Evidence map›Paper›PMID 31042146›Full record

ArticleeLife2019

Megakaryocyte emperipolesis mediates membrane transfer from intracytoplasmic neutrophils to platelets.

Pierre Cunin, Rim Bouslama, Kellie R Machlus, Marta Martínez-Bonet, Pui Y Lee, Alexandra Wactor, Nathan Nelson-Maney, Allyn Morris, Li Guo, Andrew Weyrich and 4 more

Open access · goldAbstract read
In one paragraph

Article in eLife, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 66 papers.

0numbers the graph read from it
0cells of the map it votes in
66citing papers in PubMed
9.0field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

66 citing papers in PubMed, 104 citations in OpenAlex.

  1. Trial
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  4. Integrated single-cell transcriptomic analysis identifiesBiochemistry and biophysics reports · 2026
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  19. Immunological face of megakaryocytes.Frontiers of medicine · 2024
    Review
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6 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

14 authors at 4 institutions in 2 countries.

Pierre CuninDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.ORCID 0000-0001-8550-2306
Rim BouslamaDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.ORCID 0000-0003-2767-6759
Kellie R MachlusDepartment of Medicine, Hematology Division, Brigham and Women's Hospital and Harvard Medical School, Boston, United States.
Marta Martínez-BonetDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.
Pui Y LeeDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.
Alexandra WactorDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.
Nathan Nelson-ManeyDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.
Allyn MorrisDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.
Li GuoProgram in Molecular Medicine and Department of Internal Medicine, University of Utah, Salt Lake City, United States.
Andrew WeyrichProgram in Molecular Medicine and Department of Internal Medicine, University of Utah, Salt Lake City, United States.
Martha Sola-VisnerDepartment of Neonatology, Boston Children's Hospital, Harvard Medical School, Boston, United States.
Eric BoilardCentre de Recherche en Rhumatologie et Immunologie, Centre de Recherche du Centre Hospitalier Universitaire de Québec, Faculté de Médecine de l'Université Laval, Québec, Canada.
Joseph E ItalianoDepartment of Medicine, Hematology Division, Brigham and Women's Hospital and Harvard Medical School, Boston, United States.
Peter A NigrovicDepartment of Medicine, Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Harvard Medical School, Boston, United States.ORCID 0000-0002-2126-3702
Brigham and Women's Hospital · USUniversity of Utah · USBoston Children's Hospital · USCentre hospitalier universitaire de Québec · CA

Funding

Joint Biology Consortium Resource-based CenterP30AR070253 · NIAMS · BRIGHAM AND WOMEN'S HOSPITAL · PI Peter A Nigrovic, Jeffrey Andrew Sparks · 2016 to 2026
$9.4M
Cytoskeletal Mechanisms of Platelet FormationR01HL068130 · NHLBI · BRIGHAM AND WOMEN'S HOSPITAL · PI ITALIANO, JOSEPH E · 2001 to 2021
$8.1M
Ly6 family members in neutrophil biologyR01AR065538 · NIAMS · BRIGHAM AND WOMEN'S HOSPITAL · PI NIGROVIC, PETER A · 2014 to 2024
$4.0M
T resident memory cells in arthritisR01AR075906 · NIAMS · BRIGHAM AND WOMEN'S HOSPITAL · PI NIGROVIC, PETER A · 2019 to 2023
$2.1M
Molecular mechanisms of megakaryocyte differentiation and maturation during inflammationK01DK111515 · NIDDK · BRIGHAM AND WOMEN'S HOSPITAL · PI MACHLUS, KELLIE RAE · 2016 to 2020
$793k
Pro-inflammatory role of megakaryocytes in arthritisR21AR062328 · NIAMS · BRIGHAM AND WOMEN'S HOSPITAL · PI NIGROVIC, PETER A · 2012 to 2013
$413k
Identification of molecular pathways that initiate proplatelet formationF32HL118865 · NHLBI · BRIGHAM AND WOMEN'S HOSPITAL · PI MACHLUS, KELLIE RAE · 2013 to 2016
$132k
American Heart Association 16SDG29090007American Society of Hematology Scholar AwardNHLBI NIH HHS F32 HL118865NHLBI NIH HHS R01 HL068130NIAMS NIH HHS P30 AR070253NIAMS NIH HHS R01 AR065538NIAMS NIH HHS R01 AR075906NIAMS NIH HHS R21 AR062328NIDDK NIH HHS K01 DK111515NIH HHS 5F32HL118865NIH HHS K01DK111515NIH HHS P30AR070253NIH HHS R01AR065538NIH HHS R01H168130NIH HHS R21AR062328
6 · The paper itself

Abstract

Bone marrow megakaryocytes engulf neutrophils in a phenomenon termed emperipolesis. We show here that emperipolesis is a dynamic process mediated actively by both lineages, in part through the β2-integrin/ICAM-1/ezrin pathway. Tethered neutrophils enter in membrane-bound vesicles before penetrating into the megakaryocyte cytoplasm. Intracytoplasmic neutrophils develop membrane contiguity with the demarcation membrane system, thereby transferring membrane to the megakaryocyte and to daughter platelets. This phenomenon occurs in otherwise unmanipulated murine marrow in vivo, resulting in circulating platelets that bear membrane from non-megakaryocytic hematopoietic donors. Transit through megakaryocytes can be completed as rapidly as minutes, after which neutrophils egress intact. Emperipolesis is amplified in models of murine inflammation associated with platelet overproduction, contributing to platelet production in vitro and in vivo. These findings identify emperipolesis as a new cell-in-cell interaction that enables neutrophils and potentially other cells passing through the megakaryocyte cytoplasm to modulate the production and membrane content of platelets.

Indexed as

AnimalsBlood PlateletsBone Marrow CellsCD18 AntigensCell CommunicationCytoplasmCytoskeletal ProteinsEmperipolesisEzrinHumansInflammationIntercellular Adhesion Molecule-1MegakaryocytesMembrane Transport ProteinsMiceNeutrophilsCD18 AntigensCytoskeletal ProteinsEzrinIntercellular Adhesion Molecule-1Membrane Transport Proteinscell biologyemperipolesismegakaryocytemembranemouseneutrophilplatelet

Identifiers

PMID31042146
PMCPMC6494422
OpenAlexW2949269903

What OpenQuestion holds

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LicenceCC BY
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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.