Cited by 546Bacteriophages and microbial interactionsGut microbiota and healthInflammatory Bowel Disease

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Targeted suppression of human IBD-associated gut microbiota commensals by phage consortia for treatment of intestinal inflammation

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Federici, Sara, Kredo-Russo, Sharon, Valdés-Mas, Rafael, Kviatcovsky, Denise, Weinstock, Eyal, Matiuhin, Yulia, Silberberg, Yael, Atarashi, Koji, Furuichi, Munehiro, Oka, Akihiko, Liu, Bo, Fibelman, Morine, Weiner, Iddo Nadav, Khabra, Efrat, Cullin, Nyssa, Ben-Yishai, Noa, Inbar, Dana, Ben-David, Hava, Nicenboim, Julian, Kowalsman, Noga, Lieb, Wolfgang, Kario, Edith, Cohen, Tal, Geffen, Yael Friedman, Zelcbuch, Lior, Cohen, Ariel, Rappo, Urania, Gahali-Sass, Inbar, Golembo, Myriam, Lev, Vered, Dori-Bachash, Mally, Shapiro, Hagit, Moresi, Claudia, Cuevas-Sierra, Amanda, Mohapatra, Gayatree, Kern, Lara, Zheng, Danping, Nobs, Samuel Philip, Suez, Jotham, Stettner, Noa, Harmelin, Alon, Zak, Naomi, Puttagunta, Sailaja, Bassan, Merav, Honda, Kenya, Sokol, Harry, Bang, Corinna, Franke, Andre, Schramm, Christoph, Maharshak, Nitsan, Sartor, Ryan Balfour, Sorek, Rotem, Elinav, Eran·2022·Cell

DOI 10.1016/j.cell.2022.07.003

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Abstract

Human gut commensals are increasingly suggested to impact non-communicable diseases, such as inflammatory bowel diseases (IBD), yet their targeted suppression remains a daunting unmet challenge. In four geographically distinct IBD cohorts (n = 537), we identify a clade of Klebsiella pneumoniae (Kp) strains, featuring a unique antibiotics resistance and mobilome signature, to be strongly associated with disease exacerbation and severity. Transfer of clinical IBD-associated Kp strains into colitis-prone, germ-free, and colonized mice enhances intestinal inflammation. Stepwise generation of a lytic five-phage combination, targeting sensitive and resistant IBD-associated Kp clade members through distinct mechanisms, enables effective Kp suppression in colitis-prone mice, driving an attenuated inflammation and disease severity. Proof-of-concept assessment of Kp-targeting phages in an artificial human gut and in healthy volunteers demonstrates gastric acid-dependent phage resilience, safety, and viability in the lower gut. Collectively, we demonstrate the feasibility of orally administered combination phage therapy in avoiding resistance, while effectively inhibiting non-communicable disease-contributing pathobionts.

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Authors: Federici, S., Kredo-Russo, S., Valdés-Mas, R., Kviatcovsky, D., Weinstock, E., Matiuhin, Y., Silberberg, Y., Atarashi, K., Furuichi, M., Oka, A., Liu, B., Fibelman, M., Weiner, I. N., Khabra, E., Cullin, N., Ben-Yishai, N., Inbar, D., Ben-David, H., Nicenboim, J., Kowalsman, N., Lieb, W., Kario, E., Cohen, T., Geffen, Y. F., Zelcbuch, L., Cohen, A., Rappo, U., Gahali-Sass, I., Golembo, M., Lev, V., Dori-Bachash, M., Shapiro, H., Moresi, C., Cuevas-Sierra, A., Mohapatra, G., Kern, L., Zheng, D., Nobs, S. P., Suez, J., Stettner, N., Harmelin, A., Zak, N., Puttagunta, S., Bassan, M., Honda, K., Sokol, H., Bang, C., Franke, A., Schramm, C., Maharshak, N., Sartor, R. B., Sorek, R., & Elinav, E.
Affiliations: Weizmann Institute of Science (IL)
Keio University (JP)
University of North Carolina at Chapel Hill (US)
Tel Aviv University (IL)
German Cancer Research Center (DE)
Christian-Albrechts-Universität zu Kiel (DE)
Inserm (FR)
University Medical Center Hamburg-Eppendorf (DE)
Corresponding author: Elinav, Eran
ORCID: Federici, Sara
Kviatcovsky, Denise
Matiuhin, Yulia
Atarashi, Koji
Furuichi, Munehiro
Oka, Akihiko
Liu, Bo
Weiner, Iddo Nadav
Cullin, Nyssa
Lieb, Wolfgang
Cohen, Tal
Rappo, Urania
Shapiro, Hagit
Moresi, Claudia
Kern, Lara
Zheng, Danping
Nobs, Samuel Philip
Suez, Jotham
Stettner, Noa
Harmelin, Alon
Honda, Kenya
Sokol, Harry
Bang, Corinna
Schramm, Christoph
Maharshak, Nitsan
Sartor, Ryan Balfour
Sorek, Rotem
Elinav, Eran
Venue: Cell
Publisher: Elsevier BV
Published: 2022-08
Volume: 185
Issue: 16
Pages: 2879-2898.e24
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2022.07.003
OpenAlex: W4289780574
Cited by: 542
References: 121
Citations by year: 2026: 124 · 2025: 152 · 2024: 130 · 2023: 108 · 2022: 27
FWCI: 56.34
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 368 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (publishedVersion, other-oa)
HAL (submittedVersion)
Funders: Japan Society for the Promotion of Science (20H05627)
Topics: Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Keywords: inflammatory bowel disease, Klebsiella pneumoniae, phage therapy, bacteriophages, gut commensals, intestinal inflammation, antibiotic resistance, mobilome, colitis, germ-free mice, gastric acid, pathobionts, disease severity
MeSH terms: Gastrointestinal Microbiome, Animals, Bacteriophages, Colitis, Humans, Inflammation, Klebsiella pneumoniae, Inflammatory Bowel Diseases, Mice

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Targeted suppression of human IBD-associated gut microbiota commensals by phage consortia for treatment of intestinal inflammation

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