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A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology
The eggs of the freshwater Pomacea apple snails develop above the water level, exposed to varied physical and biological stressors. Their high hatching success seems to be linked to their proteins or perivitellins, which surround the developing embryo providing nutrients, sunscreens and varied defen...
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Published in: | PloS one 2018-06, Vol.13 (6), p.e0198361-e0198361 |
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description | The eggs of the freshwater Pomacea apple snails develop above the water level, exposed to varied physical and biological stressors. Their high hatching success seems to be linked to their proteins or perivitellins, which surround the developing embryo providing nutrients, sunscreens and varied defenses. The defensive mechanism has been unveiled in P. canaliculata and P. maculata eggs, where their major perivitellins are pigmented, non-digestible and provide a warning coloration while another perivitellin acts as a toxin. In P. scalaris, a species sympatric to the former, the defense strategy seems different, since no toxin was found and the major perivitellin, PsSC, while also colored and non-digestible, is a carbohydrate-binding protein. In this study we examine the structure and function of PsSC by sequencing its subunits, characterizing its carbohydrate binding profile and evaluating its effect on gut cells. Whereas cDNA sequencing and database search showed no lectin domain, glycan array carbohydrate binding profile revealed a strong specificity for glycosphingolipids and ABO group antigens. Moreover, PsSC agglutinated bacteria in a dose-dependent manner. Inspired on the defensive properties of seed lectins we evaluated the effects of PsSC on intestinal cells both in vitro (Caco-2 and IEC-6 cells) and in the gastrointestinal tract of rats. PsSC binds to Caco-2 cell membranes without reducing its viability, while a PsSC-containing diet temporarily induces large epithelium alterations and an increased absorptive surface. Based on these results, we propose that PsSC is involved in embryo defenses by altering the gut morphophysiology of potential predators, a convergent role to plant defensive lectins. |
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Their high hatching success seems to be linked to their proteins or perivitellins, which surround the developing embryo providing nutrients, sunscreens and varied defenses. The defensive mechanism has been unveiled in P. canaliculata and P. maculata eggs, where their major perivitellins are pigmented, non-digestible and provide a warning coloration while another perivitellin acts as a toxin. In P. scalaris, a species sympatric to the former, the defense strategy seems different, since no toxin was found and the major perivitellin, PsSC, while also colored and non-digestible, is a carbohydrate-binding protein. In this study we examine the structure and function of PsSC by sequencing its subunits, characterizing its carbohydrate binding profile and evaluating its effect on gut cells. Whereas cDNA sequencing and database search showed no lectin domain, glycan array carbohydrate binding profile revealed a strong specificity for glycosphingolipids and ABO group antigens. Moreover, PsSC agglutinated bacteria in a dose-dependent manner. Inspired on the defensive properties of seed lectins we evaluated the effects of PsSC on intestinal cells both in vitro (Caco-2 and IEC-6 cells) and in the gastrointestinal tract of rats. PsSC binds to Caco-2 cell membranes without reducing its viability, while a PsSC-containing diet temporarily induces large epithelium alterations and an increased absorptive surface. Based on these results, we propose that PsSC is involved in embryo defenses by altering the gut morphophysiology of potential predators, a convergent role to plant defensive lectins.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0198361</identifier><identifier>PMID: 29856808</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>ABO system ; Absorptivity ; Agglutination ; Animal defenses ; Animals ; Antigens ; Antimicrobial agents ; Biological stress ; Biology and Life Sciences ; Caco-2 Cells ; Carbohydrates ; Cell membranes ; Cells, Cultured ; Chemical properties ; Coloration ; Defense reaction (Physiology) ; Digestive system ; Digestive tract ; Egg Proteins - physiology ; Eggs ; Eggs (Biology) ; Embryos ; Epithelium ; Gastrointestinal tract ; Gastrointestinal Tract - anatomy & histology ; Gastrointestinal Tract - drug effects ; Gastrointestinal Tract - physiology ; Glycan ; Glycosphingolipids ; Hatching ; Health aspects ; Humans ; Intestine ; Intestines - anatomy & histology ; Intestines - drug effects ; Intestines - physiology ; Laboratory animals ; Lectins ; Lectins - pharmacology ; Lectins - physiology ; Male ; Medicine and Health Sciences ; Membranes ; Metabolism ; Mollusks ; Nutrients ; Physiological aspects ; Pomacea ; Pomacea canaliculata ; Predation ; Predators ; Predatory Behavior - drug effects ; Proteins ; Rats - anatomy & histology ; Rats - physiology ; Rats, Wistar ; Research and Analysis Methods ; Sequences ; Snails ; Snails - chemistry ; Structure-function relationships ; Sun screens ; Sunscreens ; Sympatric populations ; Toxins ; Viability ; Water levels</subject><ispartof>PloS one, 2018-06, Vol.13 (6), p.e0198361-e0198361</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Ituarte et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Their high hatching success seems to be linked to their proteins or perivitellins, which surround the developing embryo providing nutrients, sunscreens and varied defenses. The defensive mechanism has been unveiled in P. canaliculata and P. maculata eggs, where their major perivitellins are pigmented, non-digestible and provide a warning coloration while another perivitellin acts as a toxin. In P. scalaris, a species sympatric to the former, the defense strategy seems different, since no toxin was found and the major perivitellin, PsSC, while also colored and non-digestible, is a carbohydrate-binding protein. In this study we examine the structure and function of PsSC by sequencing its subunits, characterizing its carbohydrate binding profile and evaluating its effect on gut cells. Whereas cDNA sequencing and database search showed no lectin domain, glycan array carbohydrate binding profile revealed a strong specificity for glycosphingolipids and ABO group antigens. Moreover, PsSC agglutinated bacteria in a dose-dependent manner. Inspired on the defensive properties of seed lectins we evaluated the effects of PsSC on intestinal cells both in vitro (Caco-2 and IEC-6 cells) and in the gastrointestinal tract of rats. PsSC binds to Caco-2 cell membranes without reducing its viability, while a PsSC-containing diet temporarily induces large epithelium alterations and an increased absorptive surface. Based on these results, we propose that PsSC is involved in embryo defenses by altering the gut morphophysiology of potential predators, a convergent role to plant defensive lectins.</description><subject>ABO system</subject><subject>Absorptivity</subject><subject>Agglutination</subject><subject>Animal defenses</subject><subject>Animals</subject><subject>Antigens</subject><subject>Antimicrobial agents</subject><subject>Biological stress</subject><subject>Biology and Life Sciences</subject><subject>Caco-2 Cells</subject><subject>Carbohydrates</subject><subject>Cell membranes</subject><subject>Cells, Cultured</subject><subject>Chemical properties</subject><subject>Coloration</subject><subject>Defense reaction (Physiology)</subject><subject>Digestive system</subject><subject>Digestive tract</subject><subject>Egg Proteins - physiology</subject><subject>Eggs</subject><subject>Eggs (Biology)</subject><subject>Embryos</subject><subject>Epithelium</subject><subject>Gastrointestinal tract</subject><subject>Gastrointestinal Tract - anatomy & histology</subject><subject>Gastrointestinal Tract - drug effects</subject><subject>Gastrointestinal Tract - physiology</subject><subject>Glycan</subject><subject>Glycosphingolipids</subject><subject>Hatching</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Intestine</subject><subject>Intestines - anatomy & histology</subject><subject>Intestines - drug effects</subject><subject>Intestines - physiology</subject><subject>Laboratory animals</subject><subject>Lectins</subject><subject>Lectins - pharmacology</subject><subject>Lectins - physiology</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Membranes</subject><subject>Metabolism</subject><subject>Mollusks</subject><subject>Nutrients</subject><subject>Physiological aspects</subject><subject>Pomacea</subject><subject>Pomacea canaliculata</subject><subject>Predation</subject><subject>Predators</subject><subject>Predatory Behavior - drug effects</subject><subject>Proteins</subject><subject>Rats - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals (DOAJ)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ituarte, Santiago</au><au>Brola, Tabata Romina</au><au>Fernández, Patricia Elena</au><au>Mu, Huawei</au><au>Qiu, Jian-Wen</au><au>Heras, Horacio</au><au>Dreon, Marcos Sebastián</au><au>Rittschof, Daniel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-06-01</date><risdate>2018</risdate><volume>13</volume><issue>6</issue><spage>e0198361</spage><epage>e0198361</epage><pages>e0198361-e0198361</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The eggs of the freshwater Pomacea apple snails develop above the water level, exposed to varied physical and biological stressors. Their high hatching success seems to be linked to their proteins or perivitellins, which surround the developing embryo providing nutrients, sunscreens and varied defenses. The defensive mechanism has been unveiled in P. canaliculata and P. maculata eggs, where their major perivitellins are pigmented, non-digestible and provide a warning coloration while another perivitellin acts as a toxin. In P. scalaris, a species sympatric to the former, the defense strategy seems different, since no toxin was found and the major perivitellin, PsSC, while also colored and non-digestible, is a carbohydrate-binding protein. In this study we examine the structure and function of PsSC by sequencing its subunits, characterizing its carbohydrate binding profile and evaluating its effect on gut cells. Whereas cDNA sequencing and database search showed no lectin domain, glycan array carbohydrate binding profile revealed a strong specificity for glycosphingolipids and ABO group antigens. Moreover, PsSC agglutinated bacteria in a dose-dependent manner. Inspired on the defensive properties of seed lectins we evaluated the effects of PsSC on intestinal cells both in vitro (Caco-2 and IEC-6 cells) and in the gastrointestinal tract of rats. PsSC binds to Caco-2 cell membranes without reducing its viability, while a PsSC-containing diet temporarily induces large epithelium alterations and an increased absorptive surface. Based on these results, we propose that PsSC is involved in embryo defenses by altering the gut morphophysiology of potential predators, a convergent role to plant defensive lectins.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29856808</pmid><doi>10.1371/journal.pone.0198361</doi><tpages>e0198361</tpages><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2018-06, Vol.13 (6), p.e0198361-e0198361 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_2049517836 |
source | PubMed Central (Open Access); Publicly Available Content (ProQuest) |
subjects | ABO system Absorptivity Agglutination Animal defenses Animals Antigens Antimicrobial agents Biological stress Biology and Life Sciences Caco-2 Cells Carbohydrates Cell membranes Cells, Cultured Chemical properties Coloration Defense reaction (Physiology) Digestive system Digestive tract Egg Proteins - physiology Eggs Eggs (Biology) Embryos Epithelium Gastrointestinal tract Gastrointestinal Tract - anatomy & histology Gastrointestinal Tract - drug effects Gastrointestinal Tract - physiology Glycan Glycosphingolipids Hatching Health aspects Humans Intestine Intestines - anatomy & histology Intestines - drug effects Intestines - physiology Laboratory animals Lectins Lectins - pharmacology Lectins - physiology Male Medicine and Health Sciences Membranes Metabolism Mollusks Nutrients Physiological aspects Pomacea Pomacea canaliculata Predation Predators Predatory Behavior - drug effects Proteins Rats - anatomy & histology Rats - physiology Rats, Wistar Research and Analysis Methods Sequences Snails Snails - chemistry Structure-function relationships Sun screens Sunscreens Sympatric populations Toxins Viability Water levels |
title | A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology |
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