CD4+ T Cell Help Confers a Cytotoxic T Cell Effector Program Including Coinhibitory Receptor Downregulation and Increased Tissue Invasiveness

Immunity

Volumn 47, Issue 5, 2017, Pages 848-861.e5

  Ahrends, Tomasz ^a   Spanjaard, Aldo ^a   Pilzecker, Bas ^a   Bąbała, Nikolina ^a   Bovens, Astrid ^a   Xiao, Yanling ^a   Jacobs, Heinz ^a   Borst, Jannie ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

CD4 T cell help; CD8 T cell; coinhibition; costimulation; CTL differentiation; migration; transcriptome; tumor immunity; vaccination; virus infection

Indexed keywords

CD27 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR4; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; MESSENGER RNA; METALLOPROTEINASE; CD70 ANTIGEN; CX3CR1 PROTEIN, MOUSE; CXCR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; ENZYME ACTIVITY; EX VIVO STUDY; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RNA SEQUENCE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTOMICS; TUMOR INVASION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL MOTION; DOWN REGULATION; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; CD27 LIGAND; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MOVEMENT; CX3C CHEMOKINE RECEPTOR 1; DOWN-REGULATION; MICE; MICE, INBRED C57BL; RECEPTORS, CXCR4; T-LYMPHOCYTES, CYTOTOXIC; TUMOR NECROSIS FACTOR RECEPTOR SUPERFAMILY, MEMBER 7;

EID: 85033227781     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.10.009     Document Type: Article

References (40)

1. Ahrends, T., Bąbała, N., Xiao, Y., Yagita, H., van Eenennaam, H., Borst, J., CD27 agonism plus PD-1 blockade recapitulates CD4+ T-cell help in therapeutic anticancer vaccination. Cancer Res. 76 (2016), 2921–2931.
2. Arens, R., Schoenberger, S.P., Plasticity in programming of effector and memory CD8 T-cell formation. Immunol. Rev. 235 (2010), 190–205.
3. Bevan, M.J., Helping the CD8(+) T-cell response. Nat. Rev. Immunol. 4 (2004), 595–602.
4. Castellino, F., Germain, R.N., Cooperation between CD4+ and CD8+ T cells: when, where, and how. Annu. Rev. Immunol. 24 (2006), 519–540.
5. Chen, D.S., Mellman, I., Oncology meets immunology: the cancer-immunity cycle. Immunity 39 (2013), 1–10.
6. Coquet, J.M., Middendorp, S., van der Horst, G., Kind, J., Veraar, E.A.M., Xiao, Y., Jacobs, H., Borst, J., The CD27 and CD70 costimulatory pathway inhibits effector function of T helper 17 cells and attenuates associated autoimmunity. Immunity 38 (2013), 53–65.
7. Croft, M., The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. Immunol. 9 (2009), 271–285.
8. D'Souza, W.N., Schluns, K.S., Masopust, D., Lefrançois, L., Essential role for IL-2 in the regulation of antiviral extralymphoid CD8 T cell responses. J. Immunol. 168 (2002), 5566–5572.
9. Dunussi-Joannopoulos, K., Zuberek, K., Runyon, K., Hawley, R.G., Wong, A., Erickson, J., Herrmann, S., Leonard, J.P., Efficacious immunomodulatory activity of the chemokine stromal cell-derived factor 1 (SDF-1): local secretion of SDF-1 at the tumor site serves as T-cell chemoattractant and mediates T-cell-dependent antitumor responses. Blood 100 (2002), 1551–1558.
10. Eickhoff, S., Brewitz, A., Gerner, M.Y., Klauschen, F., Komander, K., Hemmi, H., Garbi, N., Kaisho, T., Germain, R.N., Kastenmüller, W., Robust anti-viral immunity requires multiple distinct T cell-dendritic cell interactions. Cell 162 (2015), 1322–1337.
11. + T-cells via CD27-CD70 interactions. Nat. Commun., 3, 2012, 948.
12. Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 (2006), 1960–1964.
13. Greyer, M., Whitney, P.G., Stock, A.T., Davey, G.M., Tebartz, C., Bachem, A., Mintern, J.D., Strugnell, R.A., Turner, S.J., Gebhardt, T., et al. T cell help amplifies innate signals in CD8(+) DCs for optimal CD8(+) T cell priming. Cell Rep. 14 (2016), 586–597.
14. Groom, J.R., Richmond, J., Murooka, T.T., Sorensen, E.W., Sung, J.H., Bankert, K., von Andrian, U.H., Moon, J.J., Mempel, T.R., Luster, A.D., CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 37 (2012), 1091–1103.
15. Gros, A., Parkhurst, M.R., Tran, E., Pasetto, A., Robbins, P.F., Ilyas, S., Prickett, T.D., Gartner, J.J., Crystal, J.S., Roberts, I.M., et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat. Med. 22 (2016), 433–438.
16. Hatse, S., Princen, K., Bridger, G., De Clercq, E., Schols, D., Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett. 527 (2002), 255–262.
17. Hor, J.L., Whitney, P.G., Zaid, A., Brooks, A.G., Heath, W.R., Mueller, S.N., Spatiotemporally distinct interactions with dendritic cell subsets facilitates CD4+ and CD8+ T cell activation to localized viral infection. Immunity 43 (2015), 554–565.
18. Kaech, S.M., Cui, W., Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12 (2012), 749–761.
19. Karlström, S., Nordvall, G., Sohn, D., Hettman, A., Turek, D., Åhlin, K., Kers, A., Claesson, M., Slivo, C., Lo-Alfredsson, Y., et al. Substituted 7-amino-5-thio-thiazolo[4,5-d]pyrimidines as potent and selective antagonists of the fractalkine receptor (CX3CR1). J. Med. Chem. 56 (2013), 3177–3190.
20. Lin, K.Y., Guarnieri, F.G., Staveley-O'Carroll, K.F., Levitsky, H.I., August, J.T., Pardoll, D.M., Wu, T.C., Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res. 56 (1996), 21–26.
21. Melief, C.J.M., van Hall, T., Arens, R., Ossendorp, F., van der Burg, S.H., Therapeutic cancer vaccines. J. Clin. Invest. 125 (2015), 3401–3412.
22. Mescher, M.F., Curtsinger, J.M., Agarwal, P., Casey, K.A., Gerner, M., Hammerbeck, C.D., Popescu, F., Xiao, Z., Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 211 (2006), 81–92.
23. Mitchell, D.M., Ravkov, E.V., Williams, M.A., Distinct roles for IL-2 and IL-15 in the differentiation and survival of CD8+ effector and memory T cells. J. Immunol. 184 (2010), 6719–6730.
24. Nakanishi, Y., Lu, B., Gerard, C., Iwasaki, A., CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462 (2009), 510–513.
25. Nishimura, M., Umehara, H., Nakayama, T., Yoneda, O., Hieshima, K., Kakizaki, M., Dohmae, N., Yoshie, O., Imai, T., Dual functions of fractalkine/CX3C ligand 1 in trafficking of perforin+/granzyme B+ cytotoxic effector lymphocytes that are defined by CX3CR1 expression. J. Immunol. 168 (2002), 6173–6180.
26. Nolte, M.A., van Olffen, R.W., van Gisbergen, K.P.J.M., van Lier, R.A.W., Timing and tuning of CD27-CD70 interactions: the impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol. Rev. 229 (2009), 216–231.
27. Nolz, J.C., Starbeck-Miller, G.R., Harty, J.T., Naive, effector and memory CD8 T-cell trafficking: parallels and distinctions. Immunotherapy 3 (2011), 1223–1233.
28. Oshima, H., Nakano, H., Nohara, C., Kobata, T., Nakajima, A., Jenkins, N.A., Gilbert, D.J., Copeland, N.G., Muto, T., Yagita, H., Okumura, K., Characterization of murine CD70 by molecular cloning and mAb. Int. Immunol. 10 (1998), 517–526.
29. Owen, J.L., Iragavarapu-Charyulu, V., Gunja-Smith, Z., Herbert, L.M., Grosso, J.F., Lopez, D.M., Up-regulation of matrix metalloproteinase-9 in T lymphocytes of mammary tumor bearers: role of vascular endothelial growth factor. J. Immunol. 171 (2003), 4340–4351.
30. Peperzak, V., Veraar, E.A., Keller, A.M., Xiao, Y., Borst, J., The Pim kinase pathway contributes to survival signaling in primed CD8+ T cells upon CD27 costimulation. J. Immunol. 185 (2010), 6670–6678.
31. Pipkin, M.E., Sacks, J.A., Cruz-Guilloty, F., Lichtenheld, M.G., Bevan, M.J., Rao, A., Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32 (2010), 79–90.
32. Sakanishi, T., Yagita, H., Anti-tumor effects of depleting and non-depleting anti-CD27 monoclonal antibodies in immune-competent mice. Biochem. Biophys. Res. Commun. 393 (2010), 829–835.
33. Salmon, H., Franciszkiewicz, K., Damotte, D., Dieu-Nosjean, M.-C., Validire, P., Trautmann, A., Mami-Chouaib, F., Donnadieu, E., Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J. Clin. Invest. 122 (2012), 899–910.
34. Schietinger, A., Philip, M., Krisnawan, V.E., Chiu, E.Y., Delrow, J.J., Basom, R.S., Lauer, P., Brockstedt, D.G., Knoblaugh, S.E., Hämmerling, G.J., et al. Tumor-specific T cell dysfunction is a dynamic antigen-driven differentiation program initiated early during tumorigenesis. Immunity 45 (2016), 389–401.
35. Siddiqui, I., Erreni, M., van Brakel, M., Debets, R., Allavena, P., Enhanced recruitment of genetically modified CX3CR1-positive human T cells into Fractalkine/CX3CL1 expressing tumors: importance of the chemokine gradient. J. Immunother. Cancer, 4, 2016, 21.
36. Tumeh, P.C., Harview, C.L., Yearley, J.H., Shintaku, I.P., Taylor, E.J.M., Robert, L., Chmielowski, B., Spasic, M., Henry, G., Ciobanu, V., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515 (2014), 568–571.
37. van Oosterwijk, M.F., Juwana, H., Arens, R., Tesselaar, K., van Oers, M.H.J., Eldering, E., van Lier, R.A.W., CD27-CD70 interactions sensitise naive CD4+ T cells for IL-12-induced Th1 cell development. Int. Immunol. 19 (2007), 713–718.
38. Weng, N.P., Araki, Y., Subedi, K., The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat. Rev. Immunol. 12 (2012), 306–315.
39. Williams, M.A., Tyznik, A.J., Bevan, M.J., Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441 (2006), 890–893.
40. Wu, B., Crampton, S.P., Hughes, C.C.W., Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity 26 (2007), 227–239.