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Article ; Online: Platelet count, temperature and pH value differentially affect hemostatic and immunomodulatory functions of platelets.

Schmuckenschlager, Anna / Pirabe, Anita / Assinger, Alice / Schrottmaier, Waltraud C

2023 Volume 223, Page(s) 111–122

Abstract: Platelets are primarily recognized for their role in hemostasis, but also regulate immune responses by interacting with leukocytes. Their highly sensitive nature enables platelets to rapidly respond to micro-environmental changes, which is crucial under ... ...

Abstract	Platelets are primarily recognized for their role in hemostasis, but also regulate immune responses by interacting with leukocytes. Their highly sensitive nature enables platelets to rapidly respond to micro-environmental changes, which is crucial under physiological condition but can jeopardize in vitro analyses. Thus, we tested how platelet count and changes in pH and temperatures, which are commonly experienced during inflammation and infection but also affected by ex vivo analyses, influence platelet-leukocyte interaction and immunomodulation. Reducing platelet count by up to 90 % slightly decreased platelet activation and platelet-leukocyte aggregate formation, but did not affect CD11b activation nor CD62L shedding of monocytes or neutrophils. Acidosis (pH 6.9) slightly elevated platelet degranulation and binding to innate leukocytes, though pH changes did not modulate leukocyte activation. While platelet responsiveness was higher at room temperature than at 37 °C, incubation temperature did not affect platelet-leukocyte aggregate formation. In contrast, platelet-mediated CD11b activation and CD62L expression increased with temperature. Our data thus demonstrate the importance of standardized protocols for sample preparation and assay procedure to obtain comparable data. Further, unspecific physiologic responses such as thrombocytopenia, acidosis or temperature changes may contribute to platelet dysfunction and altered platelet-mediated immunomodulation in inflammatory and infectious disease.
MeSH term(s)	Humans ; Temperature ; Platelet Count ; Hemostatics/metabolism ; Blood Platelets/metabolism ; Platelet Activation ; Hemostasis ; Leukocytes/metabolism ; Immunity ; Acidosis/metabolism ; Hydrogen-Ion Concentration
Chemical Substances	Hemostatics
Language	English
Publishing date	2023-01-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	121852-9
ISSN	1879-2472 ; 0049-3848
ISSN (online)	1879-2472
ISSN	0049-3848
DOI	10.1016/j.thromres.2023.01.026
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Article ; Online: Platelets in Viral Infections - Brave Soldiers or Trojan Horses.

Schrottmaier, Waltraud C / Schmuckenschlager, Anna / Pirabe, Anita / Assinger, Alice

Frontiers in immunology

2022 Volume 13, Page(s) 856713

Abstract: Viral infections are often associated with platelet activation and haemostatic complications. In line, low platelet counts represent a hallmark for poor prognosis in many infectious diseases. The underlying cause of platelet dysfunction in viral ... ...

Abstract	Viral infections are often associated with platelet activation and haemostatic complications. In line, low platelet counts represent a hallmark for poor prognosis in many infectious diseases. The underlying cause of platelet dysfunction in viral infections is multifaceted and complex. While some viruses directly interact with platelets and/or megakaryocytes to modulate their function, also immune and inflammatory responses directly and indirectly favour platelet activation. Platelet activation results in increased platelet consumption and degradation, which contributes to thrombocytopenia in these patients. The role of platelets is often bi-phasic. Initial platelet hyper-activation is followed by a state of platelet exhaustion and/or hypo-responsiveness, which together with low platelet counts promotes bleeding events. Thereby infectious diseases not only increase the thrombotic but also the bleeding risk or both, which represents a most dreaded clinical complication. Treatment options in these patients are limited and new therapeutic strategies are urgently needed to prevent adverse outcome. This review summarizes the current literature on platelet-virus interactions and their impact on viral pathologies and discusses potential intervention strategies. As pandemics and concomitant haemostatic dysregulations will remain a recurrent threat, understanding the role of platelets in viral infections represents a timely and pivotal challenge.
MeSH term(s)	Blood Platelets ; Hemostatics ; Humans ; Thrombocytopenia ; Virus Diseases ; Viruses
Chemical Substances	Hemostatics
Language	English
Publishing date	2022-03-28
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.856713
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Article ; Online: Age-Dependent Surface Receptor Expression Patterns in Immature Versus Mature Platelets in Mouse Models of Regenerative Thrombocytopenia.

Pirabe, Anita / Frühwirth, Sabine / Brunnthaler, Laura / Hackl, Hubert / Schmuckenschlager, Anna / Schrottmaier, Waltraud C / Assinger, Alice

Cells

2023 Volume 12, Issue 19

Abstract: Aging is a multifaceted process that unfolds at both the individual and cellular levels, resulting in changes in platelet count and platelet reactivity. These alterations are influenced by shifts in platelet production, as well as by various ... ...

Abstract	Aging is a multifaceted process that unfolds at both the individual and cellular levels, resulting in changes in platelet count and platelet reactivity. These alterations are influenced by shifts in platelet production, as well as by various environmental factors that affect circulating platelets. Aging also triggers functional changes in platelets, including a reduction in RNA content and protein production capacity. Older individuals and RNA-rich immature platelets often exhibit hyperactivity, contributing significantly to pathologic conditions such as cardiovascular diseases, sepsis, and thrombosis. However, the impact of aging on surface receptor expression of circulating platelets, particularly whether these effects vary between immature and mature platelets, remains largely unexplored. Thus, we investigated the expression of certain surface and activation receptors on platelets from young and old mice as well as on immature and mature platelets from mouse models of regenerative thrombocytopenia by flow cytometry. Our findings indicate that aged mice show an upregulated expression of the platelet endothelial cell adhesion molecule-1 (CD31), tetraspanin-29 (CD9), and Toll-like receptor 2 (TLR2) compared to their younger counterparts. Interestingly, when comparing immature and mature platelets in both young and old mice, no differences were observed in mature platelets. However, immature platelets from young mice displayed higher surface expression compared to immature platelets from old mice. Additionally, in mouse models of regenerative thrombocytopenia, the majority of receptors were upregulated in immature platelets. These results suggest that distinct surface receptor expressions are increased on platelets from old mice and immature platelets, which may partially explain their heightened activity and contribute to an increased thrombotic risk.
MeSH term(s)	Mice ; Animals ; Receptor for Advanced Glycation End Products/metabolism ; Blood Platelets/metabolism ; Thrombocytopenia/metabolism ; Platelet Count ; RNA/metabolism
Chemical Substances	Receptor for Advanced Glycation End Products ; RNA (63231-63-0)
Language	English
Publishing date	2023-10-08
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells12192419
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Article: Horizontal MicroRNA Transfer by Platelets - Evidence and Implications.

Mussbacher, Marion / Pirabe, Anita / Brunnthaler, Laura / Schrottmaier, Waltraud C / Assinger, Alice

Frontiers in physiology

2021 Volume 12, Page(s) 678362

Abstract: For decades, platelets have been known for their central role in hemostasis and their ability to release bioactive molecules, allowing inter-platelet communication and crosstalk with the immune system and vascular cells. However, with the detection of ... ...

Abstract	For decades, platelets have been known for their central role in hemostasis and their ability to release bioactive molecules, allowing inter-platelet communication and crosstalk with the immune system and vascular cells. However, with the detection of microRNAs in platelets and platelet-derived microvesicles (MVs), a new level of inter-cellular regulation was revealed. By shedding MVs from their plasma membrane, platelets are able to release functional microRNA complexes that are protected from plasma RNases. Upon contact with macrophages, endothelial cells and smooth muscle cells platelet microRNAs are rapidly internalized and fine-tune the functionality of the recipient cell by post-transcriptional reprogramming. Moreover, microRNA transfer by platelet MVs allows infiltration into tissues with limited cellular access such as solid tumors, thereby they not only modulate tumor progression but also provide a potential route for drug delivery. Understanding the precise mechanisms of horizontal transfer of platelet microRNAs under physiological and pathological conditions allows to design side-specific therapeutic (micro)RNA delivery systems. This review summarizes the current knowledge and the scientific evidence of horizontal microRNA transfer by platelets and platelet-derived MVs into vascular and non-vascular cells and its physiological consequences.
Language	English
Publishing date	2021-06-03
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2021.678362
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Article ; Online: Comprehensive Characterization of Platelet-Enriched MicroRNAs as Biomarkers of Platelet Activation.

Krammer, Teresa L / Zeibig, Stephan / Schrottmaier, Waltraud C / Pirabe, Anita / Goebel, Silvia / Diendorfer, Andreas B / Holthoff, Hans-Peter / Assinger, Alice / Hackl, Matthias

Cells

2022 Volume 11, Issue 8

Abstract: Dysregulation of platelet function is causally connected to thrombus formation and cardiovascular diseases. Therefore, assessing platelet reactivity is crucial. However, current platelet function tests come with pitfalls, limiting clinical use. Plasma ... ...

Abstract	Dysregulation of platelet function is causally connected to thrombus formation and cardiovascular diseases. Therefore, assessing platelet reactivity is crucial. However, current platelet function tests come with pitfalls, limiting clinical use. Plasma miRNA signatures have been suggested as novel biomarkers for predicting/diagnosing cardiovascular diseases and monitoring antiplatelet therapy. Here, we provide results from a comprehensive study on the feasibility of using circulatory platelet miRNAs as surrogate markers of platelet activation. We performed small RNA-Seq on different blood cell types to confirm known and identify novel platelet-enriched miRNAs and validated a panel of 16 miRNAs using RT-qPCR. To identify the main carrier of these blood-based platelet miRNAs, we enriched and analyzed distinct microvesicle populations. Platelets were stimulated with GPVI and P2Y12 agonists in vitro to monitor the release of the selected miRNAs following activation. Finally, the miRNA panel was also measured in plasma from mice undergoing the Folts intervention (recurrent thrombus formation in the carotid artery). Applying an unbiased bioinformatics-supported workflow to our NGS data, we were able to confirm a panel of previously established miRNA biomarker candidates and identify three new candidates (i.e., miR-199a-3p, miR-151a-5p, and miR-148b-3p). Basal levels of platelet-derived miRNAs in plasma were mainly complexed with proteins, not extracellular vesicles. We show that changes in miRNA levels due to platelet activation are detectable using RT-qPCR. In addition, we highlight limitations of studying the in vitro release of miRNAs from platelets. In vivo thrombosis resulted in significant elevations of platelet-derived miRNA levels in mice. In conclusion, we provide in-depth evidence that activated platelets release miRNAs, resulting in measurable changes in circulatory miRNA levels, rendering them promising biomarker candidates.
MeSH term(s)	Animals ; Biomarkers/metabolism ; Blood Platelets/metabolism ; Cardiovascular Diseases/metabolism ; Mice ; MicroRNAs/metabolism ; Platelet Activation
Chemical Substances	Biomarkers ; MicroRNAs
Language	English
Publishing date	2022-04-07
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells11081254
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Article ; Online: Immunoglobulin G production in COVID-19 - associations with age, outcome, viral persistence, inflammation and pro-thrombotic markers.

Pirabe, Anita / Schrottmaier, Waltraud C / Heber, Stefan / Schmuckenschlager, Anna / Treiber, Sonja / Pereyra, David / Santol, Jonas / Pawelka, Erich / Traugott, Marianna / Schörgenhofer, Christian / Seitz, Tamara / Karolyi, Mario / Jilma, Bernd / Resch, Ulrike / Zoufaly, Alexander / Assinger, Alice

Journal of infection and public health

2023 Volume 16, Issue 3, Page(s) 384–392

Abstract: Age represents the major risk factor for fatal disease outcome in coronavirus disease (COVID-19) due to age-related changes in immune responses. On the one hand lymphocyte counts continuously decline with advancing age, on the other hand somatic hyper- ... ...

Abstract	Age represents the major risk factor for fatal disease outcome in coronavirus disease (COVID-19) due to age-related changes in immune responses. On the one hand lymphocyte counts continuously decline with advancing age, on the other hand somatic hyper-mutations of B-lymphocytes and levels of class-switched antibodies diminish, resulting in lower neutralizing antibody titers. To date the impact of age on immunoglobulin G (IgG) production in response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is unknown. Therefore, we investigated the impact of age on the onset of IgG production and its association with outcome, viral persistence, inflammatory and thrombotic markers in consecutive, hospitalized COVID-19 patients admitted to the Clinic Favoriten (Vienna, Austria) between April and October 2020 that fulfilled predefined inclusion criteria. Three different IgGs against SARS-CoV-2 (spike protein S1, nucleocapsid (NC), and the spike protein receptor binding domain (RBD)) were monitored in plasma of 97 patients upon admission and three times within the first week followed by weekly assessment during their entire hospital stay. We analyzed the association of clinical parameters including C-reactive protein (CRP), D-dimer levels and platelet count as well as viral persistence with the onset and concentration of different anti-SARS-CoV-2 specific IgGs. Our data demonstrate that in older individuals anti-SARS-CoV-2 IgG production increases earlier after symptom onset and that deceased patients have the highest amount of antibodies against SARS-CoV-2 whereas intensive care unit (ICU) survivors have the lowest titers. In addition, anti-SARS-CoV-2 IgG concentrations are not associated with curtailed viral infectivity, inflammatory or thrombotic markers, suggesting that not only serological memory but also other adaptive immune responses are involved in successful viral killing and protection against a severe COVID-19 infection.
MeSH term(s)	Humans ; Aged ; SARS-CoV-2 ; COVID-19 ; Immunoglobulin G ; Spike Glycoprotein, Coronavirus ; Inflammation ; Antibodies, Viral
Chemical Substances	Immunoglobulin G ; Spike Glycoprotein, Coronavirus ; Antibodies, Viral ; spike protein, SARS-CoV-2
Language	English
Publishing date	2023-01-21
Publishing country	England
Document type	Journal Article
ZDB-ID	2467587-8
ISSN	1876-035X ; 1876-0341
ISSN (online)	1876-035X
ISSN	1876-0341
DOI	10.1016/j.jiph.2023.01.016
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Article ; Online: Intrahepatic neutrophil accumulation and extracellular trap formation are associated with posthepatectomy liver failure.

Brunnthaler, Laura / Pereyra, David / Brenner, Miriam / Santol, Jonas / Herrmann, Lukas / Schrottmaier, Waltraud C / Pirabe, Anita / Schmuckenschlager, Anna / Kim, Sarang / Kern, Anna Emilia / Huber, Felix Xaver / Michels, Lisa Emilie / Brostjan, Christine / Salzmann, Manuel / Hohensinner, Philipp / Kain, Renate / Gruenberger, Thomas / Starlinger, Patrick / Assinger, Alice

Hepatology communications

2023 Volume 8, Issue 1

Abstract: Background: Posthepatectomy liver failure (PHLF) represents a life-threatening complication with limited therapeutic options. Neutrophils play a critical and dynamic role during regeneratory processes, but their role in human liver regeneration is ... ...

Abstract	Background: Posthepatectomy liver failure (PHLF) represents a life-threatening complication with limited therapeutic options. Neutrophils play a critical and dynamic role during regeneratory processes, but their role in human liver regeneration is incompletely understood, especially as underlying liver disease, detectable in the majority of patients, critically affects hepatic regeneration. Here we explored intrahepatic neutrophil accumulation and neutrophil extracellular traps (NETs) in patients with PHLF and validated the functional relevance of NETs in a murine partial hepatectomy (PHx) model. Methods: We investigated the influx of neutrophils, macrophages, eosinophils, and mast cells and the presence of their respective extracellular traps in liver biopsies of 35 patients undergoing hepatectomy (10 patients with PHLF) before and after the initiation of liver regeneration by fluorescence microscopy. In addition, NET formation and neutrophil activation were confirmed by plasma analysis of 99 patients (24 patients with PHLF) before and up to 5 days after surgery. Furthermore, we inhibited NETs via DNase I in a murine PHx model of mice with metabolically induced liver disease. Results: We detected rapid intrahepatic neutrophil accumulation, elevated levels of myeloperoxidase release, and NET formation in regenerating human livers, with a significantly higher increase of infiltrating neutrophils and NETs in patients with PHLF. Circulating markers of neutrophil activation, including elastase, myeloperoxidase, and citrullinated histone H3, correlated with markers of liver injury. In a murine PHx model, we showed that the inhibition of NET accelerated hepatocyte proliferation and liver regeneration. Conclusions: Patients with PHLF showed accelerated intrahepatic neutrophil infiltration and NET formation, which were associated with liver damage. Further, we identified postsurgical myeloperoxidase levels as predictive markers for adverse outcomes and observed that blocking NETs in a murine PHx model accelerated tissue regeneration.
MeSH term(s)	Humans ; Animals ; Mice ; Neutrophils ; Extracellular Traps ; Liver Failure/etiology ; Focal Nodular Hyperplasia ; Peroxidase
Chemical Substances	Peroxidase (EC 1.11.1.7)
Language	English
Publishing date	2023-12-15
Publishing country	United States
Document type	Journal Article
ISSN	2471-254X
ISSN (online)	2471-254X
DOI	10.1097/HC9.0000000000000348
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Article ; Online: Age Related Differences in Monocyte Subsets and Cytokine Pattern during Acute COVID-19-A Prospective Observational Longitudinal Study.

Pirabe, Anita / Heber, Stefan / Schrottmaier, Waltraud C / Schmuckenschlager, Anna / Treiber, Sonja / Pereyra, David / Santol, Jonas / Pawelka, Erich / Traugott, Marianna / Schörgenhofer, Christian / Seitz, Tamara / Karolyi, Mario / Jilma, Bernd / Resch, Ulrike / Zoufaly, Alexander / Assinger, Alice

Cells

2021 Volume 10, Issue 12

Abstract: The COVID-19 pandemic drastically highlighted the vulnerability of the elderly population towards viral and other infectious threats, illustrating that aging is accompanied by dysregulated immune responses currently summarized in terms like inflammaging ... ...

Abstract	The COVID-19 pandemic drastically highlighted the vulnerability of the elderly population towards viral and other infectious threats, illustrating that aging is accompanied by dysregulated immune responses currently summarized in terms like inflammaging and immunoparalysis. To gain a better understanding on the underlying mechanisms of the age-associated risk of adverse outcome in individuals experiencing a SARS-CoV-2 infection, we analyzed the impact of age on circulating monocyte phenotypes, activation markers and inflammatory cytokines including interleukin 6 (IL-6), IL-8 and tumor necrosis factor (TNF) in the context of COVID-19 disease progression and outcome in 110 patients. Our data indicate no age-associated differences in peripheral monocyte counts or subset composition. However, age and outcome are associated with differences in monocyte activation status. Moreover, a distinct cytokine pattern of IL-6, IL-8 and TNF in elderly survivors versus non-survivors, which consolidates over the time of hospitalization, suggests that older patients with adverse outcomes experience an inappropriate immune response, reminiscent of an inflammaging driven immunoparalysis. Our study underscores the value, necessity and importance of longitudinal monitoring in elderly COVID-19 patients, as dynamic changes after symptom onset can be observed, which allow for a differentiated insight into confounding factors that impact the complex pathogenesis following an infection with SARS-CoV-2.
MeSH term(s)	Acute Disease ; Adolescent ; Adult ; Age Factors ; Aged ; Aged, 80 and over ; Aging/pathology ; Biomarkers/metabolism ; COVID-19/blood ; COVID-19/pathology ; Cytokines/blood ; Humans ; Longitudinal Studies ; Middle Aged ; Monocytes/pathology ; Neutrophils/metabolism ; Prospective Studies ; SARS-CoV-2 ; Young Adult
Chemical Substances	Biomarkers ; Cytokines
Language	English
Publishing date	2021-11-30
Publishing country	Switzerland
Document type	Clinical Trial ; Journal Article ; Observational Study ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells10123373
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Article: Platelet Phenotype Analysis of COVID-19 Patients Reveals Progressive Changes in the Activation of Integrin αIIbβ3, F13A1, the SARS-CoV-2 Target EIF4A1 and Annexin A5.

Ercan, Huriye / Schrottmaier, Waltraud Cornelia / Pirabe, Anita / Schmuckenschlager, Anna / Pereyra, David / Santol, Jonas / Pawelka, Erich / Traugott, Marianna T / Schörgenhofer, Christian / Seitz, Tamara / Karolyi, Mario / Yang, Jae-Won / Jilma, Bernd / Zoufaly, Alexander / Assinger, Alice / Zellner, Maria

Frontiers in cardiovascular medicine

2021 Volume 8, Page(s) 779073

Abstract: Background: ...

Abstract	Background:
Language	English
Publishing date	2021-11-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2781496-8
ISSN	2297-055X
ISSN	2297-055X
DOI	10.3389/fcvm.2021.779073
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Article ; Online: Platelets mediate serological memory to neutralize viruses in vitro and in vivo.

Schrottmaier, Waltraud C / Salzmann, Manuel / Badrnya, Sigrun / Mussbacher, Marion / Kral-Pointner, Julia B / Morava, Susanne / Pirabe, Anita / Brunnthaler, Laura / Yaiw, Koon C / Heber, Ulrike M / Pereyra, David / Andersen, Jan T / Bergthaler, Andreas / Söderberg-Nauclér, Cecilia / Karlsson, Mikael C I / Assinger, Alice / Forsell, Mattias N E

Blood advances

2021 Volume 4, Issue 16, Page(s) 3971–3976

MeSH term(s)	Blood Platelets ; Viruses
Language	English
Publishing date	2021-05-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2915908-8
ISSN	2473-9537 ; 2473-9529
ISSN (online)	2473-9537
ISSN	2473-9529
DOI	10.1182/bloodadvances.2020001786
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Zs.A 7153: Show issues

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