Impaired NLRP3 inflammasome activity during fetal development regulates IL-1β production in human monocytes

Eur J Immunol. 2015 Jan;45(1):238-49. doi: 10.1002/eji.201444707. Epub 2014 Nov 17.

Abstract

Interleukin-1β (IL-1β) production is impaired in cord blood monocytes. However, the mechanism underlying this developmental attenuation remains unclear. Here, we analyzed the extent of variability within the Toll-like receptor (TLR)/NLRP3 inflammasome pathways in human neonates. We show that immature low CD14 expressing/CD16(pos) monocytes predominate before 33 weeks of gestation, and that these cells lack production of the pro-IL-1β precursor protein upon LPS stimulation. In contrast, high levels of pro-IL-1β are produced within high CD14 expressing monocytes, although these cells are unable to secrete mature IL-1β. The lack of secreted IL-1β in these monocytes parallels a reduction of NLRP3 induction following TLR stimulation resulting in a lack of caspase-1 activity before 29 weeks of gestation, whereas expression of the apoptosis-associated speck-like protein containing a CARD and function of the P2×7 receptor are preserved. Our analyses also reveal a strong inhibitory effect of placental infection on LPS/ATP-induced caspase-1 activity in cord blood monocytes. Lastly, secretion of IL-1β in preterm neonates is restored to adult levels during the neonatal period, indicating rapid maturation of these responses after birth. Collectively, our data highlight important developmental mechanisms regulating IL-1β responses early in gestation, in part due to a downregulation of TLR-mediated NLRP3 expression. Such mechanisms may serve to limit potentially damaging inflammatory responses in a developing fetus.

Keywords: Human; Inflammasome; Interleukin-1 beta (IL-1β); Neonate; Toll-like receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / pharmacology
  • Adult
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology*
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / immunology
  • Fetal Blood / cytology
  • Fetal Blood / drug effects
  • Fetal Blood / immunology
  • Fetal Development / immunology*
  • Fetus
  • Gene Expression Regulation, Developmental
  • Gestational Age
  • Humans
  • Infant, Newborn
  • Infant, Premature
  • Inflammasomes / genetics
  • Inflammasomes / immunology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology*
  • Lipopolysaccharides / pharmacology
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / immunology*
  • Monocytes / cytology
  • Monocytes / drug effects
  • Monocytes / immunology*
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Receptors, Purinergic P2X7 / genetics
  • Receptors, Purinergic P2X7 / immunology
  • Signal Transduction
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / immunology

Substances

  • CARD Signaling Adaptor Proteins
  • Carrier Proteins
  • Cytoskeletal Proteins
  • Inflammasomes
  • Interleukin-1beta
  • Lipopolysaccharides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • PYCARD protein, human
  • Receptors, Purinergic P2X7
  • Toll-Like Receptors
  • Adenosine Triphosphate