eLife (Oct 2020)
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 D Metscher,
- Karl Großschmidt,
- Shigeki Nishimori,
- Anastasia Akovantseva,
- Anna P Usanova,
- Anastasiia D Kurenkova,
- Anoop Kumar,
- Irene Linares Arregui,
- Paul Tafforeau,
- Kaj Fried,
- Mattias Carlström,
- András Simon,
- Christian Gasser,
- Henry M Kronenberg,
- Murat Bastepe,
- Kimberly L Cooper,
- Peter Timashev,
- Sophie Sanchez,
- Igor Adameyko,
- Anders Eriksson,
- Andrei S Chagin
Affiliations
- Meng Xie
- ORCiD
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
- Pavel Gol'din
- ORCiD
- Department of Evolutionary Morphology, Schmalhausen Institute of Zoology of NAS of Ukraine, Kiev, Ukraine
- Anna Nele Herdina
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden; Division of Anatomy, MIC, Medical University of Vienna, Vienna, Austria
- Jordi Estefa
- Science for Life Laboratory and Uppsala University, Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala, Sweden
- Ekaterina V Medvedeva
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation
- Lei Li
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
- Phillip T Newton
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden; Department of Women’s and Children’s Health, Karolinska Institutet and Astrid Lindgren Children’s Hospital, Karolinska University Hospital, Solna, Sweden
- Svetlana Kotova
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation; Semenov Institute of Chemical Physics, Moscow, Russian Federation
- Boris Shavkuta
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation
- Aditya Saxena
- Division of Biological Sciences, University of California San Diego, San Diego, United States
- Lauren T Shumate
- Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, United States
- Brian D Metscher
- ORCiD
- Department of Theoretical Biology, University of Vienna, Vienna, Austria
- Karl Großschmidt
- Bone and Biomaterials Research, Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria
- Shigeki Nishimori
- Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, United States
- Anastasia Akovantseva
- Institute of Photonic Technologies, Research center "Crystallography and Photonics", Moscow, Russian Federation
- Anna P Usanova
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation
- Anastasiia D Kurenkova
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation
- Anoop Kumar
- Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm, Sweden
- Irene Linares Arregui
- Department of Solid Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
- Paul Tafforeau
- ORCiD
- European Synchrotron Radiation Facility, Grenoble, France
- Kaj Fried
- Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
- Mattias Carlström
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
- András Simon
- ORCiD
- Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm, Sweden
- Christian Gasser
- Department of Solid Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
- Henry M Kronenberg
- Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, United States
- Murat Bastepe
- Endocrine Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, United States
- Kimberly L Cooper
- ORCiD
- Division of Biological Sciences, University of California San Diego, San Diego, United States
- Peter Timashev
- Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation; Semenov Institute of Chemical Physics, Moscow, Russian Federation; Institute of Photonic Technologies, Research center "Crystallography and Photonics", Moscow, Russian Federation; Chemistry Department, Lomonosov Moscow State University, Leninskiye Gory 1-3, Moscow, Russian Federation
- Sophie Sanchez
- ORCiD
- Science for Life Laboratory and Uppsala University, Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala, Sweden; European Synchrotron Radiation Facility, Grenoble, France; Sorbonne Université – CR2P – MNHN, CNRS, UPMC, Paris, France
- Igor Adameyko
- ORCiD
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden; Department of Neuroimmunology, Medical University of Vienna, Vienna, Austria
- Anders Eriksson
- Department of Mechanics, KTH Royal Institute of Technology, Stockholm, Sweden
- Andrei S Chagin
- ORCiD
- Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden; Institute for Regenerative Medicine, Sechenov University, Moscow, Russian Federation
- DOI
- https://doi.org/10.7554/eLife.55212
- Journal volume & issue
-
Vol. 9
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 the ossification pattern in mammals with specialized extremities (whales, bats, jerboa) revealed that SOC development correlates with the extent of mechanical loads. Mathematical modeling revealed that SOC reduces mechanical stress within the growth plate. Functional experiments revealed the 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.
Keywords