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Secondary ossification center induces and protects growth plate structure

Meng Xie, Pavel Gol’din, Anna Nele Herdina, Jordi Estefa, Ekaterina V Medvedeva, Lei Li, Phillip T Newton, Svetlana Kotova, Boris Shavkuta, Aditya Saxena, Lauren T Shumate, Brian Metscher, Karl Großschmidt, Shigeki Nishimori, Anastasia Akovantseva, Anna P Usanova, Anastasiia D Kurenkova, Anoop Kumar, Irene Linares Arregui, Paul Tafforeau, Kaj Fried, Mattias Carlström, Andras Simon, Christian Gasser, Henry M Kronenberg, Murat Bastepe, Kimberly L. Cooper, Peter Timashev, Sophie Sanchez, Igor Adameyko, Anders Eriksson, Andrei S Chagin
doi: https://doi.org/10.1101/571612
Meng Xie
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
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Pavel Gol’din
2Department of Evolutionary Morphology, Schmalhausen Institute of Zoology of NAS of Ukraine, Ukraine
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Anna Nele Herdina
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
19Department of Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
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Jordi Estefa
3Science for Life Laboratory and Uppsala University, Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala, Sweden
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Ekaterina V Medvedeva
4Institute for Regenerative Medicine, Sechenov University, Russia
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Lei Li
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
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Phillip T Newton
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
5Department of Women’s and Children’s Health, Astrid Lindgren Children’s Hospital, Karolinska University Hospital, Sweden
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Svetlana Kotova
4Institute for Regenerative Medicine, Sechenov University, Russia
6Semenov Institute of Chemical Physics, Russia
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Boris Shavkuta
4Institute for Regenerative Medicine, Sechenov University, Russia
7Institute of Photonic Technologies, Research center “Crystallography and Photonics”, Russia
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Aditya Saxena
8Division of Biological Sciences, University of California San Diego, USA
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Lauren T Shumate
9Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, U.S.A.
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Brian Metscher
10Department of Theoretical Biology, University of Vienna, Austria
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Karl Großschmidt
11Bone and Biomaterials Research, Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria
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Shigeki Nishimori
9Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, U.S.A.
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Anastasia Akovantseva
4Institute for Regenerative Medicine, Sechenov University, Russia
7Institute of Photonic Technologies, Research center “Crystallography and Photonics”, Russia
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Anna P Usanova
4Institute for Regenerative Medicine, Sechenov University, Russia
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Anastasiia D Kurenkova
4Institute for Regenerative Medicine, Sechenov University, Russia
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Anoop Kumar
15Department of Cell and Molecular Biology, Centre of Developmental Biology for Regenerative Medicine, Karolinska Institute, Stockholm, Sweden
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Irene Linares Arregui
12Department of Solid Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
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Paul Tafforeau
13European Synchrotron Radiation Facility, Grenoble Cedex, France
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Kaj Fried
14Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
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Mattias Carlström
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
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Andras Simon
15Department of Cell and Molecular Biology, Centre of Developmental Biology for Regenerative Medicine, Karolinska Institute, Stockholm, Sweden
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Christian Gasser
12Department of Solid Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
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Henry M Kronenberg
9Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, U.S.A.
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Murat Bastepe
9Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, U.S.A.
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Kimberly L. Cooper
8Division of Biological Sciences, University of California San Diego, USA
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Peter Timashev
4Institute for Regenerative Medicine, Sechenov University, Russia
6Semenov Institute of Chemical Physics, Russia
7Institute of Photonic Technologies, Research center “Crystallography and Photonics”, Russia
16Chemistry Department, Lomonosov Moscow State University, Leninskiye Gory 1-3, Moscow 119991, Russian Federation
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Sophie Sanchez
3Science for Life Laboratory and Uppsala University, Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala, Sweden
13European Synchrotron Radiation Facility, Grenoble Cedex, France
17Sorbonne Université – CR2P – MNHN, CNRS, UPMC, Paris, France
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Igor Adameyko
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
18Department of Molecular Neurosciences, Medical University of Vienna, Austria
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Anders Eriksson
19Department of Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
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Andrei S Chagin
1Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
4Institute for Regenerative Medicine, Sechenov University, Russia
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  • For correspondence: andrei.chagin@ki.se
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Abstract

Growth plate and articular cartilage constitute a single anatomical entity early in development, but later separate into two distinct structures by the secondary ossification center (SOC). The reason for such separation remains unknown. We found that evolutionarily SOC appears in animals conquering the land - amniotes. Analysis of ossification pattern in mammals with specialized extremities (whales, bats, jerboa) revealed that SOC development correlates with the extent of mechanical loads. Mathematical modelling revealed that SOC reduces mechanical stress within the growth plate. Functional experiments revealed high vulnerability of hypertrophic chondrocytes to mechanical stress and showed that SOC protects these cells from apoptosis caused by extensive loading. Atomic force microscopy showed that hypertrophic chondrocytes are the least mechanically stiff cells within the growth plate. Altogether, these findings suggest that SOC has evolved to protect the hypertrophic chondrocytes from the high mechanical stress encountered in the terrestrial environment.

Competing Interest Statement

The authors have declared no competing interest.

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Posted September 01, 2020.
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Secondary ossification center induces and protects growth plate structure
Meng Xie, Pavel Gol’din, Anna Nele Herdina, Jordi Estefa, Ekaterina V Medvedeva, Lei Li, Phillip T Newton, Svetlana Kotova, Boris Shavkuta, Aditya Saxena, Lauren T Shumate, Brian Metscher, Karl Großschmidt, Shigeki Nishimori, Anastasia Akovantseva, Anna P Usanova, Anastasiia D Kurenkova, Anoop Kumar, Irene Linares Arregui, Paul Tafforeau, Kaj Fried, Mattias Carlström, Andras Simon, Christian Gasser, Henry M Kronenberg, Murat Bastepe, Kimberly L. Cooper, Peter Timashev, Sophie Sanchez, Igor Adameyko, Anders Eriksson, Andrei S Chagin
bioRxiv 571612; doi: https://doi.org/10.1101/571612
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Secondary ossification center induces and protects growth plate structure
Meng Xie, Pavel Gol’din, Anna Nele Herdina, Jordi Estefa, Ekaterina V Medvedeva, Lei Li, Phillip T Newton, Svetlana Kotova, Boris Shavkuta, Aditya Saxena, Lauren T Shumate, Brian Metscher, Karl Großschmidt, Shigeki Nishimori, Anastasia Akovantseva, Anna P Usanova, Anastasiia D Kurenkova, Anoop Kumar, Irene Linares Arregui, Paul Tafforeau, Kaj Fried, Mattias Carlström, Andras Simon, Christian Gasser, Henry M Kronenberg, Murat Bastepe, Kimberly L. Cooper, Peter Timashev, Sophie Sanchez, Igor Adameyko, Anders Eriksson, Andrei S Chagin
bioRxiv 571612; doi: https://doi.org/10.1101/571612

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