Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection
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 characterist...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01088/full |
| _version_ | 1811265979116683264 |
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| author | Thibault Barbier Arnaud Machelart Amaia Zúñiga-Ripa Hubert Plovier Charlotte Hougardy Elodie Lobet Kevin Willemart Eric Muraille Xavier De Bolle Emile Van Schaftingen Ignacio Moriyón Jean-Jacques Letesson |
| author_facet | Thibault Barbier Arnaud Machelart Amaia Zúñiga-Ripa Hubert Plovier Charlotte Hougardy Elodie Lobet Kevin Willemart Eric Muraille Xavier De Bolle Emile Van Schaftingen Ignacio Moriyón Jean-Jacques Letesson |
| author_sort | Thibault Barbier |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T20:33:45Z |
| format | Article |
| id | doaj.art-575807365bd94234a9acf1ac1f3de78e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-12T20:33:45Z |
| publishDate | 2017-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-575807365bd94234a9acf1ac1f3de78e2022-12-22T03:17:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-06-01810.3389/fmicb.2017.01088274734Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella InfectionThibault Barbier0Arnaud Machelart1Amaia Zúñiga-Ripa2Hubert Plovier3Charlotte Hougardy4Elodie Lobet5Kevin Willemart6Eric Muraille7Xavier De Bolle8Emile Van Schaftingen9Ignacio Moriyón10Jean-Jacques Letesson11Research Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumDepartamento de Microbiología y Parasitología, Instituto de Salud Tropical, Instituto de Investigación Sanitaria de Navarra, Universidad de NavarraPamplona, SpainResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumLaboratoire de Parasitologie, Faculté de Médecine, Université Libre de BruxellesBrussels, BelgiumResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumWELBIO and de Duve Institute, Université Catholique de LouvainBrussels, BelgiumDepartamento de Microbiología y Parasitología, Instituto de Salud Tropical, Instituto de Investigación Sanitaria de Navarra, Universidad de NavarraPamplona, SpainResearch Unit in Biology of Microorganisms, Department of Veterinary Medicine, University of NamurNamur, BelgiumErythritol 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01088/fullBrucellaerythritolaldose reductasemurine modelbovine trophoblasthuman trophoblast |
| spellingShingle | Thibault Barbier Arnaud Machelart Amaia Zúñiga-Ripa Hubert Plovier Charlotte Hougardy Elodie Lobet Kevin Willemart Eric Muraille Xavier De Bolle Emile Van Schaftingen Ignacio Moriyón Jean-Jacques Letesson Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection Frontiers in Microbiology Brucella erythritol aldose reductase murine model bovine trophoblast human trophoblast |
| title | Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection |
| title_full | Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection |
| title_fullStr | Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection |
| title_full_unstemmed | Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection |
| title_short | Erythritol Availability in Bovine, Murine and Human Models Highlights a Potential Role for the Host Aldose Reductase during Brucella Infection |
| title_sort | erythritol availability in bovine murine and human models highlights a potential role for the host aldose reductase during brucella infection |
| topic | Brucella erythritol aldose reductase murine model bovine trophoblast human trophoblast |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01088/full |
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