Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation

Differences in the composition of the gut microbiota of infants associate with relative risk of atopy in childhood, and metabolites linked with these distinct microbial states alter T cell differentiation ex vivo . Gut microbiota bacterial depletions and altered metabolic activity at 3 months are im...

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Published in	Nature medicine Vol. 22; no. 10; pp. 1187 - 1191
Main Authors	Fujimura, Kei E, Sitarik, Alexandra R, Havstad, Suzanne, Lin, Din L, Levan, Sophia, Fadrosh, Douglas, Panzer, Ariane R, LaMere, Brandon, Rackaityte, Elze, Lukacs, Nicholas W, Wegienka, Ganesa, Boushey, Homer A, Ownby, Dennis R, Zoratti, Edward M, Levin, Albert M, Johnson, Christine C, Lynch, Susan V
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.10.2016 Nature Publishing Group
Subjects	101/58 13/106 13/31 38/23 38/77 692/698/2741/2135 692/699/249/2510/31 Abundance Age Asthma Asthma - epidemiology Asthma - immunology Atopy Bifidobacterium - genetics Biomedicine Cancer Research Candida - genetics CD25 antigen CD4 antigen CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism Cell culture Cell differentiation Cell Differentiation - immunology Child, Preschool Childhood Childhood asthma Children Differentiation (biology) Dysbacteriosis Faecalibacterium - genetics Feces Feces - chemistry Female Forkhead Transcription Factors - metabolism Foxp3 protein Fungi Gastrointestinal Microbiome - genetics Gastrointestinal Microbiome - immunology Humans Hypersensitivity - epidemiology Hypersensitivity - immunology Infant Infant, Newborn Infectious Diseases Inflammation Interleukin-2 Receptor alpha Subunit - metabolism Interleukin-4 - immunology Interleukins Intestinal microflora letter Lymphocytes Lymphocytes T Male Metabolic Diseases Metabolites Microbiomes Microbiota Microbiota (Symbiotic organisms) Molecular Medicine Neonates Neurosciences Odds Ratio Relative abundance Rhodotorula - genetics Risk RNA, Ribosomal, 16S - genetics rRNA 16S Sequence Analysis, RNA T-Lymphocytes - immunology
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Abstract	Differences in the composition of the gut microbiota of infants associate with relative risk of atopy in childhood, and metabolites linked with these distinct microbial states alter T cell differentiation ex vivo . Gut microbiota bacterial depletions and altered metabolic activity at 3 months are implicated in childhood atopy and asthma 1 . We hypothesized that compositionally distinct human neonatal gut microbiota (NGM) exist, and are differentially related to relative risk (RR) of childhood atopy and asthma. Using stool samples ( n = 298; aged 1–11 months) from a US birth cohort and 16S rRNA sequencing, neonates (median age, 35 d) were divisible into three microbiota composition states (NGM1–3). Each incurred a substantially different RR for multisensitized atopy at age 2 years and doctor-diagnosed asthma at age 4 years. The highest risk group, labeled NGM3, showed lower relative abundance of certain bacteria (for example, Bifidobacterium, Akkermansia and Faecalibacterium) , higher relative abundance of particular fungi ( Candida and Rhodotorula ) and a distinct fecal metabolome enriched for pro-inflammatory metabolites. Ex vivo culture of human adult peripheral T cells with sterile fecal water from NGM3 subjects increased the proportion of CD4 + cells producing interleukin (IL)-4 and reduced the relative abundance of CD4 + CD25 + FOXP3 + cells. 12,13-DiHOME, enriched in NGM3 versus lower-risk NGM states, recapitulated the effect of NGM3 fecal water on relative CD4 + CD25 + FOXP3 + cell abundance. These findings suggest that neonatal gut microbiome dysbiosis might promote CD4 + T cell dysfunction associated with childhood atopy.
AbstractList	Gut microbiota bacterial depletions and altered metabolic activity at 3 months are implicated in childhood atopy and asthma. We hypothesized that compositionally distinct human neonatal gut microbiota (NGM) exist, and are differentially related to relative risk (RR) of childhood atopy and asthma. Using stool samples (n = 298; aged 1-11 months) from a US birth cohort and 16S rRNA sequencing, neonates (median age, 35 d) were divisible into three microbiota composition states (NGM1-3). Each incurred a substantially different RR for multisensitized atopy at age 2 years and doctor-diagnosed asthma at age 4 years. The highest risk group, labeled NGM3, showed lower relative abundance of certain bacteria (for example, Bifidobacterium, Akkermansia and Faecalibacterium), higher relative abundance of particular fungi (Candida and Rhodotorula) and a distinct fecal metabolome enriched for pro-inflammatory metabolites. Ex vivo culture of human adult peripheral T cells with sterile fecal water from NGM3 subjects increased the proportion of CD4+ cells producing interleukin (IL)-4 and reduced the relative abundance of CD4+ CD25+ FOXP3+ cells. 12,13-DiHOME, enriched in NGM3 versus lower-risk NGM states, recapitulated the effect of NGM3 fecal water on relative CD4+ CD25+ FOXP3+ cell abundance. These findings suggest that neonatal gut microbiome dysbiosis might promote CD4+ T cell dysfunction associated with childhood atopy. Differences in the composition of the gut microbiota of infants associate with relative risk of atopy in childhood, and metabolites linked with these distinct microbial states alter T cell differentiation ex vivo . Gut microbiota bacterial depletions and altered metabolic activity at 3 months are implicated in childhood atopy and asthma 1 . We hypothesized that compositionally distinct human neonatal gut microbiota (NGM) exist, and are differentially related to relative risk (RR) of childhood atopy and asthma. Using stool samples ( n = 298; aged 1–11 months) from a US birth cohort and 16S rRNA sequencing, neonates (median age, 35 d) were divisible into three microbiota composition states (NGM1–3). Each incurred a substantially different RR for multisensitized atopy at age 2 years and doctor-diagnosed asthma at age 4 years. The highest risk group, labeled NGM3, showed lower relative abundance of certain bacteria (for example, Bifidobacterium, Akkermansia and Faecalibacterium) , higher relative abundance of particular fungi ( Candida and Rhodotorula ) and a distinct fecal metabolome enriched for pro-inflammatory metabolites. Ex vivo culture of human adult peripheral T cells with sterile fecal water from NGM3 subjects increased the proportion of CD4 + cells producing interleukin (IL)-4 and reduced the relative abundance of CD4 + CD25 + FOXP3 + cells. 12,13-DiHOME, enriched in NGM3 versus lower-risk NGM states, recapitulated the effect of NGM3 fecal water on relative CD4 + CD25 + FOXP3 + cell abundance. These findings suggest that neonatal gut microbiome dysbiosis might promote CD4 + T cell dysfunction associated with childhood atopy. Gut microbiota bacterial depletions and altered metabolic activity at 3 months are implicated in childhood atopy and asthma. We hypothesized that compositionally distinct human neonatal gut microbiota (NGM) exist, and are differentially related to relative risk (RR) of childhood atopy and asthma. Using stool samples (n = 298; aged 1-11 months) from a US birth cohort and 16S rRNA sequencing, neonates (median age, 35 d) were divisible into three microbiota composition states (NGM1-3). Each incurred a substantially different RR for multisensitized atopy at age 2 years and doctor-diagnosed asthma at age 4 years. The highest risk group, labeled NGM3, showed lower relative abundance of certain bacteria (for example, Bifidobacterium, Akkermansia and Faecalibacterium), higher relative abundance of particular fungi (Candida and Rhodotorula) and a distinct fecal metabolome enriched for pro-inflammatory metabolites. Ex vivo culture of human adult peripheral T cells with sterile fecal water from NGM3 subjects increased the proportion of CD4 cells producing interleukin (IL)-4 and reduced the relative abundance of CD4 CD25 FOXP3 cells. 12,13-DiHOME, enriched in NGM3 versus lower-risk NGM states, recapitulated the effect of NGM3 fecal water on relative CD4 CD25 FOXP3 cell abundance. These findings suggest that neonatal gut microbiome dysbiosis might promote CD4 T cell dysfunction associated with childhood atopy.
Audience	Academic
Author	Sitarik, Alexandra R Rackaityte, Elze Lynch, Susan V Fadrosh, Douglas Wegienka, Ganesa LaMere, Brandon Fujimura, Kei E Zoratti, Edward M Panzer, Ariane R Lin, Din L Lukacs, Nicholas W Ownby, Dennis R Johnson, Christine C Havstad, Suzanne Levin, Albert M Boushey, Homer A Levan, Sophia
Author_xml	– sequence: 1 givenname: Kei E surname: Fujimura fullname: Fujimura, Kei E organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 2 givenname: Alexandra R surname: Sitarik fullname: Sitarik, Alexandra R organization: Department of Public Health Sciences, Henry Ford Health System – sequence: 3 givenname: Suzanne surname: Havstad fullname: Havstad, Suzanne organization: Department of Public Health Sciences, Henry Ford Health System – sequence: 4 givenname: Din L surname: Lin fullname: Lin, Din L organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 5 givenname: Sophia surname: Levan fullname: Levan, Sophia organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 6 givenname: Douglas surname: Fadrosh fullname: Fadrosh, Douglas organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 7 givenname: Ariane R surname: Panzer fullname: Panzer, Ariane R organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 8 givenname: Brandon surname: LaMere fullname: LaMere, Brandon organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 9 givenname: Elze surname: Rackaityte fullname: Rackaityte, Elze organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 10 givenname: Nicholas W surname: Lukacs fullname: Lukacs, Nicholas W organization: Department of Pathology, University of Michigan Medical School – sequence: 11 givenname: Ganesa surname: Wegienka fullname: Wegienka, Ganesa organization: Department of Public Health Sciences, Henry Ford Health System – sequence: 12 givenname: Homer A surname: Boushey fullname: Boushey, Homer A organization: Department of Medicine, Pulmonary, Critical Care, Allergy and Sleep Medicine, University of California, San Francisco, San Francisco, California, USA – sequence: 13 givenname: Dennis R orcidid: 0000-0003-0944-6466 surname: Ownby fullname: Ownby, Dennis R organization: Section of Allergy–Immunology, Augusta University – sequence: 14 givenname: Edward M surname: Zoratti fullname: Zoratti, Edward M organization: Department of Internal Medicine, Division of Allergy and Immunology, Henry Ford Health System – sequence: 15 givenname: Albert M surname: Levin fullname: Levin, Albert M organization: Department of Public Health Sciences, Henry Ford Health System – sequence: 16 givenname: Christine C surname: Johnson fullname: Johnson, Christine C email: cjohnso1@hfhs.org organization: Department of Public Health Sciences, Henry Ford Health System – sequence: 17 givenname: Susan V surname: Lynch fullname: Lynch, Susan V email: susan.lynch@ucsf.edu organization: Division of Gastroenterology, Department of Medicine, University of California, San Francisco, San Francisco, California, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/27618652$$D View this record in MEDLINE/PubMed
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Snippet	Differences in the composition of the gut microbiota of infants associate with relative risk of atopy in childhood, and metabolites linked with these distinct... Gut microbiota bacterial depletions and altered metabolic activity at 3 months are implicated in childhood atopy and asthma. We hypothesized that...
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SubjectTerms	101/58 13/106 13/31 38/23 38/77 692/698/2741/2135 692/699/249/2510/31 Abundance Age Asthma Asthma - epidemiology Asthma - immunology Atopy Bifidobacterium - genetics Biomedicine Cancer Research Candida - genetics CD25 antigen CD4 antigen CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism Cell culture Cell differentiation Cell Differentiation - immunology Child, Preschool Childhood Childhood asthma Children Differentiation (biology) Dysbacteriosis Faecalibacterium - genetics Feces Feces - chemistry Female Forkhead Transcription Factors - metabolism Foxp3 protein Fungi Gastrointestinal Microbiome - genetics Gastrointestinal Microbiome - immunology Humans Hypersensitivity - epidemiology Hypersensitivity - immunology Infant Infant, Newborn Infectious Diseases Inflammation Interleukin-2 Receptor alpha Subunit - metabolism Interleukin-4 - immunology Interleukins Intestinal microflora letter Lymphocytes Lymphocytes T Male Metabolic Diseases Metabolites Microbiomes Microbiota Microbiota (Symbiotic organisms) Molecular Medicine Neonates Neurosciences Odds Ratio Relative abundance Rhodotorula - genetics Risk RNA, Ribosomal, 16S - genetics rRNA 16S Sequence Analysis, RNA T-Lymphocytes - immunology
Title	Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation
URI	https://link.springer.com/article/10.1038/nm.4176 https://www.ncbi.nlm.nih.gov/pubmed/27618652 https://www.proquest.com/docview/2099882360 https://www.proquest.com/docview/1835382380
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