Evidence map›Paper›PMID 31799396›Full record

ArticleScience advances2019

Mechanisms of nuclear content loading to exosomes.

Akira Yokoi, Alejandro Villar-Prados, Paul Allen Oliphint, Jianhua Zhang, Xingzhi Song, Peter De Hoff, Robert Morey, Jinsong Liu, Jason Roszik, Karen Clise-Dwyer and 4 more

Open access · goldAbstract read
In one paragraph

Article in Science advances, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 198 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
198citing papers in PubMed, 1 pooled it
11.1field-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

198 citing papers in PubMed, 1 synthesis or guideline pooled it, 276 citations in OpenAlex.

  1. Pooled it
  2. Review
  3. Review
  4. A nucleic acid labeling chemistry reveals surface DNA on exosomes.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  5. Article
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  7. Review
  8. Article
  9. Article
  10. Article
  11. Review
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  13. Article
  14. 80 years of extracellular vesicles: from discovery to clinical translation.Extracellular vesicles and circulating nucleic acids · 2026
    Review
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  17. Review
  18. A nucleic acid labeling chemistry reveals surface DNA on exosomes.bioRxiv : the preprint server for biology · 2025
    Article
  19. Review
  20. Review

138 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 3 institutions in 1 country.

Akira YokoiDepartment of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0003-0789-5102
Alejandro Villar-PradosDepartment of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0001-6900-3267
Paul Allen OliphintDepartment of Molecular Biosciences and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX, USA.ORCID 0000-0001-9713-5574
Jianhua ZhangDepartment of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0001-5412-9860
Xingzhi SongDepartment of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Peter De HoffDepartment of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA.
Robert MoreyDepartment of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA.
Jinsong LiuDepartment of Pathology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Jason RoszikDepartment of Genomic Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0002-4561-6170
Karen Clise-DwyerSection of Transplant Immunology, Department of Stem Cell Transplantation and Cellular Therapy, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Jared K BurksDepartment of Leukemia and Division of Cancer Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0002-6173-9074
Theresa J O'HalloranDepartment of Molecular Biosciences and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX, USA.
Louise C LaurentDepartment of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Diego, La Jolla, CA, USA.ORCID 0000-0002-2095-7534
Anil K SoodDepartment of Gynecologic Oncology and Reproductive Medicine, University of Texas MD Anderson Cancer Center, Houston, TX, USA.ORCID 0000-0003-4242-1762
The University of Texas MD Anderson Cancer Center · USUniversity of California San Diego · USThe University of Texas at Austin · US

Funding

Tumor Evolution and Metastasis ProgramP30CA016672 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI Scott Kopetz · 1985 to 2026
$290.8M
UPR/MDACC Partnership for Excellence in Cancer Research(Parent Grant U54 CA096297)U54CA096297 · NCI · UNIVERSITY OF PUERTO RICO MED SCIENCES · PI Ilka C Rios · 2002 to 2026
$36.9M
UNIVERSITY OF TEXAS MD ANDERSON SPORE IN OVARIAN CANCERP50CA083639 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI BAST, ROBERT C · 1999 to 2015
$33.0M
Targeting the PI3K Signaling Pathway in Endometrial CarcinomaP50CA098258 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI BODURKA, DIANE · 2003 to 2020
$32.0M
UPR/MDACC Partnership for Excellence in Cancer Research (Luis Segarra supplement)U54CA096300 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI Larkin Strong · 2002 to 2026
$23.8M
U.T. M. D. Anderson Cancer Center SPORE in Ovarian CancerP50CA217685 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI SOOD, ANIL K · 2017 to 2021
$7.9M
Harnessing the power of exosomes for non-coding RNA deliveryR35CA209904 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI SOOD, ANIL K · 2017 to 2023
$5.0M
Novel extra cellular RNA-based combinatorial RNA inhibition therapyUH3TR000943 · NCATS · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI CALIN, GEORGE A., LOPEZ-BERESTEIN, GABRIEL · 2015 to 2017
$3.2M
Targeting Stromal Influences on Glutamine Addiction in Ovarian CancerR01CA227622 · NCI · UNIVERSITY OF MICHIGAN AT ANN ARBOR · PI MOK, SAMUEL C, NAGRATH, DEEPAK · 2018 to 2022
$2.3M
Novel extra cellular RNA-based combinatorial RNA inhibition therapyUH2TR000943 · NCATS · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI CALIN, GEORGE A., LOPEZ-BERESTEIN, GABRIEL · 2013 to 2014
$1.1M
Orbitrap Elite High-Resolution Mass Spectrometer for Proteomics and MetabolomicsS10OD012304 · OD · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI HAWKE, DAVID H · 2013 to 2013
$877k
NCATS NIH HHS UH2 TR000943NCATS NIH HHS UH3 TR000943NCI NIH HHS P30 CA016672NCI NIH HHS P50 CA083639NCI NIH HHS P50 CA098258NCI NIH HHS P50 CA217685NCI NIH HHS R01 CA227622NCI NIH HHS R35 CA209904NCI NIH HHS U54 CA096297NCI NIH HHS U54 CA096300NIH HHS S10 OD012304
6 · The paper itself

Abstract

Exosome cargoes are highly varied and include proteins, small RNAs, and genomic DNA (gDNA). The presence of gDNA suggests that different intracellular compartments contribute to exosome loading, resulting in distinct exosome subpopulations. However, the loading of gDNA and other nuclear contents into exosomes (nExo) remains poorly understood. Here, we identify the relationship between cancer cell micronuclei (MN), which are markers of genomic instability, and nExo formation. Imaging flow cytometry analyses reveal that 10% of exosomes derived from cancer cells and <1% of exosomes derived from blood and ascites from patients with ovarian cancer carry nuclear contents. Treatment with genotoxic drugs resulted in increased MN and nExos both in vitro and in vivo. We observed that multivesicular body precursors and exosomal markers, such as the tetraspanins, directly interact with MN. Collectively, this work provides new insights related to nExos, which have implications for cancer biomarker development.

Indexed as

Micronuclei, Chromosome-DefectiveBiomarkers, TumorCell Line, TumorDNADNA Copy Number VariationsDNA DamageExosomesFemaleHumansOvarian NeoplasmsTetraspaninsBiomarkers, TumorDNATetraspanins

Identifiers

PMID31799396
PMCPMC6867874
OpenAlexW2991532494

What OpenQuestion holds

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LicenceCC BY-NC
Read underepoch 390

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.