Gastroenterology

Gastroenterology

Volume 143, Issue 4, October 2012, Pages 1095-1107.e2
Gastroenterology

Original Research
Basic and Translational—Pancreas
T Cells That Target Carcinoembryonic Antigen Eradicate Orthotopic Pancreatic Carcinomas Without Inducing Autoimmune Colitis in Mice

https://doi.org/10.1053/j.gastro.2012.06.037Get rights and content

Background & Aims

New treatment approaches are needed for patients with pancreatic adenocarcinoma. Carcinoembryonic antigen (CEA) is highly expressed on the surface of pancreatic adenocarcinoma cells; we investigated the effects of cytolytic T cells that recognize CEA in a mouse model of pancreatic carcinoma.

Methods

Immune-competent mice that expressed the CEA transgene (CEAtg) in the intestinal and pulmonary tracts were given intrapancreatic injections of Panc02 CEA+ cells (express CEA and click beetle luciferase) and tumors were grown for 10 days. Mice were then given single intravenous injections of T cells engineered to express a chimeric antigen receptor (CAR) with high specificity, but moderate affinity, for CEA and a luminescence marker.

Results

Injection of the anti-CEA CAR T cells reduced the size of pancreatic tumors to below the limit of detection in all mice and produced long-term tumor eradication in 67% of mice. T cells also eradicated CEA+ fibrosarcoma cells injected 45 days later. Bioluminescence imaging revealed the accumulation and persistence of the T cells at the tumor site. The efficacy of the T cells did not require lymphodepletion and was not reduced by soluble CEA. Mice developed some noninflammatory infiltrations of CAR+ T cells in intestine and lung, but there was no evidence of destruction of CEA+ healthy tissues.

Conclusions

Injection of T cells that target CEA can eradicate tumors grown from CEA+ pancreatic carcinoma cells in the pancreas of CEAtg mice without autoimmune effects.

Section snippets

Cell Lines

293T cells are human embryonic kidney cells that express the SV40 large T antigen (ATCC CRL-11268). Panc02 is a tumorigenic murine pancreatic carcinoma line.9 The Panc02 CEA+cells were derived from Panc02 cells by transfection with plasmid-encoding human CEA (kindly provided by Dr David Gilham, University of Manchester, UK). The Panc02 CEA+ and the Panc02 CEA cells coexpress green fluorescence protein and click beetle luciferase (CBLuc). MC38 is a murine fibrosarcoma line; C15A3 is a CEA+

CAR-Engineered T-Cells Target CEA+ Pancreas Carcinoma Cells

Mouse T cells were genetically engineered with the CEA-specific CAR that is entirely composed of murine domains and harbors the murine anti-CEA scFv Sca421 in the extracellular domain for targeting, and the CD28 and CD3ζ signaling endodomains for T-cell activation (Figure 1A). Both CD4+ and CD8+ T cells expressed the CAR on the cell surface (Figure 1B); both modified T-cell subsets were present in the therapeutic T-cell inoculums in same frequencies as in the peripheral blood of healthy mice.

Discussion

The study represents first strong evidence in a clinically relevant model that adoptive T-cell therapy targeting CEA is effective toward pancreas carcinoma and can be feasible without inducing severe autoimmune colitis. All mice treated with a single intravenous dose of the SCA431 CAR-engineered T cells showed profound regression of CEA+ pancreatic cancer; 6 of 8 mice were cured of pancreatic carcinoma in the long term. The anti-tumor response was specifically mediated by the engineered CAR

Acknowledgments

We thank Dr David Gilham and the Central Animal Facility, Patterson Institute for Cancer Research, Manchester, UK, for providing us with CEAtg mice.

References (24)

  • T.H. Corbett et al.

    Induction and chemotherapeutic response of two transplantable ductal adenocarcinomas of the pancreas in C57BL/6 mice

    Cancer Res

    (1984)
  • A. Bruynck et al.

    Characterisation of a humanised bispecific monoclonal antibody for cancer therapy

    Br J Cancer

    (1993)
  • Cited by (0)

    Conflict of interest The authors disclose no conflicts.

    Funding Work was funded by the Deutsche Krebshilfe, Bonn, Germany, the Wilhelm Sander-Stiftung, München, and the Else Kröner-Fresenius Stiftung, Homburg v.d.H., Germany.

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