Inhibition of PPARγ in myeloid-lineage cells induces systemic inflammation, immunosuppression, and tumorigenesis

Blood. 2012 Jan 5;119(1):115-26. doi: 10.1182/blood-2011-06-363093. Epub 2011 Nov 3.

Abstract

Peroxisome proliferator-activated receptor-γ (PPARγ) is an anti-inflammatory molecule. To study its biologic function in myeloid cells, dominant-negative PPARγ (dnPPARγ) was overexpressed in a myeloid-specific bitransgenic mouse model. In this bitransgenic system, overexpression of the dnPPARγ-Flag fusion protein in myeloid-lineage cells abnormally elevated frequencies and total numbers of IL-7Rα(-)Lin(-)c-Kit(+)Sca-1(-), Lin(-)/Scal(+)/c-Kit(+), common myeloid, and granulocyte-monocyte progenitor populations in the BM. dnPPARγ overexpression led to up-regulation of IL-1β, IL-6, and TNFα in the blood plasma. As a result, CD11b(+)Ly6G(+) cells were systemically increased in association with activation of Stat3, NF-κB, Erk1/2, and p38 molecules. Myeloid-derived suppressor cells (MDSCs) inhibited the proliferation and lymphokine production of wild-type CD4+ T cells in vitro. CD4+ T cells from doxycycline-treated bitransgenic mice displayed reduced proliferation and lymphokine release. Both CD4+ and CD8+ T-cell populations were decreased in doxycycline-treated bitransgenic mice. Multiple forms of carcinoma and sarcoma in the lung, liver, spleen, and lymph nodes were observed in doxycycline-treated bitransgenic mice. BM transplantation revealed that a myeloid-autonomous defect was responsible for MDSC expansion, immunosuppression, and tumorigenesis in these mice. These studies suggest that anti-inflammatory PPARγ in myeloid-lineage cells plays a key role in controlling pro-inflammatory cytokine synthesis, MDSC expansion, immunosuppression, and the development of cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenocarcinoma / etiology*
  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology
  • Animals
  • Blotting, Western
  • Bone Marrow Transplantation
  • Cell Proliferation
  • Chromatin Immunoprecipitation
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Genes, Dominant*
  • Hematopoietic Stem Cells
  • Humans
  • Immunoenzyme Techniques
  • Immunosuppression Therapy*
  • Inflammation / etiology*
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-1beta / blood
  • Interleukin-6 / blood
  • Liver Neoplasms / etiology
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Lung Neoplasms / etiology
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Lymph Nodes / metabolism
  • Lymph Nodes / pathology
  • Male
  • Mice
  • Mice, Transgenic
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology*
  • NF-kappa B / metabolism
  • PPAR gamma / antagonists & inhibitors
  • PPAR gamma / physiology*
  • Proto-Oncogene Proteins c-kit / metabolism
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Interleukin-7 / metabolism
  • STAT3 Transcription Factor / metabolism
  • Sarcoma / etiology*
  • Sarcoma / metabolism
  • Sarcoma / pathology
  • Signal Transduction
  • Splenic Neoplasms / etiology
  • Splenic Neoplasms / metabolism
  • Splenic Neoplasms / pathology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Tumor Necrosis Factor-alpha / blood
  • Up-Regulation

Substances

  • Interleukin-1beta
  • Interleukin-6
  • NF-kappa B
  • PPAR gamma
  • RNA, Messenger
  • Receptors, Interleukin-7
  • STAT3 Transcription Factor
  • Tumor Necrosis Factor-alpha
  • interleukin-7 receptor, alpha chain
  • Proto-Oncogene Proteins c-kit