Oxygen Sensing by T Cells Establishes an Immunologically Tolerant Metastatic Niche

Cell

Volumn 166, Issue 5, 2016, Pages 1117-1131.e14

  Clever, David ^a,b   Roychoudhuri, Rahul ^a,c   Constantinides, Michael G ^d   Askenase, Michael H ^d   Sukumar, Madhusudhanan ^a   Klebanoff, Christopher A ^a,e   Eil, Robert L ^a   Hickman, Heather D ^d   Yu, Zhiya ^a   Pan, Jenny H ^a   Palmer, Douglas C ^a   Phan, Anthony T ^f   Goulding, John ^f   Gattinoni, Luca ^a   Goldrath, Ananda W ^f   Belkaid, Yasmine ^d   Restifo, Nicholas P ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; NEUROPILIN 1; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL TRANSFER; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; LUNG METASTASIS; MOUSE; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL; TUMOR IMMUNITY; ADOPTIVE TRANSFER; ANIMAL; ENZYMOLOGY; GENETICS; GLYCOLYSIS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; LUNG NEOPLASMS; LYMPHOCYTE ACTIVATION; METABOLISM; METASTASIS; PATHOLOGY; SECONDARY;

ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; GLYCOLYSIS; INTERFERON-GAMMA; LUNG; LUNG NEOPLASMS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NEOPLASM METASTASIS; NEUROPILIN-1; OXYGEN; PROLYL HYDROXYLASES; T-LYMPHOCYTES, REGULATORY; TH1 CELLS;

EID: 84983806394     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.032     Document Type: Article

References (53)

1. Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J.R., Pfeffer, K., Coffer, P.J., Rudensky, A.Y., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
2. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331 (2011), 337–341.
3. Bluestone, J.A., Abbas, A.K., Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3 (2003), 253–257.
4. Bruick, R.K., McKnight, S.L., A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294 (2001), 1337–1340.
5. Chang, C.H., Curtis, J.D., Maggi, L.B. Jr., Faubert, B., Villarino, A.V., O'Sullivan, D., Huang, S.C., van der Windt, G.J., Blagih, J., Qiu, J., et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153 (2013), 1239–1251.
6. Chang, C.H., Qiu, J., O'Sullivan, D., Buck, M.D., Noguchi, T., Curtis, J.D., Chen, Q., Gindin, M., Gubin, M.M., van der Windt, G.J., et al. Metabolic competition in the tumor microenvironment is a driver of cancer progression. Cell 162 (2015), 1229–1241.
7. Chen, W., Jin, W., Hardegen, N., Lei, K.J., Li, L., Marinos, N., McGrady, G., Wahl, S.M., Conversion of peripheral CD4+CD25– naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198 (2003), 1875–1886.
8. Colegio, O.R., Chu, N.Q., Szabo, A.L., Chu, T., Rhebergen, A.M., Jairam, V., Cyrus, N., Brokowski, C.E., Eisenbarth, S.C., Phillips, G.M., et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 513 (2014), 559–563.
9. Cui, G., Staron, M.M., Gray, S.M., Ho, P.C., Amezquita, R.A., Wu, J., Kaech, S.M., IL-7-induced glycerol transport and TAG synthesis promotes memory CD8+ T cell longevity. Cell 161 (2015), 750–761.
10. Cummins, E.P., Berra, E., Comerford, K.M., Ginouves, A., Fitzgerald, K.T., Seeballuck, F., Godson, C., Nielsen, J.E., Moynagh, P., Pouyssegur, J., Taylor, C.T., Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. USA 103 (2006), 18154–18159.
11. Dang, E.V., Barbi, J., Yang, H.Y., Jinasena, D., Yu, H., Zheng, Y., Bordman, Z., Fu, J., Kim, Y., Yen, H.R., et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 146 (2011), 772–784.
12. de Heer, H.J., Hammad, H., Soullié, T., Hijdra, D., Vos, N., Willart, M.A., Hoogsteden, H.C., Lambrecht, B.N., Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200 (2004), 89–98.
13. Doedens, A.L., Stockmann, C., Rubinstein, M.P., Liao, D., Zhang, N., DeNardo, D.G., Coussens, L.M., Karin, M., Goldrath, A.W., Johnson, R.S., Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 70 (2010), 7465–7475.
14. Doedens, A.L., Phan, A.T., Stradner, M.H., Fujimoto, J.K., Nguyen, J.V., Yang, E., Johnson, R.S., Goldrath, A.W., Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen. Nat. Immunol. 14 (2013), 1173–1182.
15. Epstein, A.C., Gleadle, J.M., McNeill, L.A., Hewitson, K.S., O'Rourke, J., Mole, D.R., Mukherji, M., Metzen, E., Wilson, M.I., Dhanda, A., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107 (2001), 43–54.
16. Floess, S., Freyer, J., Siewert, C., Baron, U., Olek, S., Polansky, J., Schlawe, K., Chang, H.D., Bopp, T., Schmitt, E., et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol., 5, 2007, e38.
17. Gavin, M.A., Rasmussen, J.P., Fontenot, J.D., Vasta, V., Manganiello, V.C., Beavo, J.A., Rudensky, A.Y., Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445 (2007), 771–775.
18. Gerriets, V.A., Kishton, R.J., Nichols, A.G., Macintyre, A.N., Inoue, M., Ilkayeva, O., Winter, P.S., Liu, X., Priyadharshini, B., Slawinska, M.E., et al. Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J. Clin. Invest. 125 (2015), 194–207.
19. Gruber, M., Hu, C.J., Johnson, R.S., Brown, E.J., Keith, B., Simon, M.C., Acute postnatal ablation of Hif-2alpha results in anemia. Proc. Natl. Acad. Sci. USA 104 (2007), 2301–2306.
20. Ho, P.C., Bihuniak, J.D., Macintyre, A.N., Staron, M., Liu, X., Amezquita, R., Tsui, Y.C., Cui, G., Micevic, G., Perales, J.C., et al. Phosphoenolpyruvate is a metabolic checkpoint of anti-tumor T cell responses. Cell 162 (2015), 1217–1228.
21. Holt, P.G., Strickland, D.H., Wikström, M.E., Jahnsen, F.L., Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8 (2008), 142–152.
22. Jaakkola, P., Mole, D.R., Tian, Y.M., Wilson, M.I., Gielbert, J., Gaskell, S.J., von Kriegsheim, A., Hebestreit, H.F., Mukherji, M., Schofield, C.J., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292 (2001), 468–472.
23. Josefowicz, S.Z., Niec, R.E., Kim, H.Y., Treuting, P., Chinen, T., Zheng, Y., Umetsu, D.T., Rudensky, A.Y., Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 482 (2012), 395–399.
24. Joshi, N.S., Cui, W., Chandele, A., Lee, H.K., Urso, D.R., Hagman, J., Gapin, L., Kaech, S.M., Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27 (2007), 281–295.
25. Kaelin, W.G. Jr., Ratcliffe, P.J., Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30 (2008), 393–402.
26. Keith, B., Johnson, R.S., Simon, M.C., HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 12 (2012), 9–22.
27. Kim, D., Salzberg, S.L., TopHat-Fusion: An algorithm for discovery of novel fusion transcripts. Genome Biol., 12, 2011, R72.
28. Koch, M.A., Tucker-Heard, G., Perdue, N.R., Killebrew, J.R., Urdahl, K.B., Campbell, D.J., The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10 (2009), 595–602.
29. Koch, M.A., Thomas, K.R., Perdue, N.R., Smigiel, K.S., Srivastava, S., Campbell, D.J., T-bet(+) Treg cells undergo abortive Th1 cell differentiation due to impaired expression of IL-12 receptor β2. Immunity 37 (2012), 501–510.
30. Lee, J.H., Elly, C., Park, Y., Liu, Y.C., E3 ubiquitin ligase VHL regulates hypoxia-inducible factor-1α to maintain regulatory T cell stability and suppressive capacity. Immunity 42 (2015), 1062–1074.
31. Li, M.O., Sanjabi, S., Flavell, R.A., Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25 (2006), 455–471.
32. Lord, G.M., Rao, R.M., Choe, H., Sullivan, B.M., Lichtman, A.H., Luscinskas, F.W., Glimcher, L.H., T-bet is required for optimal proinflammatory CD4+ T-cell trafficking. Blood 106 (2005), 3432–3439.
33. Massagué, J., Obenauf, A.C., Metastatic colonization by circulating tumour cells. Nature 529 (2016), 298–306.
34. Minn, A.J., Gupta, G.P., Siegel, P.M., Bos, P.D., Shu, W., Giri, D.D., Viale, A., Olshen, A.B., Gerald, W.L., Massagué, J., Genes that mediate breast cancer metastasis to lung. Nature 436 (2005), 518–524.
35. Molinero, L.L., Miller, M.L., Evaristo, C., Alegre, M.L., High TCR stimuli prevent induced regulatory T cell differentiation in a NF-κB-dependent manner. J. Immunol. 186 (2011), 4609–4617.
36. Mucida, D., Kutchukhidze, N., Erazo, A., Russo, M., Lafaille, J.J., Curotto de Lafaille, M.A., Oral tolerance in the absence of naturally occurring Tregs. J. Clin. Invest. 115 (2005), 1923–1933.
37. Muranski, P., Boni, A., Antony, P.A., Cassard, L., Irvine, K.R., Kaiser, A., Paulos, C.M., Palmer, D.C., Touloukian, C.E., Ptak, K., et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 112 (2008), 362–373.
38. Pardoll, D.M., Topalian, S.L., The role of CD4+ T cell responses in antitumor immunity. Curr. Opin. Immunol. 10 (1998), 588–594.
39. Ryan, H.E., Poloni, M., McNulty, W., Elson, D., Gassmann, M., Arbeit, J.M., Johnson, R.S., Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60 (2000), 4010–4015.
40. Sakaguchi, S., Fukuma, K., Kuribayashi, K., Masuda, T., Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J. Exp. Med. 161 (1985), 72–87.
41. Semenza, G.L., Oxygen homeostasis. Wiley Interdiscip. Rev. Syst. Biol. Med. 2 (2010), 336–361.
42. Shi, L.Z., Wang, R., Huang, G., Vogel, P., Neale, G., Green, D.R., Chi, H., HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208 (2011), 1367–1376.
43. Strickland, D.H., Stumbles, P.A., Zosky, G.R., Subrata, L.S., Thomas, J.A., Turner, D.J., Sly, P.D., Holt, P.G., Reversal of airway hyperresponsiveness by induction of airway mucosal CD4+CD25+ regulatory T cells. J. Exp. Med. 203 (2006), 2649–2660.
44. Stumbles, P.A., Thomas, J.A., Pimm, C.L., Lee, P.T., Venaille, T.J., Proksch, S., Holt, P.G., Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 188 (1998), 2019–2031.
45. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
46. 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.
47. Sun, C.M., Hall, J.A., Blank, R.B., Bouladoux, N., Oukka, M., Mora, J.R., Belkaid, Y., Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204 (2007), 1775–1785.
48. Takeda, K., Ho, V.C., Takeda, H., Duan, L.J., Nagy, A., Fong, G.H., Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 26 (2006), 8336–8346.
49. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7 (2012), 562–578.
50. Valastyan, S., Weinberg, R.A., Tumor metastasis: Molecular insights and evolving paradigms. Cell 147 (2011), 275–292.
51. Weiss, J.M., Bilate, A.M., Gobert, M., Ding, Y., Curotto de Lafaille, M.A., Parkhurst, C.N., Xiong, H., Dolpady, J., Frey, A.B., Ruocco, M.G., et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 209 (2012), 1723–1742.
52. Wikstrom, M.E., Stumbles, P.A., Mouse respiratory tract dendritic cell subsets and the immunological fate of inhaled antigens. Immunol. Cell Biol. 85 (2007), 182–188.
53. Yadav, M., Louvet, C., Davini, D., Gardner, J.M., Martinez-Llordella, M., Bailey-Bucktrout, S., Anthony, B.A., Sverdrup, F.M., Head, R., Kuster, D.J., et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209 (2012), 1713–1722.