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

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Résumé

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.

langueAnglais
Numéro d'article1088
journalFrontiers in Microbiology
Volume8
NuméroJUN
Les DOIs
étatPublié - 13 juin 2017

Empreinte digitale

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

mots-clés

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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",
    day = "13",
    doi = "10.3389/fmicb.2017.01088",
    language = "English",
    volume = "8",
    journal = "Frontiers in Microbiology",
    issn = "1664-302X",
    publisher = "Frontiers Research Foundation",
    number = "JUN",

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    TY - JOUR

    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

    UR - http://www.scopus.com/inward/record.url?scp=85020487515&partnerID=8YFLogxK

    U2 - 10.3389/fmicb.2017.01088

    DO - 10.3389/fmicb.2017.01088

    M3 - Article

    VL - 8

    JO - Frontiers in Microbiology

    T2 - Frontiers in Microbiology

    JF - Frontiers in Microbiology

    SN - 1664-302X

    IS - JUN

    M1 - 1088

    ER -