International Journal of Molecular Sciences

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Open AccessEditorial

Roles of Erythrocytes in Human Health and Disease 2.0

by Francesco Misiti

Int. J. Mol. Sci. 2024, 25(8), 4446; https://doi.org/10.3390/ijms25084446 - 18 Apr 2024

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Abstract

This Special Issue titled “Roles of Erythrocytes in Human Health and Disease 2 [...] Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

Research

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Open AccessArticle

The Impact of COVID-19 on Cellular Factors Influencing Red Blood Cell Aggregation Examined in Dextran: Possible Causes and Consequences

by Maciej Bosek, Tomasz Wybranowski, Marta Napiórkowska-Mastalerz, Jerzy Pyskir, Michał Cyrankiewicz, Małgorzata Pyskir, Marta Pilaczyńska-Cemel, Alicja Szołna-Chodór, Mateusz Wrembel, Stefan Kruszewski and Grzegorz Przybylski

Int. J. Mol. Sci. 2023, 24(19), 14952; https://doi.org/10.3390/ijms241914952 - 6 Oct 2023

Cited by 2 | Viewed by 1715

Abstract

Several studies have indicated that COVID-19 can lead to alterations in blood rheology, including an increase in red blood cell aggregation. The precise mechanisms behind this phenomenon are not yet fully comprehended. The latest findings suggest that erythrocyte aggregation significantly influences microcirculation, causes [...] Read more.

Several studies have indicated that COVID-19 can lead to alterations in blood rheology, including an increase in red blood cell aggregation. The precise mechanisms behind this phenomenon are not yet fully comprehended. The latest findings suggest that erythrocyte aggregation significantly influences microcirculation, causes the formation of blood clots in blood vessels, and even damages the endothelial glycocalyx, leading to endothelial dysfunction. The focus of this research lies in investigating the cellular factors influencing these changes in aggregation and discussing potential causes and implications in the context of COVID-19 pathophysiology. For this purpose, the aggregation of erythrocytes in a group of 52 patients with COVID-19 pneumonia was examined in a 70 kDa Dextran solution, which eliminates the influence of plasma factors. Using image analysis, the velocities and sizes of the formed aggregates were investigated, determining their porosity. This study showed that the process of erythrocyte aggregation in COVID-19 patients, independent of plasma factors, leads to the formation of more compact, denser, three-dimensional aggregates. These aggregates may be less likely to disperse under circulatory shear stress, increasing the risk of thrombotic events. This study also suggests that cellular aggregation factors can be responsible for the thrombotic disorders observed long after infection, even when plasma factors have normalized. The results and subsequent broad discussion presented in this study can contribute to a better understanding of the potential complications associated with increased erythrocyte aggregation. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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10 pages, 1595 KiB

Open AccessArticle

Biophysical Profiling of Sickle Cell Disease Using Holographic Cytometry and Deep Learning

by Cindy X. Chen, George T. Funkenbusch and Adam Wax

Int. J. Mol. Sci. 2023, 24(15), 11885; https://doi.org/10.3390/ijms241511885 - 25 Jul 2023

Cited by 4 | Viewed by 1686

Abstract

Sickle cell disease (SCD) is an inherited hematological disorder associated with high mortality rates, particularly in sub-Saharan Africa. SCD arises due to the polymerization of sickle hemoglobin, which reduces flexibility of red blood cells (RBCs), causing blood vessel occlusion and leading to severe [...] Read more.

Sickle cell disease (SCD) is an inherited hematological disorder associated with high mortality rates, particularly in sub-Saharan Africa. SCD arises due to the polymerization of sickle hemoglobin, which reduces flexibility of red blood cells (RBCs), causing blood vessel occlusion and leading to severe morbidity and early mortality rates if untreated. While sickle solubility tests are available to sub-Saharan African population as a means for detecting sickle hemoglobin (HbS), the test falls short in assessing the severity of the disease and visualizing the degree of cellular deformation. Here, we propose use of holographic cytometry (HC), a high throughput, label-free imaging modality, for comprehensive morphological profiling of RBCs as a means to detect SCD. For this study, more than 2.5 million single-cell holographic images from normal and SCD patient samples were collected using the HC system. We have developed an approach for specially defining training data to improve machine learning classification. Here, we demonstrate the deep learning classifier developed using this approach can produce highly accurate classification, even on unknown patient samples. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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13 pages, 1523 KiB

Open AccessArticle

The Influence of Early Onset Preeclampsia on Perinatal Red Blood Cell Characteristics of Neonates

by Barbara Sandor, Beata Csiszar, Gergely Galos, Simone Funke, Dora Kinga Kevey, Matyas Meggyes, Laszlo Szereday and Kalman Toth

Int. J. Mol. Sci. 2023, 24(10), 8496; https://doi.org/10.3390/ijms24108496 - 9 May 2023

Cited by 1 | Viewed by 1604

Abstract

Preeclampsia is the leading cause of complicated neonatal adaptation. The present investigation aimed to study the hemorheological factors during the early perinatal period (cord blood, 24 and 72 h after delivery) in newborns of early-onset preeclamptic mothers (n = 13) and healthy [...] Read more.

Preeclampsia is the leading cause of complicated neonatal adaptation. The present investigation aimed to study the hemorheological factors during the early perinatal period (cord blood, 24 and 72 h after delivery) in newborns of early-onset preeclamptic mothers (n = 13) and healthy neonates (n = 17). Hematocrit, plasma, and whole blood viscosity (WBV), red blood cell (RBC) aggregation, and deformability were investigated. There were no significant differences in hematocrit. WBV was significantly lower in preterm neonates at birth than in the term 24 and 72 h samples. Plasma viscosity was significantly lower in preterm neonates’ cord blood than in healthy controls. RBC aggregation parameters were significantly lower in preterm newborns’ cord blood than in term neonates’ cord blood 24 and 72 h samples. RBC elongation indices were significantly lower in the term group than in preterm neonates 72 h’ sample at the high and middle shear stress range. Changes in the hemorheological parameters, especially RBC aggregation properties, refer to better microcirculation of preterm neonates at birth, which could be an adaptation mechanism to the impaired uteroplacental microcirculation in preeclampsia. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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18 pages, 4499 KiB

Open AccessArticle

Mechanochemical Synergism of Reactive Oxygen Species Influences on RBC Membrane

by Elena Kozlova, Viktoria Sergunova, Ekaterina Sherstyukova, Andrey Grechko, Snezhanna Lyapunova, Vladimir Inozemtsev, Aleksandr Kozlov, Olga Gudkova and Aleksandr Chernysh

Int. J. Mol. Sci. 2023, 24(6), 5952; https://doi.org/10.3390/ijms24065952 - 21 Mar 2023

Cited by 5 | Viewed by 1890

Abstract

The influences of various factors on blood lead to the formation of extra reactive oxygen species (ROS), resulting in the disruption of morphology and functions of red blood cells (RBCs). This study considers the mechanisms of the mechanochemical synergism of

O H^{•}

[...] Read more.

The influences of various factors on blood lead to the formation of extra reactive oxygen species (ROS), resulting in the disruption of morphology and functions of red blood cells (RBCs). This study considers the mechanisms of the mechanochemical synergism of

O H^{•}

free radicals, which are most active in the initiation of lipid peroxidation (LPO) in RBC membranes, and

H_{2} O_{2}

molecules, the largest typical diffusion path. Using kinetic models of differential equations describing

C_{H_{2} O_{2}} (t)

and

C_{O H^{•}} (t)

, we discuss two levels of mechanochemical synergism that occur simultaneously: (1) synergism that ensures the delivery of highly active free radicals

O H^{•}

to RBC membranes and (2) a positive feedback system between

H_{2} O_{2}

and

O H^{•}

, resulting in the partial restoration of spent molecules. As a result of these ROS synergisms, the efficiency of LPO in RBC membranes sharply increases. In blood, the appearance of

O H^{•}

free radicals is due to the interaction of

H_{2} O_{2}

molecules with free iron ions (

F e^{2 +}

) which arise as a result of heme degradation. We experimentally established the quantitative dependences of

C_{O H^{•}} (C_{H_{2} O_{2}})

using the methods of spectrophotometry and nonlinear curve fitting. This study extends the analysis of the influence of ROS mechanisms in RBC suspensions. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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15 pages, 1292 KiB

Open AccessArticle

The Association of Glucose Control with Circulating Levels of Red Blood Cell-Derived Vesicles in Type 2 Diabetes Mellitus Patients with Atrial Fibrillation

by Alexander A. Berezin, Zeljko Obradovic, Kristen Kopp, Tetiana A. Berezina, Michael Lichtenauer, Bernhard Wernly and Alexander E. Berezin

Int. J. Mol. Sci. 2023, 24(1), 729; https://doi.org/10.3390/ijms24010729 - 31 Dec 2022

Cited by 1 | Viewed by 2480

Abstract

Hyperglycemia is a trigger for structural alteration of red blood cells (RBCs) and their ability to release extracellular vesicles (EVs). The aim of the study was to elucidate whether glucose control in T2DM patients with concomitant HF and AF affects a circulating number [...] Read more.

Hyperglycemia is a trigger for structural alteration of red blood cells (RBCs) and their ability to release extracellular vesicles (EVs). The aim of the study was to elucidate whether glucose control in T2DM patients with concomitant HF and AF affects a circulating number of RBC-derived EVs. We prospectively included 417 T2DM patients with HF, 51 of them had atrial fibrillation and 25 healthy volunteers and 30 T2DM non-HF individuals. Clinical assessment, echocardiography examination and biomarker measures were performed at the baseline of the study. RBC-derived EVs were determined as CD235a+ PS+ particles by flow cytometry. NT-proBNP levels were measured by ELISA. AF patients with glycosylated hemoglobin (HbA1c) < 6.9% had lower levels of CD235a+ PS+ RBC-derived vesicles than those with HbA1c ≥ 7.0%. There were no significant differences in number of CD235a+ PS+ RBC-derived vesicles between patients in entire cohort and in non-AF sub-cohort with HbA1c < 6.9% and HbA1c ≥ 7.0%, respectively. Multivariate linear regression yielded that CD235a+ PS+ RBC-derived vesicles ≥ 545 particles in µL (OR = 1.06; 95% CI = 1.01–1.11, p = 0.044) independently predicted HbA1c ≥ 7.0%. Elevated levels of CD235a+ PS+ RBC-derived EVs independently predicted poor glycaemia control in T2DM patients with HF and AF. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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21 pages, 5529 KiB

Open AccessArticle

Surprising Structural and Functional Properties of Favism Erythrocytes Are Linked to Special Metabolic Regulation: A Cell Aging Study

by Simone Dinarelli, Giovanni Longo, Stefka Germanova-Taneva, Svetla Todinova, Sashka Krumova and Marco Girasole

Int. J. Mol. Sci. 2023, 24(1), 637; https://doi.org/10.3390/ijms24010637 - 30 Dec 2022

Cited by 6 | Viewed by 2504

Abstract

Favism uniquely arises from a genetic defect of the Glucose-6 Phosphate Dehydrogenase (G6PD) enzyme and results in a severe reduction of erythrocytes’ (RBCs) reducing power that impairs the cells’ ability to respond to oxidative stresses. After exposure to fava beans or a few [...] Read more.

Favism uniquely arises from a genetic defect of the Glucose-6 Phosphate Dehydrogenase (G6PD) enzyme and results in a severe reduction of erythrocytes’ (RBCs) reducing power that impairs the cells’ ability to respond to oxidative stresses. After exposure to fava beans or a few other drugs, the patients experience acute hemolytic anemia due to RBCs’ lysis both intra and extra-vascularly. In the present paper, we compared selected biochemical, biophysical, and ultra-morphological properties of normal RBCs and cells from favism patients measured along cellular aging. Along the aging path, the cells’ characteristics change, and their structural and functional properties degrade for both samples, but with different patterns and effectors that have been characterized in biophysical and biochemical terms. In particular, the analysis revealed distinct metabolic regulation in G6DP-deficient cells that determines important peculiarities in the cell properties during aging. Remarkably, the initial higher fragility and occurrence of structural/morphological alterations of favism cells develop, with longer aging times, into a stronger resistance to external stresses and higher general resilience. This surprisingly higher endurance against cell aging has been related to a special mechanism of metabolic regulation that permits lower energy consumption in environmental stress conditions. Our results provided a direct and coherent link between the RBCs’ metabolic regulation and the cell properties that would not have been possible to establish without an investigation performed during aging. The consequences of this new knowledge, in particular, can be discussed in a more general context, such as understanding the role of the present findings in determining the characteristics of the favism pathology as a whole. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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17 pages, 1358 KiB

Open AccessArticle

SARS-CoV-2 Altered Hemorheological and Hematological Parameters during One-Month Observation Period in Critically Ill COVID-19 Patients

by Daniel Alexander Bizjak, Lucas John, Lynn Matits, Alisa Uhl, Sebastian Victor Waldemar Schulz, Jana Schellenberg, Johannes Peifer, Wilhelm Bloch, Manfred Weiß, Beate Grüner, Hendrik Bracht, Jürgen Michael Steinacker and Marijke Grau

Int. J. Mol. Sci. 2022, 23(23), 15332; https://doi.org/10.3390/ijms232315332 - 5 Dec 2022

Cited by 8 | Viewed by 2688

Abstract

Hematological and hemorheological parameters are known to be altered in COVID-19; however, the value of combined monitoring in order to deduce disease severity is only scarcely examined. A total of 44 acute SARS-CoV-2-infected patients (aCOV) and 44 age-matched healthy controls (Con) were included. [...] Read more.

Hematological and hemorheological parameters are known to be altered in COVID-19; however, the value of combined monitoring in order to deduce disease severity is only scarcely examined. A total of 44 acute SARS-CoV-2-infected patients (aCOV) and 44 age-matched healthy controls (Con) were included. Blood of aCOV was sampled at admission (T0), and at day 2 (T2), day 5 (T5), day 10 (T10), and day 30 (T30) while blood of Con was only sampled once. Inter- and intra-group differences were calculated for hematological and hemorheological parameters. Except for mean cellular volume and mean cellular hemoglobin, all blood cell parameters were significantly different between aCOV and Con. During the acute disease state (T0–T5), hematological and hemorheological parameters were highly altered in aCOV; in particular, anemic conditions and increased immune cell response/inflammation, oxidative/nitrosative stress, decreased deformability, as well as increased aggregation, were observed. During treatment and convalescence until T30, almost all abnormal values of aCOV improved towards Con values. During the acute state of the COVID-19 disease, the hematological, as well as the hemorheological system, show fast and potentially pathological changes that might contribute to the progression of the disease, but changes appear to be largely reversible after four weeks. Measuring RBC deformability and aggregation, as well as oxidative stress induction, may be helpful in monitoring critically ill COVID-19 patients. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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16 pages, 2986 KiB

Open AccessArticle

Cigarette Smoke Extract Induces p38 MAPK-Initiated, Fas-Mediated Eryptosis

by Ignazio Restivo, Alessandro Attanzio, Ilenia Concetta Giardina, Francesca Di Gaudio, Luisa Tesoriere and Mario Allegra

Int. J. Mol. Sci. 2022, 23(23), 14730; https://doi.org/10.3390/ijms232314730 - 25 Nov 2022

Cited by 13 | Viewed by 2234

Abstract

Eryptosis is a physiological mechanism for the clearance of senescent or damaged erythrocytes by phagocytes. Excessive eryptosis is stimulated under several pathologies and associated with endothelial injury and thrombosis. Cigarette smoke (CS) is an established risk factor for vascular diseases and cigarette smokers [...] Read more.

Eryptosis is a physiological mechanism for the clearance of senescent or damaged erythrocytes by phagocytes. Excessive eryptosis is stimulated under several pathologies and associated with endothelial injury and thrombosis. Cigarette smoke (CS) is an established risk factor for vascular diseases and cigarette smokers have high-levels of eryptotic erythrocytes. This study, for the first time, investigates the mechanism by which CS damages red blood cells (RBCs). CS extract (CSE) from commercial cigarettes was prepared and standardized for nicotine content. Cytofluorimetric analysis demonstrated that treatment of human RBCs with CSE caused dose-dependent, phosphatidylserine externalization and cell shrinkage, hallmarks of apoptotic death. CSE did not affect cellular levels of Ca²⁺, reactive oxygen species (ROS) or glutathione (GSH). Immununoprecipitation and immunoblotting revealed the assembly of the death-inducing signaling complex (DISC) and oligomerization of Fas receptor as well as cleaved caspase-8 and caspase-3 within 6 h from the treatment. At the same time-interval, CSE elicited neutral sphyngomielinase (nSMase) activity-dependent ceramide formation and phosphorylation of p38 MAPK. Through specific inhibitors’ nSMase, caspase-8 or p38 MAPK activities, we demonstrated that p38 MAPK activation is required for caspase-8-mediated eryptosis and that ceramide generation is initiator caspase-dependent. Finally, ex vivo analysis detected phosphorylated p38 MAPK (p-p38) and Fas-associated signaling complex in erythrocytes from cigarette smokers. In conclusion, our study demonstrates that CSE exposure induces in erythrocytes an extrinsic apoptotic pathway involving p38 MAPK-initiated DISC formation followed by activation of caspase-8/caspase-3 via ceramide formation. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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18 pages, 4181 KiB

Open AccessArticle

Omics Markers of Red Blood Cell Transfusion in Trauma

by Ian S. LaCroix, Mitchell Cohen, Ernest E. Moore, Monika Dzieciatkowska, Travis Nemkov, Terry R. Schaid, Jr., Margaret Debot, Kenneth Jones, Christopher C. Silliman, Kirk C. Hansen and Angelo D’Alessandro

Int. J. Mol. Sci. 2022, 23(22), 13815; https://doi.org/10.3390/ijms232213815 - 10 Nov 2022

Cited by 9 | Viewed by 2888

Abstract

Red blood cell (RBC) transfusion is a life-saving intervention for millions of trauma patients every year worldwide. While hemoglobin thresholds are clinically driving the need for RBC transfusion, limited information is available with respect to transfusion efficacy at the molecular level in clinically [...] Read more.

Red blood cell (RBC) transfusion is a life-saving intervention for millions of trauma patients every year worldwide. While hemoglobin thresholds are clinically driving the need for RBC transfusion, limited information is available with respect to transfusion efficacy at the molecular level in clinically relevant cohorts. Here, we combined plasma metabolomic and proteomic measurements in longitudinal samples (n = 118; up to 13 time points; total samples: 690) from trauma patients enrolled in the control of major bleeding after trauma (COMBAT) study. Samples were collected in the emergency department and at continuous intervals up to 168 h (seven days) post-hospitalization. Statistical analyses were performed to determine omics correlate to transfusions of one, two, three, five, or more packed RBC units. While confounded by the concomitant transfusion of other blood components and other iatrogenic interventions (e.g., surgery), here we report that transfusion of one or more packed RBCs—mostly occurring within the first 4 h from hospitalization in this cohort—results in the increase in circulating levels of additive solution components (e.g., mannitol, phosphate) and decreases in the levels of circulating markers of hypoxia, such as lactate, carboxylic acids (e.g., succinate), sphingosine 1-phosphate, polyamines (especially spermidine), and hypoxanthine metabolites with potential roles in thromboinflammatory modulation after trauma. These correlations were the strongest in patients with the highest new injury severity scores (NISS > 25) and lowest base excess (BE < −10), and the effect observed was proportional to the number of units transfused. We thus show that transfusion of packed RBCs transiently increases the circulating levels of plasticizers—likely leaching from the blood units during refrigerated storage in the blood bank. Changes in the levels of arginine metabolites (especially citrulline to ornithine ratios) are indicative of an effect of transfusion on nitric oxide metabolism, which could potentially contribute to endothelial regulation. RBC transfusion was associated with changes in the circulating levels of coagulation factors, fibrinogen chains, and RBC-proteins. Changes in lysophospholipids and acyl-carnitines were observed upon transfusion, suggestive of an effect on the circulating lipidome—though cell-extrinsic/intrinsic effects and/or the contribution of other blood components cannot be disentangled. By showing a significant decrease in circulating markers of hypoxia, this study provides the first multi-omics characterization of RBC transfusion efficacy in a clinically relevant cohort of trauma patients. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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Review

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Open AccessReview

Erythroid Cells as Full Participants in the Tumor Microenvironment

by Julia A. Shevchenko, Kirill V. Nazarov, Alina A. Alshevskaya and Sergey V. Sennikov

Int. J. Mol. Sci. 2023, 24(20), 15141; https://doi.org/10.3390/ijms242015141 - 13 Oct 2023

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Abstract

The tumor microenvironment is an important factor that can determine the success or failure of antitumor therapy. Cells of hematopoietic origin are one of the most important mediators of the tumor–host interaction and, depending on the cell type and functional state, exert pro- [...] Read more.

The tumor microenvironment is an important factor that can determine the success or failure of antitumor therapy. Cells of hematopoietic origin are one of the most important mediators of the tumor–host interaction and, depending on the cell type and functional state, exert pro- or antitumor effects in the tumor microenvironment or in adjacent tissues. Erythroid cells can be full members of the tumor microenvironment and exhibit immunoregulatory properties. Tumor growth is accompanied by the need to obtain growth factors and oxygen, which stimulates the appearance of the foci of extramedullary erythropoiesis. Tumor cells create conditions to maintain the long-term proliferation and viability of erythroid cells. In turn, tumor erythroid cells have a number of mechanisms to suppress the antitumor immune response. This review considers current data on the existence of erythroid cells in the tumor microenvironment, formation of angiogenic clusters, and creation of optimal conditions for tumor growth. Despite being the most important life-support function of the body, erythroid cells support tumor growth and do not work against it. The study of various signaling mechanisms linking tumor growth with the mobilization of erythroid cells and the phenotypic and functional differences between erythroid cells of different origin allows us to identify potential targets for immunotherapy. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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15 pages, 1645 KiB

Open AccessReview

The Double-Edged Sword of Erythrocytes in Health and Disease via Their Adhesiveness

by Robert J. Asaro, Elisabetta Profumo, Brigitta Buttari and Pedro Cabrales

Int. J. Mol. Sci. 2023, 24(12), 10382; https://doi.org/10.3390/ijms241210382 - 20 Jun 2023

Cited by 2 | Viewed by 1810

Abstract

Their widespread presence throughout the vasculature, coupled with their reactivity, and thereby to their potential to release reactive oxidative species, or to utilize their anti-oxidative capacities, has promoted much discussion of the role(s) of red blood cells (RBCs) in the progression of health [...] Read more.

Their widespread presence throughout the vasculature, coupled with their reactivity, and thereby to their potential to release reactive oxidative species, or to utilize their anti-oxidative capacities, has promoted much discussion of the role(s) of red blood cells (RBCs) in the progression of health or, alternatively, a wide range of disease states. Moreover, these role(s) have been linked to the development of adhesiveness and, in fact, thereby to the essential pathway to their eventual clearance, e.g., by macrophages in the spleen. These disparate roles coupled with the mechanisms involved are reviewed and given. Following an analysis, novel perspectives are provided; these perspectives can lead to novel assays for identifying the potential for RBC adhesiveness as suggested herein. We describe this paradigm, that involves RBC adhesiveness, hemolysis, and ghost formation, with examples including, inter alia, the progression of atherosclerosis and the suppression of tumor growth along with other disease states. Full article

(This article belongs to the Special Issue Roles of Erythrocytes in Human Health and Disease 2.0)

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