Journal Article
. 2018 Apr; 48(4):716-729.e8.
doi: 10.1016/j.immuni.2018.03.015.

KLRG1+ Effector CD8+ T Cells Lose KLRG1, Differentiate into All Memory T Cell Lineages, and Convey Enhanced Protective Immunity

Dietmar Herndler-Brandstetter 1 Harumichi Ishigame 2 Ryo Shinnakasu 3 Valerie Plajer 1 Carmen Stecher 1 Jun Zhao 4 Melanie Lietzenmayer 1 Lina Kroehling 1 Akiko Takumi 5 Kohei Kometani 6 Takeshi Inoue 7 Yuval Kluger 8 Susan M Kaech 1 Tomohiro Kurosaki 3 Takaharu Okada 9 Richard A Flavell 10 
Affiliations
  • PMID: 29625895
  •     60 References
  •     118 citations

Abstract

Protective immunity against pathogens depends on the efficient generation of functionally diverse effector and memory T lymphocytes. However, whether plasticity during effector-to-memory CD8+ T cell differentiation affects memory lineage specification and functional versatility remains unclear. Using genetic fate mapping analysis of highly cytotoxic KLRG1+ effector CD8+ T cells, we demonstrated that KLRG1+ cells receiving intermediate amounts of activating and inflammatory signals downregulated KLRG1 during the contraction phase in a Bach2-dependent manner and differentiated into all memory T cell linages, including CX3CR1int peripheral memory cells and tissue-resident memory cells. "ExKLRG1" memory cells retained high cytotoxic and proliferative capacity distinct from other populations, which contributed to effective anti-influenza and anti-tumor immunity. Our work demonstrates that developmental plasticity of KLRG1+ effector CD8+ T cells is important in promoting functionally versatile memory cells and long-term protective immunity.

Keywords: Bach2; CD8 T cell; CX(3)CR1; cancer; fate mapping; inflammation; influenza; memory; plasticity; tissue-resident.

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J Immunother Cancer, 2020 Jul 03; 8(2). PMID: 32611686    Free PMC article.
Expansion of effector and memory T cells is associated with increased survival in recurrent glioblastomas treated with dendritic cell immunotherapy.
Marica Eoli, Cristina Corbetta, +19 authors, Serena Pellegatta.
Neurooncol Adv, 2020 Jul 10; 1(1). PMID: 32642658    Free PMC article.
Systemic dysfunction and plasticity of the immune macroenvironment in cancer models.
Breanna M Allen, Kamir J Hiam, +7 authors, Matthew H Spitzer.
Nat Med, 2020 May 27; 26(7). PMID: 32451499    Free PMC article.
Memory T cells: strategies for optimizing tumor immunotherapy.
Qingjun Liu, Zhongjie Sun, Ligong Chen.
Protein Cell, 2020 Mar 30; 11(8). PMID: 32221812    Free PMC article.
Review.
KLRG1+ Memory CD8 T Cells Combine Properties of Short-Lived Effectors and Long-Lived Memory.
Kristin R Renkema, Matthew A Huggins, +3 authors, Sara E Hamilton.
J Immunol, 2020 Jul 03; 205(4). PMID: 32611727    Free PMC article.
PTPN2 Deficiency Enhances Programmed T Cell Expansion and Survival Capacity of Activated T Cells.
Markus Flosbach, Susanne G Oberle, +11 authors, Dietmar Zehn.
Cell Rep, 2020 Jul 30; 32(4). PMID: 32726622    Free PMC article.
Lipidation Approaches Potentiate Adjuvant-Pulsed Immune Surveillance: A Design Rationale for Cancer Nanovaccine.
Junqing Wang, Harshal Zope, +6 authors, Jinjun Shi.
Front Bioeng Biotechnol, 2020 Aug 28; 8. PMID: 32850698    Free PMC article.
Cutting Edge: Batf3 Expression by CD8 T Cells Critically Regulates the Development of Memory Populations.
Zhijuan Qiu, Camille Khairallah, Galina Romanov, Brian S Sheridan.
J Immunol, 2020 Jul 17; 205(4). PMID: 32669309    Free PMC article.
p53 Hinders CRISPR/Cas9-Mediated Targeted Gene Disruption in Memory CD8 T Cells In Vivo.
Samarchith P Kurup, Steven J Moioffer, Lecia L Pewe, John T Harty.
J Immunol, 2020 Sep 06; 205(8). PMID: 32887747    Free PMC article.
A committed tissue-resident memory T cell precursor within the circulating CD8+ effector T cell pool.
Lianne Kok, Feline E Dijkgraaf, +6 authors, Ton N Schumacher.
J Exp Med, 2020 Jul 31; 217(10). PMID: 32728699    Free PMC article.
The Transcription Factor TCF1 in T Cell Differentiation and Aging.
Chulwoo Kim, Jun Jin, Cornelia M Weyand, Jörg J Goronzy.
Int J Mol Sci, 2020 Sep 10; 21(18). PMID: 32899486    Free PMC article.
Review.
Delineation of a molecularly distinct terminally differentiated memory CD8 T cell population.
J Justin Milner, Hongtuyet Nguyen, +8 authors, Ananda W Goldrath.
Proc Natl Acad Sci U S A, 2020 Sep 27; 117(41). PMID: 32978300    Free PMC article.
Cellular and Molecular Mechanisms of CD8+ T Cell Differentiation, Dysfunction and Exhaustion.
Daniel J Verdon, Matthias Mulazzani, Misty R Jenkins.
Int J Mol Sci, 2020 Oct 09; 21(19). PMID: 33027962    Free PMC article.
Review.
Multi-Omics Resolves a Sharp Disease-State Shift between Mild and Moderate COVID-19.
Yapeng Su, Daniel Chen, +53 authors, James R Heath.
Cell, 2020 Nov 11; 183(6). PMID: 33171100    Free PMC article.
Tissue-Resident Memory T Cells in the Liver-Unique Characteristics of Local Specialists.
Lea M Bartsch, Marcos P S Damasio, Sonu Subudhi, Hannah K Drescher.
Cells, 2020 Nov 15; 9(11). PMID: 33187162    Free PMC article.
Review.
Resident Memory T Cells and Their Role within the Liver.
Sonia Ghilas, Ana-Maria Valencia-Hernandez, +2 authors, Daniel Fernandez-Ruiz.
Int J Mol Sci, 2020 Nov 19; 21(22). PMID: 33202970    Free PMC article.
Review.
Characterization of abscopal effects of intratumoral electroporation-mediated IL-12 gene therapy.
Anandaroop Mukhopadhyay, Jocelyn Wright, +5 authors, Robert H Pierce.
Gene Ther, 2018 Oct 17; 26(1-2). PMID: 30323352    Free PMC article.
Tumor Infiltrating Effector Memory Antigen-Specific CD8+ T Cells Predict Response to Immune Checkpoint Therapy.
Nicola Principe, Joel Kidman, +15 authors, Jonathan Chee.
Front Immunol, 2020 Dec 03; 11. PMID: 33262762    Free PMC article.
MEK inhibition reprograms CD8+ T lymphocytes into memory stem cells with potent antitumor effects.
Vivek Verma, Nazli Jafarzadeh, +18 authors, Samir N Khleif.
Nat Immunol, 2020 Nov 25; 22(1). PMID: 33230330
The JAK1 Selective Inhibitor ABT 317 Blocks Signaling Through Interferon-γ and Common γ Chain Cytokine Receptors to Reverse Autoimmune Diabetes in NOD Mice.
Tingting Ge, Gaurang Jhala, +10 authors, Helen E Thomas.
Front Immunol, 2020 Dec 22; 11. PMID: 33343569    Free PMC article.
T cell fate mapping and lineage tracing technologies probing clonal aspects underlying the generation of CD8 T cell subsets.
Shaima Al Khabouri, Carmen Gerlach.
Scand J Immunol, 2020 Oct 11; 92(6). PMID: 33037653    Free PMC article.
Review.
A High-Dimensional Window into the Micro-Environment of Triple Negative Breast Cancer.
Iris Nederlof, Hugo M Horlings, Christina Curtis, Marleen Kok.
Cancers (Basel), 2021 Jan 21; 13(2). PMID: 33467084    Free PMC article.
Review.
Functional Heterogeneity and Therapeutic Targeting of Tissue-Resident Memory T Cells.
Esmé T I van der Gracht, Felix M Behr, Ramon Arens.
Cells, 2021 Jan 21; 10(1). PMID: 33467606    Free PMC article.
Review.
A Combination of Anti-PD-L1 Treatment and Therapeutic Vaccination Facilitates Improved Retroviral Clearance via Reactivation of Highly Exhausted T Cells.
Torben Knuschke, Sebastian Kollenda, +6 authors, Astrid M Westendorf.
mBio, 2021 Feb 04; 12(1). PMID: 33531395    Free PMC article.
BACH2 enforces the transcriptional and epigenetic programs of stem-like CD8+ T cells.
Chen Yao, Guohua Lou, +19 authors, Tuoqi Wu.
Nat Immunol, 2021 Feb 13; 22(3). PMID: 33574619    Free PMC article.
Clonal expansion of innate and adaptive lymphocytes.
Nicholas M Adams, Simon Grassmann, Joseph C Sun.
Nat Rev Immunol, 2020 May 20; 20(11). PMID: 32424244
Review.
Mechanisms Governing Immunotherapy Resistance in Pancreatic Ductal Adenocarcinoma.
Zoe C Schmiechen, Ingunn M Stromnes.
Front Immunol, 2021 Feb 16; 11. PMID: 33584701    Free PMC article.
Review.
Transcriptional regulatory network for the establishment of CD8+ T cell exhaustion.
Wooseok Seo, Chandsultana Jerin, Hiroyoshi Nishikawa.
Exp Mol Med, 2021 Feb 26; 53(2). PMID: 33627794    Free PMC article.
Review.
Tissue-resident memory T cells in breast cancer control and immunotherapy responses.
Ann Byrne, Peter Savas, +7 authors, Sherene Loi.
Nat Rev Clin Oncol, 2020 Mar 01; 17(6). PMID: 32112054
Review.
Interleukin-10 suppression enhances T-cell antitumor immunity and responses to checkpoint blockade in chronic lymphocytic leukemia.
J R Rivas, Y Liu, +12 authors, S Bondada.
Leukemia, 2021 Mar 19; 35(11). PMID: 33731852    Free PMC article.
CD40 Agonist Overcomes T Cell Exhaustion Induced by Chronic Myeloid Cell IL-27 Production in a Pancreatic Cancer Preclinical Model.
Adam L Burrack, Meagan R Rollins, +6 authors, Ingunn M Stromnes.
J Immunol, 2021 Feb 10; 206(6). PMID: 33558374    Free PMC article.
The architectural design of CD8+ T cell responses in acute and chronic infection: Parallel structures with divergent fates.
H Kay Chung, Bryan McDonald, Susan M Kaech.
J Exp Med, 2021 Mar 24; 218(4). PMID: 33755719    Free PMC article.
Review.
Discipline in Stages: Regulating CD8+ Resident Memory T Cells.
Rut Mora-Buch, Shannon K Bromley.
Front Immunol, 2021 Apr 06; 11. PMID: 33815352    Free PMC article.
Review.
Pre-existing effector T-cell levels and augmented myeloid cell composition denote response to CDK4/6 inhibitor palbociclib and pembrolizumab in hormone receptor-positive metastatic breast cancer.
Colt Egelston, Weihua Guo, +9 authors, Yuan Yuan.
J Immunother Cancer, 2021 Mar 25; 9(3). PMID: 33757987    Free PMC article.
IFN-I-tolerant oncolytic Semliki Forest virus in combination with anti-PD1 enhances T cell response against mouse glioma.
Miika Martikainen, Mohanraj Ramachandran, +6 authors, Magnus Essand.
Mol Ther Oncolytics, 2021 Apr 20; 21. PMID: 33869741    Free PMC article.
Type 1 Treg cells promote the generation of CD8+ tissue-resident memory T cells.
Cristina Ferreira, Leandro Barros, +11 authors, Marc Veldhoen.
Nat Immunol, 2020 May 20; 21(7). PMID: 32424367
mTOR signaling at the crossroads of environmental signals and T-cell fate decisions.
Hongling Huang, Lingyun Long, +2 authors, Hongbo Chi.
Immunol Rev, 2020 Mar 27; 295(1). PMID: 32212344    Free PMC article.
Review.
In vivo CRISPR screening reveals nutrient signaling processes underpinning CD8+ T cell fate decisions.
Hongling Huang, Peipei Zhou, +13 authors, Hongbo Chi.
Cell, 2021 Feb 27; 184(5). PMID: 33636132    Free PMC article.
Ptpn2 and KLRG1 regulate the generation and function of tissue-resident memory CD8+ T cells in skin.
Katharina Hochheiser, Florian Wiede, +21 authors, Thomas Gebhardt.
J Exp Med, 2021 Apr 30; 218(6). PMID: 33914023    Free PMC article.
Revisiting the gut-joint axis: links between gut inflammation and spondyloarthritis.
Eric Gracey, Lars Vereecke, +6 authors, Dirk Elewaut.
Nat Rev Rheumatol, 2020 Jul 15; 16(8). PMID: 32661321
Review.
Resident memory T cells in tumor-distant tissues fortify against metastasis formation.
Laura S Christian, Liuyang Wang, +4 authors, Qi-Jing Li.
Cell Rep, 2021 May 13; 35(6). PMID: 33979626    Free PMC article.
Memory CD8 T Cells Generated by Cytomegalovirus Vaccine Vector Expressing NKG2D Ligand Have Effector-Like Phenotype and Distinct Functional Features.
Marko Šustić, Maja Cokarić Brdovčak, +9 authors, Stipan Jonjić.
Front Immunol, 2021 Jun 26; 12. PMID: 34168650    Free PMC article.
Resident and circulating memory T cells persist for years in melanoma patients with durable responses to immunotherapy.
Jichang Han, Yanding Zhao, +12 authors, Christina V Angeles.
Nat Cancer, 2021 Jun 29; 2(3). PMID: 34179824    Free PMC article.
Expression of KLRG1 and CD127 defines distinct CD8+ subsets that differentially impact patient outcome in follicular lymphoma.
Hongyan Wu, Xinyi Tang, +6 authors, Stephen M Ansell.
J Immunother Cancer, 2021 Jul 07; 9(7). PMID: 34226281    Free PMC article.
Clinical Applications and Immunological Aspects of Electroporation-Based Therapies.
Jean Carlos Dos Santos da Luz, Fernanda Antunes, +3 authors, Bryan E Strauss.
Vaccines (Basel), 2021 Aug 07; 9(7). PMID: 34358144    Free PMC article.
Review.
Tissue-Resident Memory T Cells in Skin Diseases: A Systematic Review.
Thomas Emmanuel, Josephine Mistegård, +2 authors, Lars Iversen.
Int J Mol Sci, 2021 Aug 28; 22(16). PMID: 34445713    Free PMC article.
Systematic Review.
The precursors of CD8+ tissue resident memory T cells: from lymphoid organs to infected tissues.
Lianne Kok, David Masopust, Ton N Schumacher.
Nat Rev Immunol, 2021 Sep 05; 22(5). PMID: 34480118    Free PMC article.
Review.
Prior Exposure to Coxsackievirus A21 Does Not Mitigate Oncolytic Therapeutic Efficacy.
William J Burnett, David M Burnett, +6 authors, Matthew W VanBrocklin.
Cancers (Basel), 2021 Sep 11; 13(17). PMID: 34503272    Free PMC article.
Schrödinger's T Cells: Molecular Insights Into Stemness and Exhaustion.
Nancy M Gonzalez, Dawei Zou, Andy Gu, Wenhao Chen.
Front Immunol, 2021 Sep 14; 12. PMID: 34512656    Free PMC article.
Review.
A modular self-adjuvanting cancer vaccine combined with an oncolytic vaccine induces potent antitumor immunity.
Krishna Das, Elodie Belnoue, +13 authors, Guido Wollmann.
Nat Commun, 2021 Sep 02; 12(1). PMID: 34465781    Free PMC article.
The fellowship of regulatory and tissue-resident memory cells.
Leandro Barros, Cristina Ferreira, Marc Veldhoen.
Mucosal Immunol, 2021 Oct 06; 15(1). PMID: 34608235    Free PMC article.
Review.
Hedgehog interacting protein-expressing lung fibroblasts suppress lymphocytic inflammation in mice.
Jeong H Yun, ChangHee Lee, +9 authors, Xiaobo Zhou.
JCI Insight, 2021 Aug 11; 6(17). PMID: 34375314    Free PMC article.
Miscell: An efficient self-supervised learning approach for dissecting single-cell transcriptome.
Hongru Shen, Yang Li, +13 authors, Xiangchun Li.
iScience, 2021 Oct 30; 24(11). PMID: 34712916    Free PMC article.
Memory CD8+ T cells exhibit tissue imprinting and non-stable exposure-dependent reactivation characteristics following blood-stage Plasmodium berghei ANKA infections.
Tovah N Shaw, Michael J Haley, +6 authors, Kevin N Couper.
Immunology, 2021 Aug 19; 164(4). PMID: 34407221    Free PMC article.
Cyclophosphamide enhances the antitumor potency of GITR engagement by increasing oligoclonal cytotoxic T cell fitness.
Daniel Hirschhorn, Allison Betof Warner, +11 authors, Jedd D Wolchok.
JCI Insight, 2021 Oct 23; 6(20). PMID: 34676831    Free PMC article.
DNA Methylation and Immune Memory Response.
Nathalia Noschang Mittelstaedt, André Luiz Becker, +3 authors, Ana Paula Duarte de Souza.
Cells, 2021 Nov 28; 10(11). PMID: 34831166    Free PMC article.
Review.
Malignant and Benign T Cells Constituting Cutaneous T-Cell Lymphoma.
Shuichi Nakai, Eiji Kiyohara, Rei Watanabe.
Int J Mol Sci, 2021 Dec 11; 22(23). PMID: 34884736    Free PMC article.
Review.
Signatures and Specificity of Tissue-Resident Lymphocytes Identified in Human Renal Peritumor and Tumor Tissue.
Theresa Dornieden, Arne Sattler, +10 authors, Katja Kotsch.
J Am Soc Nephrol, 2021 Jun 03; 32(9). PMID: 34074699    Free PMC article.
Combined Inhibition of SHP2 and CXCR1/2 Promotes Antitumor T-cell Response in NSCLC.
Kwan Ho Tang, Shuai Li, +15 authors, Benjamin G Neel.
Cancer Discov, 2021 Aug 07; 12(1). PMID: 34353854    Free PMC article.
Characterizing cellular heterogeneity in fibrotic hypersensitivity pneumonitis by single-cell transcriptional analysis.
Junyi Wang, Lei Zhang, +10 authors, Guoping Li.
Cell Death Discov, 2022 Jan 30; 8(1). PMID: 35091537    Free PMC article.
Interleukin-17 contributes to Ross River virus-induced arthritis and myositis.
Helen Mostafavi, Kothila Tharmarajah, +8 authors, Ali Zaid.
PLoS Pathog, 2022 Feb 11; 18(2). PMID: 35143591    Free PMC article.
Regulation of tissue-resident memory T cells by the Microbiota.
Abigail E Overacre-Delgoffe, Timothy W Hand.
Mucosal Immunol, 2022 Feb 24; 15(3). PMID: 35194180    Free PMC article.
Review.
Fate-mapping mice: new tools and technology for immune discovery.
Scarlett E Lee, Brian D Rudd, Norah L Smith.
Trends Immunol, 2022 Feb 01; 43(3). PMID: 35094945    Free PMC article.
Review.
Cell-intrinsic view of the aryl hydrocarbon receptor in tumor immunity.
Joseph W Dean, Liang Zhou.
Trends Immunol, 2022 Feb 09; 43(3). PMID: 35131180    Free PMC article.
Review.
Identification of Tumor Antigens and Immune Subtypes in Lung Adenocarcinoma for mRNA Vaccine Development.
Ran Xu, Tong Lu, +3 authors, LinYou Zhang.
Front Cell Dev Biol, 2022 Mar 11; 10. PMID: 35265614    Free PMC article.
Developmentally distinct CD4+ Treg lineages shape the CD8+ T cell response to acute Listeria infection.
Joseph S Dolina, Joey Lee, +7 authors, Stephen P Schoenberger.
Proc Natl Acad Sci U S A, 2022 Mar 04; 119(10). PMID: 35239442    Free PMC article.
Noncognate Signals Drive Enhanced Effector CD8+ T Cell Responses through an IFNAR1-Dependent Pathway after Infection with the Prototypic Vaccine, 0ΔNLS, against Herpes Simplex Virus 1.
Grzegorz B Gmyrek, Paul Predki, Edward Gershburg, Daniel J J Carr.
J Virol, 2022 Jan 20; 96(6). PMID: 35045268    Free PMC article.
The Extracellular ATP Receptor P2RX7 Imprints a Promemory Transcriptional Signature in Effector CD8+ T Cells.
Trupti Vardam-Kaur, Sarah van Dijk, +3 authors, Henrique Borges da Silva.
J Immunol, 2022 Mar 11; 208(7). PMID: 35264459    Free PMC article.
Replicative history marks transcriptional and functional disparity in the CD8+ T cell memory pool.
Kaspar Bresser, Lianne Kok, +8 authors, Ton N Schumacher.
Nat Immunol, 2022 Apr 09; 23(5). PMID: 35393592    Free PMC article.
T cell memories of past divisions.
Lorenz Kretschmer, Veit R Buchholz.
Nat Immunol, 2022 Apr 23; 23(5). PMID: 35449418
Prioritization of autoimmune disease-associated genetic variants that perturb regulatory element activity in T cells.
Kousuke Mouri, Michael H Guo, +11 authors, John P Ray.
Nat Genet, 2022 May 06; 54(5). PMID: 35513721
Impact of Dietary Protein Restriction on the Immunogenicity and Efficacy of Whole-Sporozoite Malaria Vaccination.
Helena Nunes-Cabaço, Diana Moita, +2 authors, Miguel Prudêncio.
Front Immunol, 2022 May 10; 13. PMID: 35529859    Free PMC article.
The Yin and Yang of Targeting KLRG1+ Tregs and Effector Cells.
Samantha M Borys, Arup K Bag, Laurent Brossay, Dennis O Adeegbe.
Front Immunol, 2022 May 17; 13. PMID: 35572605    Free PMC article.
Review.