysms. The etiology and pathogenesis of HSS are incompletely known. The current consensus is that vasculitis underlies the pathogenic process, and pulmonary thrombosis follows arterial wall inflammation. As such, [...] Read more.
Hughes-Stovin syndrome is a rare disease characterized by thrombophlebitis and multiple pulmonary and/or bronchial aneurysms. The etiology and pathogenesis of HSS are incompletely known. The current consensus is that vasculitis underlies the pathogenic process, and pulmonary thrombosis follows arterial wall inflammation. As such, Hughes-Stovin syndrome may belong to the vascular cluster with lung involvement of Behçet syndrome, although oral aphtae, arthritis, and uveitis are rarely found. Behçet syndrome is a multifactorial polygenic disease with genetic, epigenetic, environmental, and mostly immunological contributors. The different Behçet syndrome phenotypes are presumably based upon different genetic determinants involving more than one pathogenic pathway. Hughes-Stovin syndrome may have common pathways with fibromuscular dysplasias and other diseases evolving with vascular aneurysms. We describe a Hughes-Stovin syndrome case fulfilling the Behçet syndrome criteria. A MYLK variant of unknown significance was detected, along with other heterozygous mutations in genes that may impact angiogenesis pathways. We discuss the possible involvement of these genetic findings, as well as other potential common determinants of Behçet/Hughes-Stovin syndrome and aneurysms in vascular Behçet syndrome. Recent advances in diagnostic techniques, including genetic testing, could help diagnose a specific Behçet syndrome subtype and other associated conditions to personalize the disease management. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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18 pages, 1187 KiB  
Review
Immunothrombosis and the Role of Platelets in Venous Thromboembolic Diseases
by Marco Heestermans, Géraldine Poenou, Anne-Claire Duchez, Hind Hamzeh-Cognasse, Laurent Bertoletti and Fabrice Cognasse
Int. J. Mol. Sci. 2022, 23(21), 13176; https://doi.org/10.3390/ijms232113176 - 29 Oct 2022
Cited by 10 | Viewed by 2131
Abstract
Venous thromboembolism (VTE) is the third leading cardiovascular cause of death and is conventionally treated with anticoagulants that directly antagonize coagulation. However, recent data have demonstrated that also platelets play a crucial role in VTE pathophysiology. In the current review, we outline how [...] Read more.
Venous thromboembolism (VTE) is the third leading cardiovascular cause of death and is conventionally treated with anticoagulants that directly antagonize coagulation. However, recent data have demonstrated that also platelets play a crucial role in VTE pathophysiology. In the current review, we outline how platelets are involved during all stages of experimental venous thrombosis. Platelets mediate initiation of the disease by attaching to the vessel wall upon which they mediate leukocyte recruitment. This process is referred to as immunothrombosis, and within this novel concept inflammatory cells such as leukocytes and platelets directly drive the progression of VTE. In addition to their involvement in immunothrombosis, activated platelets can directly drive venous thrombosis by supporting coagulation and secreting procoagulant factors. Furthermore, fibrinolysis and vessel resolution are (partly) mediated by platelets. Finally, we summarize how conventional antiplatelet therapy can prevent experimental venous thrombosis and impacts (recurrent) VTE in humans. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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Other

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10 pages, 1744 KiB  
Opinion
Evolutionary Insight into Immunothrombosis as a Healing Mechanism
by Eduardo Anitua, Roberto Prado and Sabino Padilla
Int. J. Mol. Sci. 2022, 23(15), 8346; https://doi.org/10.3390/ijms23158346 - 28 Jul 2022
Cited by 1 | Viewed by 1405
Abstract
Both invertebrates and vertebrates possess a cluster of immediate and local wound-sealing, pathogen-killing, and tissue healing responses known as immunoclotting and immunothrombosis, respectively, to cope with two life-threatening emergencies, namely, bleeding and microbial invasion. Despite their convergence in function, immunoclotting and immunothrombosis are [...] Read more.
Both invertebrates and vertebrates possess a cluster of immediate and local wound-sealing, pathogen-killing, and tissue healing responses known as immunoclotting and immunothrombosis, respectively, to cope with two life-threatening emergencies, namely, bleeding and microbial invasion. Despite their convergence in function, immunoclotting and immunothrombosis are deployed by different blood cells and intravascular multidomain proteins. In vertebrates, these proteins share some domains with intrinsic chemical affinities useful in generating cooperative networks such as pathogen and damage pattern recognition molecules. Moreover, many of the proteins involved in coagulation and fibrinolysis in humans are multifunctional molecules playing roles in other processes from inflammation to healing and beyond. In our modern society, however, the interaction of activated intravascular allosteric proteins with one another and with blood cells entails vulnerabilities posing a biological paradox: intravascular proteins that locally operate as tissue repair enhancers can nevertheless generate pathogenic processes by acting systemically. In this manuscript, we contextualize and frame the coagulation system and hemostasis through an evolutionary time scale, illustrating their role as dual players in the defense against exsanguination and pathogens while significantly influencing wound healing. Full article
(This article belongs to the Special Issue Thromboinflammation: An Evolving Multifaceted Concept)
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