Production of IL-1β by bone marrow-derived macrophages in response to chemotherapeutic drugs: synergistic effects of doxorubicin and vincristine

Cancer Biol Ther. 2014 Oct;15(10):1395-403. doi: 10.4161/cbt.29922. Epub 2014 Jul 21.

Abstract

Cytotoxic chemotherapeutic drugs, especially when used in combination, are widely employed to treat a variety of cancers in patients but often lead to serious symptoms that negatively affect physical functioning and quality of life. There is compelling evidence that implicates cytotoxic chemotherapy-induced inflammation in the etiology of these symptoms. Because IL-1β plays a central role as an initiator cytokine in immune responses, we compared doxorubicin, a drug known to induce IL-1β production, with ten other commonly prescribed chemotherapeutic drugs in their ability to lead to processing and secretion of IL-1β by primary mouse macrophages. Seven of them (melphalan, cisplatin, vincristine, etoposide, paclitaxel, methotrexate, and cytarabine) caused the production of IL-1β in cells pretreated with lipopolysaccharide. When delivered in combination with doxorubicin, one of the drugs, vincristine, was also capable of synergistically activating the NLRP3-dependent inflammasome and increasing expression of IL-1β, IL-6, and CXCL1. The absence of TNF-α and IL-1 signaling caused a partial reduction in the production of mature IL-1β. Three small-molecule inhibitors known to suppress activity of kinases situated upstream of mitogen-activated kinases (MAPKs) inhibited the expression of IL-1β, IL-6, and CXCL1 when doxorubicin and vincristine were used singly or together, so specific kinase inhibitors may be useful in reducing inflammation in patients receiving chemotherapy.

Keywords: cytokines; inflammasome; nilotinib; ponatinib; sorafenib.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Bone Marrow Cells / drug effects*
  • Bone Marrow Cells / metabolism
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Chemokine CXCL1 / metabolism
  • Doxorubicin / pharmacology*
  • Drug Synergism
  • Inflammasomes / metabolism
  • Interleukin 1 Receptor Antagonist Protein / metabolism
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Interleukin-6 / metabolism
  • Lipopolysaccharides / pharmacology
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Mice, Inbred C57BL
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • RNA, Messenger / metabolism*
  • Signal Transduction
  • Vincristine / pharmacology*

Substances

  • Antineoplastic Agents
  • CXCL1 protein, human
  • Carrier Proteins
  • Chemokine CXCL1
  • Inflammasomes
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1beta
  • Interleukin-6
  • Lipopolysaccharides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • RNA, Messenger
  • Vincristine
  • Doxorubicin