How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime

European eels (Anguilla anguilla) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto com...

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Published in:Proceedings of the Royal Society B: Biological Sciences
Main Authors: Rolvien, Tim, Nagel, Florian, Milovanovic, Petar, Wuertz, Sven, Marshall, Robert Percy, Jeschke, Anke, Schmidt, Felix N, Hahn, Michael, Witten, Paul Eckhard, Amling, Michael, Busse, Bjoern
Format: Article in Journal/Newspaper
Language:English
Published: 2016
Subjects:
Online Access:https://biblio.ugent.be/publication/8525447
http://hdl.handle.net/1854/LU-8525447
https://doi.org/10.1098/rspb.2016.1550
https://biblio.ugent.be/publication/8525447/file/8643533
id ftunivgent:oai:archive.ugent.be:8525447
record_format openpolar
spelling ftunivgent:oai:archive.ugent.be:8525447 2023-06-11T04:03:43+02:00 How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime Rolvien, Tim Nagel, Florian Milovanovic, Petar Wuertz, Sven Marshall, Robert Percy Jeschke, Anke Schmidt, Felix N Hahn, Michael Witten, Paul Eckhard Amling, Michael Busse, Bjoern 2016 application/pdf https://biblio.ugent.be/publication/8525447 http://hdl.handle.net/1854/LU-8525447 https://doi.org/10.1098/rspb.2016.1550 https://biblio.ugent.be/publication/8525447/file/8643533 eng eng https://biblio.ugent.be/publication/8525447 http://hdl.handle.net/1854/LU-8525447 http://dx.doi.org/10.1098/rspb.2016.1550 https://biblio.ugent.be/publication/8525447/file/8643533 No license (in copyright) info:eu-repo/semantics/restrictedAccess PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES ISSN: 0962-8452 ISSN: 1471-2954 Biology and Life Sciences MEDAKA OSTEOPOROSIS MODEL SALMON SALMO-SALAR TELEOST FISH SEXUAL-MATURATION ATLANTIC SALMON ACELLULAR BONE 2ND-HARMONIC GENERATION DENSITY DISTRIBUTION SPAWNING MIGRATION VERTEBRAL SKELETON European eel bone loss osteoclasts journalArticle info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 2016 ftunivgent https://doi.org/10.1098/rspb.2016.1550 2023-05-10T22:20:25Z European eels (Anguilla anguilla) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto completely obscure bone loss phenomenon occurs. To unravel mechanisms of the maturation-related decay of the skeleton, we performed a multiscale assessment of eels' bones at different life-cycle stages. Accordingly, the skeleton reflects extensive bone loss that is mediated via multinucleated bone-resorbing osteoclasts, while other resorption mechanisms such as osteocytic osteolysis or matrix demineralization were not observed. Preserving mechanical stability and releasing minerals for energy metabolism are two mutually exclusive functions of the skeleton that are orchestrated in eels through the presence of two spatially segregated hard tissues: cellular bone and acellular notochord. The cellular bone serves as a source of mineral release following osteoclastic resorption, whereas the mineralized notochord sheath, which is inaccessible for resorption processes due to an unmineralized cover layer, ensures sufficient mechanical stability as a part of the notochord sheath. Clearly, an eel's skeleton is structurally optimized to meet the metabolic challenge of fasting and simultaneous sexual development during an exhausting journey to spawning areas, while the function of the vertebral column is maintained to achieve this goal. Article in Journal/Newspaper Anguilla anguilla Atlantic salmon North Atlantic Salmo salar Ghent University Academic Bibliography Proceedings of the Royal Society B: Biological Sciences 283 1841 20161550
institution Open Polar
collection Ghent University Academic Bibliography
op_collection_id ftunivgent
language English
topic Biology and Life Sciences
MEDAKA OSTEOPOROSIS MODEL
SALMON SALMO-SALAR
TELEOST FISH
SEXUAL-MATURATION
ATLANTIC SALMON
ACELLULAR BONE
2ND-HARMONIC
GENERATION
DENSITY DISTRIBUTION
SPAWNING MIGRATION
VERTEBRAL SKELETON
European eel
bone loss
osteoclasts
spellingShingle Biology and Life Sciences
MEDAKA OSTEOPOROSIS MODEL
SALMON SALMO-SALAR
TELEOST FISH
SEXUAL-MATURATION
ATLANTIC SALMON
ACELLULAR BONE
2ND-HARMONIC
GENERATION
DENSITY DISTRIBUTION
SPAWNING MIGRATION
VERTEBRAL SKELETON
European eel
bone loss
osteoclasts
Rolvien, Tim
Nagel, Florian
Milovanovic, Petar
Wuertz, Sven
Marshall, Robert Percy
Jeschke, Anke
Schmidt, Felix N
Hahn, Michael
Witten, Paul Eckhard
Amling, Michael
Busse, Bjoern
How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
topic_facet Biology and Life Sciences
MEDAKA OSTEOPOROSIS MODEL
SALMON SALMO-SALAR
TELEOST FISH
SEXUAL-MATURATION
ATLANTIC SALMON
ACELLULAR BONE
2ND-HARMONIC
GENERATION
DENSITY DISTRIBUTION
SPAWNING MIGRATION
VERTEBRAL SKELETON
European eel
bone loss
osteoclasts
description European eels (Anguilla anguilla) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto completely obscure bone loss phenomenon occurs. To unravel mechanisms of the maturation-related decay of the skeleton, we performed a multiscale assessment of eels' bones at different life-cycle stages. Accordingly, the skeleton reflects extensive bone loss that is mediated via multinucleated bone-resorbing osteoclasts, while other resorption mechanisms such as osteocytic osteolysis or matrix demineralization were not observed. Preserving mechanical stability and releasing minerals for energy metabolism are two mutually exclusive functions of the skeleton that are orchestrated in eels through the presence of two spatially segregated hard tissues: cellular bone and acellular notochord. The cellular bone serves as a source of mineral release following osteoclastic resorption, whereas the mineralized notochord sheath, which is inaccessible for resorption processes due to an unmineralized cover layer, ensures sufficient mechanical stability as a part of the notochord sheath. Clearly, an eel's skeleton is structurally optimized to meet the metabolic challenge of fasting and simultaneous sexual development during an exhausting journey to spawning areas, while the function of the vertebral column is maintained to achieve this goal.
format Article in Journal/Newspaper
author Rolvien, Tim
Nagel, Florian
Milovanovic, Petar
Wuertz, Sven
Marshall, Robert Percy
Jeschke, Anke
Schmidt, Felix N
Hahn, Michael
Witten, Paul Eckhard
Amling, Michael
Busse, Bjoern
author_facet Rolvien, Tim
Nagel, Florian
Milovanovic, Petar
Wuertz, Sven
Marshall, Robert Percy
Jeschke, Anke
Schmidt, Felix N
Hahn, Michael
Witten, Paul Eckhard
Amling, Michael
Busse, Bjoern
author_sort Rolvien, Tim
title How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
title_short How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
title_full How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
title_fullStr How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
title_full_unstemmed How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime
title_sort how the european eel (anguilla anguilla) loses its skeletal framework across lifetime
publishDate 2016
url https://biblio.ugent.be/publication/8525447
http://hdl.handle.net/1854/LU-8525447
https://doi.org/10.1098/rspb.2016.1550
https://biblio.ugent.be/publication/8525447/file/8643533
genre Anguilla anguilla
Atlantic salmon
North Atlantic
Salmo salar
genre_facet Anguilla anguilla
Atlantic salmon
North Atlantic
Salmo salar
op_source PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
ISSN: 0962-8452
ISSN: 1471-2954
op_relation https://biblio.ugent.be/publication/8525447
http://hdl.handle.net/1854/LU-8525447
http://dx.doi.org/10.1098/rspb.2016.1550
https://biblio.ugent.be/publication/8525447/file/8643533
op_rights No license (in copyright)
info:eu-repo/semantics/restrictedAccess
op_doi https://doi.org/10.1098/rspb.2016.1550
container_title Proceedings of the Royal Society B: Biological Sciences
container_volume 283
container_issue 1841
container_start_page 20161550
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