Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties

Rachel L Rutishauser ¹, Gislâine A Martins , Sergey Kalachikov , Anmol Chandele , Ian A Parish , Eric Meffre , Joshy Jacob , Kathryn Calame , Susan M Kaech

Affiliations

¹ Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA.

PMID: 19664941
62 References
307 citations

Abstract

During acute infections, a small population of effector CD8(+) T cells evades terminal differentiation and survives as long-lived memory T cells. We demonstrate that the transcriptional repressor Blimp-1 enhanced the formation of terminally differentiated CD8(+) T cells during lymphocytic choriomeningitis virus (LCMV) infection, and Blimp-1 deficiency promoted the acquisition of memory cell properties by effector cells. Blimp-1 expression was preferentially increased in terminally differentiated effector and "effector memory" (Tem) CD8(+) T cells, and gradually decayed after infection as central memory (Tcm) cells developed. Blimp-1-deficient effector CD8(+) T cells showed some reduction in effector molecule expression, but primarily developed into memory precursor cells that survived better and more rapidly acquired several Tcm cell attributes, including CD62L and IL-2 expression and enhanced proliferative responses. These results reveal a critical role for Blimp-1 in controlling terminal differentiation and suppressing memory cell developmental potential in effector CD8(+) T cells during viral infection.

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A human memory T cell subset with stem cell-like properties. Luca Gattinoni, Enrico Lugli, +14 authors, Nicholas P Restifo. less Nat Med, 2011 Sep 20; 17(10). PMID: 21926977 Free PMC article. Highly Cited.
Increased numbers of preexisting memory CD8 T cells and decreased T-bet expression can restrain terminal differentiation of secondary effector and memory CD8 T cells. Nikhil S Joshi, Weiguo Cui, +3 authors, Susan M Kaech. less J Immunol, 2011 Sep 21; 187(8). PMID: 21930973 Free PMC article.
Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Ben Youngblood, Kenneth J Oestreich, +9 authors, Rafi Ahmed. less Immunity, 2011 Sep 29; 35(3). PMID: 21943489 Free PMC article. Highly Cited.
The basis of distinctive IL-2- and IL-15-dependent signaling: weak CD122-dependent signaling favors CD8+ T central-memory cell survival but not T effector-memory cell development. Iris Castro, Aixin Yu, Michael J Dee, Thomas R Malek. J Immunol, 2011 Oct 11; 187(10). PMID: 21984699 Free PMC article.
Pathogen-induced inflammatory environment controls effector and memory CD8+ T cell differentiation. Joshua J Obar, Evan R Jellison, +4 authors, Leo Lefrançois. less J Immunol, 2011 Oct 12; 187(10). PMID: 21987662 Free PMC article. Highly Cited.
Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ T cells. Yun Ji, Zoltan Pos, +12 authors, Luca Gattinoni. less Nat Immunol, 2011 Nov 08; 12(12). PMID: 22057288 Free PMC article.
The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Cliff Y Yang, J Adam Best, +10 authors, Ananda W Goldrath. less Nat Immunol, 2011 Nov 08; 12(12). PMID: 22057289 Free PMC article. Highly Cited.
An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Weiguo Cui, Ying Liu, +2 authors, Jason S Weinstein, Joseph Craft, Susan M Kaech. less Immunity, 2011 Nov 29; 35(5). PMID: 22118527 Free PMC article. Highly Cited.
A critical role for STAT3 transcription factor signaling in the development and maintenance of human T cell memory. Andrea M Siegel, Jennifer Heimall, +8 authors, Joshua D Milner. less Immunity, 2011 Nov 29; 35(5). PMID: 22118528 Free PMC article. Highly Cited.
Th17 cells are long lived and retain a stem cell-like molecular signature. Pawel Muranski, Zachary A Borman, +19 authors, Nicholas P Restifo. less Immunity, 2011 Dec 20; 35(6). PMID: 22177921 Free PMC article. Highly Cited.
CD40-activated B cells can efficiently prime antigen-specific naïve CD8+ T cells to generate effector but not memory T cells. Mélissa Mathieu, Natacha Cotta-Grand, +3 authors, Nathalie Labrecque. less PLoS One, 2012 Feb 01; 7(1). PMID: 22291907 Free PMC article.
The role of interleukin-2 during homeostasis and activation of the immune system. Onur Boyman, Jonathan Sprent. Nat Rev Immunol, 2012 Feb 22; 12(3). PMID: 22343569 Highly Cited. Review.
T-cell biology in aging, with a focus on lung disease. Naeun Lee, Min Sun Shin, Insoo Kang. J Gerontol A Biol Sci Med Sci, 2012 Mar 08; 67(3). PMID: 22396471 Free PMC article. Review.
CD27 stimulation promotes the frequency of IL-7 receptor-expressing memory precursors and prevents IL-12-mediated loss of CD8(+) T cell memory in the absence of CD4(+) T cell help. Han Dong, Nathan A Franklin, +3 authors, Timothy N J Bullock. less J Immunol, 2012 Mar 17; 188(8). PMID: 22422886 Free PMC article.
Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Shankar Subramanian Iyer, Gehong Cheng. Crit Rev Immunol, 2012 Mar 21; 32(1). PMID: 22428854 Free PMC article. Highly Cited. Review.
CD8 T cells recruited early in mouse polyomavirus infection undergo exhaustion. Jarad J Wilson, Christopher D Pack, +7 authors, Aron E Lukacher. less J Immunol, 2012 Mar 27; 188(9). PMID: 22447978 Free PMC article.
Homeostatic maintenance of T cells and natural killer cells. Onur Boyman, Carsten Krieg, Dirk Homann, Jonathan Sprent. Cell Mol Life Sci, 2012 Mar 31; 69(10). PMID: 22460580 Free PMC article. Review.
Signal integration by Akt regulates CD8 T cell effector and memory differentiation. Eui Ho Kim, Jeremy A Sullivan, +4 authors, M Suresh. less J Immunol, 2012 Apr 03; 188(9). PMID: 22467649 Free PMC article. Highly Cited.
Heterogeneity within T Cell Memory: Implications for Transplant Tolerance. Scott M Krummey, Mandy L Ford. Front Immunol, 2012 May 09; 3. PMID: 22566919 Free PMC article.
Loss of E protein transcription factors E2A and HEB delays memory-precursor formation during the CD8+ T-cell immune response. Louise M D'Cruz, Kristin Camfield Lind, +2 authors, Bei Bei Wu, Jessica K Fujimoto, Ananda W Goldrath. less Eur J Immunol, 2012 May 16; 42(8). PMID: 22585759 Free PMC article.
Alternative splicing regulates Prdm1/Blimp-1 DNA binding activities and corepressor interactions. Marc A J Morgan, Arne W Mould, +2 authors, Li Li, Elizabeth J Robertson, Elizabeth K Bikoff. less Mol Cell Biol, 2012 Jun 27; 32(17). PMID: 22733990 Free PMC article.
The effects of TLR activation on T-cell development and differentiation. Bo Jin, Tao Sun, +2 authors, Xiao-Hong Yu, Ying-Xiang Yang, Anthony E T Yeo. less Clin Dev Immunol, 2012 Jun 28; 2012. PMID: 22737174 Free PMC article. Review.
Activation of the Hippo pathway by CTLA-4 regulates the expression of Blimp-1 in the CD8+ T cell. James E D Thaventhiran, Anja Hoffmann, +4 authors, Douglas T Fearon. less Proc Natl Acad Sci U S A, 2012 Jun 30; 109(33). PMID: 22745171 Free PMC article.
Transcriptional regulator Id2 is required for the CD4 T cell immune response in the development of experimental autoimmune encephalomyelitis. Yen-Yu Lin, Mary E Jones-Mason, +5 authors, Yuan Zhuang. less J Immunol, 2012 Jun 30; 189(3). PMID: 22745378 Free PMC article.
ZBTB32 is an early repressor of the CIITA and MHC class II gene expression during B cell differentiation to plasma cells. Hye Suk Yoon, Christopher D Scharer, +7 authors, Jeremy M Boss. less J Immunol, 2012 Aug 02; 189(5). PMID: 22851713 Free PMC article.
FoxP3⁺ regulatory CD4 T cells control the generation of functional CD8 memory. M G de Goër de Herve, S Jaafoura, M Vallée, Y Taoufik. Nat Commun, 2012 Aug 09; 3. PMID: 22871805 Free PMC article.
Cutting edge: generation of memory precursors and functional memory CD8+ T cells depends on T cell factor-1 and lymphoid enhancer-binding factor-1. Xinyuan Zhou, Hai-Hui Xue. J Immunol, 2012 Aug 10; 189(6). PMID: 22875805 Free PMC article.
Mouse Hobit is a homolog of the transcriptional repressor Blimp-1 that regulates NKT cell effector differentiation. Klaas P J M van Gisbergen, Natasja A M Kragten, +5 authors, Rene A W van Lier. less Nat Immunol, 2012 Aug 14; 13(9). PMID: 22885984
Phenotype and function of protective, CD4-independent CD8 T cell memory. Lindsay E Edwards, Catherine Haluszczak, Ross M Kedl. Immunol Res, 2012 Sep 06; 55(1-3). PMID: 22948808 Free PMC article.
Peroxiredoxin II regulates effector and secondary memory CD8+ T cell responses. Ryan D Michalek, Katie E Crump, +6 authors, Jason M Grayson. less J Virol, 2012 Oct 12; 86(24). PMID: 23055551 Free PMC article.
Transcriptional control of effector and memory CD8+ T cell differentiation. Susan M Kaech, Weiguo Cui. Nat Rev Immunol, 2012 Oct 20; 12(11). PMID: 23080391 Free PMC article. Highly Cited. Review.
B lymphocyte-induced maturation protein-1 contributes to intestinal mucosa homeostasis by limiting the number of IL-17-producing CD4+ T cells. Soofia Salehi, Rashmi Bankoti, +7 authors, Gislâine A Martins. less J Immunol, 2012 Nov 20; 189(12). PMID: 23162130 Free PMC article.
Anti-viral CD8 T cells and the cytokines that they love. Maureen A Cox, Shannon M Kahan, Allan J Zajac. Virology, 2012 Dec 12; 435(1). PMID: 23217625 Free PMC article. Review.
Use it or lose it: establishment and persistence of T cell memory. Katherine Kedzierska, Sophie A Valkenburg, +2 authors, Peter C Doherty, Miles P Davenport, Vanessa Venturi. less Front Immunol, 2012 Dec 12; 3. PMID: 23230439 Free PMC article.
Defining the molecular blueprint that drives CD8(+) T cell differentiation in response to infection. Brendan E Russ, Alice E Denton, +3 authors, Stephen J Turner. less Front Immunol, 2012 Dec 26; 3. PMID: 23267358 Free PMC article.
Id2 influences differentiation of killer cell lectin-like receptor G1(hi) short-lived CD8+ effector T cells. Jamie Knell, J Adam Best, +3 authors, Ananda W Goldrath. less J Immunol, 2013 Jan 18; 190(4). PMID: 23325888 Free PMC article.
Critical role for all-trans retinoic acid for optimal effector and effector memory CD8 T cell differentiation. S Rameeza Allie, Weijun Zhang, +2 authors, Ching-Yi Tsai, Randolph J Noelle, Edward J Usherwood. less J Immunol, 2013 Jan 23; 190(5). PMID: 23338237 Free PMC article.
Protecting and rescuing the effectors: roles of differentiation and survival in the control of memory T cell development. Sema Kurtulus, Pulak Tripathi, David A Hildeman. Front Immunol, 2013 Jan 25; 3. PMID: 23346085 Free PMC article.
Transcriptional insights into the CD8(+) T cell response to infection and memory T cell formation. J Adam Best, David A Blair, +6 authors, Immunological Genome Project Consortium. less Nat Immunol, 2013 Feb 12; 14(4). PMID: 23396170 Free PMC article. Highly Cited.
Disparate roles for STAT5 in primary and secondary CTL responses. Diana M Mitchell, Matthew A Williams. J Immunol, 2013 Feb 27; 190(7). PMID: 23440411 Free PMC article.
Constitutively CD40-activated B cells regulate CD8 T cell inflammatory response by IL-10 induction. Pandelakis A Koni, Anna Bolduc, +9 authors, Michiko Shimoda. less J Immunol, 2013 Feb 27; 190(7). PMID: 23440421 Free PMC article.
Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. Youn Soo Choi, Jessica A Yang, +4 authors, Shane Crotty. less J Immunol, 2013 Mar 15; 190(8). PMID: 23487426 Free PMC article. Highly Cited.
Molecular signatures of T-cell inhibition in HIV-1 infection. Marie Larsson, Esaki M Shankar, +5 authors, Adeeba Kamarulzaman. less Retrovirology, 2013 Mar 22; 10. PMID: 23514593 Free PMC article. Review.
Id2-mediated inhibition of E2A represses memory CD8+ T cell differentiation. Frederick Masson, Martina Minnich, +7 authors, Gabrielle T Belz. less J Immunol, 2013 Mar 29; 190(9). PMID: 23536629 Free PMC article.
IL-27 receptor signalling restricts the formation of pathogenic, terminally differentiated Th1 cells during malaria infection by repressing IL-12 dependent signals. Ana Villegas-Mendez, J Brian de Souza, +7 authors, Kevin N Couper. less PLoS Pathog, 2013 Apr 18; 9(4). PMID: 23593003 Free PMC article.
Differentiation of CD8 memory T cells depends on Foxo1. Rodrigo Hess Michelini, Andrew L Doedens, Ananda W Goldrath, Stephen M Hedrick. J Exp Med, 2013 May 29; 210(6). PMID: 23712431 Free PMC article. Highly Cited.
FoxO1 controls effector-to-memory transition and maintenance of functional CD8 T cell memory. Melba Marie Tejera, Eui Ho Kim, +2 authors, Jeremy A Sullivan, Erin H Plisch, M Suresh. less J Immunol, 2013 Jun 05; 191(1). PMID: 23733882 Free PMC article.
Transcriptional regulation of effector and memory CD8+ T cell fates. James E D Thaventhiran, Douglas T Fearon, Luca Gattinoni. Curr Opin Immunol, 2013 Jun 12; 25(3). PMID: 23747000 Free PMC article. Review.
CD8(+) T-cell effector function and transcriptional regulation during HIV pathogenesis. Korey R Demers, Morgan A Reuter, Michael R Betts. Immunol Rev, 2013 Jun 19; 254(1). PMID: 23772621 Free PMC article. Review.
Donor CD8+ T cells prevent Toxoplasma gondii de-encystation but fail to rescue the exhausted endogenous CD8+ T cell population. Rajarshi Bhadra, Dustin A Cobb, Imtiaz A Khan. Infect Immun, 2013 Jul 03; 81(9). PMID: 23817617 Free PMC article.
Signal transducer and activator of transcription 3 (STAT3) mutations underlying autosomal dominant hyper-IgE syndrome impair human CD8(+) T-cell memory formation and function. Megan L Ives, Cindy S Ma, +24 authors, Elissa K Deenick. less J Allergy Clin Immunol, 2013 Jul 09; 132(2). PMID: 23830147 Free PMC article.
Nicotine inhibits memory CTL programming. Zhifeng Sun, Kendra Smyth, +3 authors, Karla Garcia, Elliot Mattson, Lei Li, Zhengguo Xiao. less PLoS One, 2013 Jul 12; 8(7). PMID: 23844169 Free PMC article.
Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny. Caitlin D Castro, Yuko Ohta, Helen Dooley, Martin F Flajnik. Eur J Immunol, 2013 Jul 31; 43(11). PMID: 23897025 Free PMC article.
Environmental cues dictate the fate of individual CD8+ T cells responding to infection. Courtney R Plumlee, Brian S Sheridan, Basak B Cicek, Leo Lefrançois. Immunity, 2013 Aug 13; 39(2). PMID: 23932571 Free PMC article.
The transcription factor Interferon Regulatory Factor 4 is required for the generation of protective effector CD8+ T cells. Friederike Raczkowski, Josephine Ritter, +13 authors, Magdalena Huber. less Proc Natl Acad Sci U S A, 2013 Aug 28; 110(37). PMID: 23980171 Free PMC article.
Histone methyltransferase and histone methylation in inflammatory T-cell responses. Shan He, Qing Tong, Dennis Keith Bishop, Yi Zhang. Immunotherapy, 2013 Sep 04; 5(9). PMID: 23998733 Free PMC article. Review.
The transcription factor IRF4 is essential for TCR affinity-mediated metabolic programming and clonal expansion of T cells. Kevin Man, Maria Miasari, +9 authors, Axel Kallies. less Nat Immunol, 2013 Sep 24; 14(11). PMID: 24056747 Highly Cited.
Inhibiting glycolytic metabolism enhances CD8+ T cell memory and antitumor function. Madhusudhanan Sukumar, Jie Liu, +13 authors, Luca Gattinoni. less J Clin Invest, 2013 Oct 05; 123(10). PMID: 24091329 Free PMC article. Highly Cited.
Epigenetic modifications induced by Blimp-1 Regulate CD8⁺ T cell memory progression during acute virus infection. Hyun Mu Shin, Varun Kapoor, +3 authors, Leslie J Berg. less Immunity, 2013 Oct 15; 39(4). PMID: 24120360 Free PMC article.
Lineage relationship of effector and memory T cells. Nicholas P Restifo, Luca Gattinoni. Curr Opin Immunol, 2013 Oct 24; 25(5). PMID: 24148236 Free PMC article. Review.
Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Payal B Watchmaker, Katharina Lahl, +9 authors, Eugene C Butcher. less Nat Immunol, 2013 Dec 03; 15(1). PMID: 24292363 Free PMC article. Highly Cited.
Aptamer-targeted inhibition of mTOR in T cells enhances antitumor immunity. Alexey Berezhnoy, Iris Castro, +2 authors, Agata Levay, Thomas R Malek, Eli Gilboa. less J Clin Invest, 2013 Dec 03; 124(1). PMID: 24292708 Free PMC article.
T cell responses: naive to memory and everything in between. Nathan D Pennock, Jason T White, +3 authors, Ross M Kedl. less Adv Physiol Educ, 2013 Dec 03; 37(4). PMID: 24292902 Free PMC article.
A genome-wide regulatory network identifies key transcription factors for memory CD8⁺ T-cell development. Guangan Hu, Jianzhu Chen. Nat Commun, 2013 Dec 18; 4. PMID: 24335726 Free PMC article.
Identification and expression profiles of prdm1 in medaka Oryzias latipes. Haobin Zhao, Xiaosha Zhang, +6 authors, Yaping Wang. less Mol Biol Rep, 2013 Dec 18; 41(2). PMID: 24343424
A replicative self-renewal model for long-lived plasma cells: questioning irreversible cell cycle exit. Reuben M Tooze. Front Immunol, 2014 Jan 05; 4. PMID: 24385976 Free PMC article. Review.
Early specification of CD8+ T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses. Janilyn Arsenio, Boyko Kakaradov, +3 authors, John T Chang. less Nat Immunol, 2014 Mar 04; 15(4). PMID: 24584088 Free PMC article. Highly Cited.
The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+ T cells. Makoto Kurachi, R Anthony Barnitz, +9 authors, W Nicholas Haining. less Nat Immunol, 2014 Mar 04; 15(4). PMID: 24584090 Free PMC article. Highly Cited.
Blimp-1 represses CD8 T cell expression of PD-1 using a feed-forward transcriptional circuit during acute viral infection. Peiyuan Lu, Benjamin A Youngblood, +4 authors, Jeremy M Boss. less J Exp Med, 2014 Mar 05; 211(3). PMID: 24590765 Free PMC article.
Distinct dendritic cell subsets dictate the fate decision between effector and memory CD8(+) T cell differentiation by a CD24-dependent mechanism. Taeg S Kim, Stacey A Gorski, +2 authors, Steven Hahn, Kenneth M Murphy, Thomas J Braciale. less Immunity, 2014 Mar 19; 40(3). PMID: 24631155 Free PMC article. Highly Cited.
TLR4 ligands lipopolysaccharide and monophosphoryl lipid a differentially regulate effector and memory CD8+ T Cell differentiation. Weiguo Cui, Nikhil S Joshi, +3 authors, Susan M Kaech. less J Immunol, 2014 Mar 25; 192(9). PMID: 24659688 Free PMC article.
Intrinsic TGF-β signaling promotes age-dependent CD8+ T cell polyfunctionality attrition. Rajarshi Bhadra, Magali M Moretto, +7 authors, Imtiaz A Khan. less J Clin Invest, 2014 Apr 26; 124(6). PMID: 24762437 Free PMC article.
Early Decision: Effector and Effector Memory T Cell Differentiation in Chronic Infection. Michael M Opata, Robin Stephens. Curr Immunol Rev, 2014 May 03; 9(3). PMID: 24790593 Free PMC article.
Graded levels of IRF4 regulate CD8+ T cell differentiation and expansion, but not attrition, in response to acute virus infection. Ribhu Nayar, Elizabeth Schutten, +7 authors, Leslie J Berg. less J Immunol, 2014 May 20; 192(12). PMID: 24835398 Free PMC article.
Cutting edge: CXCR4 is critical for CD8+ memory T cell homeostatic self-renewal but not rechallenge self-renewal. Julie Chaix, Simone A Nish, +4 authors, Steven L Reiner. less J Immunol, 2014 Jun 29; 193(3). PMID: 24973450 Free PMC article.
Chronic viral infection promotes sustained Th1-derived immunoregulatory IL-10 via BLIMP-1. Ian A Parish, Heather D Marshall, +10 authors, Susan M Kaech. less J Clin Invest, 2014 Jul 09; 124(8). PMID: 25003188 Free PMC article.
A clinically useful approach to enhance immunological memory and antitumor immunity. Alex Berezhnoy, Anugraha Rajagopalan, Eli Gilboa. Oncoimmunology, 2014 Jul 25; 3. PMID: 25057446 Free PMC article.
Memory B cells contribute to rapid Bcl6 expression by memory follicular helper T cells. Wataru Ise, Takeshi Inoue, +4 authors, Tomohiro Kurosaki. less Proc Natl Acad Sci U S A, 2014 Jul 30; 111(32). PMID: 25071203 Free PMC article.
Transcriptional and epigenetic networks of helper T and innate lymphoid cells. Han-Yu Shih, Giuseppe Sciumè, +8 authors, John J O'Shea. less Immunol Rev, 2014 Aug 16; 261(1). PMID: 25123275 Free PMC article. Review.
The interface between transcriptional and epigenetic control of effector and memory CD8⁺ T-cell differentiation. Simon M Gray, Susan M Kaech, Matthew M Staron. Immunol Rev, 2014 Aug 16; 261(1). PMID: 25123283 Free PMC article. Review.
Bim controls IL-15 availability and limits engagement of multiple BH3-only proteins. S Kurtulus, A Sholl, +5 authors, D A Hildeman. less Cell Death Differ, 2014 Aug 16; 22(1). PMID: 25124553 Free PMC article.
Gammaherpesvirus latency differentially impacts the generation of primary versus secondary memory CD8+ T cells during subsequent infection. Erik S Barton, Sujana Rajkarnikar, +2 authors, P Kent Langston, Madeline J Price, Jason M Grayson. less J Virol, 2014 Aug 22; 88(21). PMID: 25142586 Free PMC article.
In vivo RNA interference screens identify regulators of antiviral CD4(+) and CD8(+) T cell differentiation. Runqiang Chen, Simon Bélanger, +9 authors, Matthew E Pipkin. less Immunity, 2014 Aug 26; 41(2). PMID: 25148027 Free PMC article.
A central role for Notch in effector CD8(+) T cell differentiation. Ronald A Backer, Christina Helbig, +14 authors, Derk Amsen. less Nat Immunol, 2014 Oct 27; 15(12). PMID: 25344724 Free PMC article.
Targeting miR-23a in CD8+ cytotoxic T lymphocytes prevents tumor-dependent immunosuppression. Regina Lin, Ling Chen, +7 authors, Qi-Jing Li. less J Clin Invest, 2014 Oct 28; 124(12). PMID: 25347474 Free PMC article.
IL-6 receptor α defines effector memory CD8+ T cells producing Th2 cytokines and expanding in asthma. Naeun Lee, Sungyong You, +13 authors, Insoo Kang. less Am J Respir Crit Care Med, 2014 Nov 13; 190(12). PMID: 25390970 Free PMC article.
Molecular regulation of effector and memory T cell differentiation. John T Chang, E John Wherry, Ananda W Goldrath. Nat Immunol, 2014 Nov 15; 15(12). PMID: 25396352 Free PMC article. Highly Cited. Review.
MCL1 enhances the survival of CD8+ memory T Cells after viral infection. Jingang Gui, Zhuting Hu, +7 authors, Edward J Usherwood. less J Virol, 2014 Dec 17; 89(4). PMID: 25505074 Free PMC article.
Blimp-1, an intrinsic factor that represses HIV-1 proviral transcription in memory CD4+ T cells. Katarzyna Kaczmarek Michaels, Malini Natarajan, +3 authors, Andrew J Henderson. less J Immunol, 2015 Feb 25; 194(7). PMID: 25710909 Free PMC article.
Characterization of CD8+ T cell differentiation following SIVΔnef vaccination by transcription factor expression profiling. James M Billingsley, Premeela A Rajakumar, +10 authors, R Paul Johnson. less PLoS Pathog, 2015 Mar 15; 11(3). PMID: 25768938 Free PMC article.
Lineage relationship of CD8(+) T cell subsets is revealed by progressive changes in the epigenetic landscape. Joseph G Crompton, Manikandan Narayanan, +14 authors, Nicholas P Restifo. less Cell Mol Immunol, 2015 Apr 29; 13(4). PMID: 25914936 Free PMC article.
In vivo RNAi screens: concepts and applications. Shane Crotty, Matthew E Pipkin. Trends Immunol, 2015 May 06; 36(5). PMID: 25937561 Free PMC article. Review.
CD8+ T Cell Fate and Function Influenced by Antigen-Specific Virus-Like Nanoparticles Co-Expressing Membrane Tethered IL-2. Daniela Wojta-Stremayr, Alina Neunkirchner, +3 authors, Winfried F Pickl. less PLoS One, 2015 May 07; 10(5). PMID: 25946103 Free PMC article.
c-IAP ubiquitin protein ligase activity is required for 4-1BB signaling and CD8(+) memory T-cell survival. Maria Letizia Giardino Torchia, Ivana Munitic, +3 authors, Jonathan D Ashwell. less Eur J Immunol, 2015 Jun 23; 45(9). PMID: 26096449 Free PMC article.
Memory CD8 T cell transcriptional plasticity. Ben Youngblood, J Scott Hale, Rafi Ahmed. F1000Prime Rep, 2015 Jun 23; 7. PMID: 26097712 Free PMC article. Review.
The Evolving Roles of Memory Immune Cells in Transplantation. Wenhao Chen, Rafik M Ghobrial, Xian C Li. Transplantation, 2015 Jun 24; 99(10). PMID: 26102615 Free PMC article. Review.
Production of IL-10 by CD4(+) regulatory T cells during the resolution of infection promotes the maturation of memory CD8(+) T cells. Brian J Laidlaw, Weiguo Cui, +8 authors, Susan M Kaech. less Nat Immunol, 2015 Jul 07; 16(8). PMID: 26147684 Free PMC article. Highly Cited.
Blimp1/Prdm1 Functions in Opposition to Irf1 to Maintain Neonatal Tolerance during Postnatal Intestinal Maturation. Arne W Mould, Marc A J Morgan, +2 authors, Andrew C Nelson, Elizabeth K Bikoff, Elizabeth J Robertson. less PLoS Genet, 2015 Jul 15; 11(7). PMID: 26158850 Free PMC article.
Targeting Transcriptional Regulators of CD8+ T Cell Dysfunction to Boost Anti-Tumor Immunity. Katherine A Waugh, Sonia M Leach, Jill E Slansky. Vaccines (Basel), 2015 Sep 24; 3(3). PMID: 26393659 Free PMC article. Review.
Acute Viral Respiratory Infection Rapidly Induces a CD8+ T Cell Exhaustion-like Phenotype. John J Erickson, Pengcheng Lu, +5 authors, John V Williams. less J Immunol, 2015 Sep 25; 195(9). PMID: 26401005 Free PMC article.
The Interleukin-2-mTORc1 Kinase Axis Defines the Signaling, Differentiation, and Metabolism of T Helper 1 and Follicular B Helper T Cells. John P Ray, Matthew M Staron, +8 authors, Joe Craft. less Immunity, 2015 Sep 28; 43(4). PMID: 26410627 Free PMC article. Highly Cited.
The Timing of Stimulation and IL-2 Signaling Regulate Secondary CD8 T Cell Responses. Shaniya H Khan, Matthew D Martin, +3 authors, Vladimir P Badovinac. less PLoS Pathog, 2015 Oct 03; 11(10). PMID: 26431533 Free PMC article.
Oct1 and OCA-B are selectively required for CD4 memory T cell function. Arvind Shakya, Alon Goren, +8 authors, Dean Tantin. less J Exp Med, 2015 Oct 21; 212(12). PMID: 26481684 Free PMC article.
The transcription factors ZEB2 and T-bet cooperate to program cytotoxic T cell terminal differentiation in response to LCMV viral infection. Claudia X Dominguez, Robert A Amezquita, +4 authors, Susan M Kaech. less J Exp Med, 2015 Oct 28; 212(12). PMID: 26503446 Free PMC article. Highly Cited.
IRF4-Dependent and IRF4-Independent Pathways Contribute to DC Dysfunction in Lupus. Michela Manni, Sanjay Gupta, +3 authors, Alessandra B Pernis. less PLoS One, 2015 Nov 07; 10(11). PMID: 26544714 Free PMC article.
Smad4 represses the generation of memory-precursor effector T cells but is required for the differentiation of central memory T cells. J Cao, X Zhang, +11 authors, J Zhang. less Cell Death Dis, 2015 Nov 20; 6. PMID: 26583325 Free PMC article.
IL-21 Is Important for Induction of KLRG1+ Effector CD8 T Cells during Acute Intracellular Infection. Magali M Moretto, Imtiaz A Khan. J Immunol, 2015 Nov 26; 196(1). PMID: 26597007 Free PMC article.
Memory T cell-driven differentiation of naive cells impairs adoptive immunotherapy. Christopher A Klebanoff, Christopher D Scott, +24 authors, Nicholas P Restifo. less J Clin Invest, 2015 Dec 15; 126(1). PMID: 26657860 Free PMC article. Highly Cited.
Natural killer group 2D and CD28 receptors differentially activate mammalian/mechanistic target of rapamycin to alter murine effector CD8+ T-cell differentiation. Bryan McQueen, Kelsey Trace, +2 authors, Emily Whitman, Taylor Bedsworth, Amorette Barber. less Immunology, 2015 Dec 15; 147(3). PMID: 26661515 Free PMC article.
SLE-associated risk factors affect DC function. Myoungsun Son, Sun Jung Kim, Betty Diamond. Immunol Rev, 2015 Dec 20; 269(1). PMID: 26683148 Free PMC article. Review.
Regulatory T cell memory. Michael D Rosenblum, Sing Sing Way, Abul K Abbas. Nat Rev Immunol, 2015 Dec 22; 16(2). PMID: 26688349 Free PMC article. Highly Cited. Review.
Enhancing adoptive T cell immunotherapy with microRNA therapeutics. Yun Ji, James D Hocker, Luca Gattinoni. Semin Immunol, 2015 Dec 30; 28(1). PMID: 26710685 Free PMC article. Review.
IRF4 Regulates the Ratio of T-Bet to Eomesodermin in CD8+ T Cells Responding to Persistent LCMV Infection. Ribhu Nayar, Elizabeth Schutten, +7 authors, Leslie J Berg. less PLoS One, 2015 Dec 30; 10(12). PMID: 26714260 Free PMC article.
Retrogenic ICOS Expression Increases Differentiation of KLRG-1hiCD127loCD8+ T Cells during Listeria Infection and Diminishes Recall Responses. Danya Liu, Eileen M Burd, Craig M Coopersmith, Mandy L Ford. J Immunol, 2016 Jan 06; 196(3). PMID: 26729800 Free PMC article.
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Single-Cell Transcriptomics Reveals Core Regulatory Programs That Determine the Heterogeneity of Circulating and Tissue-Resident Memory CD8+ T Cells. Yao Chen, Jian Shen, +2 authors, Moujtaba Y Kasmani, Paytsar Topchyan, Weiguo Cui. less Cells, 2021 Aug 28; 10(8). PMID: 34440912 Free PMC article.
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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. less JCI Insight, 2021 Oct 23; 6(20). PMID: 34676831 Free PMC article.
A reservoir of stem-like CD8+ T cells in the tumor-draining lymph node preserves the ongoing antitumor immune response. Kelli A Connolly, Manik Kuchroo, +19 authors, Nikhil S Joshi. less Sci Immunol, 2021 Oct 02; 6(64). PMID: 34597124 Free PMC article.
Single-Cell Analysis of Antigen-Specific CD8+ T-Cell Transcripts Reveals Profiles Specific to mRNA or Adjuvanted Protein Vaccines. Trine Sundebo Meldgaard, Fabiola Blengio, +7 authors, Sylvie Bertholet. less Front Immunol, 2021 Nov 16; 12. PMID: 34777370 Free PMC article.
Enhancing T Cell Chemotaxis and Infiltration in Glioblastoma. Kirit Singh, Kelly M Hotchkiss, +4 authors, John H Sampson. less Cancers (Basel), 2021 Nov 14; 13(21). PMID: 34771532 Free PMC article. Review.
Dependence on Bcl6 and Blimp1 drive distinct differentiation of murine memory and follicular helper CD4+ T cells. Thomas Ciucci, Melanie S Vacchio, +5 authors, Rémy Bosselut. less J Exp Med, 2021 Nov 19; 219(1). PMID: 34792530 Free PMC article.
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