Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine

Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of ne...

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Veröffentlicht in:Veterinary microbiology 2013-01, Vol.161 (3-4), p.315-324
Hauptverfasser: Erume, Joseph, Wijemanne, Prageeth, Berberov, Emil M., Kachman, Stephen D., Oestmann, Daniel J., Francis, David H., Moxley, Rodney A.
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container_end_page 324
container_issue 3-4
container_start_page 315
container_title Veterinary microbiology
container_volume 161
creator Erume, Joseph
Wijemanne, Prageeth
Berberov, Emil M.
Kachman, Stephen D.
Oestmann, Daniel J.
Francis, David H.
Moxley, Rodney A.
description Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6–8-week-old). Each pig was inoculated with six F4ac+E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb− (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT− STb− (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P
doi_str_mv 10.1016/j.vetmic.2012.07.048
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Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6–8-week-old). Each pig was inoculated with six F4ac+E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb− (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT− STb− (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P&lt;0.0001). Conversely, bacterial adherence scores based on immunohistochemistry and CFU/g of washed mucosa were both lowest in the strains that expressed STb and highest in those that did not. For the two experiments combined, the Pearson correlation coefficient (R) between fluid volume (ml/cm) and log CFU per gram was −0.57021 (P&lt;0.0001); R2=0.3521 (n=197). 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All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c419t-36b969599232a442d312367a76bbd7d23a44f36bb89c9383517f5d39624269513</citedby><cites>FETCH-LOGICAL-c419t-36b969599232a442d312367a76bbd7d23a44f36bb89c9383517f5d39624269513</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.vetmic.2012.07.048$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22901529$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Erume, Joseph</creatorcontrib><creatorcontrib>Wijemanne, Prageeth</creatorcontrib><creatorcontrib>Berberov, Emil M.</creatorcontrib><creatorcontrib>Kachman, Stephen D.</creatorcontrib><creatorcontrib>Oestmann, Daniel J.</creatorcontrib><creatorcontrib>Francis, David H.</creatorcontrib><creatorcontrib>Moxley, Rodney A.</creatorcontrib><title>Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine</title><title>Veterinary microbiology</title><addtitle>Vet Microbiol</addtitle><description>Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6–8-week-old). Each pig was inoculated with six F4ac+E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb− (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT− STb− (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P&lt;0.0001). Conversely, bacterial adherence scores based on immunohistochemistry and CFU/g of washed mucosa were both lowest in the strains that expressed STb and highest in those that did not. For the two experiments combined, the Pearson correlation coefficient (R) between fluid volume (ml/cm) and log CFU per gram was −0.57021 (P&lt;0.0001); R2=0.3521 (n=197). These results support the hypothesis that enterotoxin-induced fluid accumulation flushes progeny organisms into the lumen of the bowel, thereby increasing the likelihood of fecal shedding and transmission of the pathogen to new hosts.</description><subject>Animals</subject><subject>bacterial adhesion</subject><subject>Bacterial Adhesion - physiology</subject><subject>Bacterial Toxins - biosynthesis</subject><subject>Bacterial Toxins - metabolism</subject><subject>correlation</subject><subject>enterocytes</subject><subject>Enterocytes - microbiology</subject><subject>Enterocytes - pathology</subject><subject>enterotoxigenic Escherichia coli</subject><subject>Enterotoxigenic Escherichia coli - metabolism</subject><subject>Enterotoxigenic Escherichia coli - physiology</subject><subject>Enterotoxins - biosynthesis</subject><subject>Enterotoxins - metabolism</subject><subject>Escherichia coli</subject><subject>Escherichia coli Infections - metabolism</subject><subject>Escherichia coli Infections - microbiology</subject><subject>Escherichia coli Infections - pathology</subject><subject>Escherichia coli Infections - veterinary</subject><subject>Escherichia coli Proteins - biosynthesis</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Fimbria</subject><subject>Fimbriae, Bacterial - metabolism</subject><subject>Fimbriae, Bacterial - pathology</subject><subject>glycoproteins</subject><subject>heat stability</subject><subject>Heat-labile enterotoxin</subject><subject>Heat-stable enterotoxin-b</subject><subject>histopathology</subject><subject>hosts</subject><subject>immunohistochemistry</subject><subject>Jejunum - microbiology</subject><subject>Jejunum - pathology</subject><subject>Microvilli - metabolism</subject><subject>Microvilli - microbiology</subject><subject>Microvilli - pathology</subject><subject>Mucin-4 - genetics</subject><subject>Mucin-4 - metabolism</subject><subject>Mucin-4 gene</subject><subject>mucosa</subject><subject>mutants</subject><subject>parents</subject><subject>pathogens</subject><subject>Polymorphism, Genetic</subject><subject>progeny</subject><subject>shedding</subject><subject>Swine</subject><subject>Swine Diseases - metabolism</subject><subject>Swine Diseases - microbiology</subject><subject>Swine Diseases - pathology</subject><subject>toxins</subject><issn>0378-1135</issn><issn>1873-2542</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkctu1DAUhiMEosPAGyDwkk1S33LxBglVLVSqxAK6thz7ZMajxA62My0PyvvgUYbLCrGydPT937HOXxSvCa4IJs3loTpCmqyuKCa0wm2Fefek2JCuZSWtOX1abDBru5IQVl8UL2I8YIy5aPDz4oJSgUlNxab4ceuOECKgAKNK1ru4tzPqIT0AOLQHlVBMqh8BgUsQfPKP1pU9ss4sGgwaxsUapLRepmUVIOXywOwhgNOA_IBuuNLl7KNN9vi3ZwfOanQddWat3luFtB9tVqPR7lTK9gMcFqdGNHo_x7Oqv1QaDXbqQw4E0DAnH_7o44N18LJ4Nqgxwqvzuy3ub66_Xn0q7z5_vL36cFdqTkQqWdOLRtRCUEYV59QwQlnTqrbpe9MayvJwyFDfCS1Yx2rSDrVhoqGc5hxh2-Ld6p2D_7ZATHKyUcM4Kgd-iZLQrs5lUVr_B0pJV7Ou4RnlK6qDjzHAIOdgJxW-S4LlqXt5kGv38tS9xK3M3efYm_OGpZ_A_A79KjsDb1dgUF6qXbBR3n_JBo5xXs3zFbbF-5WAfLSjhSCjtqcajc2XTtJ4--8__ATuuc7e</recordid><startdate>20130125</startdate><enddate>20130125</enddate><creator>Erume, Joseph</creator><creator>Wijemanne, Prageeth</creator><creator>Berberov, Emil M.</creator><creator>Kachman, Stephen D.</creator><creator>Oestmann, Daniel J.</creator><creator>Francis, David H.</creator><creator>Moxley, Rodney A.</creator><general>Elsevier B.V</general><scope>FBQ</scope><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>7X8</scope><scope>7QL</scope><scope>C1K</scope></search><sort><creationdate>20130125</creationdate><title>Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine</title><author>Erume, Joseph ; Wijemanne, Prageeth ; Berberov, Emil M. ; Kachman, Stephen D. ; Oestmann, Daniel J. ; Francis, David H. ; Moxley, Rodney A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c419t-36b969599232a442d312367a76bbd7d23a44f36bb89c9383517f5d39624269513</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>bacterial adhesion</topic><topic>Bacterial Adhesion - physiology</topic><topic>Bacterial Toxins - biosynthesis</topic><topic>Bacterial Toxins - metabolism</topic><topic>correlation</topic><topic>enterocytes</topic><topic>Enterocytes - microbiology</topic><topic>Enterocytes - pathology</topic><topic>enterotoxigenic Escherichia coli</topic><topic>Enterotoxigenic Escherichia coli - metabolism</topic><topic>Enterotoxigenic Escherichia coli - physiology</topic><topic>Enterotoxins - biosynthesis</topic><topic>Enterotoxins - metabolism</topic><topic>Escherichia coli</topic><topic>Escherichia coli Infections - metabolism</topic><topic>Escherichia coli Infections - microbiology</topic><topic>Escherichia coli Infections - pathology</topic><topic>Escherichia coli Infections - veterinary</topic><topic>Escherichia coli Proteins - biosynthesis</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Fimbria</topic><topic>Fimbriae, Bacterial - metabolism</topic><topic>Fimbriae, Bacterial - pathology</topic><topic>glycoproteins</topic><topic>heat stability</topic><topic>Heat-labile enterotoxin</topic><topic>Heat-stable enterotoxin-b</topic><topic>histopathology</topic><topic>hosts</topic><topic>immunohistochemistry</topic><topic>Jejunum - microbiology</topic><topic>Jejunum - pathology</topic><topic>Microvilli - metabolism</topic><topic>Microvilli - microbiology</topic><topic>Microvilli - pathology</topic><topic>Mucin-4 - genetics</topic><topic>Mucin-4 - metabolism</topic><topic>Mucin-4 gene</topic><topic>mucosa</topic><topic>mutants</topic><topic>parents</topic><topic>pathogens</topic><topic>Polymorphism, Genetic</topic><topic>progeny</topic><topic>shedding</topic><topic>Swine</topic><topic>Swine Diseases - metabolism</topic><topic>Swine Diseases - microbiology</topic><topic>Swine Diseases - pathology</topic><topic>toxins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Erume, Joseph</creatorcontrib><creatorcontrib>Wijemanne, Prageeth</creatorcontrib><creatorcontrib>Berberov, Emil M.</creatorcontrib><creatorcontrib>Kachman, Stephen D.</creatorcontrib><creatorcontrib>Oestmann, Daniel J.</creatorcontrib><creatorcontrib>Francis, David H.</creatorcontrib><creatorcontrib>Moxley, Rodney A.</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environmental Sciences and Pollution Management</collection><jtitle>Veterinary microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Erume, Joseph</au><au>Wijemanne, Prageeth</au><au>Berberov, Emil M.</au><au>Kachman, Stephen D.</au><au>Oestmann, Daniel J.</au><au>Francis, David H.</au><au>Moxley, Rodney A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine</atitle><jtitle>Veterinary microbiology</jtitle><addtitle>Vet Microbiol</addtitle><date>2013-01-25</date><risdate>2013</risdate><volume>161</volume><issue>3-4</issue><spage>315</spage><epage>324</epage><pages>315-324</pages><issn>0378-1135</issn><eissn>1873-2542</eissn><abstract>Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6–8-week-old). Each pig was inoculated with six F4ac+E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb− (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT− STb− (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P&lt;0.0001). Conversely, bacterial adherence scores based on immunohistochemistry and CFU/g of washed mucosa were both lowest in the strains that expressed STb and highest in those that did not. For the two experiments combined, the Pearson correlation coefficient (R) between fluid volume (ml/cm) and log CFU per gram was −0.57021 (P&lt;0.0001); R2=0.3521 (n=197). These results support the hypothesis that enterotoxin-induced fluid accumulation flushes progeny organisms into the lumen of the bowel, thereby increasing the likelihood of fecal shedding and transmission of the pathogen to new hosts.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>22901529</pmid><doi>10.1016/j.vetmic.2012.07.048</doi><tpages>10</tpages></addata></record>
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identifier ISSN: 0378-1135
ispartof Veterinary microbiology, 2013-01, Vol.161 (3-4), p.315-324
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source MEDLINE; Elsevier ScienceDirect Journals Complete
subjects Animals
bacterial adhesion
Bacterial Adhesion - physiology
Bacterial Toxins - biosynthesis
Bacterial Toxins - metabolism
correlation
enterocytes
Enterocytes - microbiology
Enterocytes - pathology
enterotoxigenic Escherichia coli
Enterotoxigenic Escherichia coli - metabolism
Enterotoxigenic Escherichia coli - physiology
Enterotoxins - biosynthesis
Enterotoxins - metabolism
Escherichia coli
Escherichia coli Infections - metabolism
Escherichia coli Infections - microbiology
Escherichia coli Infections - pathology
Escherichia coli Infections - veterinary
Escherichia coli Proteins - biosynthesis
Escherichia coli Proteins - metabolism
Fimbria
Fimbriae, Bacterial - metabolism
Fimbriae, Bacterial - pathology
glycoproteins
heat stability
Heat-labile enterotoxin
Heat-stable enterotoxin-b
histopathology
hosts
immunohistochemistry
Jejunum - microbiology
Jejunum - pathology
Microvilli - metabolism
Microvilli - microbiology
Microvilli - pathology
Mucin-4 - genetics
Mucin-4 - metabolism
Mucin-4 gene
mucosa
mutants
parents
pathogens
Polymorphism, Genetic
progeny
shedding
Swine
Swine Diseases - metabolism
Swine Diseases - microbiology
Swine Diseases - pathology
toxins
title Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine
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