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Gut microbiome communication with bone marrow regulates susceptibility to amebiasis
Stacey L. Burgess, … , Rashidul Haque, William A. Petri Jr.
Stacey L. Burgess, … , Rashidul Haque, William A. Petri Jr.
Published May 5, 2020
Citation Information: J Clin Invest. 2020;130(8):4019-4024. https://doi.org/10.1172/JCI133605.
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Concise Communication Immunology Infectious disease Article has an altmetric score of 12

Gut microbiome communication with bone marrow regulates susceptibility to amebiasis

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Abstract

The microbiome provides resistance to infection. However, the underlying mechanisms are poorly understood. We demonstrate that colonization with the intestinal bacterium Clostridium scindens protects from Entamoeba histolytica colitis via innate immunity. Introduction of C. scindens into the gut microbiota epigenetically altered and expanded bone marrow granulocyte-monocyte progenitors (GMPs) and resulted in increased intestinal neutrophils with subsequent challenge with E. histolytica. Introduction of C. scindens alone was sufficient to expand GMPs in gnotobiotic mice. Adoptive transfer of bone marrow from C. scindens–colonized mice into naive mice protected against amebic colitis and increased intestinal neutrophils. Children without E. histolytica diarrhea also had a higher abundance of Lachnoclostridia. Lachnoclostridia C. scindens can metabolize the bile salt cholate, so we measured deoxycholate and discovered that it was increased in the sera of C. scindens–colonized specific pathogen–free and gnotobiotic mice, as well as in children protected from amebiasis. Administration of deoxycholate alone increased GMPs and provided protection from amebiasis. We elucidated a mechanism by which C. scindens and the microbially metabolized bile salt deoxycholic acid alter hematopoietic precursors and provide innate protection from later infection with E. histolytica.

Authors

Stacey L. Burgess, Jhansi L. Leslie, Jashim Uddin, David N. Oakland, Carol Gilchrist, G. Brett Moreau, Koji Watanabe, Mahmoud Saleh, Morgan Simpson, Brandon A. Thompson, David T. Auble, Stephen D. Turner, Natasa Giallourou, Jonathan Swann, Zhen Pu, Jennie Z. Ma, Rashidul Haque, William A. Petri Jr.

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Figure 1

Lachnoclostridium are associated with protection from Entamoeba histolytica in children, and introduction of Lachnoclostridium Clostridium scindens to the gut microbiota provides innate protection from Entamoeba histolytica in a murine model.

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Lachnoclostridium are associated with protection from Entamoeba histoly...
(A) Principal coordinates analysis (PCoA) of Bray-Curtis dissimilarities (β-diversity) of fecal microbiota from surveillance reference stool or E. histolytica–infected children was performed. The groups are significantly different by PERMANOVA: P < 0.05. (B) Relative abundance of the genus Lachnoclostridium from samples described in A. The groups are significantly different by Wilcoxon’s rank-sum test with continuity correction: P < 0.05; n = 20 children per condition. CBA/J mice (C–I) or C57BL/6 Rag1–/– mice (J and K) were colonized with bile acid 7α–dehydroxylating bacteria C. scindens (ATCC 35704) over 3 weeks before intracecal infection with E. histolytica. (C) Gut neutrophil infiltration was determined before amoeba infection via flow cytometry. (D and J) Percentage of mice infected with Entamoeba on day 6 following infection was determined via cecal culture in trophozoite culture media. (E–I and K) Gut immune cell infiltration was determined via flow cytometry. *P < 0.05 by Student’s t test (C, E–I, and K) or Mann-Whitney U test (D and J). Horizontal bars indicate the mean. n = 4–9 mice per group.

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ISSN: 0021-9738 (print), 1558-8238 (online)

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