Memory T cells: strategies for optimizing tumor immunotherapy

Qingjun Liu, Zhongjie Sun, Ligong Chen

PDF(971 KB)
PDF(971 KB)
Protein Cell ›› DOI: 10.1007/s13238-020-00707-9
REVIEW

Memory T cells: strategies for optimizing tumor immunotherapy

Author information +
History +

Abstract

Several studies have demonstrated that memory T cells including stem cell memory (Tscm) T cells and central memory (Tcm) T cells show superior persistence and antitumor immunity compared with effector memory T (Tem) cells and effector T (Teff) cells. Furthermore, the Tcm/Teff ratio has been reported to be a predictive biomarker of immune responses against some tumors. Thus, a system-level understanding of the mechanisms underlying the differentiation of effector and memory T cells is of increasing importance for developing immunological strategies against various tumors. This review focuses on recent advances in efficacy against tumors, the origin, formation mechanisms of memory T cells, and the role of the gut microbiota in memory T cell formation. Furthermore, we summarize strategies to generate memory T cells in (ex) vivo that, might be applicable in clinical practice.

Keywords

memory T cells / tumor immunology / metabolism / gut microbiota

Cite this article

Download citation ▾
Qingjun Liu, Zhongjie Sun, Ligong Chen. Memory T cells: strategies for optimizing tumor immunotherapy. Protein Cell, https://doi.org/10.1007/s13238-020-00707-9

References

[1]
Adachi K, Kano Y, Nagai T, Okuyama N, Sakoda Y, Tamada K (2018) IL-7 and CCL19 expression in CAR-T cells improves immune cell infiltration and CAR-T cell survival in the tumor. Nat Biotechnol 36:346–351
CrossRef Google scholar
[2]
Ahlers JD, Belyakov IM (2010) Memories that last forever: strategies for optimizing vaccine T-cell memory. Blood 115:1678–1689
CrossRef Google scholar
[3]
Ahlers JD, Belyakov IM, Terabe M, Koka R, Donaldson DD, Thomas EK, Berzofsky JA (2002) A push-pull approach to maximize vaccine efficacy: abrogating suppression with an IL-13 inhibitor while augmenting help with granulocyte/macrophage colonystimulating factor and CD40L. Proc Natl Acad Sci U S A 99:13020–13025
CrossRef Google scholar
[4]
Ahonen CL, Doxsee CL, McGurran SM, Riter TR, Wade WF, Barth RJ, Vasilakos JP, Noelle RJ, Kedl RM (2004) Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J Exp Med 199:775–784
CrossRef Google scholar
[5]
Akondy RS, Fitch M, Edupuganti S, Yang S, Kissick HT, Li KW, Youngblood BA, Abdelsamed HA, McGuire DJ, Cohen KW et al (2017) Origin and differentiation of human memory CD8 T cells after vaccination. Nature 552:362–367
CrossRef Google scholar
[6]
Alspach E, Lussier DM, Miceli AP, Kizhvatov I, DuPage M, Luoma AM, Meng W, Lichti CF, Esaulova E, Vomund AN et al (2019) MHC-II neoantigens shape tumour immunity and response to immunotherapy. Nature 574:696–701
CrossRef Google scholar
[7]
Araki K, Turner AP, Shaffer VO, Gangappa S,Keller SA, Bachmann MF, Larsen CP, Ahmed R (2009) mTOR regulates memory CD8 T-cell differentiation. Nature 460:108–112
CrossRef Google scholar
[8]
Bachem A, Makhlouf C, Binger KJ, de Souza DP, Tull D, Hochheiser K, Whitney PG, Fernandez-Ruiz D, Dahling S, Kastenmuller W et al (2019) Microbiota-derived short-chain fatty acids promote the memory potential of antigen-activated CD8(+) T cells. Immunity 51(2):285–297.e5
CrossRef Google scholar
[9]
Badovinac VP, Messingham KA, Griffith TS, Harty JT (2006) TRAIL deficiency delays, but does not prevent, erosion in the quality of “helpless” memory CD8 T cells. J Immunol 177:999–1006
CrossRef Google scholar
[10]
Barski A, Cuddapah S, Kartashov AV, Liu C, Imamichi H, Yang W, Peng W, Lane HC, Zhao K (2017) Rapid recall ability of memory T cells is encoded in their epigenome. Sci Rep 7:39785
CrossRef Google scholar
[11]
Battaglia M, Stabilini A, Roncarolo MG (2005) Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 105:4743–4748
CrossRef Google scholar
[12]
Bell JJ, Ellis JS, Guloglu FB, Tartar DM, Lee HH, Divekar RD, Jain R, Yu P, Hoeman CM, Zaghouani H (2008) Early effector T cells producing significant IFN-gamma develop into memory. J Immunol 180:179–187
CrossRef Google scholar
[13]
Berger C, Jensen MC, Lansdorp PM, Gough M, Elliott C, Riddell SR (2008) Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 118:294–305
CrossRef Google scholar
[14]
Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey KA, Thompson EA, Fraser KA, Rosato PC, Filali-Mouhim A et al (2016) Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532:512–516
CrossRef Google scholar
[15]
Bevan MJ (2004) Helping the CD8(+) T-cell response. Nat Rev Immunol 4:595–602
CrossRef Google scholar
[16]
Blank CU, Haining WN, Held W, Hogan PG, Kallies A, Lugli E, Lynn RC, Philip M, Rao A, Restifo NP et al (2019) Defining ‘T cell exhaustion’. Nat Rev Immunol 19:665–674
CrossRef Google scholar
[17]
Blankenstein T, Coulie PG, Gilboa E, Jaffee EM (2012) The determinants of tumour immunogenicity. Nat Rev Cancer 12:307–313
CrossRef Google scholar
[18]
Borges da Silva H, Beura LK, Wang H, Hanse EA, Gore R, Scott MC, Walsh DA, Block KE, Fonseca R, Yan Y et al (2018) The purinergic receptor P2RX7 directs metabolic fitness of long-lived memory CD8(+) T cells. Nature 559:264–268
CrossRef Google scholar
[19]
Brown EM, Kenny DJ, Xavier RJ (2019) Gut microbiota regulation of Tcells during inflammation and autoimmunity. Annu Rev Immunol 37:599–624
CrossRef Google scholar
[20]
Butler MO, Lee JS, Ansen S, Neuberg D, Hodi FS, Murray AP, Drury L, Berezovskaya A, Mulligan RC, Nadler LM et al (2007) Longlived antitumor CD8+ lymphocytes for adoptive therapy generated using an artificial antigen-presenting cell. Clin Cancer Res 13:1857–1867
CrossRef Google scholar
[21]
Butler MO, Friedlander P, Milstein MI, Mooney MM, Metzler G, Murray AP, Tanaka M, Berezovskaya A, Imataki O, Drury L et al (2011) Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Sci Transl Med 3:80ra34
CrossRef Google scholar
[22]
Carrio R, Bathe OF, Malek TR (2004) Initial antigen encounter programs CD8+ T cells competent to develop into memory cells that are activated in an antigen-free, IL-7- and IL-15-rich environment. J Immunol 172:7315–7323
CrossRef Google scholar
[23]
Chang JT, Palanivel VR, Kinjyo I, Schambach F, Intlekofer AM, Banerjee A, Longworth SA, Vinup KE, Mrass P, Oliaro J et al (2007) Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315:1687–1691
CrossRef Google scholar
[24]
Cieri N, Camisa B, Cocchiarella F, Forcato M, Oliveira G, Provasi E, Bondanza A, Bordignon C, Peccatori J,Ciceri F et al (2013) IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood 121:573–584
CrossRef Google scholar
[25]
Crompton JG, Sukumar M, Roychoudhuri R, Clever D, Gros A, Eil RL, Tran E, Hanada K, Yu Z, Palmer DC et al (2015) Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res 75:296–305
CrossRef Google scholar
[26]
Dolfi DV, Boesteanu AC, Petrovas C, Xia D, Butz EA, Katsikis PD (2008) Late signals from CD27 prevent Fas-dependent apoptosis of primary CD8+ T cells. J Immunol 180:2912–2921
CrossRef Google scholar
[27]
Dudley ME, Wunderlich JR, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry RM, Marincola FM, Leitman SF, Seipp CA et al (2002) A phase I study of nonmyeloablative chemotherapy and adoptive transfer of autologous tumor antigen-specific T lymphocytes in patients with metastatic melanoma. J Immunother 25:243–251
CrossRef Google scholar
[28]
Eil R, Vodnala SK, Clever D, Klebanoff CA, Sukumar M, Pan JH, Palmer DC, Gros A, Yamamoto TN, Patel SJ et al (2016) Ionic immune suppression within the tumour microenvironment limits T cell effector function. Nature 537:539–543
CrossRef Google scholar
[29]
Farber DL, Acuto O, Bottomly K (1997) Differential T cell receptormediated signaling in naive and memory CD4 T cells. Eur J Immunol 27:2094–2101
CrossRef Google scholar
[30]
Farber DL, Yudanin NA, Restifo NP (2014) Human memory T cells: generation, compartmentalization and homeostasis. Nat Rev Immunol 14:24–35
CrossRef Google scholar
[31]
Feuerer M, Rocha M, Bai L,Umansky V,Solomayer E-F, Bastert G, Diel IJ, Schirrmacher V (2001) Enrichment of memory T cells and other profound immunological changes in the bone marrow from untreated breast cancer patients. Int J Cancer 92:96–105
CrossRef Google scholar
[32]
Fos C, Salles A, Lang V, Carrette F, Audebert S, Pastor S, Ghiotto M, Olive D, Bismuth G, Nunes JA (2008) ICOS ligation recruits the p50alpha PI3K regulatory subunit to the immunological synapse. J Immunol 181:1969–1977
CrossRef Google scholar
[33]
Fridman WH, Pagès F, Sautès-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306
CrossRef Google scholar
[34]
Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C et al (2011) A human memory T cell subset with stem cell-like properties. Nat Med 17:1290–1297
CrossRef Google scholar
[35]
Geginat J, Sallusto F, Lanzavecchia A (2001) Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells. J Exp Med 194:1711–1719
CrossRef Google scholar
[36]
Geiger R, Rieckmann JC, Wolf T, Basso C,Feng Y, Fuhrer T, Kogadeeva M, Picotti P, Meissner F, Mann M et al (2016) L-Arginine modulates T cell metabolism and enhances survival and anti-tumor activity. Cell 167(829–842):e813
CrossRef Google scholar
[37]
Goc J, Hepworth MR, Sonnenberg GF (2015) Group 3 innate lymphoid cells: regulating host–commensal bacteria interactions in inflammation and cancer. Int Immunol 28(1):43–52
CrossRef Google scholar
[38]
Golubovskaya V, Wu L (2016) Different subsets of T cells, memory, effector functions, and CAR-T immunotherapy. Cancers (Basel).https://doi.org/10.3390/cancers8030036
CrossRef Google scholar
[39]
Gomez-Eerland R, Nuijen B, Heemskerk B,van Rooij N, van den Berg JH, Beijnen JH, Uckert W, Kvistborg P,Schumacher TN, Haanen JB et al (2014) Manufacture of gene-modified human T-cells with a memory stem/central memory phenotype. Hum Gene Ther Methods 25:277–287
CrossRef Google scholar
[40]
Gopalakrishnan V, Helmink BA, Spencer CN, Reuben A, Wargo JA (2018a) The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy. Cancer Cell 33:570–580
CrossRef Google scholar
[41]
Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC et al (2018b) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359:97–103
[42]
Greene TT, Labarta-Bajo L, Zuniga EI (2018) Dangerously fit: extracellular ATP aids memory T cell metabolism. Immunity 49:208–210
CrossRef Google scholar
[43]
Haining WN, Ebert BL, Subrmanian A, Wherry EJ, Eichbaum Q, Evans JW, Mak R, Rivoli S, Pretz J, Angelosanto J et al (2008) Identification of an evolutionarily conserved transcriptional signature of CD8 memory differentiation that is shared by T and B cells. J Immunol 181:1859–1868
CrossRef Google scholar
[44]
Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, This S,Danne C, Campion S, Duncan SH et al (2017) Circulating and tissue-resident CD4(+) T cells with reactivity to intestinal microbiota are abundant in healthy individuals and function is altered during inflammation. Gastroenterology 153:1320–1337.e1316
CrossRef Google scholar
[45]
Hendriks J, Xiao Y, Rossen JW, van der Sluijs KF, Sugamura K, Ishii N, Borst J (2005) During viral infection of the respiratory tract, CD27, 4-1BB, and OX40 collectively determine formation of CD8+ memory T cells and their capacity for secondary expansion. J Immunol 175:1665–1676
CrossRef Google scholar
[46]
Herndler-Brandstetter D, Ishigame H, Shinnakasu R,Plajer V, Stecher C,Zhao J, Lietzenmayer M, Kroehling L, Takumi A, Kometani K et al (2018) KLRG1(+) effector CD8(+) T cells lose KLRG1, differentiate into all memory T cell lineages, and convey enhanced protective immunity. Immunity 48(716–729):e718
CrossRef Google scholar
[47]
Hikono H, Kohlmeier JE, Takamura S, Wittmer ST, Roberts AD, Woodland DL (2007) Activation phenotype, rather than central- or effector-memory phenotype, predicts the recall efficacy of memory CD8+ T cells. J Exp Med 204:1625–1636
CrossRef Google scholar
[48]
Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R,Yu Z, Sanchez-Perez L, Muranski P,Kern SJ, Logun C et al (2009) Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci U S A 106:17469–17474
CrossRef Google scholar
[49]
Hu X, Majchrzak K, Liu X, Wyatt MM, Spooner CJ, Moisan J, Zou W, Carter LL, Paulos CM (2018) In vitro priming of adoptively transferred t cells with a RORgamma agonist confers durable memory and stemness in vivo. Cancer Res 78:3888–3898
CrossRef Google scholar
[50]
Huda MN, Ahmad SM, Alam MJ, Khanam A, Kalanetra KM, Taft DH, Raqib R, Underwood MA, Mills DA, Stephensen CB (2019) Bifidobacterium abundance in early infancy and vaccine response at 2 years of age. Pediatrics 143:e20181489
CrossRef Google scholar
[51]
Hussain SF, Anderson CF, Farber DL (2002) Differential SLP-76 expression and TCR-mediated signaling in effector and memory CD4 T cells. J Immunol 168:1557–1565
CrossRef Google scholar
[52]
Huster KM, Busch V, Schiemann M,Linkemann K, Kerksiek KM, Wagner H, Busch DH (2004) Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc Natl Acad Sci U S A 101:5610–5615
CrossRef Google scholar
[53]
Ichii H, Sakamoto A, Kuroda Y, Tokuhisa T (2004) Bcl6 acts as an amplifier for the generation and proliferative capacity of central memory CD8+ T cells. J Immunol 173:883–891
CrossRef Google scholar
[54]
Ignacio A, Morales CI, Câmara NOS, Almeida RR (2016) Innate sensing of the gut microbiota: modulation of inflammatory and autoimmune diseases. Front Immuno l 7:54–54
CrossRef Google scholar
[55]
Intlekofer AM, Takemoto N, Kao C, Banerjee A, Schambach F,Northrop JK, Shen H, Wherry EJ, Reiner SL (2007) Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J Exp Med 204:2015–2021
CrossRef Google scholar
[56]
Jabbari A, Harty JT (2005) Cutting edge: differential self-peptide/MHC requirement for maintaining CD8 T cell function versus homeostatic proliferation. J Immunol 175:4829–4833
CrossRef Google scholar
[57]
Jansen CS, Prokhnevska N, Master VA, Sanda MG, Carlisle JW, Bilen MA, Cardenas M, Wilkinson S, Lake R, Sowalsky AG et al (2019) An intra-tumoral niche maintains and differentiates stemlike CD8 T cells. Nature 576:465–470
CrossRef Google scholar
[58]
Jin Y, Dong H, Xia L, Yang Y, Zhu Y, Shen Y, Zheng H, Yao C, Wang Y, Lu S (2019) The diversity of gut microbiome is associated with favorable responses to anti-programmed death 1 immunotherapy in chinese patients with NSCLC. J Thorac Oncol 14:1378–1389
CrossRef Google scholar
[59]
Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, Kammula US, Royal RE, Sherry RM, Wunderlich JR et al (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114:535–546
CrossRef Google scholar
[60]
Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, Gapin L, Kaech SM (2007) Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281–295
CrossRef Google scholar
[61]
Kaech SM, Hemby S, Kersh E, Ahmed R (2002) Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111:837–851
CrossRef Google scholar
[62]
Kersh EN, Kaech SM, Onami TM, Moran M, Wherry EJ, Miceli MC, Ahmed R (2003) TCR signal transduction in antigen-specific memory CD8 T cells. J Immunol 170:5455–5463
CrossRef Google scholar
[63]
Klarquist J, Chitrakar A, Pennock ND, Kilgore AM, Blain T, Zheng C, Danhorn T, Walton K, Jiang L, Sun J et al (2018) Clonal expansion of vaccine-elicited T cells is independent of aerobic glycolysis. Sci Immunol.https://doi.org/10.1126/sciimmunol. aas9822
CrossRef Google scholar
[64]
Klebanoff CA, Finkelstein SE, Surman DR, Lichtman MK, Gattinoni L, Theoret MR, Grewal N, Spiess PJ, Antony PA, Palmer DC et al (2004) IL-15 enhances the in vivo antitumor activity of tumorreactive CD8+ T cells. Proc Natl Acad Sci U S A 101:1969–1974
CrossRef Google scholar
[65]
Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, Palmer DC, Antony PA, Hwang ST, Rosenberg SA et al (2005) Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 102:9571–9576
CrossRef Google scholar
[66]
Klebanoff CA, Gattinoni L, Restifo NP (2006) CD8+ T-cell memory in tumor immunology and immunotherapy. Immunol Rev 211:214–224
CrossRef Google scholar
[67]
Klebanoff CA, Scott CD, Leonardi AJ, Yamamoto TN, Cruz AC, Ouyang C, Ramaswamy M, Roychoudhuri R, Ji Y,Eil RL et al (2016) Memory T cell-driven differentiation of naive cells impairs adoptive immunotherapy. J Clin Invest 126:318–334
CrossRef Google scholar
[68]
Klonowski KD, Lefrancois L (2005) The CD8 memory T cell subsystem: integration of homeostatic signaling during migration. Semin Immunol 17:219–229
CrossRef Google scholar
[69]
Kocak E, Lute K, Chang X, May KF Jr,Exten KR, Zhang H, Abdessalam SF, Lehman AM, Jarjoura D, Zheng P et al (2006) Combination therapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res 66:7276–7284
CrossRef Google scholar
[70]
Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202:637–650
CrossRef Google scholar
[71]
Kopf H, de la Rosa GM, Howard OM, Chen X (2007) Rapamycin inhibits differentiation of Th17 cells and promotes generation of FoxP3+ T regulatory cells. Int Immunopharmacol 7:1819–1824
CrossRef Google scholar
[72]
Krieg C, Boyman O, Fu YX, Kaye J (2007) B and T lymphocyte attenuator regulates CD8+ T cell-intrinsic homeostasis and memory cell generation. Nat Immunol 8:162–171
CrossRef Google scholar
[73]
Kubinak JL, Petersen C, Stephens WZ, Soto R, Bake E,O’Connell RM, Round JL (2015) MyD88 signaling in T cells directs IgAmediated control of the microbiota to promote health. Cell Host Microbe 17:153–163
CrossRef Google scholar
[74]
Lai W, Yu M, Huang MN, Okoye F, Keegan AD, Farber DL (2011) Transcriptional control of rapid recall by memory CD4 T cells. J Immunol 187:133–140
CrossRef Google scholar
[75]
Lanzavecchia A,Sallusto F (2001) Regulation of T cell immunity by dendritic cells. Cell 106:263–266
CrossRef Google scholar
[76]
Li X, Wenes M, Romero P,Huang SC, Fendt SM, Ho PC (2019) Navigating metabolic pathways to enhance antitumour immunity and immunotherapy. Nat Rev Clin Oncol 16(7):425–441
CrossRef Google scholar
[77]
Liu QJ, Gao B (2008) Manipulation of MHC-I/TCR interaction for immune therapy. Cell Mol Immunol 5:171–182
CrossRef Google scholar
[78]
Liu Z, Dai H, Wan N, Wang T, Bertera S, Trucco M, Dai Z(2007) Suppression of memory CD8 T cell generation and function by tryptophan catabolism. J Immunol 178:4260–4266
CrossRef Google scholar
[79]
Ma A, Koka R, Burkett P (2006) Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 24:657–679
CrossRef Google scholar
[80]
Mahnke YD, Schwendemann J, Beckhove P, Schirrmacher V (2005) Maintenance of long-term tumour-specific T-cell memory by residual dormant tumour cells. Immunology 115:325–336
CrossRef Google scholar
[81]
Manjarrez-Orduno N, Menard LC, Kansal S,Fischer P, Kakrecha B, Jiang C,Cunningham M,Greenawalt D, Patel V, Yang M et al (2018) Circulating T cell subpopulations correlate with immune responses at the tumor site and clinical response to PD1 inhibition in non-small cell lung cancer. Front Immunol 9:1613
CrossRef Google scholar
[82]
Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489:231–241
CrossRef Google scholar
[83]
McFall-Ngai M (2007) Care for the community. Nature 445:153–153
CrossRef Google scholar
[84]
Mehlhop-Williams ER, Bevan MJ (2014) Memory CD8+ T cells exhibit increased antigen threshold requirements for recall proliferation. J Exp Med 211:345–356
CrossRef Google scholar
[85]
Merino D, San Segundo D, Medina JM, Rodrigo E, Asensio E, Irure J, Fernandez-Fresnedo G,Arias MA, Lopez-Hoyos M (2016) Different in vitro proliferation and cytokine-production inhibition of memory T-cell subsets after calcineurin and mammalian target of rapamycin inhibitors treatment. Immunology 148:206–215
CrossRef Google scholar
[86]
Monteleone I, Rizzo A, Sarra M, Sica G, Sileri P, Biancone L, MacDonald TT, Pallone F,Monteleone G (2011) Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141:237–248.e231
CrossRef Google scholar
[87]
Mortier E, Bernard J,Plet A, Jacques Y (2004) Natural, proteolytic release of a soluble form of human IL-15 receptor alpha-chain that behaves as a specific, high affinity IL-15 antagonist. J Immunol 173:1681–1688
CrossRef Google scholar
[88]
Mortier E, Quemener A, Vusio P, Lorenzen I, Boublik Y, Grotzinger J,Plet A, Jacques Y(2006) Soluble interleukin-15 receptor alpha (IL-15R alpha)-sushi as a selective and potent agonist of IL-15 action through IL-15R beta/gamma. Hyperagonist IL-15 x IL-15R alpha fusion proteins. J Biol Chem 281:1612–1619
CrossRef Google scholar
[89]
Murali-Krishna K, Lau LL, Sambhara S, Lemonnier F,Altman J, Ahmed R (1999) Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 286:1377–1381
CrossRef Google scholar
[90]
Panthel K, Meinel KM, Sevil Domenech VE, Geginat G, Linkemann K, Busch DH, Russmann H (2006) Prophylactic anti-tumor immunity against a murine fibrosarcoma triggered by the Salmonella type III secretion system. Microbes Infect 8:2539–2546
CrossRef Google scholar
[91]
Park SL, Gebhardt T, Mackay LK (2019) Tissue-Resident Memory T Cells in Cancer Immunosurveillance. Trends Immunol 40:735–747
CrossRef Google scholar
[92]
Pearce EL, Shen H (2007) Generation of CD8 T cell memory is regulated by IL-12. J Immunol 179:2074–2081
CrossRef Google scholar
[93]
Pitt JM, Vetizou M, Waldschmitt N, Kroemer G,Chamaillard M, Boneca IG, Zitvogel L (2016) Fine-tuning cancer immunotherapy: optimizing the gut microbiome. Cancer Res 76:4602–4607
CrossRef Google scholar
[94]
Polic B, Kunkel D, Scheffold A, Rajewsky K (2001) How alpha beta T cells deal with induced TCR alpha ablation. Proc Natl Acad Sci U S A 98:8744–8749
CrossRef Google scholar
[95]
Powell DJ Jr, Dudley ME, Robbins PF, Rosenberg SA (2005) Transition of late-stage effector T cells to CD27+ CD28+ tumorreactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105:241–250
CrossRef Google scholar
[96]
Proietti M, Cornacchione V, Rezzonico Jost T, Romagnani A, Faliti CE, Perruzza L, Rigoni R, Radaelli E,Caprioli F, Preziuso S et al (2014) ATP-gated ionotropic P2X7 receptor controls follicular T helper cell numbers in Peyer’s patches to promote host-microbiota mutualism. Immunity 41:789–801
CrossRef Google scholar
[97]
Proietti M, Perruzza L, Scribano D, Pellegrini G, D’Antuono R, Strati F, Raffaelli M, Gonzalez SF, Thelen M, Hardt W-D et al (2019) ATP released by intestinal bacteria limits the generation of protective IgA against enteropathogens. Nat Commun 10:250–250
CrossRef Google scholar
[98]
Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, Huls MH, Liu E, Gee AP, Mei Z et al (2008) Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14:1264–1270
CrossRef Google scholar
[99]
Pulle G, Vidric M, Watts TH (2006) IL-15-dependent induction of 4-1BB promotes antigen-independent CD8 memory T cell survival. J Immunol 176:2739–2748
CrossRef Google scholar
[100]
Quemener A, Bernard J, Mortier E, Plet A, Jacques Y, Tran V (2006) Docking of human interleukin-15 to its specific receptor alpha chain: correlation between molecular modeling and mutagenesis experimental data. Proteins 65:623–636
CrossRef Google scholar
[101]
Reboursiere E, Gac AC, Garnier A, Salaun V, Reman O, Pham AD, Cabrera Q, Khoy K, Vilque JP, Fruchart C et al (2018) Increased frequencies of circulating and tumor-resident Vdelta1(+) T cells in patients with diffuse large B-cell lymphoma. Leuk Lymphoma 59:187–195
CrossRef Google scholar
[102]
Ribas A, Wolchok JD (2018) Cancer immunotherapy using checkpoint blockade. Science 359:1350–1355
CrossRef Google scholar
[103]
Riquelme E, Zhang Y,Zhang L, Montiel M, Zoltan M, Dong W, Quesada P, Sahin I, Chandra V,San Lucas Aet al (2019) Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell 178(795–806):e712
CrossRef Google scholar
[104]
Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR et al (2011) Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17:4550–4557
CrossRef Google scholar
[105]
Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323
CrossRef Google scholar
[106]
Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillere R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP et al (2018) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359:91–97
CrossRef Google scholar
[107]
Rubinstein MP, Kovar M, Purton JF, Cho JH, Boyman O, Surh CD, Sprent J (2006) Converting IL-15 to a superagonist by binding to soluble IL-15R{alpha}. Proc Natl Acad Sci U S A 103:9166–9171
CrossRef Google scholar
[108]
Sabbagh L, Pulle G, Liu Y, Tsitsikov EN, Watts TH (2008) ERKdependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo. J Immunol 180:8093–8101
CrossRef Google scholar
[109]
Sallusto F, Lenig D, Förster R,Lipp M, Lanzavecchia A (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708
CrossRef Google scholar
[110]
Sallusto F, Geginat J, Lanzavecchia A (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22:745–763
CrossRef Google scholar
[111]
Sanchez PJ, McWilliams JA, Haluszczak C, Yagita H, Kedl RM (2007) Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J Immunol 178:1564–1572
CrossRef Google scholar
[112]
Sanmamed MF, Chen L (2018) A paradigm shift in cancer immunotherapy: from enhancement to normalization. Cell 175:313–326
CrossRef Google scholar
[113]
Sarkar S, Kalia V,Haining WN, Konieczny BT, Subramaniam S, Ahmed R (2008) Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 205:625–640
CrossRef Google scholar
[114]
Schulz EG, Mariani L, Radbruch A, Hofer T (2009) Sequential polarization and imprinting of type 1 T helper lymphocytes by interferon-gamma and interleukin-12. Immunity 30:673–683
CrossRef Google scholar
[115]
Setoguchi R, Hori S,Takahashi T, Sakaguchi S (2005) Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201:723–735
CrossRef Google scholar
[116]
Setoguchi R, Matsui Y, Mouri K (2015) mTOR signaling promotes a robust and continuous production of IFN-gamma by human memory CD8+ T cells and their proliferation. Eur J Immunol 45:893–902
CrossRef Google scholar
[117]
Smith-Garvin JE, Koretzky GA, Jordan MS (2009) T Cell Activation. Annu Rev Immunol 27:591–619
CrossRef Google scholar
[118]
Sorini C, Cardoso RF, Gagliani N, Villablanca EJ (2018) Commensal bacteria-specific CD4+ T cell responses in health and disease. Front Immunol 9:2667
CrossRef Google scholar
[119]
Steggerda SM, Bennett MK, Chen J, Emberley E, Huang T, Janes JR, Li W, MacKinnon AL, Makkouk A, Marguier G et al (2017) Inhibition of arginase by CB-1158 blocks myeloid cell-mediated immune suppression in the tumor microenvironment. J Immunother Cancer 5:101
CrossRef Google scholar
[120]
Sun JC, Williams MA, Bevan MJ (2004) CD4+ Tcells are required for the maintenance, not programming, of memory CD8+ Tcells after acute infection. Nat Immunol 5:927–933
CrossRef Google scholar
[121]
Surh CD, Sprent J (2005) Regulation of mature T cell homeostasis. Semin Immunol 17:183–191
CrossRef Google scholar
[122]
Tanoue T, Morita S, Plichta DR, Skelly AN, Suda W, Sugiura Y, Narushima S,Vlamakis H, Motoo I, Sugita K et al (2019) A defined commensal consortium elicits CD8 T cells and anticancer immunity. Nature 565:600–605
CrossRef Google scholar
[123]
Tomayko MM, Anderson SM, Brayton CE, Sadanand S, Steinel NC, Behrens TW, Shlomchik MJ (2008) Systematic comparison of gene expression between murine memory and naive B cells demonstrates that memory B cells have unique signaling capabilities. J Immunol 181:27–38
CrossRef Google scholar
[124]
Unsoeld H, Pircher H (2005) Complex memory T-cell phenotypes revealed by coexpression of CD62L and CCR7. J Virol 79:4510–4513
CrossRef Google scholar
[125]
Uribe-Herranz M, Bittinger K, Rafail S, Guedan S, Pierini S, Tanes C, Ganetsky A, Morgan MA, Gill S, Tanyi JL et al (2018) Gut microbiota modulates adoptive cell therapy via CD8α dendritic cells and IL-12. JCI insight 3:e94952
CrossRef Google scholar
[126]
Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP et al (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350:1079–1084
CrossRef Google scholar
[127]
Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D,Enot DP, Pfirschke C, Engblom C, Pittet MJ et al (2013) The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342:971–976
CrossRef Google scholar
[128]
Wang D (2018) The essential role of G protein-coupled receptor (GPCR) signaling in regulating T cell immunity. Immunopharmacol Immunotoxicol 40:187–192
CrossRef Google scholar
[129]
Wang GY, Zhang Q, Yang Y,Chen WJ, Liu W, Jiang N, Chen GH (2012) Rapamycin combined with allogenic immature dendritic cells selectively expands CD4+CD25+Foxp3+ regulatory T cells in rats. Hepatobiliary Pancreat Dis Int 11:203–208
CrossRef Google scholar
[130]
Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian UH, Ahmed R (2003) Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 4:225–234
CrossRef Google scholar
[131]
Whitmire JK, Eam B, Benning N, Whitton JL (2007) Direct interferongamma signaling dramatically enhances CD4+ and CD8+ T cell memory. J Immunol 179:1190–1197
CrossRef Google scholar
[132]
Williams MA, Bevan MJ (2007) Effector and memory CTL differentiation. Annu Rev Immunol 25:171–192
CrossRef Google scholar
[133]
Williams MA, Ravkov EV, Bevan MJ (2008) Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity 28:533–545
CrossRef Google scholar
[134]
Wlodarska M, Thaiss CA, Nowarski R, Henao-Mejia J, Zhang J-P, Brown EM, Frankel G, Levy M, Katz MN, Philbrick WM et al (2014) NLRP6 inflammasome orchestrates the colonic hostmicrobial interface by regulating goblet cell mucus secretion. Cell 156:1045–1059
CrossRef Google scholar
[135]
Yang J, Brook MO, Carvalho-Gaspar M, Zhang J, Ramon HE, Sayegh MH, Wood KJ, Turka LA, Jones ND (2007) Allograft rejection mediated by memory T cells is resistant to regulation. Proc Natl Acad Sci U S A 104:19954–19959
CrossRef Google scholar
[136]
Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, Greenberg PD (2002) Adoptive T cell therapy using antigenspecific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 99:16168–16173
CrossRef Google scholar
[137]
Youngblood B, Hale JS, Kissick HT, Ahn E, Xu X, Wieland A, Araki K, West EE, Ghoneim HE, Fan Y et al (2017) Effector CD8 Tcells dedifferentiate into long-lived memory cells. Nature 552:404 Zhang L-J, Gallo RL (2016) Antimicrobial peptides. Curr Biol CB 26: R14–R19
CrossRef Google scholar

RIGHTS & PERMISSIONS

2020 The Author(s)
AI Summary AI Mindmap
PDF(971 KB)

Accesses

Citations

Detail

Sections
Recommended

/