HIF-2α Promotes Dissemination of Plasma Cells in Multiple Myeloma by Regulating CXCL12/CXCR4 and CCR1

Cancer Res. 2017 Oct 15;77(20):5452-5463. doi: 10.1158/0008-5472.CAN-17-0115. Epub 2017 Aug 30.

Abstract

Disease progression and relapse in multiple myeloma is dependent on the ability of the multiple myeloma plasma cells (PC) to reenter the circulation and disseminate throughout the bone marrow. Increased bone marrow hypoxia is associated with increased recirculation of multiple myeloma PCs. Accordingly, we hypothesized that during chronic hypoxia, activation of HIF-2α may overcome the bone marrow retention signal provided by stromal-derived CXCL12, thereby enabling dissemination of multiple myeloma PCs. Here we demonstrate that HIF-2α upregulates multiple myeloma PC CXCL12 expression, decreasing migration toward CXCL12 and reducing adhesion to mesenchymal stromal cells in vitro We also found that HIF-2α strongly induced expression of the chemokine receptor CCR1 in multiple myeloma PCs. CCR1 activation potently induces multiple myeloma PC migration toward CCL3 while abrogating the multiple myeloma PC migratory response to CXCL12. In addition, increased CCR1 expression by multiple myeloma PCs conferred poor prognosis in newly diagnosed multiple myeloma patients and was associated with an increase in circulating multiple myeloma PCs in these patients. Taken together, our results suggest a role for hypoxia-mediated CCR1 upregulation in driving the egress of multiple myeloma PCs from the bone marrow. Targeting CCR1 may represent a novel strategy to prevent dissemination and overt relapse in multiple myeloma. Cancer Res; 77(20); 5452-63. ©2017 AACR.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Chemokine CXCL12 / metabolism*
  • Disease Progression
  • Female
  • Gene Expression Profiling
  • Humans
  • Male
  • Middle Aged
  • Multiple Myeloma / metabolism*
  • Multiple Myeloma / pathology*
  • Plasma Cells / metabolism
  • Plasma Cells / pathology*
  • Receptors, CCR1 / metabolism*
  • Receptors, CXCR4 / metabolism*
  • Tumor Cells, Cultured

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • CCR1 protein, human
  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Receptors, CCR1
  • Receptors, CXCR4
  • endothelial PAS domain-containing protein 1