The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice

Research output: Contribution to journal › Journal article › Research › peer-review

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The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice. / Fan, Yong; Støving, René Klinkby; Berreira Ibraim, Samar; Hyötyläinen, Tuulia; Thirion, Florence; Arora, Tulika; Lyu, Liwei; Stankevic, Evelina; Hansen, Tue Haldor; Déchelotte, Pierre; Sinioja, Tim; Ragnarsdottir, Oddny; Pons, Nicolas; Galleron, Nathalie; Quinquis, Benoît; Levenez, Florence; Roume, Hugo; Falony, Gwen; Vieira-Silva, Sara; Raes, Jeroen; Clausen, Loa; Telléus, Gry Kjaersdam; Bäckhed, Fredrik; Oresic, Matej; Ehrlich, S. Dusko; Pedersen, Oluf.

In: Nature Microbiology, Vol. 8, 2023, p. 787–802.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Fan, Y, Støving, RK, Berreira Ibraim, S, Hyötyläinen, T, Thirion, F, Arora, T, Lyu, L, Stankevic, E, Hansen, TH, Déchelotte, P, Sinioja, T, Ragnarsdottir, O, Pons, N, Galleron, N, Quinquis, B, Levenez, F, Roume, H, Falony, G, Vieira-Silva, S, Raes, J, Clausen, L, Telléus, GK, Bäckhed, F, Oresic, M, Ehrlich, SD & Pedersen, O 2023, 'The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice', Nature Microbiology, vol. 8, pp. 787–802. https://doi.org/10.1038/s41564-023-01355-5

APA

Fan, Y., Støving, R. K., Berreira Ibraim, S., Hyötyläinen, T., Thirion, F., Arora, T., Lyu, L., Stankevic, E., Hansen, T. H., Déchelotte, P., Sinioja, T., Ragnarsdottir, O., Pons, N., Galleron, N., Quinquis, B., Levenez, F., Roume, H., Falony, G., Vieira-Silva, S., ... Pedersen, O. (2023). The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice. Nature Microbiology, 8, 787–802. https://doi.org/10.1038/s41564-023-01355-5

Vancouver

Fan Y, Støving RK, Berreira Ibraim S, Hyötyläinen T, Thirion F, Arora T et al. The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice. Nature Microbiology. 2023;8:787–802. https://doi.org/10.1038/s41564-023-01355-5

Author

Fan, Yong ; Støving, René Klinkby ; Berreira Ibraim, Samar ; Hyötyläinen, Tuulia ; Thirion, Florence ; Arora, Tulika ; Lyu, Liwei ; Stankevic, Evelina ; Hansen, Tue Haldor ; Déchelotte, Pierre ; Sinioja, Tim ; Ragnarsdottir, Oddny ; Pons, Nicolas ; Galleron, Nathalie ; Quinquis, Benoît ; Levenez, Florence ; Roume, Hugo ; Falony, Gwen ; Vieira-Silva, Sara ; Raes, Jeroen ; Clausen, Loa ; Telléus, Gry Kjaersdam ; Bäckhed, Fredrik ; Oresic, Matej ; Ehrlich, S. Dusko ; Pedersen, Oluf. / The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice. In: Nature Microbiology. 2023 ; Vol. 8. pp. 787–802.

Bibtex

@article{63df69e88d9b4a22a8f06ed2a283320e,
title = "The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice",
abstract = "Anorexia nervosa (AN) is an eating disorder with a high mortality. About 95% of cases are women and it has a population prevalence of about 1%, but evidence-based treatment is lacking. The pathogenesis of AN probably involves genetics and various environmental factors, and an altered gut microbiota has been observed in individuals with AN using amplicon sequencing and relatively small cohorts. Here we investigated whether a disrupted gut microbiota contributes to AN pathogenesis. Shotgun metagenomics and metabolomics were performed on faecal and serum samples, respectively, from a cohort of 77 females with AN and 70 healthy females. Multiple bacterial taxa (for example, Clostridium species) were altered in AN and correlated with estimates of eating behaviour and mental health. The gut virome was also altered in AN including a reduction in viral–bacterial interactions. Bacterial functional modules associated with the degradation of neurotransmitters were enriched in AN and various structural variants in bacteria were linked to metabolic features of AN. Serum metabolomics revealed an increase in metabolites associated with reduced food intake (for example, indole-3-propionic acid). Causal inference analyses implied that serum bacterial metabolites are potentially mediating the impact of an altered gut microbiota on AN behaviour. Further, we performed faecal microbiota transplantation from AN cases to germ-free mice under energy-restricted feeding to mirror AN eating behaviour. We found that the reduced weight gain and induced hypothalamic and adipose tissue gene expression were related to aberrant energy metabolism and eating behaviour. Our {\textquoteleft}omics{\textquoteright} and mechanistic studies imply that a disruptive gut microbiome may contribute to AN pathogenesis.",
author = "Yong Fan and St{\o}ving, {Ren{\'e} Klinkby} and {Berreira Ibraim}, Samar and Tuulia Hy{\"o}tyl{\"a}inen and Florence Thirion and Tulika Arora and Liwei Lyu and Evelina Stankevic and Hansen, {Tue Haldor} and Pierre D{\'e}chelotte and Tim Sinioja and Oddny Ragnarsdottir and Nicolas Pons and Nathalie Galleron and Beno{\^i}t Quinquis and Florence Levenez and Hugo Roume and Gwen Falony and Sara Vieira-Silva and Jeroen Raes and Loa Clausen and Tell{\'e}us, {Gry Kjaersdam} and Fredrik B{\"a}ckhed and Matej Oresic and Ehrlich, {S. Dusko} and Oluf Pedersen",
note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",
year = "2023",
doi = "10.1038/s41564-023-01355-5",
language = "English",
volume = "8",
pages = "787–802",
journal = "Nature Microbiology",
issn = "2058-5276",
publisher = "nature publishing group",

}

RIS

TY - JOUR

T1 - The gut microbiota contributes to the pathogenesis of anorexia nervosa in humans and mice

AU - Fan, Yong

AU - Støving, René Klinkby

AU - Berreira Ibraim, Samar

AU - Hyötyläinen, Tuulia

AU - Thirion, Florence

AU - Arora, Tulika

AU - Lyu, Liwei

AU - Stankevic, Evelina

AU - Hansen, Tue Haldor

AU - Déchelotte, Pierre

AU - Sinioja, Tim

AU - Ragnarsdottir, Oddny

AU - Pons, Nicolas

AU - Galleron, Nathalie

AU - Quinquis, Benoît

AU - Levenez, Florence

AU - Roume, Hugo

AU - Falony, Gwen

AU - Vieira-Silva, Sara

AU - Raes, Jeroen

AU - Clausen, Loa

AU - Telléus, Gry Kjaersdam

AU - Bäckhed, Fredrik

AU - Oresic, Matej

AU - Ehrlich, S. Dusko

AU - Pedersen, Oluf

N1 - Publisher Copyright: © 2023, The Author(s).

PY - 2023

Y1 - 2023

N2 - Anorexia nervosa (AN) is an eating disorder with a high mortality. About 95% of cases are women and it has a population prevalence of about 1%, but evidence-based treatment is lacking. The pathogenesis of AN probably involves genetics and various environmental factors, and an altered gut microbiota has been observed in individuals with AN using amplicon sequencing and relatively small cohorts. Here we investigated whether a disrupted gut microbiota contributes to AN pathogenesis. Shotgun metagenomics and metabolomics were performed on faecal and serum samples, respectively, from a cohort of 77 females with AN and 70 healthy females. Multiple bacterial taxa (for example, Clostridium species) were altered in AN and correlated with estimates of eating behaviour and mental health. The gut virome was also altered in AN including a reduction in viral–bacterial interactions. Bacterial functional modules associated with the degradation of neurotransmitters were enriched in AN and various structural variants in bacteria were linked to metabolic features of AN. Serum metabolomics revealed an increase in metabolites associated with reduced food intake (for example, indole-3-propionic acid). Causal inference analyses implied that serum bacterial metabolites are potentially mediating the impact of an altered gut microbiota on AN behaviour. Further, we performed faecal microbiota transplantation from AN cases to germ-free mice under energy-restricted feeding to mirror AN eating behaviour. We found that the reduced weight gain and induced hypothalamic and adipose tissue gene expression were related to aberrant energy metabolism and eating behaviour. Our ‘omics’ and mechanistic studies imply that a disruptive gut microbiome may contribute to AN pathogenesis.

AB - Anorexia nervosa (AN) is an eating disorder with a high mortality. About 95% of cases are women and it has a population prevalence of about 1%, but evidence-based treatment is lacking. The pathogenesis of AN probably involves genetics and various environmental factors, and an altered gut microbiota has been observed in individuals with AN using amplicon sequencing and relatively small cohorts. Here we investigated whether a disrupted gut microbiota contributes to AN pathogenesis. Shotgun metagenomics and metabolomics were performed on faecal and serum samples, respectively, from a cohort of 77 females with AN and 70 healthy females. Multiple bacterial taxa (for example, Clostridium species) were altered in AN and correlated with estimates of eating behaviour and mental health. The gut virome was also altered in AN including a reduction in viral–bacterial interactions. Bacterial functional modules associated with the degradation of neurotransmitters were enriched in AN and various structural variants in bacteria were linked to metabolic features of AN. Serum metabolomics revealed an increase in metabolites associated with reduced food intake (for example, indole-3-propionic acid). Causal inference analyses implied that serum bacterial metabolites are potentially mediating the impact of an altered gut microbiota on AN behaviour. Further, we performed faecal microbiota transplantation from AN cases to germ-free mice under energy-restricted feeding to mirror AN eating behaviour. We found that the reduced weight gain and induced hypothalamic and adipose tissue gene expression were related to aberrant energy metabolism and eating behaviour. Our ‘omics’ and mechanistic studies imply that a disruptive gut microbiome may contribute to AN pathogenesis.

U2 - 10.1038/s41564-023-01355-5

DO - 10.1038/s41564-023-01355-5

M3 - Journal article

C2 - 37069399

AN - SCOPUS:85153050793

VL - 8

SP - 787

EP - 802

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

ER -

ID: 345645247