Paclitaxel Enhances the Innate Immunity by Promoting NLRP3 Inflammasome Activation in Macrophages

Front Immunol. 2019 Jan 29:10:72. doi: 10.3389/fimmu.2019.00072. eCollection 2019.

Abstract

Microtubules play critical roles in regulating the activation of NLRP3 inflammasome and microtubule-destabilizing agents such as colchicine have been shown to suppress the activation of this inflammasome. However, it remains largely unknown whether paclitaxel, a microtubule-stabilizing agent being used in cancer therapy, has any influences on NLRP3 inflammasome activation. Here we showed that paclitaxel pre-treatment greatly enhanced ATP- or nigericin-induced NLRP3 inflammasome activation as indicated by increased release of cleaved caspase-1 and mature IL-1β, enhanced formation of ASC speck, and increased gasdermin D cleavage and pyroptosis. Paclitaxel time- and dose-dependently induced α-tubulin acetylation in LPS-primed murine and human macrophages and further increased ATP- or nigericin-induced α-tubulin acetylation. Such increased α-tubulin acetylation was significantly suppressed either by resveratrol or NAD+ (coenzyme required for deacetylase activity of SIRT2), or by genetic knockdown of MEC-17 (gene encoding α-tubulin acetyltransferase 1). Concurrently, the paclitaxel-mediated enhancement of NLRP3 inflammasome activation was significantly suppressed by resveratrol, NAD+, or MEC-17 knockdown, indicating the involvement of paclitaxel-induced α-tubulin acetylation in the augmentation of NLRP3 inflammasome activation. Similar to paclitaxel, epothilone B that is another microtubule-stabilizing agent also induced α-tubulin acetylation and increased NLRP3 inflammasome activation in macrophages in response to ATP treatment. Consistent with the in vitro results, intraperitoneal administration of paclitaxel significantly increased serum IL-1β levels, reduced bacterial burden, dampened infiltration of inflammatory cells in the liver, and improved animal survival in a mouse model of bacterial infection. Collectively, our data indicate that paclitaxel potentiated NLRP3 inflammasome activation by inducing α-tubulin acetylation and thereby conferred enhanced antibacterial innate responses, suggesting its potential application against pathogenic infections beyond its use as a chemotherapeutic agent.

Keywords: MEC-17; NLRP3 inflammasome; SIRT2; epothilone B; paclitaxel; α-tubulin acetylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation / drug effects
  • Acetyltransferases / genetics
  • Animals
  • Bacterial Infections / immunology
  • Cell Line
  • Disease Models, Animal
  • Epothilones / pharmacology
  • Gene Knockdown Techniques
  • Humans
  • Immunity, Innate / drug effects*
  • Inflammasomes / metabolism*
  • Interleukin-1beta / blood
  • Interleukin-1beta / metabolism
  • Macrophages / metabolism*
  • Mice
  • Microtubule Proteins / genetics
  • Microtubules / drug effects
  • Microtubules / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Nigericin / pharmacology
  • Paclitaxel / administration & dosage
  • Paclitaxel / pharmacology*
  • Pyroptosis / drug effects
  • Signal Transduction / drug effects
  • THP-1 Cells
  • Tubulin / metabolism

Substances

  • Epothilones
  • IL1B protein, human
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • Microtubule Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • Tubulin
  • Acetyltransferases
  • ATAT1 protein, human
  • ATAT1 protein, mouse
  • Paclitaxel
  • Nigericin
  • epothilone B