A defective TLR4 signaling for IFN-β expression is responsible for the innately lower ability of BALB/c macrophages to produce NO in response to LPS as compared to C57BL/6

PLoS One. 2014 Jun 9;9(6):e98913. doi: 10.1371/journal.pone.0098913. eCollection 2014.

Abstract

C57BL/6 mice macrophages innately produce higher levels of NO than BALB/c cells when stimulated with LPS. Here, we investigated the molecular events that account for this intrinsic differential production of NO. We found that the lower production of NO in BALB/c is not due to a subtraction of L-arginine by arginase, and correlates with a lower iNOS accumulation, which is independent of its degradation rate. Instead, the lower accumulation of iNOS is due to the lower levels of iNOS mRNA, previously shown to be also independent of its stability, suggesting that iNOS transcription is less efficient in BALB/c than in C57BL/6 macrophages. Activation of NFκB is more efficient in BALB/c, thus not correlating with iNOS expression. Conversely, activation of STAT-1 does correlate with iNOS expression, being more prominent in C57BL/6 than in BALB/c macrophages. IFN-β and IL-10 are more highly expressed in C57BL/6 than in BALB/c macrophages, and the opposite is true for TNF-α. Whereas IL-10 and TNF-α do not seem to participate in their differential production of NO, IFN-β has a determinant role since 1) anti-IFN-β neutralizing antibodies abolish STAT-1 activation reducing NO production in C57BL/6 macrophages to levels as low as in BALB/c cells and 2) exogenous rIFN-β confers to LPS-stimulated BALB/c macrophages the ability to phosphorylate STAT-1 and to produce NO as efficiently as C57BL/6 cells. We demonstrate, for the first time, that BALB/c macrophages are innately lower NO producers than C57BL/6 cells because they are defective in the TLR-4-induced IFN-β-mediated STAT-1 activation pathway.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • Gene Expression Regulation / drug effects*
  • Gene Expression Regulation, Enzymologic / drug effects
  • Interferon-beta / genetics*
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Nitric Oxide / biosynthesis*
  • Nitric Oxide Synthase Type II / genetics
  • Phenotype
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction / drug effects*
  • Species Specificity
  • Toll-Like Receptor 4 / metabolism*
  • Transcription, Genetic / drug effects

Substances

  • Lipopolysaccharides
  • RNA, Messenger
  • STAT1 Transcription Factor
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Nitric Oxide
  • Interferon-beta
  • Nitric Oxide Synthase Type II
  • Arginase

Grants and funding

This work was supported by the following Brazilian financing programs or institutions: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). LSO, LVSV, FSO, NMGPQ, and MBHC and were supported by CNPq. TGM was supported by CAPES. SCO, AMF, LQV and MFH are CNPq research fellows. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.