Memory T cell, exhaustion, and tumor immunity

References

• Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015;15(8):486–499.
   PubMed Web of Science ®Google Scholar
• Maecker HT, McCoy JP, Nussenblatt R. Standardizing immunophenotyping for the Human Immunology Project. Nat Rev Immunol. 2012;12(3):191–200.
   PubMed Web of Science ®Google Scholar
• Mueller SN, Gebhardt T, Carbone FR, et al. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol. 2013;31(1):137–161.
   Web of Science ®Google Scholar
• Jameson SC, Masopust D. Understanding subset diversity in T cell memory. Immunity. 2018;48(2):214–226.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Lugli E, Ji Y, et al. A human memory T cell subset with stem cell-like properties. Nat Med. 2011;17(10):1290–1297.
   PubMed Web of Science ®Google Scholar
• Pulko V, Davies JS, Martinez C, et al. Human memory T cells with a naive phenotype accumulate with aging and respond to persistent viruses. Nat Immunol. 2016;17(8):966–975.
   Web of Science ®Google Scholar
• Miron M, Kumar BV, Meng W, et al. Human lymph nodes maintain TCF-1(hi) memory T cells with high functional potential and clonal diversity throughout life. J Immunol. 2018;201(7):2132–2140.
   Web of Science ®Google Scholar
• Kurtulus S, Madi A, Escobar G, et al. Checkpoint blockade immunotherapy induces dynamic changes in PD-1(-)CD8(+) tumor-infiltrating T cells. Immunity. 2019;50(1):181–194.e6.
   PubMed Web of Science ®Google Scholar
• Kaech SM, Cui W. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol. 2012;12(11):749–761.
   PubMed Web of Science ®Google Scholar
• Siddiqui I, Schaeuble K, Chennupati V, et al. Intratumoral Tcf1(+)PD-1(+)CD8(+) T cells with stem-like properties promote tumor control in response to vaccination and checkpoint blockade immunotherapy. Immunity. 2019;50(1):195–211.e10.
   PubMed Web of Science ®Google Scholar
• Li H, van der Leun AM, Yofe I, et al. Dysfunctional CD8 T cells form a proliferative, dynamically regulated compartment within human melanoma. Cell. 2019;176(4):775–789.e18.
   PubMed Web of Science ®Google Scholar
• Clarke J, Panwar B, Madrigal A, et al. Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer. J Exp Med. 2019;216(9):2128–2149.
   PubMed Web of Science ®Google Scholar
• Jerby-Arnon L, Shah P, Cuoco MS, et al. A cancer cell program promotes T cell exclusion and resistance to checkpoint blockade. Cell. 2018;175(4):984–997.e24.
   PubMed Web of Science ®Google Scholar
• Wang B, Zhang W, Jankovic V, et al. Combination cancer immunotherapy targeting PD-1 and GITR can rescue CD8(+) T cell dysfunction and maintain memory phenotype. Sci Immunol. 2018;3:eaat7061.
   PubMed Web of Science ®Google Scholar
• Yost KE, Satpathy AT, Wells DK, et al. Clonal replacement of tumor-specific T cells following PD-1 blockade. Nat Med. 2019;25(8):1251–1259.
   PubMed Web of Science ®Google Scholar
• Miller BC, Sen DR, Al Abosy R, et al. Subsets of exhausted CD8(+) T cells differentially mediate tumor control and respond to checkpoint blockade. Nat Immunol. 2019;20(3):326–336.
   PubMed Web of Science ®Google Scholar
• Fraietta JA, Lacey SF, Orlando EJ, et al. Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia. Nat Med. 2018;24(5):563–571.
   PubMed Web of Science ®Google Scholar
• Paley MA, Kroy DC, Odorizzi PM, et al. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science. 2012;338(6111):1220–1225.
   PubMed Web of Science ®Google Scholar
• He R, Hou S, Liu C, et al. Follicular CXCR5- expressing CD8(+) T cells curtail chronic viral infection. Nature. 2016;537(7620):412–428.
   PubMed Web of Science ®Google Scholar
• Im SJ, Hashimoto M, Gerner MY, et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature. 2016;537(7620):417–421.
   PubMed Web of Science ®Google Scholar
• Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006;439(7077):682–687.
   PubMed Web of Science ®Google Scholar
• Martinez GJ, Pereira RM, Aijo T, et al. The transcription factor NFAT promotes exhaustion of activated CD8(+) T cells. Immunity. 2015;42(2):265–278.
   PubMed Web of Science ®Google Scholar
• Mognol GP, Spreafico R, Wong V, et al. Exhaustion-associated regulatory regions in CD8(+) tumor-infiltrating T cells. Proc Natl Acad Sci U S A. 2017;114(13):E2776–e85.
   PubMed Web of Science ®Google Scholar
• Kao C, Oestreich KJ, Paley MA, et al. Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat Immunol. 2011;12(7):663–671.
   PubMed Web of Science ®Google Scholar
• Doering TA, Crawford A, Angelosanto JM, et al. Network analysis reveals centrally connected genes and pathways involved in CD8+ T cell exhaustion versus memory. Immunity. 2012;37(6):1130–1144.
   PubMed Web of Science ®Google Scholar
• Quigley M, Pereyra F, Nilsson B, et al. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med. 2010;16(10):1147–1151.
   PubMed Web of Science ®Google Scholar
• Man K, Gabriel SS, Liao Y, et al. Transcription factor IRF4 promotes CD8(+) T cell exhaustion and limits the development of memory-like T cells during chronic infection. Immunity. 2017;47(6):1129–1141.e5.
   PubMed Web of Science ®Google Scholar
• Sen DR, Kaminski J, Barnitz RA, et al. The epigenetic landscape of T cell exhaustion. Science. 2016;354(6316):1165–1169.
   PubMed Web of Science ®Google Scholar
• Scott-Browne JP, Lopez-Moyado IF, Trifari S, et al. Dynamic changes in chromatin accessibility occur in CD8(+) T cells responding to viral infection. Immunity. 2016;45(6):1327–1340.
   Web of Science ®Google Scholar
• Sekiya T, Kashiwagi I, Inoue N, et al. The nuclear orphan receptor Nr4a2 induces Foxp3 and regulates differentiation of CD4+ T cells. Nat Commun. 2011;2(1):269.
   Web of Science ®Google Scholar
• Hill JA, Feuerer M, Tash K, et al. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory T cell transcriptional signature. Immunity. 2007;27(5):786–800.
   PubMed Web of Science ®Google Scholar
• Lin W, Haribhai D, Relland LM, et al. Regulatory T cell development in the absence of functional Foxp3. Nat Immunol . 2007;8(4):359–368.
   PubMed Web of Science ®Google Scholar
• Moran AE, Holzapfel KL, Xing Y, et al. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med. 2011;208(6):1279–1289.
   Web of Science ®Google Scholar
• Wei G, Wei L, Zhu J, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity. 2009;30(1):155–167.
   PubMed Web of Science ®Google Scholar
• Sekiya T, Kashiwagi I, Yoshida R, et al. Nr4a receptors are essential for thymic regulatory T cell development and immune homeostasis. Nat Immunol. 2013;14(3):230–237.
   Web of Science ®Google Scholar
• Sekiya T, Kondo T, Shichita T, et al. Suppression of Th2 and Tfh immune reactions by Nr4a receptors in mature T reg cells. J Exp Med. 2015;212(10):1623–1640.
   Web of Science ®Google Scholar
• Nowyhed HN, Huynh TR, Thomas GD, et al. Cutting edge: the orphan nuclear receptor Nr4a1 regulates CD8+ T cell expansion and effector function through direct repression of Irf4. J Immunol. 2015;195(8):3515–3519.
   Web of Science ®Google Scholar
• Nowyhed HN, Huynh TR, Blatchley A, et al. The nuclear receptor nr4a1 controls CD8 T cell development through transcriptional suppression of runx3. Sci Rep. 2015;5(1):9059.
   Web of Science ®Google Scholar
• Liu X, Wang Y, Lu H, et al. Genome-wide analysis identifies NR4A1 as a key mediator of T cell dysfunction. Nature. 2019;567(7749):525–529.
   PubMed Web of Science ®Google Scholar
• Hibino S, Chikuma S, Kondo T, et al. Inhibition of Nr4a receptors enhances antitumor immunity by breaking Treg-mediated immune tolerance. Cancer Res. 2018;78(11):3027–3040.
   PubMed Web of Science ®Google Scholar
• Alfei F, Kanev K, Hofmann M, et al. TOX reinforces the phenotype and longevity of exhausted T cells in chronic viral infection. Nature. 2019;571(7764):265–269.
   PubMed Web of Science ®Google Scholar
• Khan O, Giles JR, McDonald S, Manne S, et al. TOX transcriptionally and epigenetically programs CD8(+) T cell exhaustion. Nature. 2019;571(7764):211–218.
   PubMed Web of Science ®Google Scholar
• Scott AC, Dundar F, Zumbo P, et al. TOX is a critical regulator of tumour-specific T cell differentiation. Nature. 2019;571(7764):270–274.
   PubMed Web of Science ®Google Scholar
• Seo H, Chen J, Gonzalez-Avalos E, et al. TOX and TOX2 transcription factors cooperate with NR4A transcription factors to impose CD8(+) T cell exhaustion. Proc Natl Acad Sci U S A. 2019;116(25):12410–12415.
   PubMed Web of Science ®Google Scholar
• Yao C, Sun HW, Lacey NE, et al. Single-cell RNA-seq reveals TOX as a key regulator of CD8(+) T cell persistence in chronic infection. Nat Immunol. 2019;20(7):890–901.
   PubMed Web of Science ®Google Scholar
• Mann TH, Kaech SM. Tick-TOX, it’s time for T cell exhaustion. Nat Immunol. 2019;20(9):1092–1094.
   Web of Science ®Google Scholar
• Kagoya Y, Nakatsugawa M, Ochi T, Cen Y, et al. Transient stimulation expands superior antitumor T cells for adoptive therapy. JCI Insight. 2017;2(2):e89580.
   Web of Science ®Google Scholar
• Kagoya Y, Nakatsugawa M, Yamashita Y, et al. BET bromodomain inhibition enhances T cell persistence and function in adoptive immunotherapy models. J Clin Invest. 2016;126(9):3479–3494.
   PubMed Web of Science ®Google Scholar
• Kagoya Y, Tanaka S, Guo T, et al. A novel chimeric antigen receptor containing a JAK-STAT signaling domain mediates superior antitumor effects. Nat Med. 2018;24(3):352–359.
   PubMed Web of Science ®Google Scholar
• Alvarez-Fernandez C, Escriba-Garcia L, Vidal S, et al. A short CD3/CD28 costimulation combined with IL-21 enhance the generation of human memory stem T cells for adoptive immunotherapy. J Transl Med. 2016;14:214.
   Web of Science ®Google Scholar
• Nishimura T, Kaneko S, Kawana-Tachikawa A, et al. Generation of rejuvenated antigen-specific T cells by reprogramming to pluripotency and redifferentiation. Cell Stem Cell. 2013;12(1):114–126.
   PubMed Web of Science ®Google Scholar
• Vizcardo R, Masuda K, Yamada D, et al. Regeneration of human tumor antigen-specific T cells from iPSCs derived from mature CD8+ T cells. Cell Stem Cell. 2013;12(1):31–36.
   Web of Science ®Google Scholar
• Kawamoto H, Masuda K, Nagano S, et al. Cloning and expansion of antigen-specific T cells using iPS cell technology: development of “off-the-shelf” T cells for the use in allogeneic transfusion settings. Int J Hematol. 2018;107(3):271–277.
   Web of Science ®Google Scholar
• Minagawa A, Yoshikawa T, Yasukawa M, et al. Enhancing T cell receptor stability in rejuvenated iPSC-derived T cells improves their use in cancer immunotherapy. Cell Stem Cell. 2018;23(6):850–858.e4.
   Web of Science ®Google Scholar
• Sabatino M, Hu J, Sommariva M, et al. Generation of clinical-grade CD19-specific CAR-modified CD8+ memory stem cells for the treatment of human B-cell malignancies. Blood. 2016;128(4):519–528.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Speiser DE, Lichterfeld M, et al. T memory stem cells in health and disease. Nat Med. 2017;23(1):18–27.
   PubMed Web of Science ®Google Scholar
• Park JH, Riviere I, Gonen M, et al. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N Engl J Med. 2018;378(5):449–459.
   PubMed Web of Science ®Google Scholar
• Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439–448.
   PubMed Web of Science ®Google Scholar
• Kershaw MH, Westwood JA, Parker LL, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12(20):6106–6115.
   PubMed Web of Science ®Google Scholar
• Jensen MC, Popplewell L, Cooper LJ, et al. Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol Blood Marrow Transplant. 2010;16(9):1245–1256.
   PubMed Web of Science ®Google Scholar
• Lamers CH, Gratama JW, Pouw NM, et al. Parallel detection of transduced T lymphocytes after immunogene therapy of renal cell cancer by flow cytometry and real-time polymerase chain reaction: implications for loss of transgene expression. Hum Gene Ther. 2005;16(12):1452–1462.
   PubMed Web of Science ®Google Scholar
• Levine BL, Miskin J, Wonnacott K, et al. Global manufacturing of CAR T cell therapy. Mol Ther Methods Clin Dev. 2017;4:92–101.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Zhong X-S, Palmer DC, et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat Med. 2009;15(7):808–813.
   PubMed Web of Science ®Google Scholar
• Jeza VT, Li X, Chen J, et al. IL-21 augments rapamycin in expansion of alpha fetoprotein antigen specific stem-cell-like memory T cells in vitro. Pan Afr Med J. 2017;27:163.
   Web of Science ®Google Scholar
• van der Waart AB, van de Weem NM, Maas F, et al. Inhibition of Akt signaling promotes the generation of superior tumor-reactive T cells for adoptive immunotherapy. Blood. 2014;124(23):3490–3500.
   Web of Science ®Google Scholar
• Scholz G, Jandus C, Zhang L, et al. Modulation of mTOR signalling triggers the formation of stem cell-like memory T cells. EBioMedicine. 2016;4:50–61.
   Web of Science ®Google Scholar
• Kondo T, Imura Y, Chikuma S, et al. Generation and application of human induced-stem cell memory T cells for adoptive immunotherapy. Cancer Sci. 2018;109(7):2130–2140.
   Web of Science ®Google Scholar
• Kondo T, Morita R, Okuzono Y, et al. Notch-mediated conversion of activated T cells into stem cell memory-like T cells for adoptive immunotherapy. Nat Commun. 2017;8(1):15338.
   Web of Science ®Google Scholar
• Kondo T, Ando M, Nagai N, et al. The NOTCH-FOXM1 axis plays a key role in mitochondrial biogenesis in the induction of human stem cell memory-like CAR-T cells. Cancer Res. 2019. pii: canres.1196.2019. DOI:10.1158/0008-5472.CAN-19-1196.
   Google Scholar
• O'Sullivan D. The metabolic spectrum of memory T cells. Immunol Cell Biol. 2019;97:636–646.
   Web of Science ®Google Scholar
• Sukumar M, Liu J, Ji Y, et al. Inhibiting glycolytic metabolism enhances CD8+ T cell memory and antitumor function. J Clin Invest. 2013;123(10):4479–4488.
   PubMed Web of Science ®Google Scholar
• Crompton JG, Sukumar M, Roychoudhuri R, et al. Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res. 2015;75(2):296–305.
   PubMed Web of Science ®Google Scholar
• Klebanoff CA, Crompton JG, Leonardi AJ, et al. Inhibition of AKT signaling uncouples T cell differentiation from expansion for receptor-engineered adoptive immunotherapy. JCI Insight. 2017;2(23):e95103.
   PubMed Web of Science ®Google Scholar
• Mousset CM, Hobo W, Ji Y, et al. Ex vivo AKT-inhibition facilitates generation of polyfunctional stem cell memory-like CD8(+) T cells for adoptive immunotherapy. Oncoimmunology. 2018;7(10):e1488565.
   PubMed Web of Science ®Google Scholar
• Pilipow K, Scamardella E, Puccio S, et al. Antioxidant metabolism regulates CD8+ T memory stem cell formation and antitumor immunity. JCI Insight. 2018;3(18):e122299.
   Web of Science ®Google Scholar
• Loschinski R, Bottcher M, Stoll A, et al. IL-21 modulates memory and exhaustion phenotype of T-cells in a fatty acid oxidation-dependent manner. Oncotarget. 2018;9(17):13125–13138.
   Google Scholar
• Chen J, Lopez-Moyado IF, Seo H, et al. NR4A transcription factors limit CAR T cell function in solid tumours. Nature. 2019;567(7749):530–534.
   PubMed Web of Science ®Google Scholar