Evidence map›Paper›PMID 29937354›Full record

ArticleCancer cell2018

Apoptotic Cell-Derived Extracellular Vesicles Promote Malignancy of Glioblastoma Via Intercellular Transfer of Splicing Factors.

Marat S Pavlyukov, Hai Yu, Soniya Bastola, Mutsuko Minata, Victoria O Shender, Yeri Lee, Suojun Zhang, Jia Wang, Svetlana Komarova, Jun Wang and 17 more

Open access · bronzeAbstract read
In one paragraph

Article in Cancer cell, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 210 papers, 2 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
210citing papers in PubMed, 2 pooled it
11.7field-weighted citation impact, top 1% 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

210 citing papers in PubMed, 2 syntheses or guidelines pooled it, 315 citations in OpenAlex.

  1. Pooled it
  2. Pooled it
  3. Article
  4. Plasma Extracellular Vesicles from Glioblastoma Patients Affect Phenotype and Activate Receptor Tyrosine Kinases in Glioblastoma Cells.Doklady biological sciences : proceedings of the Academy of Sciences of the USSR, Biological sciences sections · 2026
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  14. Apoptotic extracellular vesicles: unveiling mechanisms, diverse functions, and biomedical implications.Apoptosis : an international journal on programmed cell death · 2026
    Review
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150 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

27 authors at 13 institutions in 4 countries.

Marat S PavlyukovDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA; Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation.
Hai YuDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA; Department of Neurosurgery, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, China.
Soniya BastolaDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Mutsuko MinataDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Victoria O ShenderShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation; Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow 119435, Russian Federation.
Yeri LeeInstitute for Refractory Cancer Research, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea; Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea.
Suojun ZhangDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA; Department of Neurosurgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430073, China.
Jia WangDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA; Department of Neurosurgery, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, China.
Svetlana KomarovaDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Jun WangDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Shinobu YamaguchiDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Heba Allah AlsheikhDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA.
Junfeng ShiDepartment of Mechanical Engineering, Ohio State University, Columbus, OH 43210, USA.
Dongquan ChenDivision of Preventive Medicine, University of Alabama at Birmingham, Birmingham, AL 35233, USA.
Ahmed MohyeldinDepartment of Neurosurgery, James Comprehensive Cancer Center, Ohio State University, Columbus, OH 43210, USA.
Sung-Hak KimDivision of Animal Science, Chonnam National University, Gwangju 61186, Republic of Korea.
Yong Jae ShinInstitute for Refractory Cancer Research, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea.
Ksenia AnufrievaShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation; Moscow Institute of Physics and Technology, Dolgoprudny 141701, Russian Federation; Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow 119435, Russian Federation.
Evgeniy G EvtushenkoFaculty of Chemistry, Lomonosov Moscow State University, Moscow 119991, Russian Federation.
Nadezhda V AntipovaShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation; Peoples' Friendship University of Russia, Moscow 117198, Russian Federation.
Georgij P ArapidiShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation; Moscow Institute of Physics and Technology, Dolgoprudny 141701, Russian Federation.
Vadim GovorunShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation; Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow 119435, Russian Federation.
Nikolay B PestovShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation.
Mikhail I ShakhparonovShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow 117997, Russian Federation.
L James LeeDepartment of Mechanical Engineering, Ohio State University, Columbus, OH 43210, USA; Department of Chemical and Biomolecular Engineering, Ohio State University, Columbus, OH 43210, USA.
Do-Hyun NamInstitute for Refractory Cancer Research, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea; Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea; Department of Health Science & Technology, Samsung Advanced Institute for Health Science & Technology, Sungkyunkwan University, Seoul 06351, Korea.
Ichiro NakanoDepartment of Neurosurgery, University of Alabama at Birmingham, Wallace Tumor Institute, 410F, 1720 2nd Avenue S, Birmingham, AL 35294-3300, USA; Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL 35294, USA. Electronic address: inakano@uabmc.edu.
University of Alabama at Birmingham · USInstitute of Bioorganic Chemistry · RUThe Ohio State University · USChonnam National University · KRFirst Affiliated Hospital of Xi'an Jiaotong University · CNLomonosov Moscow State University · RUMoscow Institute of Physics and Technology · RUResearch Institute of Physical Chemical Medicine · RUSamsung Medical Center · KRSamsung (South Korea) · KRSungkyunkwan University · KRThe Ohio State University Comprehensive Cancer Center – Arthur G. James Cancer Hospital and Richard J. Solove Research Institute · USTongji Hospital · CN

Funding

XRAY CRYSTALLOGRAPHYP30CA013148 · NCI · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI Robert S Welner · 1985 to 2026
$165.9M
Translational Therapeutics Research Program (TT)P30CA016058 · NCI · OHIO STATE UNIVERSITY · PI Jennifer A. Woyach · 1985 to 2026
$132.3M
The unique roles of the GTP-binding/protein crosslinking enzyme transglutaminase-2 and signaling partners in aggressive cancersR01CA201402 · NCI · CORNELL UNIVERSITY · PI CERIONE, RICHARD A. · 2016 to 2024
$4.3M
Metabolism Informs Intertumoral & Intratumoral HeterogeneityR01NS087913 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI NAKANO, ICHIRO, RICH, JEREMY N · 2014 to 2018
$2.0M
Novel role of compensatory proliferation in human brain tumorR01CA183991 · NCI · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI NAKANO, ICHIRO · 2015 to 2019
$1.6M
Targeting MELK-mediated EZH2 signaling in glioma stem cellsR01NS083767 · NINDS · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI LEE, JEONGWU, NAKANO, ICHIRO · 2013 to 2017
$1.3M
NCI NIH HHS P30 CA013148NCI NIH HHS P30 CA016058NCI NIH HHS R01 CA183991NCI NIH HHS R01 CA201402NINDS NIH HHS R01 NS083767NINDS NIH HHS R01 NS087913
6 · The paper itself

Abstract

Aggressive cancers such as glioblastoma (GBM) contain intermingled apoptotic cells adjacent to proliferating tumor cells. Nonetheless, intercellular signaling between apoptotic and surviving cancer cells remain elusive. In this study, we demonstrate that apoptotic GBM cells paradoxically promote proliferation and therapy resistance of surviving tumor cells by secreting apoptotic extracellular vesicles (apoEVs) enriched with various components of spliceosomes. apoEVs alter RNA splicing in recipient cells, thereby promoting their therapy resistance and aggressive migratory phenotype. Mechanistically, we identified RBM11 as a representative splicing factor that is upregulated in tumors after therapy and shed in extracellular vesicles upon induction of apoptosis. Once internalized in recipient cells, exogenous RBM11 switches splicing of MDM4 and Cyclin D1 toward the expression of more oncogenic isoforms.

Indexed as

ApoptosisAnimalsBrain NeoplasmsCell CommunicationCell Cycle ProteinsCell Line, TumorCell MovementCell ProliferationCyclin D1Drug Resistance, NeoplasmExtracellular VesiclesFemaleGlioblastomaHumansMice, Inbred NODMice, SCIDCCND1 protein, humanCell Cycle ProteinsCyclin D1MDM4 protein, humanNuclear ProteinsProto-Oncogene ProteinsRBM11 protein, humanRNA-Binding Proteinsalternative splicingapoptosisextracellular vesiclesglioblastomagliomaproneural-to-mesenchymal transitionspliceosome

Identifiers

PMID29937354
PMCPMC6048596
OpenAlexW2808930783

What OpenQuestion holds

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Registered trials

None linked

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.