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Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels

During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European ee...

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Autores principales: Freese, Marko, Rizzo, Larissa Yokota, Pohlmann, Jan-Dag, Marohn, Lasse, Witten, Paul Eckhard, Gremse, Felix, Rütten, Stephan, Güvener, Nihan, Michael, Sabrina, Wysujack, Klaus, Lammers, Twan, Kiessling, Fabian, Hollert, Henner, Hanel, Reinhold, Brinkmann, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/
https://www.ncbi.nlm.nih.gov/pubmed/31085642
http://dx.doi.org/10.1073/pnas.1817738116
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author Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
author_facet Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
author_sort Freese, Marko
collection PubMed
description During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels’ bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.
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spelling pubmed-65612372019-06-17 Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels Freese, Marko Rizzo, Larissa Yokota Pohlmann, Jan-Dag Marohn, Lasse Witten, Paul Eckhard Gremse, Felix Rütten, Stephan Güvener, Nihan Michael, Sabrina Wysujack, Klaus Lammers, Twan Kiessling, Fabian Hollert, Henner Hanel, Reinhold Brinkmann, Markus Proc Natl Acad Sci U S A Biological Sciences During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels’ bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species. National Academy of Sciences 2019-06-04 2019-05-13 /pmc/articles/PMC6561237/ /pubmed/31085642 http://dx.doi.org/10.1073/pnas.1817738116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Freese, Marko
Rizzo, Larissa Yokota
Pohlmann, Jan-Dag
Marohn, Lasse
Witten, Paul Eckhard
Gremse, Felix
Rütten, Stephan
Güvener, Nihan
Michael, Sabrina
Wysujack, Klaus
Lammers, Twan
Kiessling, Fabian
Hollert, Henner
Hanel, Reinhold
Brinkmann, Markus
Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_full Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_fullStr Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_full_unstemmed Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_short Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
title_sort bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6561237/
https://www.ncbi.nlm.nih.gov/pubmed/31085642
http://dx.doi.org/10.1073/pnas.1817738116
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