Erythritol availability in bovine, murine and human models highlights a potential role for the host aldose reductase during Brucella infection

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Abstract

Erythritol is the preferential carbon source for most brucellae, a group of facultative intracellular bacteria that cause a worldwide zoonosis. Since this polyol is abundant in genital organs of ruminants and swine, it is widely accepted that erythritol accounts at least in part for the characteristic genital tropism of brucellae. Nevertheless, proof of erythritol availability and essentiality during Brucella intracellular multiplication has remained elusive. To investigate this relationship, we compared ΔeryH (erythritol-sensitive and thus predicted to be attenuated if erythritol is present), ΔeryA (erythritol-tolerant but showing reduced growth if erythritol is a crucial nutrient) and wild type B. abortus in various infection models. This reporting system indicated that erythritol was available but not required for B. abortus multiplication in bovine trophoblasts. However, mice and humans have been considered to lack erythritol, and we found that it was available but not required for B. abortus multiplication in human and murine trophoblastic and macrophage-like cells, and in mouse spleen and conceptus (fetus, placenta and envelopes). Using this animal model, we found that B. abortus infected cells and tissues contained aldose reductase, an enzyme that can account for the production of erythritol from pentose cycle precursors.

Original languageEnglish
Article number1088
JournalFrontiers in Microbiology
Volume8
Issue numberJUN
DOIs
Publication statusPublished - 13 Jun 2017

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Erythritol
Aldehyde Reductase
Brucella
Infection
Pentoses
Tropism
Genitalia
Zoonoses
Trophoblasts
Ruminants
Placenta
Fetus
Swine
Carbon
Spleen
Animal Models
Macrophages

Keywords

  • Aldose reductase
  • Bovine trophoblast
  • Brucella
  • Erythritol
  • Human trophoblast
  • Murine model
  • Pentose phosphate cycle
  • Polyol pathway

Cite this

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title = "Erythritol availability in bovine, murine and human models highlights a potential role for the host aldose reductase during Brucella infection",
abstract = "Erythritol is the preferential carbon source for most brucellae, a group of facultative intracellular bacteria that cause a worldwide zoonosis. Since this polyol is abundant in genital organs of ruminants and swine, it is widely accepted that erythritol accounts at least in part for the characteristic genital tropism of brucellae. Nevertheless, proof of erythritol availability and essentiality during Brucella intracellular multiplication has remained elusive. To investigate this relationship, we compared ΔeryH (erythritol-sensitive and thus predicted to be attenuated if erythritol is present), ΔeryA (erythritol-tolerant but showing reduced growth if erythritol is a crucial nutrient) and wild type B. abortus in various infection models. This reporting system indicated that erythritol was available but not required for B. abortus multiplication in bovine trophoblasts. However, mice and humans have been considered to lack erythritol, and we found that it was available but not required for B. abortus multiplication in human and murine trophoblastic and macrophage-like cells, and in mouse spleen and conceptus (fetus, placenta and envelopes). Using this animal model, we found that B. abortus infected cells and tissues contained aldose reductase, an enzyme that can account for the production of erythritol from pentose cycle precursors.",
keywords = "Aldose reductase, Bovine trophoblast, Brucella, Erythritol, Human trophoblast, Murine model, Pentose phosphate cycle, Polyol pathway",
author = "Thibault Barbier and Arnaud Machelart and Amaia Z{\'u}{\~n}iga-Ripa and Hubert Plovier and Charlotte Hougardy and Elodie Lobet and Kevin Willemart and Eric Muraille and {De Bolle}, Xavier and {Van Schaftingen}, Emile and Ignacio Moriy{\'o}n and Letesson, {Jean Jacques}",
year = "2017",
month = "6",
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journal = "Frontiers in Microbiology",
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T1 - Erythritol availability in bovine, murine and human models highlights a potential role for the host aldose reductase during Brucella infection

AU - Barbier, Thibault

AU - Machelart, Arnaud

AU - Zúñiga-Ripa, Amaia

AU - Plovier, Hubert

AU - Hougardy, Charlotte

AU - Lobet, Elodie

AU - Willemart, Kevin

AU - Muraille, Eric

AU - De Bolle, Xavier

AU - Van Schaftingen, Emile

AU - Moriyón, Ignacio

AU - Letesson, Jean Jacques

PY - 2017/6/13

Y1 - 2017/6/13

N2 - Erythritol is the preferential carbon source for most brucellae, a group of facultative intracellular bacteria that cause a worldwide zoonosis. Since this polyol is abundant in genital organs of ruminants and swine, it is widely accepted that erythritol accounts at least in part for the characteristic genital tropism of brucellae. Nevertheless, proof of erythritol availability and essentiality during Brucella intracellular multiplication has remained elusive. To investigate this relationship, we compared ΔeryH (erythritol-sensitive and thus predicted to be attenuated if erythritol is present), ΔeryA (erythritol-tolerant but showing reduced growth if erythritol is a crucial nutrient) and wild type B. abortus in various infection models. This reporting system indicated that erythritol was available but not required for B. abortus multiplication in bovine trophoblasts. However, mice and humans have been considered to lack erythritol, and we found that it was available but not required for B. abortus multiplication in human and murine trophoblastic and macrophage-like cells, and in mouse spleen and conceptus (fetus, placenta and envelopes). Using this animal model, we found that B. abortus infected cells and tissues contained aldose reductase, an enzyme that can account for the production of erythritol from pentose cycle precursors.

AB - Erythritol is the preferential carbon source for most brucellae, a group of facultative intracellular bacteria that cause a worldwide zoonosis. Since this polyol is abundant in genital organs of ruminants and swine, it is widely accepted that erythritol accounts at least in part for the characteristic genital tropism of brucellae. Nevertheless, proof of erythritol availability and essentiality during Brucella intracellular multiplication has remained elusive. To investigate this relationship, we compared ΔeryH (erythritol-sensitive and thus predicted to be attenuated if erythritol is present), ΔeryA (erythritol-tolerant but showing reduced growth if erythritol is a crucial nutrient) and wild type B. abortus in various infection models. This reporting system indicated that erythritol was available but not required for B. abortus multiplication in bovine trophoblasts. However, mice and humans have been considered to lack erythritol, and we found that it was available but not required for B. abortus multiplication in human and murine trophoblastic and macrophage-like cells, and in mouse spleen and conceptus (fetus, placenta and envelopes). Using this animal model, we found that B. abortus infected cells and tissues contained aldose reductase, an enzyme that can account for the production of erythritol from pentose cycle precursors.

KW - Aldose reductase

KW - Bovine trophoblast

KW - Brucella

KW - Erythritol

KW - Human trophoblast

KW - Murine model

KW - Pentose phosphate cycle

KW - Polyol pathway

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