Multi-level analysis of the gut-brain axis shows autism spectrum disorder-associated molecular and microbial profiles.

Humans Gastrointestinal Microbiome / genetics Brain-Gut Axis Autism Spectrum Disorder / genetics Cross-Sectional Studies Bayes Theorem Reproducibility of Results Cytokines

Journal

Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671

Informations de publication

Date de publication:
07 2023
Historique:
received: 11 11 2022
accepted: 13 05 2023
medline: 7 7 2023
pubmed: 27 6 2023
entrez: 26 6 2023
Statut: ppublish

Résumé

Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by heterogeneous cognitive, behavioral and communication impairments. Disruption of the gut-brain axis (GBA) has been implicated in ASD although with limited reproducibility across studies. In this study, we developed a Bayesian differential ranking algorithm to identify ASD-associated molecular and taxa profiles across 10 cross-sectional microbiome datasets and 15 other datasets, including dietary patterns, metabolomics, cytokine profiles and human brain gene expression profiles. We found a functional architecture along the GBA that correlates with heterogeneity of ASD phenotypes, and it is characterized by ASD-associated amino acid, carbohydrate and lipid profiles predominantly encoded by microbial species in the genera Prevotella, Bifidobacterium, Desulfovibrio and Bacteroides and correlates with brain gene expression changes, restrictive dietary patterns and pro-inflammatory cytokine profiles. The functional architecture revealed in age-matched and sex-matched cohorts is not present in sibling-matched cohorts. We also show a strong association between temporal changes in microbiome composition and ASD phenotypes. In summary, we propose a framework to leverage multi-omic datasets from well-defined cohorts and investigate how the GBA influences ASD.

Identifiants

DOI: 10.1038/s41593-023-01361-0 PMID: 37365313 PMC: PMC10322709
pubmed: 37365313
doi: 10.1038/s41593-023-01361-0
pii: 10.1038/s41593-023-01361-0
pmc: PMC10322709
doi:

Substances chimiques

Cytokines 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1208-1217

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT206194
Pays : United Kingdom

Informations de copyright

© 2023. The Author(s).

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Auteurs

James T Morton (JT)

Center for Computational Biology, Flatiron Institute, Simons Foundation, New York, NY, USA.
Biostatistics & Bioinformatics Branch, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA.
ORCID: 0000-0003-3189-2681

Dong-Min Jin (DM)

Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY, USA.

Robert H Mills (RH)

Precidiag, Inc., Watertown, MA, USA.

Yan Shao (Y)

Host-Microbiota Interactions Laboratory, Wellcome Sanger Institute, Hinxton, UK.
ORCID: 0000-0002-8662-0504

Gibraan Rahman (G)

Bioinformatics and Systems Biology Program, University of California, San Diego, La Jolla, CA, USA.
Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.

Daniel McDonald (D)

Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.

Qiyun Zhu (Q)

School of Life Sciences, Arizona State University, Tempe, AZ, USA.
Biodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ, USA.

Metin Balaban (M)

Bioinformatics and Systems Biology Program, University of California, San Diego, La Jolla, CA, USA.

Yueyu Jiang (Y)

Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA.

Kalen Cantrell (K)

Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.
Department of Computer Science and Engineering, Jacobs School of Engineering, University of California, San Diego, La Jolla, CA, USA.

Antonio Gonzalez (A)

Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.

Julie Carmel (J)

Azrieli Faculty of Medicine, Bar Ilan University, Safed, Israel.

Linoy Mia Frankiensztajn (LM)

Azrieli Faculty of Medicine, Bar Ilan University, Safed, Israel.

Sandra Martin-Brevet (S)

Laboratory for Research in Neuroimaging, Centre for Research in Neurosciences, Department of Clinical Neurosciences, Centre Hospitalier Universitaire Vaudois, University of Lausanne, Lausanne, Switzerland.

Kirsten Berding (K)

Division of Nutritional Sciences, University of Illinois, Urbana, IL, USA.

Brittany D Needham (BD)

Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA.
Department of Anatomy, Cell Biology and Physiology, Indiana University School of Medicine, Indianapolis, IN, USA.
ORCID: 0000-0002-0280-1886

María Fernanda Zurita (MF)

Microbiology Institute and Health Science College, Universidad San Francisco de Quito, Quito, Ecuador.
ORCID: 0000-0001-7530-5624

Maude David (M)

Departments of Microbiology & Pharmaceutical Sciences, Oregon State University, Corvallis, OR, USA.

Olga V Averina (OV)

Vavilov Institute of General Genetics Russian Academy of Sciences, Moscow, Russia.

Alexey S Kovtun (AS)

Vavilov Institute of General Genetics Russian Academy of Sciences, Moscow, Russia.
Skolkovo Institute of Science and Technology, Skolkovo, Russia.

Antonio Noto (A)

Department of Biomedical Sciences, School of Medicine, University of Cagliari, Cagliari, Italy.
ORCID: 0000-0003-3538-0050

Michele Mussap (M)

Laboratory Medicine, Department of Surgical Sciences, School of Medicine, University of Cagliari, Cagliari, Italy.

Mingbang Wang (M)

Shanghai Key Laboratory of Birth Defects, Division of Neonatology, Children's Hospital of Fudan University, National Center for Children's Health, Shanghai, China.
Microbiome Therapy Center, South China Hospital, Health Science Center, Shenzhen University, Shenzhen, China.
ORCID: 0000-0002-5989-5377

Daniel N Frank (DN)

Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO, USA.
ORCID: 0000-0001-6669-228X

Ellen Li (E)

Department of Medicine, Division of Gastroenterology and Hepatology, Stony Brook University, Stony Brook, NY, USA.
ORCID: 0000-0002-1141-0406

Wenhao Zhou (W)

Shanghai Key Laboratory of Birth Defects, Division of Neonatology, Children's Hospital of Fudan University, National Center for Children's Health, Shanghai, China.
ORCID: 0000-0001-8956-7238

Vassilios Fanos (V)

Neonatal Intensive Care Unit and Neonatal Pathology, Department of Surgical Sciences, School of Medicine, University of Cagliari, Cagliari, Italy.

Valery N Danilenko (VN)

Vavilov Institute of General Genetics Russian Academy of Sciences, Moscow, Russia.

Dennis P Wall (DP)

Pediatrics (Systems Medicine), Biomedical Data Science, and Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
ORCID: 0000-0002-7889-9146

Paúl Cárdenas (P)

Institute of Microbiology, COCIBA, Universidad San Francisco de Quito, Quito, Ecuador.
ORCID: 0000-0001-9626-4489

Manuel E Baldeón (ME)

Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del Ecuador, Quito, Ecuador.
ORCID: 0000-0002-1243-7467

Sébastien Jacquemont (S)

Sainte Justine Hospital Research Center, Montréal, QC, Canada.
Department of Pediatrics, Université de Montréal, Montréal, QC, Canada.
ORCID: 0000-0001-6838-8767

Omry Koren (O)

Azrieli Faculty of Medicine, Bar Ilan University, Safed, Israel.

Evan Elliott (E)

Azrieli Faculty of Medicine, Bar Ilan University, Safed, Israel.
The Leslie and Susan Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel.
ORCID: 0000-0002-1630-969X

Ramnik J Xavier (RJ)

Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA.
Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital, Boston, MA, USA.
ORCID: 0000-0002-5630-5167

Sarkis K Mazmanian (SK)

Division of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA, USA.
ORCID: 0000-0003-2713-1513

Rob Knight (R)

Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.
Department of Computer Science and Engineering, Jacobs School of Engineering, University of California, San Diego, La Jolla, CA, USA.
Department of Bioengineering, University of California, San Diego, La Jolla, California, USA.
Center for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA.
ORCID: 0000-0002-0975-9019

Jack A Gilbert (JA)

Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA.
Center for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA.
Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, USA.
ORCID: 0000-0001-7920-7001

Sharon M Donovan (SM)

Division of Nutritional Sciences, University of Illinois, Urbana, IL, USA.

Trevor D Lawley (TD)

Host-Microbiota Interactions Laboratory, Wellcome Sanger Institute, Hinxton, UK.
ORCID: 0000-0002-4805-621X

Bob Carpenter (B)

Center for Computational Biology, Flatiron Institute, Simons Foundation, New York, NY, USA.

Richard Bonneau (R)

Center for Computational Biology, Flatiron Institute, Simons Foundation, New York, NY, USA.
Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY, USA.
Prescient Design, a Genentech Accelerator, New York, NY, USA.

Gaspar Taroncher-Oldenburg (G)

Gaspar Taroncher Consulting, Philadelphia, PA, USA. gtaroncher@gmail.com.
Simons Foundation Autism Research Initiative, Simons Foundation, New York, NY, USA. gtaroncher@gmail.com.
ORCID: 0000-0003-2840-1415

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Classifications MeSH

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