SATB1 Expression Governs Epigenetic Repression of PD-1 in Tumor-Reactive T Cells

Immunity

Volumn 46, Issue 1, 2017, Pages 51-64

  Stephen, Tom L ^a   Payne, Kyle K ^a   Chaurio, Ricardo A ^a   Allegrezza, Michael J ^a   Zhu, Hengrui ^a   Perez Sanz, Jairo ^a   Perales Puchalt, Alfredo ^a   Nguyen, Jenny M ^a   Vara Ailor, Ana E ^a   Eruslanov, Evgeniy B ^b   Borowsky, Mark E ^c   Zhang, Rugang ^a   Laufer, Terri M ^b   Conejo Garcia, Jose R ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HELEN F GRAHAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PROGRAMMED DEATH 1 RECEPTOR; SMAD PROTEIN; SPECIAL AT RICH SEQUENCE BINDING PROTEIN 1; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MATRIX ATTACHMENT REGION BINDING PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DEACETYLATION; ENHANCER REGION; EPIGENETIC REPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; REPRESSOR GENE; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; ENZYME LINKED IMMUNOSPOT ASSAY; GENE EXPRESSION REGULATION; IMMUNOLOGY; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASM; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; ENZYME-LINKED IMMUNOSPOT ASSAY; EPIGENETIC REPRESSION; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; MATRIX ATTACHMENT REGION BINDING PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS; PROGRAMMED CELL DEATH 1 RECEPTOR;

EID: 85009517413     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.12.015     Document Type: Article

References (51)

1. Ahmadzadeh, M., Rosenberg, S.A., TGF-beta 1 attenuates the acquisition and expression of effector function by tumor antigen-specific human memory CD8 T cells. J. Immunol. 174 (2005), 5215–5223.
2. Alvarez, J.D., Yasui, D.H., Niida, H., Joh, T., Loh, D.Y., Kohwi-Shigematsu, T., The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev. 14 (2000), 521–535.
3. Austin, J.W., Lu, P., Majumder, P., Ahmed, R., Boss, J.M., STAT3, STAT4, NFATc1, and CTCF regulate PD-1 through multiple novel regulatory regions in murine T cells. J. Immunol. 192 (2014), 4876–4886.
4. Avram, D., Califano, D., The multifaceted roles of Bcl11b in thymic and peripheral T cells: impact on immune diseases. J. Immunol. 193 (2014), 2059–2065.
5. Baas, M., Besançon, A., Goncalves, T., Valette, F., Yagita, H., Sawitzki, B., Volk, H.D., Waeckel-Enée, E., Rocha, B., Chatenoud, L., You, S., TGFβ-dependent expression of PD-1 and PD-L1 controls CD8(+) T cell anergy in transplant tolerance. eLife, 5, 2016, e08133.
6. Bally, A.P., Austin, J.W., Boss, J.M., Genetic and Epigenetic Regulation of PD-1 Expression. J. Immunol. 196 (2016), 2431–2437.
7. Barber, D.L., Wherry, E.J., Masopust, D., Zhu, B., Allison, J.P., Sharpe, A.H., Freeman, G.J., Ahmed, R., Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 (2006), 682–687.
8. Brahmer, J.R., Tykodi, S.S., Chow, L.Q., Hwu, W.J., Topalian, S.L., Hwu, P., Drake, C.G., Camacho, L.H., Kauh, J., Odunsi, K., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366 (2012), 2455–2465.
9. Cai, S., Han, H.J., Kohwi-Shigematsu, T., Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet. 34 (2003), 42–51.
10. 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.
11. Chen, M.L., Pittet, M.J., Gorelik, L., Flavell, R.A., Weissleder, R., von Boehmer, H., Khazaie, K., Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc. Natl. Acad. Sci. USA 102 (2005), 419–424.
12. Conejo-Garcia, J.R., Benencia, F., Courreges, M.C., Kang, E., Mohamed-Hadley, A., Buckanovich, R.J., Holtz, D.O., Jenkins, A., Na, H., Zhang, L., et al. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat. Med. 10 (2004), 950–958.
13. Cubillos-Ruiz, J.R., Engle, X., Scarlett, U.K., Martinez, D., Barber, A., Elgueta, R., Wang, L., Nesbeth, Y., Durant, Y., Gewirtz, A.T., et al. Polyethylenimine-based siRNA nanocomplexes reprogram tumor-associated dendritic cells via TLR5 to elicit therapeutic antitumor immunity. J. Clin. Invest. 119 (2009), 2231–2244.
14. Cui, T.X., Kryczek, I., Zhao, L., Zhao, E., Kuick, R., Roh, M.H., Vatan, L., Szeliga, W., Mao, Y., Thomas, D.G., et al. Myeloid-Derived Suppressor Cells Enhance Stemness of Cancer Cells by Inducing MicroRNA101 and Suppressing the Corepressor CtBP2. Immunity, 2013.
15. Dege, C., Hagman, J., Mi-2/NuRD chromatin remodeling complexes regulate B and T-lymphocyte development and function. Immunol. Rev. 261 (2014), 126–140.
16. Dickinson, L.A., Joh, T., Kohwi, Y., Kohwi-Shigematsu, T., A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70 (1992), 631–645.
17. Flavell, R.A., Sanjabi, S., Wrzesinski, S.H., Licona-Limón, P., The polarization of immune cells in the tumour environment by TGFbeta. Nat. Rev. Immunol. 10 (2010), 554–567.
18. Furuya, Y., Furuya, A.K., Roberts, S., Sanfilippo, A.M., Salmon, S.L., Metzger, D.W., Prevention of Influenza Virus-Induced Immunopathology by TGF-β Produced during Allergic Asthma. PLoS Pathog., 11, 2015, e1005180.
19. Gaillard, S.L., Secord, A.A., Monk, B., The role of immune checkpoint inhibition in the treatment of ovarian cancer. Gynecol. Oncol. Res. Pract., 3, 2016, 11.
20. Garidou, L., Heydari, S., Gossa, S., McGavern, D.B., Therapeutic blockade of transforming growth factor beta fails to promote clearance of a persistent viral infection. J. Virol. 86 (2012), 7060–7071.
21. Garon, E.B., Rizvi, N.A., Hui, R., Leighl, N., Balmanoukian, A.S., Eder, J.P., Patnaik, A., Aggarwal, C., Gubens, M., Horn, L., et al., KEYNOTE-001 Investigators. Pembrolizumab for the treatment of non-small-cell lung cancer. N. Engl. J. Med. 372 (2015), 2018–2028.
22. Gorelik, L., Flavell, R.A., Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12 (2000), 171–181.
23. Hamanishi, J., Mandai, M., Ikeda, T., Minami, M., Kawaguchi, A., Murayama, T., Kanai, M., Mori, Y., Matsumoto, S., Chikuma, S., et al. Safety and Antitumor Activity of Anti-PD-1 Antibody, Nivolumab, in Patients With Platinum-Resistant Ovarian Cancer. J. Clin. Oncol. 33 (2015), 4015–4022.
24. Hugo, W., Zaretsky, J.M., Sun, L., Song, C., Moreno, B.H., Hu-Lieskovan, S., Berent-Maoz, B., Pang, J., Chmielowski, B., Cherry, G., et al. Genomic and Transcriptomic Features of Response to Anti-PD-1 Therapy in Metastatic Melanoma. Cell 165 (2016), 35–44.
25. Kao, C., Oestreich, K.J., Paley, M.A., Crawford, A., Angelosanto, J.M., Ali, M.A., Intlekofer, A.M., Boss, J.M., Reiner, S.L., Weinmann, A.S., Wherry, E.J., 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. 12 (2011), 663–671.
26. Kloet, S.L., Baymaz, H.I., Makowski, M., Groenewold, V., Jansen, P.W., Berendsen, M., Niazi, H., Kops, G.J., Vermeulen, M., Towards elucidating the stability, dynamics and architecture of the nucleosome remodeling and deacetylase complex by using quantitative interaction proteomics. FEBS J. 282 (2015), 1774–1785.
27. Lewis, G.M., Macal, M., Hesser, C.R., Zuñiga, E.I., Constitutive but not inducible attenuation of transforming growth factor β signaling increases natural killer cell responses without directly affecting dendritic cells early after persistent viral infection. J. Virol. 89 (2015), 3343–3355.
28. Lu, P., Youngblood, B.A., Austin, J.W., Mohammed, A.U., Butler, R., Ahmed, R., Boss, J.M., Blimp-1 represses CD8 T cell expression of PD-1 using a feed-forward transcriptional circuit during acute viral infection. J. Exp. Med. 211 (2014), 515–527.
29. Massagué, J., TGFbeta in Cancer. Cell 134 (2008), 215–230.
30. McPherson, R.C., Konkel, J.E., Prendergast, C.T., Thomson, J.P., Ottaviano, R., Leech, M.D., Kay, O., Zandee, S.E., Sweenie, C.H., Wraith, D.C., et al. Epigenetic modification of the PD-1 (Pdcd1) promoter in effector CD4(+) T cells tolerized by peptide immunotherapy. eLife, 3, 2014, e03416.
31. Nesbeth, Y., Scarlett, U., Cubillos-Ruiz, J., Martinez, D., Engle, X., Turk, M.J., Conejo-Garcia, J.R., CCL5-mediated endogenous antitumor immunity elicited by adoptively transferred lymphocytes and dendritic cell depletion. Cancer Res. 69 (2009), 6331–6338.
32. Nesbeth, Y.C., Martinez, D.G., Toraya, S., Scarlett, U.K., Cubillos-Ruiz, J.R., Rutkowski, M.R., Conejo-Garcia, J.R., CD4+ T cells elicit host immune responses to MHC class II-negative ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J. Immunol. 184 (2010), 5654–5662.
33. Notani, D., Gottimukkala, K.P., Jayani, R.S., Limaye, A.S., Damle, M.V., Mehta, S., Purbey, P.K., Joseph, J., Galande, S., Global regulator SATB1 recruits beta-catenin and regulates T(H)2 differentiation in Wnt-dependent manner. PLoS Biol., 8, 2010, e1000296.
34. Oestreich, K.J., Yoon, H., Ahmed, R., Boss, J.M., NFATc1 regulates PD-1 expression upon T cell activation. J. Immunol. 181 (2008), 4832–4839.
35. Park, B.V., Freeman, Z.T., Ghasemzadeh, A., Chattergoon, M.A., Rutebemberwa, A., Steigner, J., Winter, M.E., Huynh, T.V., Sebald, S.M., Lee, S.J., et al. TGF-beta1-Mediated Smad3 Enhances PD-1 Expression on Antigen-Specific T Cells in Cancer. Cancer Discov, 2016.
36. Pauken, K.E., Sammons, M.A., Odorizzi, P.M., Manne, S., Godec, J., Khan, O., Drake, A.M., Chen, Z., Sen, D.R., Kurachi, M., et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354 (2016), 1160–1165.
37. Roby, K.F., Taylor, C.C., Sweetwood, J.P., Cheng, Y., Pace, J.L., Tawfik, O., Persons, D.L., Smith, P.G., Terranova, P.F., Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21 (2000), 585–591.
38. Sen, D.R., Kaminski, J., Barnitz, R.A., Kurachi, M., Gerdemann, U., Yates, K.B., Tsao, H.W., Godec, J., LaFleur, M.W., Brown, F.D., et al. The epigenetic landscape of T cell exhaustion. Science 354 (2016), 1165–1169.
39. Stephen, T.L., Rutkowski, M.R., Allegrezza, M.J., Perales-Puchalt, A., Tesone, A.J., Svoronos, N., Nguyen, J.M., Sarmin, F., Borowsky, M.E., Tchou, J., Conejo-Garcia, J.R., Transforming growth factor β-mediated suppression of antitumor T cells requires FoxP1 transcription factor expression. Immunity 41 (2014), 427–439.
40. Tesone, A.J., Rutkowski, M.R., Brencicova, E., Svoronos, N., Perales-Puchalt, A., Stephen, T.L., Allegrezza, M.J., Payne, K.K., Nguyen, J.M., Wickramasinghe, J., et al. Satb1 Overexpression Drives Tumor-Promoting Activities in Cancer-Associated Dendritic Cells. Cell Rep. 14 (2016), 1774–1786.
41. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., Powderly, J.D., Carvajal, R.D., Sosman, J.A., Atkins, M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366 (2012), 2443–2454.
42. Topalian, S.L., Drake, C.G., Pardoll, D.M., Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 27 (2015), 450–461.
43. Tserel, L., Kolde, R., Limbach, M., Tretyakov, K., Kasela, S., Kisand, K., Saare, M., Vilo, J., Metspalu, A., Milani, L., Peterson, P., Age-related profiling of DNA methylation in CD8+ T cells reveals changes in immune response and transcriptional regulator genes. Sci. Rep., 5, 2015, 13107.
44. Wherry, E.J., Ha, S.J., Kaech, S.M., Haining, W.N., Sarkar, S., Kalia, V., Subramaniam, S., Blattman, J.N., Barber, D.L., Ahmed, R., Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27 (2007), 670–684.
45. Woods, D.M., Sodré, A.L., Villagra, A., Sarnaik, A., Sotomayor, E.M., Weber, J., HDAC Inhibition Upregulates PD-1 Ligands in Melanoma and Augments Immunotherapy with PD-1 Blockade. Cancer Immunol. Res. 3 (2015), 1375–1385.
46. Wrzesinski, S.H., Wan, Y.Y., Flavell, R.A., Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin. Cancer Res. 13 (2007), 5262–5270.
47. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P., Kohwi-Shigematsu, T., SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419 (2002), 641–645.
48. Youngblood, B., Oestreich, K.J., Ha, S.J., Duraiswamy, J., Akondy, R.S., West, E.E., Wei, Z., Lu, P., Austin, J.W., Riley, J.L., et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 35 (2011), 400–412.
49. Zhao, E., Maj, T., Kryczek, I., Li, W., Wu, K., Zhao, L., Wei, S., Crespo, J., Wan, S., Vatan, L., et al. Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction. Nat. Immunol. 17 (2016), 95–103.
50. Zou, W., Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5 (2005), 263–274.
51. Zou, W., Wolchok, J.D., Chen, L., PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci. Transl. Med., 8, 2016, 328rv4.