Targeting both tumour-associated CXCR2+ neutrophils and CCR2+ macrophages disrupts myeloid recruitment and improves chemotherapeutic responses in pancreatic ductal adenocarcinoma

Gut. 2018 Jun;67(6):1112-1123. doi: 10.1136/gutjnl-2017-313738. Epub 2017 Dec 1.

Abstract

Objective: Chemokine pathways are co-opted by pancreatic adenocarcinoma (PDAC) to facilitate myeloid cell recruitment from the bone marrow to establish an immunosuppressive tumour microenvironment (TME). Targeting tumour-associated CXCR2+neutrophils (TAN) or tumour-associated CCR2+ macrophages (TAM) alone improves antitumour immunity in preclinical models. However, a compensatory influx of an alternative myeloid subset may result in a persistent immunosuppressive TME and promote therapeutic resistance. Here, we show CCR2 and CXCR2 combined blockade reduces total tumour-infiltrating myeloids, promoting a more robust antitumour immune response in PDAC compared with either strategy alone.

Methods: Blood, bone marrow and tumours were analysed from PDAC patients and controls. Treatment response and correlative studies were performed in mice with established orthotopic PDAC tumours treated with a small molecule CCR2 inhibitor (CCR2i) and CXCR2 inhibitor (CXCR2i), alone and in combination with chemotherapy.

Results: A systemic increase in CXCR2+ TAN correlates with poor prognosis in PDAC, and patients receiving CCR2i showed increased tumour-infiltrating CXCR2+ TAN following treatment. In an orthotopic PDAC model, CXCR2 blockade prevented neutrophil mobilisation from the circulation and augmented chemotherapeutic efficacy. However, depletion of either CXCR2+ TAN or CCR2+ TAM resulted in a compensatory response of the alternative myeloid subset, recapitulating human disease. This was overcome by combined CCR2i and CXCR2i, which augmented antitumour immunity and improved response to FOLFIRINOX chemotherapy.

Conclusion: Dual targeting of CCR2+ TAM and CXCR2+ TAN improves antitumour immunity and chemotherapeutic response in PDAC compared with either strategy alone.

Keywords: cytokines; immune response; immunoregulation; inflammatory mechanisms; pancreatic cancer.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Carcinoma, Pancreatic Ductal / drug therapy
  • Carcinoma, Pancreatic Ductal / immunology*
  • Carcinoma, Pancreatic Ductal / metabolism
  • Databases, Factual
  • Flow Cytometry
  • Humans
  • Immunohistochemistry
  • Immunomodulation
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Myeloid Cells / drug effects
  • Neutrophil Infiltration / drug effects
  • Neutrophils / drug effects*
  • Neutrophils / metabolism
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / immunology*
  • Pancreatic Neoplasms / metabolism
  • Real-Time Polymerase Chain Reaction
  • Receptors, CCR2 / antagonists & inhibitors
  • Receptors, CCR2 / metabolism
  • Receptors, Interleukin-8B / antagonists & inhibitors
  • Receptors, Interleukin-8B / metabolism
  • Tissue Array Analysis
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology*

Substances

  • CCR2 protein, human
  • Receptors, CCR2
  • Receptors, Interleukin-8B