Glioblastoma-Derived IL6 Induces Immunosuppressive Peripheral Myeloid Cell PD-L1 and Promotes Tumor Growth

Authors

Jonathan B. Lamano, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Jason Balquidera Lamano, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Yuping D. Li, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Joseph D. DiDomenico, Department of Neurosurgery, Barrow Neurological Institute, Phoenix, Arizona.Follow
Winward Choy, Department of Neurological Surgery, University of California San Francisco, San Francisco, California.
Dorina Veliceasa, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Daniel E. Oyon, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Shayan Fakurnejad, Stanford School of Medicine, Stanford University, Stanford, California.
Leonel Ampie, Department of Neurosurgery, University of Virginia School of Medicine, University of Virginia, Charlottesville, Virginia.
Kartik Kesavabhotla, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Rajwant Kaur, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Gurvinder Kaur, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Dauren Biyashev, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Dusten J. Unruh, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Craig M. Horbinski, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
C David James, Department of Neurological Surgery, Northwestern University, Chicago, Illinois.
Andrew T. Parsa
Orin Bloch, Department of Neurological Surgery, Northwestern University, Chicago, Illinois. orin.bloch@northwestern.edu.

Document Type

Article

Abstract

PURPOSE: Upregulation of programmed death-ligand 1 (PD-L1) on circulating and tumor-infiltrating myeloid cells is a critical component of GBM-mediated immunosuppression that has been associated with diminished response to vaccine immunotherapy and poor survival. Although GBM-derived soluble factors have been implicated in myeloid PD-L1 expression, the identity of such factors has remained unknown. This study aimed to identify factors responsible for myeloid PD-L1 upregulation as potential targets for immune modulation. EXPERIMENTAL DESIGN: Conditioned media from patient-derived GBM explant cell cultures was assessed for cytokine expression and utilized to stimulate naïve myeloid cells. Myeloid PD-L1 induction was quantified by flow cytometry. Candidate cytokines correlated with PD-L1 induction were evaluated in tumor sections and plasma for relationships with survival and myeloid PD-L1 expression. The role of identified cytokines on immunosuppression and survival was investigated in vivo utilizing immunocompetent C57BL/6 mice bearing syngeneic GL261 and CT-2A tumors. RESULTS: GBM-derived IL6 was identified as a cytokine that is necessary and sufficient for myeloid PD-L1 induction in GBM through a STAT3-dependent mechanism. Inhibition of IL6 signaling in orthotopic murine glioma models was associated with reduced myeloid PD-L1 expression, diminished tumor growth, and increased survival. The therapeutic benefit of anti-IL6 therapy proved to be CD8 T-cell dependent, and the antitumor activity was additive with that provided by programmed death-1 (PD-1)-targeted immunotherapy. CONCLUSIONS: Our findings suggest that disruption of IL6 signaling in GBM reduces local and systemic myeloid-driven immunosuppression and enhances immune-mediated antitumor responses against GBM.

Medical Subject Headings

Animals; B7-H1 Antigen (immunology); Brain Neoplasms (immunology, metabolism, pathology); Cell Proliferation; Glioblastoma (immunology, metabolism, pathology); Humans; Immunosuppression Therapy; Interleukin-6 (blood, immunology, pharmacology); Mice; Mice, Inbred C57BL; Myeloid Cells (immunology); Prognosis; Survival Rate; Tumor Cells, Cultured; Tumor Microenvironment (immunology)

Publication Date

6-15-2019

Publication Title

Clinical cancer research : an official journal of the American Association for Cancer Research

E-ISSN

1557-3265

Volume

25

Issue

12

First Page

3643

Last Page

3657

PubMed ID

30824583

Digital Object Identifier (DOI)

10.1158/1078-0432.CCR-18-2402

Share

COinS