Role of Serum Amyloid A, Granulocyte-Macrophage Colony-Stimulating Factor, and Bone Marrow Granulocyte-Monocyte Precursor Expansion in Segmented Filamentous Bacterium-Mediated Protection from Entamoeba histolytica
Intestinal segmented filamentous bacteria (SFB) protect from ameba infection, and protection is transferable with bone marrow dendritic cells (BMDCs). SFB cause an increase in serum amyloid A (SAA), suggesting that SAA might mediate SFB's effects on BMDCs. Here we further explored the role of b...
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| Veröffentlicht in: | Infection and immunity 2016-10, Vol.84 (10), p.2824-2832 |
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| creator | Burgess, Stacey L Saleh, Mahmoud Cowardin, Carrie A Buonomo, Erica Noor, Zannatun Watanabe, Koji Abhyankar, Mayuresh Lajoie, Stephane Wills-Karp, Marsha Petri, Jr, William A |
| description | Intestinal segmented filamentous bacteria (SFB) protect from ameba infection, and protection is transferable with bone marrow dendritic cells (BMDCs). SFB cause an increase in serum amyloid A (SAA), suggesting that SAA might mediate SFB's effects on BMDCs. Here we further explored the role of bone marrow in SFB-mediated protection. Transient gut colonization with SFB or SAA administration alone transiently increased the H3K27 histone demethylase Jmjd3, persistently increased bone marrow Csf2ra expression and granulocyte monocyte precursors (GMPs), and protected from ameba infection. Pharmacologic inhibition of Jmjd3 H3K27 demethylase activity during SAA treatment or blockade of granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling in SFB-colonized mice prevented GMP expansion, decreased gut neutrophils, and blocked protection from ameba infection. These results indicate that alteration of the microbiota and systemic exposure to SAA can influence myelopoiesis and susceptibility to amebiasis via epigenetic mechanisms. Gut microbiota-marrow communication is a previously unrecognized mechanism of innate protection from infection. |
| doi_str_mv | 10.1128/IAI.00316-16 |
| format | Article |
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B.</contributor><creatorcontrib>Burgess, Stacey L ; Saleh, Mahmoud ; Cowardin, Carrie A ; Buonomo, Erica ; Noor, Zannatun ; Watanabe, Koji ; Abhyankar, Mayuresh ; Lajoie, Stephane ; Wills-Karp, Marsha ; Petri, Jr, William A ; Young, V. B.</creatorcontrib><description>Intestinal segmented filamentous bacteria (SFB) protect from ameba infection, and protection is transferable with bone marrow dendritic cells (BMDCs). SFB cause an increase in serum amyloid A (SAA), suggesting that SAA might mediate SFB's effects on BMDCs. Here we further explored the role of bone marrow in SFB-mediated protection. Transient gut colonization with SFB or SAA administration alone transiently increased the H3K27 histone demethylase Jmjd3, persistently increased bone marrow Csf2ra expression and granulocyte monocyte precursors (GMPs), and protected from ameba infection. Pharmacologic inhibition of Jmjd3 H3K27 demethylase activity during SAA treatment or blockade of granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling in SFB-colonized mice prevented GMP expansion, decreased gut neutrophils, and blocked protection from ameba infection. These results indicate that alteration of the microbiota and systemic exposure to SAA can influence myelopoiesis and susceptibility to amebiasis via epigenetic mechanisms. Gut microbiota-marrow communication is a previously unrecognized mechanism of innate protection from infection.</description><identifier>ISSN: 0019-9567</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/IAI.00316-16</identifier><identifier>PMID: 27456830</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Animals ; Bacteria ; Bone Marrow - metabolism ; Bone Marrow Cells - cytology ; Bone Marrow Cells - physiology ; Dendritic Cells - metabolism ; Disease Models, Animal ; Entamoeba histolytica - physiology ; Entamoebiasis - physiopathology ; Fungal and Parasitic Infections ; Gastrointestinal Tract - microbiology ; Granulocyte-Macrophage Colony-Stimulating Factor - physiology ; Granulocyte-Macrophage Progenitor Cells ; Jumonji Domain-Containing Histone Demethylases - metabolism ; Male ; Mice ; Mice, Inbred C57BL ; Receptors, Granulocyte-Macrophage Colony-Stimulating Factor - metabolism ; Serum Amyloid A Protein - physiology</subject><ispartof>Infection and immunity, 2016-10, Vol.84 (10), p.2824-2832</ispartof><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved.</rights><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved. 2016 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c384t-368de030f711b2c252efc03f9d54b5a415a339e8ba2339a346f95f3be374a3bd3</citedby><cites>FETCH-LOGICAL-c384t-368de030f711b2c252efc03f9d54b5a415a339e8ba2339a346f95f3be374a3bd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5038085/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5038085/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27456830$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Young, V. B.</contributor><creatorcontrib>Burgess, Stacey L</creatorcontrib><creatorcontrib>Saleh, Mahmoud</creatorcontrib><creatorcontrib>Cowardin, Carrie A</creatorcontrib><creatorcontrib>Buonomo, Erica</creatorcontrib><creatorcontrib>Noor, Zannatun</creatorcontrib><creatorcontrib>Watanabe, Koji</creatorcontrib><creatorcontrib>Abhyankar, Mayuresh</creatorcontrib><creatorcontrib>Lajoie, Stephane</creatorcontrib><creatorcontrib>Wills-Karp, Marsha</creatorcontrib><creatorcontrib>Petri, Jr, William A</creatorcontrib><title>Role of Serum Amyloid A, Granulocyte-Macrophage Colony-Stimulating Factor, and Bone Marrow Granulocyte-Monocyte Precursor Expansion in Segmented Filamentous Bacterium-Mediated Protection from Entamoeba histolytica</title><title>Infection and immunity</title><addtitle>Infect Immun</addtitle><description>Intestinal segmented filamentous bacteria (SFB) protect from ameba infection, and protection is transferable with bone marrow dendritic cells (BMDCs). SFB cause an increase in serum amyloid A (SAA), suggesting that SAA might mediate SFB's effects on BMDCs. Here we further explored the role of bone marrow in SFB-mediated protection. Transient gut colonization with SFB or SAA administration alone transiently increased the H3K27 histone demethylase Jmjd3, persistently increased bone marrow Csf2ra expression and granulocyte monocyte precursors (GMPs), and protected from ameba infection. Pharmacologic inhibition of Jmjd3 H3K27 demethylase activity during SAA treatment or blockade of granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling in SFB-colonized mice prevented GMP expansion, decreased gut neutrophils, and blocked protection from ameba infection. These results indicate that alteration of the microbiota and systemic exposure to SAA can influence myelopoiesis and susceptibility to amebiasis via epigenetic mechanisms. Gut microbiota-marrow communication is a previously unrecognized mechanism of innate protection from infection.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Bone Marrow - metabolism</subject><subject>Bone Marrow Cells - cytology</subject><subject>Bone Marrow Cells - physiology</subject><subject>Dendritic Cells - metabolism</subject><subject>Disease Models, Animal</subject><subject>Entamoeba histolytica - physiology</subject><subject>Entamoebiasis - physiopathology</subject><subject>Fungal and Parasitic Infections</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Granulocyte-Macrophage Colony-Stimulating Factor - physiology</subject><subject>Granulocyte-Macrophage Progenitor Cells</subject><subject>Jumonji Domain-Containing Histone Demethylases - metabolism</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Receptors, Granulocyte-Macrophage Colony-Stimulating Factor - metabolism</subject><subject>Serum Amyloid A Protein - physiology</subject><issn>0019-9567</issn><issn>1098-5522</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkcFu2zAMhoVhw5p2u-086AHiTrIsx74MSIOkDdBgxbqdDVqmEw2yGMhyNz_o3mdOuxXriSRIfj_Bn7EPUlxKmRaftsvtpRBK5onMX7GZFGWRaJ2mr9lMCFkmpc4XZ-y8739MZZZlxVt2li4ynRdKzNjvr-SQU8vvMQwdX3ajI9vw5ZxfB_CDIzNGTHZgAh0PsEe-Ikd-TO6j7QYH0fo934CJFOYcfMOvyCPfQQj08yWB_GPC7wKaIfQU-PrXEXxvyXPrJ_l9hz5iwzfWwSmloedXExmDHbpkh42FU_suUEQTT2ttoI6vfYSOsAZ-sH0kN0Zr4B1704Lr8f3feMG-b9bfVjfJ7Zfr7Wp5mxhVZDFRedGgUKJdSFmnJtUptkaotmx0VmvIpAalSixqSKcIKsvbUreqRrXIQNWNumCfn7jHoe6wMdPZAVx1DLaDMFYEtnrZ8fZQ7emh0kIVotATYP4EmP7b9wHb510pqpO91WRv9WhvJfNp_OP_es_D__xUfwDmJKds</recordid><startdate>20161001</startdate><enddate>20161001</enddate><creator>Burgess, Stacey L</creator><creator>Saleh, Mahmoud</creator><creator>Cowardin, Carrie A</creator><creator>Buonomo, Erica</creator><creator>Noor, Zannatun</creator><creator>Watanabe, Koji</creator><creator>Abhyankar, Mayuresh</creator><creator>Lajoie, Stephane</creator><creator>Wills-Karp, Marsha</creator><creator>Petri, Jr, William A</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope></search><sort><creationdate>20161001</creationdate><title>Role of Serum Amyloid A, Granulocyte-Macrophage Colony-Stimulating Factor, and Bone Marrow Granulocyte-Monocyte Precursor Expansion in Segmented Filamentous Bacterium-Mediated Protection from Entamoeba histolytica</title><author>Burgess, Stacey L ; Saleh, Mahmoud ; Cowardin, Carrie A ; Buonomo, Erica ; Noor, Zannatun ; Watanabe, Koji ; Abhyankar, Mayuresh ; Lajoie, Stephane ; Wills-Karp, Marsha ; Petri, Jr, William A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c384t-368de030f711b2c252efc03f9d54b5a415a339e8ba2339a346f95f3be374a3bd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Bone Marrow - metabolism</topic><topic>Bone Marrow Cells - cytology</topic><topic>Bone Marrow Cells - physiology</topic><topic>Dendritic Cells - metabolism</topic><topic>Disease Models, Animal</topic><topic>Entamoeba histolytica - physiology</topic><topic>Entamoebiasis - physiopathology</topic><topic>Fungal and Parasitic Infections</topic><topic>Gastrointestinal Tract - microbiology</topic><topic>Granulocyte-Macrophage Colony-Stimulating Factor - physiology</topic><topic>Granulocyte-Macrophage Progenitor Cells</topic><topic>Jumonji Domain-Containing Histone Demethylases - metabolism</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Receptors, Granulocyte-Macrophage Colony-Stimulating Factor - metabolism</topic><topic>Serum Amyloid A Protein - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Burgess, Stacey L</creatorcontrib><creatorcontrib>Saleh, Mahmoud</creatorcontrib><creatorcontrib>Cowardin, Carrie A</creatorcontrib><creatorcontrib>Buonomo, Erica</creatorcontrib><creatorcontrib>Noor, Zannatun</creatorcontrib><creatorcontrib>Watanabe, Koji</creatorcontrib><creatorcontrib>Abhyankar, Mayuresh</creatorcontrib><creatorcontrib>Lajoie, Stephane</creatorcontrib><creatorcontrib>Wills-Karp, Marsha</creatorcontrib><creatorcontrib>Petri, Jr, William A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Infection and immunity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Burgess, Stacey L</au><au>Saleh, Mahmoud</au><au>Cowardin, Carrie A</au><au>Buonomo, Erica</au><au>Noor, Zannatun</au><au>Watanabe, Koji</au><au>Abhyankar, Mayuresh</au><au>Lajoie, Stephane</au><au>Wills-Karp, Marsha</au><au>Petri, Jr, William A</au><au>Young, V. B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of Serum Amyloid A, Granulocyte-Macrophage Colony-Stimulating Factor, and Bone Marrow Granulocyte-Monocyte Precursor Expansion in Segmented Filamentous Bacterium-Mediated Protection from Entamoeba histolytica</atitle><jtitle>Infection and immunity</jtitle><addtitle>Infect Immun</addtitle><date>2016-10-01</date><risdate>2016</risdate><volume>84</volume><issue>10</issue><spage>2824</spage><epage>2832</epage><pages>2824-2832</pages><issn>0019-9567</issn><eissn>1098-5522</eissn><abstract>Intestinal segmented filamentous bacteria (SFB) protect from ameba infection, and protection is transferable with bone marrow dendritic cells (BMDCs). SFB cause an increase in serum amyloid A (SAA), suggesting that SAA might mediate SFB's effects on BMDCs. Here we further explored the role of bone marrow in SFB-mediated protection. Transient gut colonization with SFB or SAA administration alone transiently increased the H3K27 histone demethylase Jmjd3, persistently increased bone marrow Csf2ra expression and granulocyte monocyte precursors (GMPs), and protected from ameba infection. Pharmacologic inhibition of Jmjd3 H3K27 demethylase activity during SAA treatment or blockade of granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling in SFB-colonized mice prevented GMP expansion, decreased gut neutrophils, and blocked protection from ameba infection. These results indicate that alteration of the microbiota and systemic exposure to SAA can influence myelopoiesis and susceptibility to amebiasis via epigenetic mechanisms. Gut microbiota-marrow communication is a previously unrecognized mechanism of innate protection from infection.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>27456830</pmid><doi>10.1128/IAI.00316-16</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| source | American Society for Microbiology; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Animals Bacteria Bone Marrow - metabolism Bone Marrow Cells - cytology Bone Marrow Cells - physiology Dendritic Cells - metabolism Disease Models, Animal Entamoeba histolytica - physiology Entamoebiasis - physiopathology Fungal and Parasitic Infections Gastrointestinal Tract - microbiology Granulocyte-Macrophage Colony-Stimulating Factor - physiology Granulocyte-Macrophage Progenitor Cells Jumonji Domain-Containing Histone Demethylases - metabolism Male Mice Mice, Inbred C57BL Receptors, Granulocyte-Macrophage Colony-Stimulating Factor - metabolism Serum Amyloid A Protein - physiology |
| title | Role of Serum Amyloid A, Granulocyte-Macrophage Colony-Stimulating Factor, and Bone Marrow Granulocyte-Monocyte Precursor Expansion in Segmented Filamentous Bacterium-Mediated Protection from Entamoeba histolytica |
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