Modulation of mTOR Signalling Triggers the Formation of Stem Cell-like Memory T Cells

EBioMedicine

Volumn 4, Issue , 2016, Pages 50-61

  Dormond, Olivier ^c   Romero, Pedro ^a,c   Zhang, Lianjun ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Adoptive cell transfer therapy; Human T cells; Rapamycin; T cell differentiation

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; OLIGOMYCIN; PALMITIC ACID; RAPAMYCIN; TRANSCRIPTOME; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE; TARGET OF RAPAMYCIN KINASE; TWS 119;

ACIDIFICATION; ANIMAL EXPERIMENT; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; EXTRACELLULAR ACIDIFICATION RATE; FATTY ACID OXIDATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GLYCOLYSIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; MODULATION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; RNA SEQUENCE; STEM CELL LIKE MEMORY T CELL; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOPOIESIS; METABOLISM; PRE T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOPOIESIS; MICE; MULTIPROTEIN COMPLEXES; PRECURSOR CELLS, T-LYMPHOID; PYRIMIDINES; PYRROLES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84955561490     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.01.019     Document Type: Article

References (43)

1. Amarnath, S., Flomerfelt, F.A., Costanzo, C.M., Foley, J.E., Mariotti, J., Konecki, D.M., Gangopadhyay, A., Eckhaus, M., Wong, S., Levine, B.L., et al. Rapamycin generates anti-apoptotic human Th1/Tc1 cells via autophagy for induction of xenogeneic GVHD. Autophagy 6 (2010), 523–541.
2. Araki, K., Turner, A.P., Shaffer, V.O., Gangappa, S., Keller, S.A., Bachmann, M.F., Larsen, C.P., Ahmed, R., mTOR regulates memory CD8 T-cell differentiation. Nature 460 (2009), 108–112.
3. Baan, C.C., van der Mast, B.J., Klepper, M., Mol, W.M., Peeters, A.M.a., Korevaar, S.S., Balk, A.H.M.M., Weimar, W., Differential effect of calcineurin inhibitors, anti-CD25 antibodies and rapamycin on the induction of FOXP3 in human T cells. Transplantation 80 (2005), 110–117.
4. Berger, C., Jensen, M.C., Lansdorp, P.M., Gough, M., Elliott, C., Riddell, S.R., Adoptive transfer of effector CD8 + T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 118 (2008), 294–305.
5. Cao, W., Manicassamy, S., Tang, H., Kasturi, S.P., Pirani, A., Murthy, N., Pulendran, B., Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway. Nat. Immunol. 9 (2008), 1157–1164.
6. Cham, C.M., Driessens, G., O'Keefe, J.P., Gajewski, T.F., Glucose deprivation inhibits multiple key gene expression events and effector functions in CD8 + T cells. Eur. J. Immunol. 38 (2008), 2438–2450.
7. Chi, H., Regulation and function of mTOR signalling in T cell fate decisions. Nat. Rev. Immunol. 12 (2012), 325–338.
8. Choo, A.Y., Yoon, S.-O., Kim, S.G., Roux, P.P., Blenis, J., Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 17414–17419.
9. Chresta, C.M., Davies, B.R., Hickson, I., Harding, T., Cosulich, S., Critchlow, S.E., Vincent, J.P., Ellston, R., Jones, D., Sini, P., et al. AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res. 70 (2010), 288–298.
10. Cobbold, S.P., The mTOR pathway and integrating immune regulation. Immunology, 391-398, 2013.
11. Diken, M., Kreiter, S., Vascotto, F., Selmi, A., Attig, S., Diekmann, J., Huber, C., Türeci, Ö., Sahin, U., mTOR inhibition improves antitumor effects of vaccination with antigen-encoding RNA. Cancer immunol. res. 1 (2013), 386–392.
12. Driessens, G., Zheng, Y., Gajewski, T.F., Beta-catenin does not regulate memory T cell phenotype. Nat. Med. 16 (2010), 513–514 author reply 514-515.
13. Feldman, M.E., Apsel, B., Uotila, A., Loewith, R., Knight, Z.A., Ruggero, D., Shokat, K.M., Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol., 7, 2009, e38.
14. Ferrer, I.R., Wagener, M.E., Robertson, J.M., Turner, A.P., Araki, K., Ahmed, R., Kirk, A.D., Larsen, C.P., Ford, M.L., Cutting edge: rapamycin augments pathogen-specific but not graft-reactive CD8 + T cell responses. J. Immunol. 185 (2010), 2004–2008.
15. Ferrer, I.R., Araki, K., Ford, M.L., Paradoxical aspects of rapamycin immunobiology in transplantation. Am. J. Transplant. 11 (2011), 654–659.
16. Fox, C.J., Hammerman, P.S., Thompson, C.B., Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5 (2005), 844–852.
17. Gattinoni, L., Zhong, X.S., Palmer, D.C., Ji, Y., Hinrichs, C.S., Yu, Z., Wrzesinski, C., Boni, A., Cassard, L., Garvin, L.M., et al. Wnt signaling arrests effector T cell differentiation and generates CD8 + memory stem cells. Nat. Med. 15 (2009), 808–813.
18. Gattinoni, L., Lugli, E., Ji, Y., Pos, Z., Paulos, C.M., Quigley, M.F., Almeida, J.R., Gostick, E., Yu, Z., Carpenito, C., et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 17 (2011), 1290–1297.
19. Graef, P., Buchholz, V.R., Stemberger, C., Flossdorf, M., Henkel, L., Schiemann, M., Drexler, I., Höfer, T., Riddell, S.R., Busch, D.H., Serial transfer of single-cell-derived immunocompetence reveals stemness of CD8 + central memory T cells. Immunity 41 (2014), 116–126.
20. Igney, F.H., Krammer, P.H., Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2 (2002), 277–288.
21. Kamphorst, A.O., Ahmed, R., CD4 T-cell immunotherapy for chronic viral infections and cancer. Immunotherapy 5 (2013), 975–987.
22. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J.L., Bonenfant, D., Oppliger, W., Jenoe, P., Hall, M.N., Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10 (2002), 457–468.
23. Lohoff, M., Mak, T.W., Roles of interferon-regulatory factors in T-helper-cell differentiation. Nat. Rev. Immunol. 5 (2005), 125–135.
24. Lugli, E., Gattinoni, L., Roberto, A., Mavilio, D., Price, D.A., Restifo, N.P., Roederer, M., Identification, isolation and in vitro expansion of human and nonhuman primate T stem cell memory cells. Nat. Protoc. 8 (2013), 33–42.
25. Markley, J.C., Sadelain, M., IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human T cell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood 115 (2010), 3508–3519.
26. + T cells. Curr. Opin. Immunol. 21 (2009), 200–208.
27. Oberdoerffer, S., Moita, L.F., Neems, D., Freitas, R.P., Hacohen, N., Rao, A., Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL. Science 321 (2008), 686–691.
28. Pearce, E.L., Walsh, M.C., Cejas, P.J., Harms, G.M., Shen, H., Wang, L.S., Jones, R.G., Choi, Y., Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460 (2009), 103–107.
29. Powers, J.M., Trobridge, G.D., Identification of hematopoietic stem cell engraftment genes in gene therapy studies. J.Stem Cell Res. Ther. 2013 (2013), 1–15.
30. Prlic, M., Bevan, M.J., Cutting edge: β-catenin is dispensable for T cell effector differentiation, memory formation, and recall responses. J. Immunol. 187 (2011), 1542–1546.
31. Rao, R.R., Li, Q., Odunsi, K., Shrikant, P.A., The mTOR kinase determines effector versus memory CD8 + T cell fate by regulating the expression of transcription factors T-bet and eomesodermin. Immunity 32 (2010), 67–78.
32. Slavik, J.M., Lim, D.-g., Burakoff, S.J., Hafler, D.A., Rapamycin-resistant proliferation of CD8 + T cells correlates with p27kip1 down-regulation and bcl-xL induction, and is prevented by an inhibitor of phosphoinositide 3-kinase activity. J. Biol. Chem. 279 (2004), 910–919.
33. Sukumar, M., Liu, J., Crompton, J., Rao, M., Ji, Y., Finkel, T., Gattinoni, L., Restifo, N., Mitochondrial activity regulates T cell memory, self renewal and anti tumor function in CD8 + T cells. J. ImmunoTherapy of Cancer, 1, 2013, O11-O11.
34. Sukumar, M., Liu, J., Ji, Y., Subramanian, M., Crompton, J.G., Yu, Z., Roychoudhuri, R., Palmer, D.C., Muranski, P., Karoly, E.D., et al. Inhibiting glycolytic metabolism enhances CD8 + T cell memory and antitumor function. J. Clin. Invest. 123 (2013), 4479–4488.
35. Thomson, A.W., Turnquist, H.R., Raimondi, G., Immunoregulatory functions of mTOR inhibition. Nat. Rev. Immunol. 9 (2009), 324–337.
36. Turner, A.P., Shaffer, V.O., Araki, K., Martens, C., Turner, P.L., Gangappa, S., Ford, M.L., Ahmed, R., Kirk, A.D., Larsen, C.P., Sirolimus enhances the magnitude and quality of viral-specific CD8 + T-cell responses to vaccinia virus vaccination in rhesus macaques. Am. J. Transplant. 11 (2011), 613–618.
37. van der Windt, G.J.W., Everts, B., Chang, C.-H., Curtis, J.D., Freitas, T.C., Amiel, E., Pearce, E.J., Pearce, E.L., Mitochondrial respiratory capacity is a critical regulator of CD8 + T cell memory development. Immunity 36 (2012), 68–78.
38. Vermeulen, K., Van Bockstaele, D.R., Berneman, Z.N., The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 36 (2003), 131–149.
39. Wherry, E.J., Teichgräber, V., Becker, T.C., Masopust, D., Kaech, S.M., Antia, R., von Andrian, U.H., Ahmed, R., Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4 (2003), 225–234.
40. Xiao, Z., Sun, Z., Smyth, K., Li, L., Wnt signaling inhibits CTL memory programming. Mol. Immunol. 56 (2013), 423–433.
41. Yang, X., Zhang, M., Ramos, C., Durett, A., Liu, E., Dakhova, O., Liu, H., Creighton, C.J., Gee, A.P., Heslop, H.E., et al. (2014). Closely-related T-memory stem cells correlate with in-vivo expansion of CAR.CD19-T cells in patients and are preserved by IL-7 and IL-15. Blood.
42. Zhang, Y., Joe, G., Hexner, E., Zhu, J., Emerson, S.G., Host-reactive CD8 + memory stem cells in graft-versus-host disease. Nat. Med. 11 (2005), 1299–1305.
43. Zheng, Y., Delgoffe, G.M., Meyer, C.F., Chan, W., Powell, J.D., Anergic T cells are metabolically anergic. J. Immunol. 183 (2009), 6095–6101.