Individuals at risk for rheumatoid arthritis harbor differential intestinal bacteriophage communities with distinct metabolic potential

Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP) antibodies. RA is linked to the intestinal microbiota, yet the association of microbes with CCP serology and their contribution to RA is unclear. We...

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Published inCell host & microbe Vol. 29; no. 5; pp. 726 - 739.e5
Main Authors Mangalea, Mihnea R., Paez-Espino, David, Kieft, Kristopher, Chatterjee, Anushila, Chriswell, Meagan E., Seifert, Jennifer A., Feser, Marie L., Demoruelle, M. Kristen, Sakatos, Alexandra, Anantharaman, Karthik, Deane, Kevin D., Kuhn, Kristine A., Holers, V. Michael, Duerkop, Breck A.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 12.05.2021
Subjects
Adult
Aged
Anti-Citrullinated Protein Antibodies - blood
Arthritis, Rheumatoid - blood
Arthritis, Rheumatoid - metabolism
Arthritis, Rheumatoid - virology
autoimmune disease
bacteriophages
Bacteriophages - classification
Bacteriophages - genetics
Bacteriophages - isolation & purification
Female
Humans
Intestines - virology
Male
microbiome
Microbiota
Middle Aged
phage-host interaction
phage-host metabolism
Phylogeny
rheumatoid arthritis
Risk Factors
phage-host interaction
rheumatoid arthritis
autoimmune disease
microbiome
phage-host metabolism
bacteriophages
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Abstract Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP) antibodies. RA is linked to the intestinal microbiota, yet the association of microbes with CCP serology and their contribution to RA is unclear. We describe intestinal phage communities of individuals at risk for developing RA, with or without anti-CCP antibodies, whose first-degree relatives have been diagnosed with RA. We show that at-risk individuals harbor intestinal phage compositions that diverge based on CCP serology, are dominated by Streptococcaceae, Bacteroidaceae, and Lachnospiraceae phages, and may originate from disparate ecosystems. These phages encode unique repertoires of auxiliary metabolic genes, which associate with anti-CCP status, suggesting that these phages directly influence the metabolic and immunomodulatory capability of the microbiota. This work sets the stage for the use of phages as preclinical biomarkers and provides insight into a possible microbial-based causation of RA disease development. [Display omitted] •Unique intestinal phage compositions correlate to at-risk RA anti-CCP serology•Lachnospiraceae phage-host interactions dominate in CCP+ individuals at risk for RA•Phages from CCP+ individuals may originate from disparate ecological niches•Phage AMGs contribute to cohort-associated differences Mangalea et al. characterize intestinal bacteriophage communities from humans at risk of developing rheumatoid arthritis. Bacteriophage profiles diverge based on anti-cyclic citrullinated protein autoantibody status compared to healthy controls. Bacteriophage profiling could complement existing diagnostics as a microbial biomarker for preclinical rheumatoid arthritis.
AbstractList Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP) antibodies. RA is linked to the intestinal microbiota, yet the association of microbes with CCP serology and their contribution to RA is unclear. We describe intestinal phage communities of individuals at risk for developing RA, with or without anti-CCP antibodies, whose first-degree relatives have been diagnosed with RA. We show that at-risk individuals harbor intestinal phage compositions that diverge based on CCP serology, are dominated by Streptococcaceae, Bacteroidaceae, and Lachnospiraceae phages, and may originate from disparate ecosystems. These phages encode unique repertoires of auxiliary metabolic genes which associate with anti-CCP status, suggesting that these phages directly influence the metabolic and immunomodulatory capability of the microbiota. This work sets the stage for the use of phages as preclinical biomarkers and provides insight into a possible microbial-based causation of RA disease development. Mangalea et al. characterize intestinal bacteriophage communities from humans at-risk of developing rheumatoid arthritis. Bacteriophage profiles diverge based on anti-cyclic citrullinated protein autoantibody status compared to healthy controls. Bacteriophage profiling could complement existing diagnostics as a microbial biomarker for preclinical rheumatoid arthritis.
Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP) antibodies. RA is linked to the intestinal microbiota, yet the association of microbes with CCP serology and their contribution to RA is unclear. We describe intestinal phage communities of individuals at risk for developing RA, with or without anti-CCP antibodies, whose first-degree relatives have been diagnosed with RA. We show that at-risk individuals harbor intestinal phage compositions that diverge based on CCP serology, are dominated by Streptococcaceae, Bacteroidaceae, and Lachnospiraceae phages, and may originate from disparate ecosystems. These phages encode unique repertoires of auxiliary metabolic genes, which associate with anti-CCP status, suggesting that these phages directly influence the metabolic and immunomodulatory capability of the microbiota. This work sets the stage for the use of phages as preclinical biomarkers and provides insight into a possible microbial-based causation of RA disease development. [Display omitted] •Unique intestinal phage compositions correlate to at-risk RA anti-CCP serology•Lachnospiraceae phage-host interactions dominate in CCP+ individuals at risk for RA•Phages from CCP+ individuals may originate from disparate ecological niches•Phage AMGs contribute to cohort-associated differences Mangalea et al. characterize intestinal bacteriophage communities from humans at risk of developing rheumatoid arthritis. Bacteriophage profiles diverge based on anti-cyclic citrullinated protein autoantibody status compared to healthy controls. Bacteriophage profiling could complement existing diagnostics as a microbial biomarker for preclinical rheumatoid arthritis.
Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP) antibodies. RA is linked to the intestinal microbiota, yet the association of microbes with CCP serology and their contribution to RA is unclear. We describe intestinal phage communities of individuals at risk for developing RA, with or without anti-CCP antibodies, whose first-degree relatives have been diagnosed with RA. We show that at-risk individuals harbor intestinal phage compositions that diverge based on CCP serology, are dominated by Streptococcaceae, Bacteroidaceae, and Lachnospiraceae phages, and may originate from disparate ecosystems. These phages encode unique repertoires of auxiliary metabolic genes, which associate with anti-CCP status, suggesting that these phages directly influence the metabolic and immunomodulatory capability of the microbiota. This work sets the stage for the use of phages as preclinical biomarkers and provides insight into a possible microbial-based causation of RA disease development.
Author Chriswell, Meagan E.
Holers, V. Michael
Sakatos, Alexandra
Demoruelle, M. Kristen
Duerkop, Breck A.
Paez-Espino, David
Kuhn, Kristine A.
Feser, Marie L.
Chatterjee, Anushila
Seifert, Jennifer A.
Kieft, Kristopher
Anantharaman, Karthik
Mangalea, Mihnea R.
Deane, Kevin D.
AuthorAffiliation 5 Lead Contact
1 Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, CO 80045, USA
2 Ancilia Biosciences, New York, NY 19808, USA
4 Division of Rheumatology, University of Colorado School of Medicine, Aurora, CO 80045, USA
3 Department of Bacteriology, University of Wisconsin-Madison, Madison, WI 53715, USA
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– name: 4 Division of Rheumatology, University of Colorado School of Medicine, Aurora, CO 80045, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33957082$$D View this record in MEDLINE/PubMed
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Keywords phage-host interaction
rheumatoid arthritis
autoimmune disease
microbiome
phage-host metabolism
bacteriophages
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Conceptualization, M.R.M, D.P., A.C., K.A.K., and B.A.D.; Methodology, M.R.M., D.P., K.K., A.C., J.A.S., M.L.F., K.A., M.K.D., and B.A.D.; Investigation, M.R.M, D.P., K.K., A.C., M.E.C.; Sample Procurement, M.E.C., J.A.S., M.L.F., and M.K.D.; Visualization, M.R.M, D.P. and K.K.; Writing – Original Draft, M.R.M and B.A.D.; Writing – Review & Editing, M.R.M, D.P., K.K., A.C., M.E.C, A.S., K.D.D., V.M.H., K.A.K. and B.A.D.; Funding Acquisition, V.M.H., K.A.K. and B.A.D.; Resources, B.A.D.; Supervision, B.A.D., V.M.H., K.D.D., K.A., A.S. and K.A.K.
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Snippet Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP)...
Rheumatoid arthritis (RA) is an autoimmune disease characterized in seropositive individuals by the presence of anti-cyclic citrullinated protein (CCP)...
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SubjectTerms Adult
Aged
Anti-Citrullinated Protein Antibodies - blood
Arthritis, Rheumatoid - blood
Arthritis, Rheumatoid - metabolism
Arthritis, Rheumatoid - virology
autoimmune disease
bacteriophages
Bacteriophages - classification
Bacteriophages - genetics
Bacteriophages - isolation & purification
Female
Humans
Intestines - virology
Male
microbiome
Microbiota
Middle Aged
phage-host interaction
phage-host metabolism
Phylogeny
rheumatoid arthritis
Risk Factors
Title Individuals at risk for rheumatoid arthritis harbor differential intestinal bacteriophage communities with distinct metabolic potential
URI https://dx.doi.org/10.1016/j.chom.2021.03.020
https://www.ncbi.nlm.nih.gov/pubmed/33957082
https://search.proquest.com/docview/2524357194
https://pubmed.ncbi.nlm.nih.gov/PMC8186507
Volume 29
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