Oriented clonal cell dynamics enables accurate growth and shaping of vertebrate cartilage

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Abstract

Cartilaginous structures are at the core of embryo growth and shaping before the bone forms. Here we report a novel principle of vertebrate cartilage growth that is based on introducing transversally-oriented clones into pre-existing cartilage. This mechanism of growth uncouples the lateral expansion of curved cartilaginous sheets from the control of cartilage thickness, a process which might be the evolutionary mechanism underlying adaptations of facial shape. In rod-shaped cartilage structures (Meckel, ribs and skeletal elements in developing limbs), the transverse integration of clonal columns determines the well-defined diameter and resulting rod-like morphology. We were able to alter cartilage shape by experimentally manipulating clonal geometries. Using in silico modeling, we discovered that anisotropic proliferation might explain cartilage bending and groove formation at the macro-scale.

DOI: http://dx.doi.org/10.7554/eLife.25902.001

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Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels.

Christa Maes, Tatsuya Kobayashi, Martin Selig … (2010)

During endochondral bone development, the first osteoblasts differentiate in the perichondrium surrounding avascular cartilaginous rudiments; the source of trabecular osteoblasts inside the later bone is, however, unknown. Here, we generated tamoxifen-inducible transgenic mice bred to Rosa26R-LacZ reporter mice to follow the fates of stage-selective subsets of osteoblast lineage cells. Pulse-chase studies showed that osterix-expressing osteoblast precursors, labeled in the perichondrium prior to vascular invasion of the cartilage, give rise to trabecular osteoblasts, osteocytes, and stromal cells inside the developing bone. Throughout the translocation, some precursors were found to intimately associate with invading blood vessels, in pericyte-like fashion. A similar coinvasion occurs during endochondral healing of bone fractures. In contrast, perichondrial mature osteoblasts did not exhibit perivascular localization and remained in the outer cortex of developing bones. These findings reveal the specific involvement of immature osteoblast precursors in the coupled vascular and osteogenic transformation essential to endochondral bone development and repair. 2010 Elsevier Inc. All rights reserved.

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Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains.

R Feil, J. Wagner, D. Metzger … (1997)

Ligand-dependent chimeric Cre recombinases are powerful tools to induce specific DNA rearrangements in cultured cells and in mice. We report here the construction and characterization of a series of chimeric recombinases, each consisting of Cre fused to a mutated human oestrogen receptor (ER) ligand-binding domain (LBD). Two new ligand-dependent recombinases which contain either the G400V/M543A/L544A or the G400V/L539A/L540A triple mutation of the human ER LBD are efficiently induced by the synthetic ER antagonists 4-hydroxytamoxifen (OHT) and ICI 182,780 (ICI), respectively, but are insensitive to 17 beta-oestradiol (E2). Both chimeric recombinases should be useful for efficient spatio-temporally controlled site-directed somatic mutagenesis.

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The control of chondrogenesis.

Mary Goldring, Kaneyuki Tsuchimochi, Kosei Ijiri (2006)

Chondrogenesis is the earliest phase of skeletal development, involving mesenchymal cell recruitment and migration, condensation of progenitors, and chondrocyte differentiation, and maturation and resulting in the formation of cartilage and bone during endochondral ossification. This process is controlled exquisitely by cellular interactions with the surrounding matrix, growth and differentiation factors, and other environmental factors that initiate or suppress cellular signaling pathways and transcription of specific genes in a temporal-spatial manner. Vertebrate limb development is controlled by interacting patterning systems involving prominently the fibroblast growth factor (FGF), bone morphogenetic protein (BMP), and hedgehog pathways. Both positive and negative signaling kinases and transcription factors, such as Sox9 and Runx2, and interactions among them determine whether the differentiated chondrocytes remain within cartilage elements in articular joints or undergo hypertrophic maturation prior to ossification. The latter process requires extracellular matrix remodeling and vascularization controlled by mechanisms that are not understood completely. Recent work has revealed novel roles for mediators such as GADD45beta, transcription factors of the Dlx, bHLH, leucine zipper, and AP-1 families, and the Wnt/beta-catenin pathway that interact at different stages during chondrogenesis. (c) 2005 Wiley-Liss, Inc.

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Author and article information

Contributors

Marianne Bronner: Role: Reviewing editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (hwp): eLife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 17 April 2017

Publication date Collection: 2017

Volume: 6

Electronic Location Identifier: e25902

Affiliations

[1 ]deptDepartment of Physiology and Pharmacology , Karolinska Institutet , Stockholm, Sweden

[2 ]deptCenter for Brain Research , Medical University Vienna , Vienna, Austria

[3 ]deptCentral European Institute of Technology , Brno University of Technology , Brno, Czech Republic

[4 ]deptUnit of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics , Karolinska Institutet , Stockholm, Sweden

[5 ]deptDepartment of Information Technology , Uppsala University , Uppsala, Sweden

[6 ]deptDepartment of Histology and Embryology, Medical Faculty , Masaryk University , Brno, Czech Republic

[7 ]deptDepartment of Neuroscience , Karolinska Institutet , Stockholm, Sweden

[8 ]deptDepartment of Medicine , Karolinska Institutet , Stockholm, Sweden

[9 ]deptDepartment of Biologic and Materials Sciences , University of Michigan School of Dentistry , Ann Arbor, United States

[10 ]deptCenter for Regenerative Therapies , Technische Universität Dresden , Dresden, Germany

[11 ]deptDepartment of Genetics, Cell Biology and Anatomy , University of Nebraska Medical Center , Omaha, United States

[12 ]deptScience for Life Laboratory , Royal Institute of Technology , Solna, Sweden

[13 ]John Innes Centre , Norwich, United Kingdom

[14 ]National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health , Bethesda, United States

[15 ]deptInstitute for Regenerative Medicine , Sechenov First Moscow State Medical University , Moscow, Russia

California Institute of Technology , United States

Author notes

kaj.fried@ 123456ki.se (KF);

igor.adameyko@ 123456ki.se (IA)

Author information

Marketa Kaucka http://orcid.org/0000-0002-8781-9769

Hjalmar Brismar http://orcid.org/0000-0003-0578-4003

Enrico Coen http://orcid.org/0000-0001-8454-8767

Andrei S Chagin http://orcid.org/0000-0002-2696-5850

Igor Adameyko http://orcid.org/0000-0001-5471-0356

Article

Publisher ID: 25902

DOI: 10.7554/eLife.25902

PMC ID: 5417851

PubMed ID: 28414273

SO-VID: e5d8bf46-26bc-4f42-a6d0-3d9113d65559

License:

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

History

Date received : 09 February 2017

Date accepted : 16 April 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004410, European Molecular Biology Organization;

Award ID: ALTF 216-2013

Award Recipient : Marketa Kaucka

Funded by: FundRef http://dx.doi.org/10.13039/501100003748, Svenska Sällskapet för Medicinsk Forskning;

Award Recipient : Marketa Kaucka

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award Recipient : Andreas Hellander

Funded by: FundRef http://dx.doi.org/10.13039/501100001862, Svenska Forskningsrådet Formas;

Award Recipient : Phillip T Newton Andrei S Chagin Kaj Fried Igor Adameyko

Funded by: FundRef http://dx.doi.org/10.13039/501100004047, Karolinska Institutet;

Award Recipient : Phillip T Newton Andrei S Chagin Kaj Fried Igor Adameyko

Funded by: FundRef http://dx.doi.org/10.13039/501100006516, Bertil Hållstens Forskningsstiftelse;

Award Recipient : Igor Adameyko

Funded by: Åke Wiberg Stiftelse;

Award Recipient : Igor Adameyko

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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elife-xml-version 2.5

Author impact statement The clonal oriented cell dynamics enables directional expansion and accurate scaling of sheet-like or rod-like cartilaginous elements and uncouples the mechanisms of elongation from thickness or diameter control.

ScienceOpen disciplines: Life sciences

Keywords: chondrocranium,scaling and shaping,facial cartilage growth,mouse mutants,mathematical and material modelling,wnt/pcp,bmp,gsalpha,mouse

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: chondrocranium, scaling and shaping, facial cartilage growth, mouse mutants, mathematical and material modelling, wnt/pcp, bmp, gsalpha, mouse

Oriented clonal cell dynamics enables accurate growth and shaping of vertebrate cartilage

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Most cited references 49

Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels.

Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains.

The control of chondrogenesis.

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