Disruption of TET2 promotes the therapeutic efficacy of CD19-targeted T cells

Nature - Tập 558 Số 7709 - Trang 307-312 - 2018
Joseph A. Fraietta1, Christopher L. Nobles2, Morgan A. Sammons3, Stefan Lundh1, Shannon A. Carty4, Tyler J. Reich1, Alexandria P. Cogdill1, Jennifer J.D. Morrissette5, Jamie E. DeNizio6, Shantan Reddy2, Young Sun Hwang2, Mercy Gohil1, Irina Kulikovskaya1, Farzana Nazimuddin1, Minnal Gupta1, Fang Chen1, J.K. Everett2, Katherine A. Alexander3, Enrique Lin-Shiao3, Marvin H. Gee7, Xiaojun Liu1, Regina M. Young4, David E Ambrose1, Yan Wang4, Jun Xu4, Martha S. Jordan4, Katherine T. Marcucci4, Bruce L. Levine4, K. Christopher García7, Yangbing Zhao4, Michael Kalos1, David Porter4, Rahul M. Kohli2, Simon F. Lacey4, Shelley L. Berger3, Frederic D. Bushman2, Carl H. June4, J. Joseph Melenhorst5
1Center for Cellular Immunotherapies, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
2Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
3Department of Cell and Developmental Biology, Epigenetics Program, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
4Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
5Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
6Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
7Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA, USA

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Porter, D. L., Levine, B. L., Kalos, M., Bagg, A. & June, C. H. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725–733 (2011).

Schuster, S. J. et al. Chimeric antigen receptor T cells in refractory B cell lymphomas. N. Engl. J. Med. 377, 2545–2554 (2017).

Maude, S. L. et al. Tisagenlecleucel in children and young adults with B cell lymphoblastic leukemia. N. Engl. J. Med. 378, 439–448 (2018).

Porter, D. L. et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci. Transl. Med. 7, 303ra139 (2015).

Savoldo, B. et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J. Clin. Invest. 121, 1822–1826 (2011).

Turtle, C. J. et al. CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients. J. Clin. Invest. 126, 2123–2138 (2016).

Busque, L. et al. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat. Genet. 44, 1179–1181 (2012).

Tefferi, A. et al. Detection of mutant TET2 in myeloid malignancies other than myeloproliferative neoplasms: CMML, MDS, MDS/MPN and AML. Leukemia 23, 1343–1345 (2009).

Delhommeau, F. et al. Mutation in TET2 in myeloid cancers. N. Engl. J. Med. 360, 2289–2301 (2009).

Quivoron, C. et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20, 25–38 (2011).

Yeh, C. H. et al. Mutation of epigenetic regulators TET2 and MLL3 in patients with HTLV-I-induced acute adult T cell leukemia. Mol. Cancer 15, 15 (2016).

Zang, S. et al. Mutations in 5-methylcytosine oxidase TET2 and RhoA cooperatively disrupt T cell homeostasis. J. Clin. Invest. 127, 2998–3012 (2017).

Aslanyan, M. G. et al. Clinical and biological impact of TET2 mutations and expression in younger adult AML patients treated within the EORTC/GIMEMA AML-12 clinical trial. Ann. Hematol. 93, 1401–1412 (2014).

Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935 (2009).

Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929–930 (2009).

Ito, S. et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129–1133 (2010).

Pfaffeneder, T. et al. The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. 50, 7008–7012 (2011).

He, Y. F. et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303–1307 (2011).

Ito, S. et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300–1303 (2011).

Zhang, H. et al. 4-1BB is superior to CD28 costimulation for generating CD8+ cytotoxic lymphocytes for adoptive immunotherapy. J. Immunol. 179, 4910–4918 (2007).

Scharer, C. D., Barwick, B. G., Youngblood, B. A., Ahmed, R. & Boss, J. M. Global DNA methylation remodeling accompanies CD8 T cell effector function. J. Immunol. 191, 3419–3429 (2013).

Hertlein, E. et al. Characterization of a new chronic lymphocytic leukemia cell line for mechanistic in vitro and in vivo studies relevant to disease. PLoS ONE 8, e76607 (2013).

Barrett, D. M. et al. Treatment of advanced leukemia in mice with mRNA engineered T cells. Hum. Gene Ther. 22, 1575–1586 (2011).

Maude, S. L. et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371, 1507–1517 (2014).

Jena, B. et al. Chimeric antigen receptor (CAR)-specific monoclonal antibody to detect CD19-specific T cells in clinical trials. PLoS ONE 8, e57838 (2013).

Brady, T. et al. A method to sequence and quantify DNA integration for monitoring outcome in gene therapy. Nucleic Acids Res. 39, e72 (2011).

Berry, C., Hannenhalli, S., Leipzig, J. & Bushman, F. D. Selection of target sites for mobile DNA integration in the human genome. PLOS Comput. Biol. 2, e157 (2006).

Berry, C. C. et al. Estimating abundances of retroviral insertion sites from DNA fragment length data. Bioinformatics 28, 755–762 (2012).

Berry, C. C., Ocwieja, K. E., Malani, N. & Bushman, F. D. Comparing DNA integration site clusters with scan statistics. Bioinformatics 30, 1493–1500 (2014).

Scholler, J. et al. Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci. Transl. Med. 4, 132ra53 (2012).

Daber, R., Sukhadia, S. & Morrissette, J. J. Understanding the limitations of next generation sequencing informatics, an approach to clinical pipeline validation using artificial data sets. Cancer Genet. 206, 441–448 (2013).

Liu, M. Y. et al. Mutations along a TET2 active site scaffold stall oxidation at 5-hydroxymethylcytosine. Nat. Chem. Bio. 13, 181–187 (2017).

Hu, L. et al. Crystal structure of TET2-DNA complex: insight into TET-mediated 5mC oxidation. Cell 155, 1545–1555 (2013).

Liu, M. Y., DeNizio, J. E. & Kohli, R. M. Quantification of oxidized 5-methylcytosine bases and TET enzyme activity. Methods Enzymol. 573, 365–385 (2016).

Jin, J. et al. Simplified method of the growth of human tumor infiltrating lymphocytes in gas-permeable flasks to numbers needed for patient treatment. J. Immunother. 35, 283–292 (2012).

Carty, S. A. et al. The loss of TET2 promotes CD8+ T cell memory differentiation. J. Immunol. 200, 82–91 (2018).

Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).

Pauken, K. E. et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354, 1160–1165 (2016).

Xu, J. et al. Landscape of monoallelic DNA accessibility in mouse embryonic stem cells and neural progenitor cells. Nat. Genet. 49, 377–386 (2017).

Laport, G. G. et al. Adoptive transfer of costimulated T cells induces lymphocytosis in patients with relapsed/refractory non-Hodgkin lymphoma following CD34+-selected hematopoietic cell transplantation. Blood 102, 2004–2013 (2003).

Fraietta, J. A. et al. Ibrutinib enhances chimeric antigen receptor T cell engraftment and efficacy in leukemia. Blood 127, 1117–1127 (2016).

Gattinoni, L. et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 17, 1290–1297 (2011).

Carvalho, B. S. & Irizarry, R. A. A framework for oligonucleotide microarray preprocessing. Bioinformatics 26, 2363–2367 (2010).

Irizarry, R. A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).

Brady, T. et al. Integration target site selection by a resurrected human endogenous retrovirus. Genes Dev. 23, 633–642 (2009).

Ocwieja, K. E. et al. HIV integration targeting: a pathway involving Transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog. 7, e1001313 (2011).

Moskowitz, D. M. et al. Epigenomics of human CD8 T cell differentiation and aging. Sci. Immunol. 2, eaag0192 (2017).