Extravascular red blood cells and hemoglobin promote tumor growth and therapeutic resistance as endogenous danger signals

J Immunol. 2015 Jan 1;194(1):429-37. doi: 10.4049/jimmunol.1400643. Epub 2014 Nov 26.

Abstract

Hemorrhage is a common clinical manifestation in patients with cancer. Intratumor hemorrhage has been demonstrated to be a poor prognostic factor for cancer patients. In this study, we investigated the role of RBCs and hemoglobin (Hb) in the process of tumor progression and therapeutical response. RBCs and Hb potently promoted tumor cell proliferation and syngenic tumor growth. RBCs and Hb activated the reactive oxygen species-NF-κB pathway in both tumor cells and macrophages. RBCs and Hb also induced chemoresistance mediated, in part, by upregulating ABCB1 gene expression. Tumor growth induced by RBCs was accompanied by an inflammatory signature, increased tumor vasculature, and influx of M2 macrophages. In both the peritoneal cavity and tumor microenvironment, extravascular RBCs rapidly recruited monocyte-macrophages into the lesion sites. In addition, RBCs and Hb increased several nucleotide-binding oligomerization domain-like receptors' expression and induced IL-1β release. Our results provide novel insights into the protumor function of RBCs and Hb as endogenous danger signals, which can promote tumor cell proliferation, macrophage recruitment, and polarization. Hemorrhage may represent a useful prognostic factor for cancer patients because of its role in tumor promotion and chemoresistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B / biosynthesis
  • ATP Binding Cassette Transporter, Subfamily B / genetics
  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Cell Movement / immunology
  • Cell Proliferation
  • Cisplatin / pharmacology
  • Doxorubicin / pharmacology
  • Drug Resistance, Neoplasm / drug effects*
  • Erythrocytes / pathology*
  • Hemoglobins / pharmacology*
  • Hemorrhage / pathology*
  • Inflammation / immunology
  • Interleukin-1beta / metabolism
  • Macrophages / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms / blood supply
  • Neoplasms / drug therapy
  • Neoplasms / pathology*
  • Neovascularization, Pathologic
  • Oxidative Stress / drug effects
  • Paclitaxel / pharmacology
  • Reactive Oxygen Species / metabolism
  • Transcription Factor RelA / biosynthesis
  • Transcription Factor RelA / metabolism
  • Tumor Microenvironment / immunology

Substances

  • ABCB1 protein, human
  • ATP Binding Cassette Transporter, Subfamily B
  • Antineoplastic Agents
  • Hemoglobins
  • IL1B protein, human
  • Interleukin-1beta
  • Reactive Oxygen Species
  • Rela protein, mouse
  • Transcription Factor RelA
  • Doxorubicin
  • Paclitaxel
  • Cisplatin