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Article ; Online: Diversity of Megakaryocytes.

Puhm, Florian / Laroche, Audrée / Boilard, Eric

Arteriosclerosis, thrombosis, and vascular biology

2023 Volume 43, Issue 11, Page(s) 2088–2098

Abstract: Megakaryocytes are commonly known as large, polyploid, bone marrow resident cells that contribute to hemostasis through the production of platelets. Soon after their discovery in the 19th century, megakaryocytes were described in tissue locations other ... ...

Abstract	Megakaryocytes are commonly known as large, polyploid, bone marrow resident cells that contribute to hemostasis through the production of platelets. Soon after their discovery in the 19th century, megakaryocytes were described in tissue locations other than the bone marrow, specifically in the lungs and the blood circulation. However, the localization of megakaryocytes in the lungs and the contribution of lung megakaryocytes to the general platelet pool has only recently been appreciated. Moreover, the conception of megakaryocytes as uniform cells with the sole purpose of platelet production has been challenged. Here, we review the literature on megakaryocyte cell identity and location with a special focus on recent observations of megakaryocyte subpopulations identified by transcriptomic analyses.
MeSH term(s)	Megakaryocytes ; Blood Platelets ; Bone Marrow ; Bone Marrow Cells ; Thrombopoiesis/genetics
Language	English
Publishing date	2023-09-07
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	1221433-4
ISSN	1524-4636 ; 1079-5642
ISSN (online)	1524-4636
ISSN	1079-5642
DOI	10.1161/ATVBAHA.123.318782
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Article ; Online: Role of platelets and megakaryocytes in adaptive immunity.

Marcoux, Genevieve / Laroche, Audrée / Espinoza Romero, Jenifer / Boilard, Eric

Platelets

2020 Volume 32, Issue 3, Page(s) 340–351

Abstract: The immune system is comprised of two principal interconnected components called innate and adaptive immunity. While the innate immune system mounts a nonspecific response that provides protection against the spread of foreign pathogens, the adaptive ... ...

Abstract	The immune system is comprised of two principal interconnected components called innate and adaptive immunity. While the innate immune system mounts a nonspecific response that provides protection against the spread of foreign pathogens, the adaptive immune system has developed to specifically recognize a given pathogen and lead to immunological memory. Platelets are small fragments produced from megakaryocytes in bone marrow and lungs. They circulate throughout the blood to monitor the integrity of the vasculature and to prevent bleeding. Given their large repertoire of immune receptors and inflammatory molecules, platelets and megakaryocytes can contribute to both innate and adaptive immunity. In adaptive immunity, platelets and megakaryocytes can process and present antigens to lymphocytes. Moreover, platelets,
MeSH term(s)	Adaptive Immunity/immunology ; Blood Platelets/metabolism ; Humans ; Megakaryocytes/metabolism
Language	English
Publishing date	2020-06-27
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1034283-7
ISSN	1369-1635 ; 0953-7104
ISSN (online)	1369-1635
ISSN	0953-7104
DOI	10.1080/09537104.2020.1786043
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Zs.A 2888: Show issues

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Article ; Online: Live imaging of platelets and neutrophils during antibody-mediated neurovascular thrombosis.

Laroche, Audree / Soulet, Denis / Bazin, Marc / Levesque, Tania / Allaeys, Isabelle / Vallières, Nicolas / Gunzer, Matthias / Flamand, Louis / Lacroix, Steve / Boilard, Eric

Blood advances

2022 Volume 6, Issue 12, Page(s) 3697–3702

Abstract: Immune complexes form in systemic disorders such as rheumatological, autoimmune, and allergic diseases or in response to infections or medications. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) adenoviral vector vaccines have been ... ...

Abstract	Immune complexes form in systemic disorders such as rheumatological, autoimmune, and allergic diseases or in response to infections or medications. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) adenoviral vector vaccines have been associated with rare yet serious thrombotic complications in the brain due to the formation of immune complexes that activate platelets. There are currently no data visualizing the interplay of platelets with leukocytes and the brain vasculature endothelium in response to immune complexes. This is in part due to the absence of FcγRIIA in mice, a receptor for immune complexes implicated in these thrombotic incidents. Here, we describe and illustrate events at the cellular level that take place in the brain vasculature in response to systemic administration of surrogate immune complexes. We used Ly6gCre+/-::Rosa26-TdT+/-::CD41-YFP+/- mice expressing the FcγRIIA transgene and fluorescence in neutrophils and platelets. Using real-time videomicroscopy to capture high-velocity events in conjunction with unbiased computer-assisted analyses, we provide images and quantifications of the cellular responses downstream of FcγRIIA stimulation. We observed transient and stable platelet-neutrophil interactions, platelets forming thrombi, and neutrophil adhesion to blood vessel walls. This imaging approach in a quadruple transgenic animal model can be used for the study of the pathogenic roles of immune complexes in disease.
MeSH term(s)	Animals ; Antigen-Antibody Complex ; Blood Platelets/pathology ; COVID-19 ; Mice ; Mice, Transgenic ; Neutrophils ; SARS-CoV-2 ; Thrombosis
Chemical Substances	Antigen-Antibody Complex
Language	English
Publishing date	2022-04-22
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.2021006728
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Zs.A 7153: Show issues

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Article ; Online: Platelet-derived extracellular vesicles infiltrate and modify the bone marrow during inflammation.

French, Shauna L / Butov, Kirill R / Allaeys, Isabelle / Canas, Jorge / Morad, Golnaz / Davenport, Patricia / Laroche, Audrée / Trubina, Natalia M / Italiano, Joseph E / Moses, Marsha A / Sola-Visner, Martha / Boilard, Eric / Panteleev, Mikhail A / Machlus, Kellie R

Blood advances

2020 Volume 4, Issue 13, Page(s) 3011–3023

Abstract: During inflammation, steady-state hematopoiesis switches to emergency hematopoiesis to repopulate myeloid cells, with a bias toward the megakaryocytic lineage. Soluble inflammatory cues are thought to be largely responsible for these alterations. However, ...

Abstract	During inflammation, steady-state hematopoiesis switches to emergency hematopoiesis to repopulate myeloid cells, with a bias toward the megakaryocytic lineage. Soluble inflammatory cues are thought to be largely responsible for these alterations. However, how these plasma factors rapidly alter the bone marrow (BM) is not understood. Inflammation also drives platelet activation, causing the release of platelet-derived extracellular vesicles (PEVs), which package diverse cargo and reprogram target cells. We hypothesized that PEVs infiltrate the BM, providing a direct mode of communication between the plasma and BM environments. We transfused fluorescent, wild-type (MPL+) platelets into recipient cMpl-/-mice before triggering systemic inflammation. Twenty hours postinfusion, we observed significant infiltration of donor platelet-derived particles in the BM, which we tracked immunophenotypically (MPL+ immunohistochemistry staining) and quantified by flow cytometry. To determine if this phenomenon relates to humans, we extensively characterized both megakaryocyte-derived and PEVs generated in vitro and in vivo, and found enrichment of extracellular vesicles in bone marrow compared with autologous peripheral blood. Last, BM from cMpl-/- mice was cultured in the presence or absence of wild-type (MPL+) PEVs. After 72 hours, flow cytometry revealed increased megakaryocytes only in cultures with added PEVs. The majority of CD41+ cells were bound to PEVs, suggesting a PEV-mediated rescue of megakaryopoiesis. In conclusion, we report for the first time that plasma-residing PEVs infiltrate the BM. Further, PEVs interact with BM cells in vivo and in vitro, causing functional reprogramming that may represent a novel model of inflammation-induced hematopoiesis.
MeSH term(s)	Animals ; Blood Platelets ; Bone Marrow ; Extracellular Vesicles ; Inflammation ; Megakaryocytes ; Mice
Language	English
Publishing date	2020-06-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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.2020001758
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Article ; Online: Platelet-derived extracellular vesicles convey mitochondrial DAMPs in platelet concentrates and their levels are associated with adverse reactions.

Marcoux, Genevieve / Magron, Audrey / Sut, Caroline / Laroche, Audree / Laradi, Sandrine / Hamzeh-Cognasse, Hind / Allaeys, Isabelle / Cabon, Ophelie / Julien, Anne-Sophie / Garraud, Olivier / Cognasse, Fabrice / Boilard, Eric

Transfusion

2019 Volume 59, Issue 7, Page(s) 2403–2414

Abstract: Background: Whereas platelet transfusion is a common medical procedure, inflammation still occurs in a fraction of transfused individuals despite the absence of any apparent infectious agents. Platelets can shed membrane vesicles, called extracellular ... ...

Abstract	Background: Whereas platelet transfusion is a common medical procedure, inflammation still occurs in a fraction of transfused individuals despite the absence of any apparent infectious agents. Platelets can shed membrane vesicles, called extracellular vesicles (EVs), some of which contain mitochondria (mito+EV). With its content of damage-associated molecular pattern (DAMP), the mitochondrion can stimulate the innate immune system. Mitochondrial DNA (mtDNA) is a recognized DAMP detected in the extracellular milieu in numerous inflammatory conditions and in platelet concentrates. We hypothesized that platelet-derived mitochondria encapsulated in EVs may represent a reservoir of mtDNA. Study design and methods: Herein, we explored the implication of mito+EVs in the occurrence of mtDNA quantified in platelet concentrate supernatants that induced or did not induce transfusion adverse reactions. Results: We observed that EVs were abundant in platelet concentrates, and platelet-derived mito+EVs were more abundant in platelet concentrates that induced adverse reactions. A significant correlation (r Conclusion: This study suggests that platelet-derived EVs, such as those that convey mitochondrial DAMPs, may be a useful biomarker for the prediction of potential risk of adverse transfusion reactions. Moreover, our work implies that investigations are necessary to determine whether there is a causal pathogenic role of mitochondrial DAMP encapsulated in EVs as opposed to mtDNA in solution.
MeSH term(s)	Blood Platelets/metabolism ; DNA, Mitochondrial/metabolism ; Extracellular Vesicles/metabolism ; Humans ; Inflammation/metabolism ; Platelet Transfusion ; Transfusion Reaction/metabolism
Chemical Substances	DNA, Mitochondrial
Language	English
Publishing date	2019-04-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208417-x
ISSN	1537-2995 ; 0041-1132
ISSN (online)	1537-2995
ISSN	0041-1132
DOI	10.1111/trf.15300
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Article ; Online: Platelets release mitochondrial antigens in systemic lupus erythematosus.

Science translational medicine

2021 Volume 13, Issue 581

Abstract: The accumulation of DNA and nuclear components in blood and their recognition by autoantibodies play a central role in the pathophysiology of systemic lupus erythematosus (SLE). Despite the efforts, the sources of circulating autoantigens in SLE are ... ...

Abstract	The accumulation of DNA and nuclear components in blood and their recognition by autoantibodies play a central role in the pathophysiology of systemic lupus erythematosus (SLE). Despite the efforts, the sources of circulating autoantigens in SLE are still unclear. Here, we show that in SLE, platelets release mitochondrial DNA, the majority of which is associated with the extracellular mitochondrial organelle. Mitochondrial release in patients with SLE correlates with platelet degranulation. This process requires the stimulation of platelet FcγRIIA, a receptor for immune complexes. Because mice lack FcγRIIA and murine platelets are completely devoid of receptor capable of binding IgG-containing immune complexes, we used transgenic mice expressing FcγRIIA for our in vivo investigations. FcγRIIA expression in lupus-prone mice led to the recruitment of platelets in kidneys and to the release of mitochondria in vivo. Using a reporter mouse with red fluorescent protein targeted to the mitochondrion, we confirmed platelets as a source of extracellular mitochondria driven by FcγRIIA and its cosignaling by the fibrinogen receptor α2bβ3 in vivo. These findings suggest that platelets might be a key source of mitochondrial antigens in SLE and might be a therapeutic target for treating SLE.
MeSH term(s)	Animals ; Antigen-Antibody Complex ; Autoantibodies/metabolism ; Blood Platelets/metabolism ; Humans ; Lupus Erythematosus, Systemic/metabolism ; Mice ; Mitochondria ; Receptors, IgG/metabolism
Chemical Substances	Antigen-Antibody Complex ; Autoantibodies ; Receptors, IgG
Language	English
Publishing date	2021-02-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2518854-9
ISSN	1946-6242 ; 1946-6234
ISSN (online)	1946-6242
ISSN	1946-6234
DOI	10.1126/scitranslmed.aav5928
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Article ; Online: Platelet EVs contain an active proteasome involved in protein processing for antigen presentation via MHC-I molecules.

Marcoux, Genevieve / Laroche, Audrée / Hasse, Stephan / Bellio, Marie / Mbarik, Maroua / Tamagne, Marie / Allaeys, Isabelle / Zufferey, Anne / Lévesque, Tania / Rebetz, Johan / Karakeussian-Rimbaud, Annie / Turgeon, Julie / Bourgoin, Sylvain G / Hamzeh-Cognasse, Hind / Cognasse, Fabrice / Kapur, Rick / Semple, John W / Hébert, Marie-Josée / Pirenne, France /

Overkleeft, Herman S / Florea, Bogdan I / Dieude, Mélanie / Vingert, Benoît / Boilard, Eric

Blood

2021 Volume 138, Issue 25, Page(s) 2607–2620

Abstract: In addition to their hemostatic role, platelets play a significant role in immunity. Once activated, platelets release extracellular vesicles (EVs) formed by the budding of their cytoplasmic membranes. Because of their heterogeneity, platelet EVs (PEVs) ... ...

Abstract	In addition to their hemostatic role, platelets play a significant role in immunity. Once activated, platelets release extracellular vesicles (EVs) formed by the budding of their cytoplasmic membranes. Because of their heterogeneity, platelet EVs (PEVs) are thought to perform diverse functions. It is unknown, however, whether the proteasome is transferred from platelets to PEVs or whether its function is retained. We hypothesized that functional protein processing and antigen presentation machinery are transferred to PEVs by activated platelets. Using molecular and functional assays, we found that the active 20S proteasome was enriched in PEVs, along with major histocompatibility complex class I (MHC-I) and lymphocyte costimulatory molecules (CD40L and OX40L). Proteasome-containing PEVs were identified in healthy donor blood, but did not increase in platelet concentrates that caused adverse transfusion reactions. They were augmented, however, after immune complex injections in mice. The complete biodistribution of murine PEVs after injection into mice revealed that they principally reached lymphoid organs, such as spleen and lymph nodes, in addition to the bone marrow, and to a lesser extent, liver and lungs. The PEV proteasome processed exogenous ovalbumin (OVA) and loaded its antigenic peptide onto MHC-I molecules, which promoted OVA-specific CD8+ T-lymphocyte proliferation. These results suggest that PEVs contribute to adaptive immunity through cross-presentation of antigens and have privileged access to immune cells through the lymphatic system, a tissue location that is inaccessible to platelets.
MeSH term(s)	Animals ; Antigen Presentation ; Blood Platelets/chemistry ; Blood Platelets/immunology ; Extracellular Vesicles/chemistry ; Extracellular Vesicles/immunology ; Histocompatibility Antigens Class I/analysis ; Histocompatibility Antigens Class I/immunology ; Humans ; Mice ; Mice, Inbred C57BL ; Proteasome Endopeptidase Complex/analysis ; Proteasome Endopeptidase Complex/immunology
Chemical Substances	Histocompatibility Antigens Class I ; Proteasome Endopeptidase Complex (EC 3.4.25.1)
Language	English
Publishing date	2021-07-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80069-7
ISSN	1528-0020 ; 0006-4971
ISSN (online)	1528-0020
ISSN	0006-4971
DOI	10.1182/blood.2020009957
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Article ; Online: Submovement interpersonal coupling is associated to audio-motor coordination performance.

Laroche, Julien / Tomassini, Alice / Fadiga, Luciano / D'Ausilio, Alessandro

Scientific reports

2024 Volume 14, Issue 1, Page(s) 4662

Abstract: ... by auditory feedback only. Importantly, the accuracy of task-instructed interpersonal coordination at the movement ...

Abstract	Acting in concert with others, a key aspect of our social life, requires behavioral coordination between persons on multiple timescales. When zooming in on the kinematic properties of movements, it appears that small speed fluctuations, called submovements, are embedded within otherwise smooth end-point trajectories. Submovements, by occurring at a faster timescale than that of movements, offer a novel window upon the functional relationship between distinct motor timescales. In this regard, it has previously been shown that when partners visually synchronize their movements, they also coordinate the timing of their submovement by following an alternated pattern. However, it remains unclear whether the mechanisms behind submovement coordination are domain-general or specific to the visual modality, and whether they have relevance for interpersonal coordination also at the scale of whole movements. In a series of solo and dyadic tasks, we show that submovements are also present and coordinated across partners when sensorimotor interactions are mediated by auditory feedback only. Importantly, the accuracy of task-instructed interpersonal coordination at the movement level correlates with the strength of submovement coordination. These results demonstrate that submovement coordination is a potentially fundamental mechanism that participates in interpersonal motor coordination regardless of the sensory domain mediating the interaction.
MeSH term(s)	Psychomotor Performance ; Movement ; Biomechanical Phenomena
Language	English
Publishing date	2024-02-26
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-024-51629-z
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Article ; Online: FcγRIIA expression accelerates nephritis and increases platelet activation in systemic lupus erythematosus.

Blood

2020 Volume 136, Issue 25, Page(s) 2933–2945

Abstract: Systemic lupus erythematosus (SLE) is an autoimmune inflammatory disease characterized by deposits of immune complexes (ICs) in organs and tissues. The expression of FcγRIIA by human platelets, which is their unique receptor for immunoglobulin G ... ...

Abstract	Systemic lupus erythematosus (SLE) is an autoimmune inflammatory disease characterized by deposits of immune complexes (ICs) in organs and tissues. The expression of FcγRIIA by human platelets, which is their unique receptor for immunoglobulin G antibodies, positions them to ideally respond to circulating ICs. Whereas chronic platelet activation and thrombosis are well-recognized features of human SLE, the exact mechanisms underlying platelet activation in SLE remain unknown. Here, we evaluated the involvement of FcγRIIA in the course of SLE and platelet activation. In patients with SLE, levels of ICs are associated with platelet activation. Because FcγRIIA is absent in mice, and murine platelets do not respond to ICs in any existing mouse model of SLE, we introduced the FcγRIIA (FCGR2A) transgene into the NZB/NZWF1 mouse model of SLE. In mice, FcγRIIA expression by bone marrow cells severely aggravated lupus nephritis and accelerated death. Lupus onset initiated major changes to the platelet transcriptome, both in FcγRIIA-expressing and nonexpressing mice, but enrichment for type I interferon response gene changes was specifically observed in the FcγRIIA mice. Moreover, circulating platelets were degranulated and were found to interact with neutrophils in FcγRIIA-expressing lupus mice. FcγRIIA expression in lupus mice also led to thrombosis in lungs and kidneys. The model recapitulates hallmarks of human SLE and can be used to identify contributions of different cellular lineages in the manifestations of SLE. The study further reveals a role for FcγRIIA in nephritis and in platelet activation in SLE.
MeSH term(s)	Animals ; Autoantibodies/genetics ; Autoantibodies/immunology ; Blood Platelets/immunology ; Blood Platelets/pathology ; Disease Models, Animal ; Immunoglobulin G/genetics ; Immunoglobulin G/immunology ; Lupus Nephritis/genetics ; Lupus Nephritis/immunology ; Lupus Nephritis/pathology ; Mice ; Mice, Transgenic ; Platelet Activation/genetics ; Platelet Activation/immunology ; Receptors, IgG/genetics ; Receptors, IgG/immunology
Chemical Substances	Autoantibodies ; Immunoglobulin G ; Receptors, IgG
Language	English
Publishing date	2020-12-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80069-7
ISSN	1528-0020 ; 0006-4971
ISSN (online)	1528-0020
ISSN	0006-4971
DOI	10.1182/blood.2020004974
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Article ; Online: Pediatrician Perspectives on Brief Resolved Unexplained Events.

Maksimowski, Karolina / Haddad, Rita / DeLaroche, Amy M

Hospital pediatrics

2021 Volume 11, Issue 9, Page(s) 996–1003

Abstract: ... in a single state. Interviews were audio-recorded and transcribed and demographic information was also ...

Abstract	Background and objective: The objective with this study was to describe pediatric emergency department (ED) physicians' perspective on the evaluation and management of brief resolved unexplained events (BRUEs) to help support the development of quality improvement interventions for this population. Methods: We conducted qualitative semistructured interviews with pediatric ED providers who practice in a single state. Interviews were audio-recorded and transcribed and demographic information was also obtained. The 6-phase approach to reflexive thematic analysis was used to conduct the qualitative analysis. Results: Nineteen pediatric ED physicians practicing in 4 institutions across our state participated in the study. The majority of participants (95%) practice in a university-affiliated setting. The primary themes related to providing care for patients with a BRUE identified in our analysis were (1) reassurance, (2) caregiver or provider concern, and (3) clinical practice guideline availability and interpretation. Closely intertwined underlying topics informing BRUE patient management were also noted: (1) ambiguity in the BRUE diagnosis and its management; (2) a need for shared decision-making between the caregiver and the provider; and (3) concern over the increased time spent with caregivers during an ED visit for a diagnosis of BRUE. These complex relationships were found to influence patient evaluation and disposition. Conclusion: Multifaceted quality improvement interventions should address caregiver and provider concerns regarding the diagnosis of BRUE while providing decision aids to support shared decision-making with caregivers.
MeSH term(s)	Brief, Resolved, Unexplained Event ; Caregivers ; Child ; Decision Making, Shared ; Emergency Service, Hospital ; Humans ; Pediatricians
Language	English
Publishing date	2021-08-24
Publishing country	United States
Document type	Journal Article
ISSN	2154-1671
ISSN (online)	2154-1671
DOI	10.1542/hpeds.2021-005805
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