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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
Main Authors: Ituarte, Santiago, Brola, Tabata Romina, Fernández, Patricia Elena, Mu, Huawei, Qiu, Jian-Wen, Heras, Horacio, Dreon, Marcos Sebastián
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Brola, Tabata Romina
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Dreon, Marcos Sebastián
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.
doi_str_mv 10.1371/journal.pone.0198361
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Medical Complete (Alumni)</collection><collection>https://resources.nclive.org/materials</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - 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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