Arginase 1 is a key driver of immune suppression in pancreatic cancer

  • Elife. 2023 Feb 2:12:e80721. doi: 10.7554/eLife.80721.
Rosa E Menjivar  1 ,  Zeribe C Nwosu  2 ,  Wenting Du  3 ,  Katelyn L Donahue  4 ,  Hanna S Hong  5 ,  Carlos Espinoza  3 ,  Kristee Brown  3 ,  Ashley Velez-Delgado  6 ,  Wei Yan  3 ,  Fatima Lima  3 ,  Allison Bischoff  4 ,  Padma Kadiyala  5 ,  Daniel Salas-Escabillas  4 ,  Howard C Crawford  7 ,  Filip Bednar  3  8 ,  Eileen Carpenter  8  9 ,  Yaqing Zhang  3  8 ,  Christopher J Halbrook  10  11 ,  Costas A Lyssiotis  2  4  8  9 ,  Marina Pasca di Magliano  1  4  6  7  8
Affiliations
  • 1. Cellular and Molecular Biology Program, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 2. Department of Molecular and Integrative Physiology, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 3. Department of Surgery, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 4. Cancer Biology Program, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 5. Department of Immunology, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 6. Department of Cell and Developmental Biology, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 7. Henry Ford Pancreatic Cancer Center, Detroit, United States.
  • 8. Rogel Cancer Center, Ann Arbor, United States.
  • 9. Department of Internal Medicine, Division of Gastroenterolog, University of Michigan-Ann Arbor, Ann Arbor, United States.
  • 10. Department of Molecular Biology and Biochemistry, University of California, Irvine, Irvine, United States.
  • 11. Chao Family Comprehensive Cancer Center, University of California, Irvine, Irvine, United States.
Abstract

An extensive fibroinflammatory stroma rich in Macrophages is a hallmark of Pancreatic Cancer. In this disease, it is well appreciated that Macrophages are immunosuppressive and contribute to the poor response to immunotherapy; however, the mechanisms of immune suppression are complex and not fully understood. Immunosuppressive Macrophages are classically defined by the expression of the enzyme Arginase 1 (ARG1), which we demonstrated is potently expressed in pancreatic tumor-associated Macrophages from both human patients and mouse models. While routinely used as a polarization marker, ARG1 also catabolizes arginine, an amino acid required for T cell activation and proliferation. To investigate this metabolic function, we used a genetic and a pharmacologic approach to target Arg1 in Pancreatic Cancer. Genetic inactivation of Arg1 in Macrophages, using a dual recombinase genetically engineered mouse model of Pancreatic Cancer, delayed formation of invasive disease, while increasing CD8+ T cell infiltration. Additionally, Arg1 deletion induced compensatory mechanisms, including Arg1 overexpression in epithelial cells, namely Tuft cells, and Arg2 overexpression in a subset of Macrophages. To overcome these compensatory mechanisms, we used a pharmacological approach to inhibit Arginase. Treatment of established Tumors with the Arginase inhibitor CB-1158 exhibited further increased CD8+ T cell infiltration, beyond that seen with the macrophage-specific knockout, and sensitized the Tumors to anti-PD1 immune checkpoint blockade. Our data demonstrate that Arg1 drives immune suppression in Pancreatic Cancer by depleting arginine and inhibiting T cell activation.

Keywords
CD8 T cells; PDA; arginase; cancer biology; human; immunosuppression; immunotherapy; mouse; myeloid.