Propionic acid stimulates superoxide generation in human neutrophils

Sumi Nakao, Yoshiko Moriya, Shunsuke Furuyama, Richard Niederman, Hiroshi Sugiya

Research output: Contribution to journalArticle

Abstract

Short-chain carboxylic acids are the metabolic by-products of pathogenic anaerobic bacteria and are found at sites of infection in millimolar quantities. We previously reported that propionic acid, one of the short-chain carboxylic acids, induces an increase in intracellular Ca2+ ([Ca2+](i)) in human neutrophils. Here we investigate the effect of propionic acid on superoxide generation in human neutrophils. Propionic acid (10 mM) induced inositol 1,4,5-trisphosphate (IP3) formation and a rapidly transient increase in [Ca2+](i), but not superoxide generation, whereas 1 μM formylmethionyl-leucyl-phenylalanine (fMLP), a widely used neutrophil-stimulating bacterial peptide, stimulated not only IP3 formation and Ca2+ mobilization but also superoxide generation. The IP3 level induced by propionic acid was slightly lower than that induced by fMLP. The transient increase in [Ca2+](i) induced by propionic acid immediately returned to the basal level, whereas a sustained increase in [Ca2+](i), which was higher than the basal level, following a transient increase in [Ca2+](i) was induced by fMLP. The peak level induced by propionic acid was lower than that with fMLP. In the absence of extracellular Ca2+ thapsigargin, a potent inhibitor of endoplasmic reticulum Ca2+-ATPase, induced an increase in [Ca2+](i) even after propionic acid stimulation, but not after fMLP. The Ca2+ ionophore A23187 and thapsigargin induced superoxide generation by themselves. Propionic acid enhanced the superoxide generating effect of A23187 and thapsigargin. These results suggest that Ca2+ mobilization induced by propionic acid is much weaker than that with fMLP, and propionic acid is able to generate superoxide in the presence of a Ca2+ ionophore and a Ca2+ influx activator.

Original languageEnglish (US)
Pages (from-to)331-337
Number of pages7
JournalCell Biology International
Volume22
Issue number5
DOIs
StatePublished - May 1998

Fingerprint

Superoxides
Neutrophils
N-Formylmethionine Leucyl-Phenylalanine
Thapsigargin
Ionophores
Calcimycin
Carboxylic Acids
propionic acid
Inositol 1,4,5-Trisphosphate
Anaerobic Bacteria
Calcium-Transporting ATPases
Endoplasmic Reticulum
Peptides
Infection

Keywords

  • Calcium influx
  • Neutrophils (human)
  • Propionic acid
  • Superoxide

ASJC Scopus subject areas

  • Cell Biology

Cite this

Propionic acid stimulates superoxide generation in human neutrophils. / Nakao, Sumi; Moriya, Yoshiko; Furuyama, Shunsuke; Niederman, Richard; Sugiya, Hiroshi.

In: Cell Biology International, Vol. 22, No. 5, 05.1998, p. 331-337.

Research output: Contribution to journalArticle

Nakao, Sumi ; Moriya, Yoshiko ; Furuyama, Shunsuke ; Niederman, Richard ; Sugiya, Hiroshi. / Propionic acid stimulates superoxide generation in human neutrophils. In: Cell Biology International. 1998 ; Vol. 22, No. 5. pp. 331-337.
@article{81f2dcaa6d6f4e6cacbc4f6d4141ba27,
title = "Propionic acid stimulates superoxide generation in human neutrophils",
abstract = "Short-chain carboxylic acids are the metabolic by-products of pathogenic anaerobic bacteria and are found at sites of infection in millimolar quantities. We previously reported that propionic acid, one of the short-chain carboxylic acids, induces an increase in intracellular Ca2+ ([Ca2+](i)) in human neutrophils. Here we investigate the effect of propionic acid on superoxide generation in human neutrophils. Propionic acid (10 mM) induced inositol 1,4,5-trisphosphate (IP3) formation and a rapidly transient increase in [Ca2+](i), but not superoxide generation, whereas 1 μM formylmethionyl-leucyl-phenylalanine (fMLP), a widely used neutrophil-stimulating bacterial peptide, stimulated not only IP3 formation and Ca2+ mobilization but also superoxide generation. The IP3 level induced by propionic acid was slightly lower than that induced by fMLP. The transient increase in [Ca2+](i) induced by propionic acid immediately returned to the basal level, whereas a sustained increase in [Ca2+](i), which was higher than the basal level, following a transient increase in [Ca2+](i) was induced by fMLP. The peak level induced by propionic acid was lower than that with fMLP. In the absence of extracellular Ca2+ thapsigargin, a potent inhibitor of endoplasmic reticulum Ca2+-ATPase, induced an increase in [Ca2+](i) even after propionic acid stimulation, but not after fMLP. The Ca2+ ionophore A23187 and thapsigargin induced superoxide generation by themselves. Propionic acid enhanced the superoxide generating effect of A23187 and thapsigargin. These results suggest that Ca2+ mobilization induced by propionic acid is much weaker than that with fMLP, and propionic acid is able to generate superoxide in the presence of a Ca2+ ionophore and a Ca2+ influx activator.",
keywords = "Calcium influx, Neutrophils (human), Propionic acid, Superoxide",
author = "Sumi Nakao and Yoshiko Moriya and Shunsuke Furuyama and Richard Niederman and Hiroshi Sugiya",
year = "1998",
month = "5",
doi = "10.1006/cbir.1998.0263",
language = "English (US)",
volume = "22",
pages = "331--337",
journal = "Cell Biology International",
issn = "1065-6995",
publisher = "Portland Press Ltd.",
number = "5",

}

TY - JOUR

T1 - Propionic acid stimulates superoxide generation in human neutrophils

AU - Nakao, Sumi

AU - Moriya, Yoshiko

AU - Furuyama, Shunsuke

AU - Niederman, Richard

AU - Sugiya, Hiroshi

PY - 1998/5

Y1 - 1998/5

N2 - Short-chain carboxylic acids are the metabolic by-products of pathogenic anaerobic bacteria and are found at sites of infection in millimolar quantities. We previously reported that propionic acid, one of the short-chain carboxylic acids, induces an increase in intracellular Ca2+ ([Ca2+](i)) in human neutrophils. Here we investigate the effect of propionic acid on superoxide generation in human neutrophils. Propionic acid (10 mM) induced inositol 1,4,5-trisphosphate (IP3) formation and a rapidly transient increase in [Ca2+](i), but not superoxide generation, whereas 1 μM formylmethionyl-leucyl-phenylalanine (fMLP), a widely used neutrophil-stimulating bacterial peptide, stimulated not only IP3 formation and Ca2+ mobilization but also superoxide generation. The IP3 level induced by propionic acid was slightly lower than that induced by fMLP. The transient increase in [Ca2+](i) induced by propionic acid immediately returned to the basal level, whereas a sustained increase in [Ca2+](i), which was higher than the basal level, following a transient increase in [Ca2+](i) was induced by fMLP. The peak level induced by propionic acid was lower than that with fMLP. In the absence of extracellular Ca2+ thapsigargin, a potent inhibitor of endoplasmic reticulum Ca2+-ATPase, induced an increase in [Ca2+](i) even after propionic acid stimulation, but not after fMLP. The Ca2+ ionophore A23187 and thapsigargin induced superoxide generation by themselves. Propionic acid enhanced the superoxide generating effect of A23187 and thapsigargin. These results suggest that Ca2+ mobilization induced by propionic acid is much weaker than that with fMLP, and propionic acid is able to generate superoxide in the presence of a Ca2+ ionophore and a Ca2+ influx activator.

AB - Short-chain carboxylic acids are the metabolic by-products of pathogenic anaerobic bacteria and are found at sites of infection in millimolar quantities. We previously reported that propionic acid, one of the short-chain carboxylic acids, induces an increase in intracellular Ca2+ ([Ca2+](i)) in human neutrophils. Here we investigate the effect of propionic acid on superoxide generation in human neutrophils. Propionic acid (10 mM) induced inositol 1,4,5-trisphosphate (IP3) formation and a rapidly transient increase in [Ca2+](i), but not superoxide generation, whereas 1 μM formylmethionyl-leucyl-phenylalanine (fMLP), a widely used neutrophil-stimulating bacterial peptide, stimulated not only IP3 formation and Ca2+ mobilization but also superoxide generation. The IP3 level induced by propionic acid was slightly lower than that induced by fMLP. The transient increase in [Ca2+](i) induced by propionic acid immediately returned to the basal level, whereas a sustained increase in [Ca2+](i), which was higher than the basal level, following a transient increase in [Ca2+](i) was induced by fMLP. The peak level induced by propionic acid was lower than that with fMLP. In the absence of extracellular Ca2+ thapsigargin, a potent inhibitor of endoplasmic reticulum Ca2+-ATPase, induced an increase in [Ca2+](i) even after propionic acid stimulation, but not after fMLP. The Ca2+ ionophore A23187 and thapsigargin induced superoxide generation by themselves. Propionic acid enhanced the superoxide generating effect of A23187 and thapsigargin. These results suggest that Ca2+ mobilization induced by propionic acid is much weaker than that with fMLP, and propionic acid is able to generate superoxide in the presence of a Ca2+ ionophore and a Ca2+ influx activator.

KW - Calcium influx

KW - Neutrophils (human)

KW - Propionic acid

KW - Superoxide

UR - http://www.scopus.com/inward/record.url?scp=0032468642&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032468642&partnerID=8YFLogxK

U2 - 10.1006/cbir.1998.0263

DO - 10.1006/cbir.1998.0263

M3 - Article

C2 - 10198152

AN - SCOPUS:0032468642

VL - 22

SP - 331

EP - 337

JO - Cell Biology International

JF - Cell Biology International

SN - 1065-6995

IS - 5

ER -