A Neonatal Murine Escherichia coli Sepsis Model Demonstrates That Adjunctive Pentoxifylline Enhances the Ratio of Anti- vs. Pro-inflammatory Cytokines in Blood and Organ Tissues

Front Immunol. 2020 Sep 23:11:577878. doi: 10.3389/fimmu.2020.577878. eCollection 2020.

Abstract

Introduction: Neonatal sepsis triggers an inflammatory response that contributes to mortality and multiple organ injury. Pentoxifylline (PTX), a phosphodiesterase inhibitor which suppresses pro-inflammatory cytokines, is a candidate adjunctive therapy for newborn sepsis. We hypothesized that administration of PTX in addition to antibiotics decreases live bacteria-induced pro-inflammatory and/or enhances anti-inflammatory cytokine production in septic neonatal mice without augmenting bacterial growth. Methods: Newborn C57BL/6J mice (< 24 h old) were injected intravenously with 105 colony forming units (CFUs)/g weight of a bioluminescent derivative of the encapsulated clinical isolate Escherichia coli O18:K1. Adequacy of intravenous injections was validated using in vivo bioluminescence imaging and Evans blue. Pups were treated with gentamicin (GENT), PTX, (GENT + PTX) or saline at 0, 1.5, or 4 h after sepsis initiation, and euthanized after an additional 4 h. CFUs and cytokines were measured from blood and homogenized organ tissues. Results: GENT alone inhibited bacterial growth, IL-1β, and IL-6 production in blood and organs. Addition of PTX to GENT profoundly inhibited E. coli-induced TNF and enhanced IL-10 in blood of newborn mice at all timepoints, whereas it primarily upregulated IL-10 production in peripheral organs (lung, spleen, brain). PTX, whether alone or adjunctive to GENT, did not increase microbial colony counts in blood and organs. Conclusion: Addition of PTX to antibiotics in murine neonatal E. coli sepsis promoted an anti-inflammatory milieu through inhibition of plasma TNF and enhancement of IL-10 production in plasma and organs without increasing bacterial growth, supporting its utility as a potential adjunctive agent for newborn sepsis.

Keywords: Escherichia coli; anti-inflammatory; cytokines; interleukin 10; newborn; pentoxifylline; sepsis.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Animals, Newborn
  • Anti-Bacterial Agents / pharmacology*
  • Anti-Inflammatory Agents / pharmacology*
  • Cytokines / blood*
  • Disease Models, Animal
  • Drug Therapy, Combination
  • Escherichia coli / drug effects*
  • Escherichia coli / growth & development
  • Escherichia coli / pathogenicity
  • Escherichia coli Infections / blood
  • Escherichia coli Infections / drug therapy*
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / microbiology
  • Gentamicins / pharmacology*
  • Host-Pathogen Interactions
  • Inflammation Mediators / blood*
  • Mice, Inbred C57BL
  • Neonatal Sepsis / blood
  • Neonatal Sepsis / drug therapy*
  • Neonatal Sepsis / immunology
  • Neonatal Sepsis / microbiology
  • Pentoxifylline / pharmacology*
  • Phosphodiesterase Inhibitors / pharmacology

Substances

  • Anti-Bacterial Agents
  • Anti-Inflammatory Agents
  • Cytokines
  • Gentamicins
  • Inflammation Mediators
  • Phosphodiesterase Inhibitors
  • Pentoxifylline