Evidence map›Paper›PMID 31227606›Full record

ArticleProceedings of the National Academy of Sciences of the United States of America2019

Epigenetic signature of PD-1+ TCF1+ CD8 T cells that act as resource cells during chronic viral infection and respond to PD-1 blockade.

Rohit R Jadhav, Se Jin Im, Bin Hu, Masao Hashimoto, Peng Li, Jian-Xin Lin, Warren J Leonard, William J Greenleaf, Rafi Ahmed, Jorg J Goronzy

Abstract read
In one paragraph

Article in Proceedings of the National Academy of Sciences of the United States of America, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 151 papers.

0numbers the graph read from it
0cells of the map it votes in
151citing papers in PubMed
10.7field-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

151 citing papers in PubMed, 213 citations in OpenAlex.

  1. Trial
  2. Article
  3. CD8Cell reports. Medicine · 2026
    Review
  4. Review
  5. Article
  6. Article
  7. Article
  8. Article
  9. Review
  10. Article
  11. Regulators of CD8Nature reviews. Immunology · 2026
    Review
  12. Review
  13. Targeting innate immunity to overcome immune evasion in HPV-associated cancers.Frontiers in cellular and infection microbiology · 2026
    Review
  14. Article
  15. Article
  16. Transcriptional dynamics of CD8Molecular cancer · 2025
    Article
  17. Review
  18. Article
  19. Article
  20. Article

91 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

10 authors at 4 institutions in 1 country.

Rohit R JadhavDivision of Immunology and Rheumatology, Department of Medicine, Stanford University, Stanford, CA 94305.
Se Jin ImEmory Vaccine Center, Emory University School of Medicine, Atlanta, GA 30322.
Bin HuDivision of Immunology and Rheumatology, Department of Medicine, Stanford University, Stanford, CA 94305.
Masao HashimotoEmory Vaccine Center, Emory University School of Medicine, Atlanta, GA 30322.
Peng LiLaboratory of Molecular Immunology, Immunology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892.
Jian-Xin LinLaboratory of Molecular Immunology, Immunology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892.
Warren J LeonardLaboratory of Molecular Immunology, Immunology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892.
William J GreenleafCenter for Personal Dynamic Regulomes, Stanford University, Stanford, CA 94305.ORCID 0000-0003-1409-3095
Rafi AhmedEmory Vaccine Center, Emory University School of Medicine, Atlanta, GA 30322; rahmed@emory.edu jgoronzy@stanford.edu.
Jorg J GoronzyDivision of Immunology and Rheumatology, Department of Medicine, Stanford University, Stanford, CA 94305; rahmed@emory.edu jgoronzy@stanford.edu.
Emory University · USNational Institutes of Health · USVA Palo Alto Health Care System · USStanford University · US

Funding

VACCINE INDUCED IMMUNITY IN THE YOUNG AND AGEDU19AI057266 · NIAID · EMORY UNIVERSITY · PI Rafi Ahmed · 2003 to 2026
$81.7M
Systems Biological Analysis of Innate and Adaptive Responses to VaccinationU19AI090023 · NIAID · EMORY UNIVERSITY · PI AHMED, RAFI, LI, SHUZHAO · 2010 to 2021
$45.0M
Transgenic/KnockoutP01AI056299 · NIAID · HARVARD UNIVERSITY (MEDICAL SCHOOL) · PI BLAZAR, BRUCE R · 2003 to 2023
$42.5M
IL-2 Family Cytokines and their Receptors-- Molecular Regulation via STATsZIAHL005402 · NHLBI · NATIONAL HEART, LUNG, AND BLOOD INSTITUTE · PI LEONARD, WARREN J · 2009 to 2025
$26.8M
T CELL MEMORY TO VIRUSESR01AI030048 · NIAID · UNIVERSITY OF CALIFORNIA LOS ANGELES · PI AHMED, RAFI · 1990 to 2022
$5.2M
microRNA Regulation of T Cell SenescenceR01AI108891 · NIAID · PALO ALTO VETERANS INSTIT FOR RESEARCH · PI GORONZY, JORG J · 2014 to 2023
$4.6M
Memory T Cell Development and Survival in T Cell Responses of Older IndividualsR01AI129191 · NIAID · PALO ALTO VETERANS INSTIT FOR RESEARCH · PI GORONZY, JORG J · 2017 to 2021
$1.9M
NIAID NIH HHS P01 AI056299NIAID NIH HHS R01 AI030048NIAID NIH HHS R01 AI108891NIAID NIH HHS R01 AI129191NIAID NIH HHS U19 AI057266NIAID NIH HHS U19 AI090023
6 · The paper itself

Abstract

We have recently defined a novel population of PD-1 (programmed cell death 1)+ TCF1 (T cell factor 1)+ virus-specific CD8 T cells that function as resource cells during chronic LCMV infection and provide the proliferative burst seen after PD-1 blockade. Such CD8 T cells have been found in other chronic infections and also in cancer in mice and humans. These CD8 T cells exhibit stem-like properties undergoing self-renewal and also differentiating into the terminally exhausted CD8 T cells. Here we compared the epigenetic signature of stem-like CD8 T cells with exhausted CD8 T cells. ATAC-seq analysis showed that stem-like CD8 T cells had a unique signature implicating activity of HMG (TCF) and RHD (NF-κB) transcription factor family members in contrast to higher accessibility to ETS and RUNX motifs in exhausted CD8 T cells. In addition, regulatory regions of the transcription factors

Indexed as

AnimalsCD8-Positive T-LymphocytesCell LineageEpigenesis, GeneticGene Expression RegulationHepatocyte Nuclear Factor 1-alphaHumansImmunotherapyInhibitor of Differentiation Protein 2Inhibitor of Differentiation ProteinsLymphocytic ChoriomeningitisLymphocytic choriomeningitis virusMicePositive Regulatory Domain I-Binding Factor 1Programmed Cell Death 1 ReceptorT-Lymphocyte SubsetsHepatocyte Nuclear Factor 1-alphaHnf1a protein, mouseIdb2 protein, mouseIdb3 protein, mouseInhibitor of Differentiation Protein 2Inhibitor of Differentiation ProteinsPdcd1 protein, mousePositive Regulatory Domain I-Binding Factor 1Prdm1 protein, mouseProgrammed Cell Death 1 ReceptorATAC-seqCD8 T cell exhaustionepigenetic profiles

Identifiers

PMID31227606
PMCPMC6628832
OpenAlexW2950341312

What OpenQuestion holds

Textmetadata
LicenceCC BY-NC-ND
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.