Cited by 1,721Osteoarthritis Treatment and MechanismsDevelopmental Biology and Gene RegulationBone Tumor Diagnosis and Treatments

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The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6

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Akiyama, Haruhiko, Chaboissier, Marie-Christine, Martin, James F., Schedl, Andreas, de Crombrugghe, Benoit·2002·Genes & Development

DOI 10.1101/gad.1017802PMC PMC187468

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Abstract

To examine whether the transcription factor Sox9 has an essential role during the sequential steps of chondrocyte differentiation, we have used the Cre/ loxP recombination system to generate mouse embryos in which either Sox9 is missing from undifferentiated mesenchymal cells of limb buds or the Sox9 gene is inactivated after chondrogenic mesenchymal condensations. Inactivation of Sox9 in limb buds before mesenchymal condensations resulted in a complete absence of both cartilage and bone, but markers for the different axes of limb development showed a normal pattern of expression. Apoptotic domains within the developing limbs were expanded, suggesting that Sox9 suppresses apoptosis. Expression of Sox5 and Sox6 , two other Sox genes involved in chondrogenesis, was no longer detected. Moreover, expression of Runx2 , a transcription factor needed for osteoblast differentiation, was also abolished. Embryos, in which Sox9 was deleted after mesenchymal condensations, exhibited a severe generalized chondrodysplasia, similar to that in Sox5 ; Sox6 double-null mutant mice. Most cells were arrested as condensed mesenchymal cells and did not undergo overt differentiation into chondrocytes. Furthermore, chondrocyte proliferation was severely inhibited and joint formation was defective. Although Indian hedgehog , Patched1 , parathyroid hormone-related peptide ( Pthrp ), and Pth/Pthrp receptor were expressed, their expression was down-regulated. Our experiments further suggested that Sox9 is also needed to prevent conversion of proliferating chondrocytes into hypertrophic chondrocytes. We conclude that Sox9 is required during sequential steps of the chondrocyte differentiation pathway.

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Cbfa1, a Candidate Gene for Cleidocranial Dysplasia Syndrome, Is Essential for Osteoblast Differentiation and Bone Development
Otto, F., Thornell, A., Crompton, T., Denzel, A., Gilmour, K. C., Rosewell, I. R., Stamp, G., Beddington, R. S. P., Mundlos, S., Olsen, B. R., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80259-7 · Cited by 2,813
Regulation of Rate of Cartilage Differentiation by Indian Hedgehog and PTH-Related Protein
Vortkamp, A., Lee, K., Lanske, B., Segre, G. V., Kronenberg, H. M., & Tabin, C. J. (1996) · Science · doi:10.1126/science.273.5275.613 · Cited by 1,999
Sox9 is required for cartilage formation
Bi, W., Deng, J. M., Zhang, Z., Behringer, R. R., & Crombrugghe, B. D. (1999) · Nature Genetics · doi:10.1038/8792 · Cited by 1,760
Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formationPreprint
St‐Jacques, B., Hammerschmidt, M., & McMahon, A. P. (1999) · Genes & Development · doi:10.1101/gad.13.16.2072 · Cited by 1,742
Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene
Foster, J. W., Dominguez-Steglich, M., Guioli, S., Kwok, C., Weller, P., Stevanović, M., Weissenbach, J., Mansour, S., Young, I., Goodfellow, P., et al. (1994) · Nature · doi:10.1038/372525a0 · Cited by 1,602
Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9.
Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F. D., Keutel, J., Hustert, E., et al. (1994) · Cell · doi:10.1016/0092-8674(94)90041-8 · Cited by 1,592
Deletion of a DNA Polymerase β Gene Segment in T Cells Using Cell Type-Specific Gene Targeting
Gu, H., Marth, J. D., Orban, P. C., Mossmann, H., & Rajewsky, K. (1994) · Science · doi:10.1126/science.8016642 · Cited by 1,397
PTH/PTHrP Receptor in Early Development and Indian Hedgehog—Regulated Bone Growth
Lanske, B., Karaplis, A. C., Lee, K., Luz, A., Vortkamp, A., Pirro, A. E., Karperien, M., Defize, L. H. K., Ho, C., Mulligan, R. C., et al. (1996) · Science · doi:10.1126/science.273.5275.663 · Cited by 1,325
A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells
Schwenk, F., Baron, U., & Rajewsky, K. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.24.5080 · Cited by 1,289
Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene.Preprint
Karaplis, A. C., Luz, A., Glowacki, J., Bronson, R. T., Tybulewicz, V. L. J., Kronenberg, H. M., & Mulligan, R. C. (1994) · Genes & Development · doi:10.1101/gad.8.3.277 · Cited by 1,151

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Show all 47 references

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Hogan B. Beddington R. Costantini F. Lucy E. (1994) Manipulating the mouse embryo. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), 2nd Edition.

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Ichinohe, T., Kanno, N., Harada, Y., Yogo, T., TAGAWA, M., Soeta, S., AMASAKI, H., & Hara, Y. (2015) · Journal of Veterinary Medical Science · doi:10.1292/jvms.14-0383 · Cited by 20
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Nayak, S. C., Bhad, W. A., & Doshi, U. H. (2014) · Journal of Orthodontics · doi:10.1179/1465313313y.0000000091 · Cited by 20
Analysis of chick (Gallus gallus) middle ear columella formation
Wood, J. L., Hughes, A., Mercer, K. J., & Chapman, S. C. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-16 · Cited by 20
Enhanced Chondrogenic Differentiation Activities in Human Bone Marrow Aspirates via sox9 Overexpression Mediated by pNaSS-Grafted PCL Film-Guided rAAV Gene Transfer
Venkatesan, J. K., Meng, W., Rey‐Rico, A., Schmitt, G., Speicher‐Mentges, S., Falentin‐Daudre, C., Leroux, A., Madry, H., Migonney, V., & Cucchiarini, M. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12030280 · Cited by 20
Loss of receptor tyrosine kinase-like orphan receptor 2 impairs the osteogenesis of mBMSCs by inhibiting signal transducer and activator of transcription 3
Lei, L., Huang, Z., Feng, J., Huang, Z., Tao, Y., Hu, X., & Zhang, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01646-2 · Cited by 20
Enamel matrix derivative stimulates chondrogenic differentiation of ATDC5 cells
Narukawa, M., Suzuki, N., Takayama, T., Shoji, T., Otsuka, K., & Ito, K. (2006) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2006.00926.x · Cited by 20
Regulatory elements of Xenopus col2a1 drive cartilaginous gene expression in transgenic frogs
Kerney, R. R., Hall, B. K., & Hanken, J. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.092848rk · Cited by 20
The hedgehog target Vlk genetically interacts with Gli3 to regulate chondrocyte differentiation during mouse long bone development
Probst, S., Zeller, R., & Zúñiga, A. (2013) · Differentiation · doi:10.1016/j.diff.2013.03.002 · Cited by 20
Chondrogenic differentiation of ATDC5-cells under the influence of Mg and Mg alloy degradation
Sánchez, A. H. M., Feyerabend, F., Laipple, D., Willumeit‐Römer, R., Weinberg, A., & Luthringer-Feyerabend, B. (2016) · Materials Science and Engineering C · doi:10.1016/j.msec.2016.11.062 · Cited by 20
Chondrogenic Differentiation of Adipose-Derived Stem Cells by Radiofrequency Electric Stimulation
Hernández‐Bule, M. L., Trillo, M. Á., Garcia, M. A. M., Abilahoud, C., & Ubeda, A. (2017) · Journal of Stem Cell Research & Therapy · doi:10.4172/2157-7633.1000407 · Cited by 21
Stem Cells for Osteochondral Regeneration
Canadas, R. F., Pirraco, R. P., Oliveira, J. M., Reis, R. L., & Marques, A. P. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-76735-2_10 · Cited by 20
Anatomy, molecular structures, and hyaluronic acid – Gelatin injectable hydrogels as a therapeutic alternative for hyaline cartilage recovery: A review
Vaca‐González, J. J., Culma, J. J. S., Nova, L. M. H., & Garzón–Alvarado, D. A. (2023) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.35261 · Cited by 19
Exercise improves subchondral bone microenvironment through regulating bone-cartilage crosstalk
Zhang, S., Li, T., Yao, F., Zhang, K., Zou, J., Weng, X., Yuan, Y. J., & Zhang, L. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1159393 · Cited by 26
Epigenetic regulation of Tbx18 gene expression during endochondral bone formation
Haraguchi, R., Kitazawa, R., & Kitazawa, S. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-2028-0 · Cited by 19
A role for GATA-6 in vertebrate chondrogenesis
Alexandrovich, A., Qureishi, A., Coudert, A. E., Zhang, L., Grigoriadis, A. E., Shah, A. M., Brewer, A. C., & Pizzey, J. A. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2007.12.001 · Cited by 20
Transcriptional heterochrony in talpid mole autopods
Bickelmann, C., Mitgutsch, C., Richardson, M. K., Jiménez, R., Bakker, M., & Sánchez-Villagra, M. R. (2012) · EvoDevo · doi:10.1186/2041-9139-3-16 · Cited by 19
The apical ectodermal ridge of the mouse model of ectrodactylyDlx5;Dlx6−/−shows altered stratification and cell polarity, which are restored by exogenous Wnt5a ligand
Conte, D., Garaffo, G., Iacono, N. L., Mantero, S., Piccolo, S., Cordenonsi, M., Pérez-Morga, D. L., Orecchia, V., Poli, V., & Merlo, G. R. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv514 · Cited by 19
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A transition from SoxB1 to SoxE transcription factors is essential for progression from pluripotent blastula cells to neural crest cells
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Dysregulated BMP signaling through ACVR1 impairs digit joint development in fibrodysplasia ossificans progressiva (FOP)
Towler, O. W., Peck, S. H., Kaplan, F. S., & Shore, E. M. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.11.004 · Cited by 19
Retinoid Agonists in the Targeting of Heterotopic Ossification
Pignolo, R. J., & Pacifici, M. (2021) · Cells · doi:10.3390/cells10113245 · Cited by 19
Post-transcriptional regulation in cranial neural crest cells expands developmental potential
Keuls, R. A., Oh, Y. S., Patel, I., & Parchem, R. J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212578120 · Cited by 25
The Response of Articular Chondrocytes to Type II Collagen–Au Nanocomposites
Hsu, S., Yen, H., & Tsai, C. (2007) · Artificial Organs · doi:10.1111/j.1525-1594.2007.00482.x · Cited by 19
Molecular Biology in Orthopaedics: The Advent of Molecular Orthopaedics
Evans, C. H. (2005) · Journal of Bone and Joint Surgery · doi:10.2106/jbjs.e.00019 · Cited by 19
Effect of Melatonin on the Proliferation and Differentiation of Chondrocytes from Rat Vertebral Body Growth Plate In Vitro
Zhong, Z., Li, T., Xu, Z., Meng, T., Zeng, J., Zheng, S., Ye, W.-B., Wu, Q., & Chen, J.-T. (2013) · International Journal of Medical Sciences · doi:10.7150/ijms.5645 · Cited by 19
Functional constraints on SoxE proteins in neural crest development: The importance of differential expression for evolution of protein activity
Lee, E. M., Yuan, T., Ballim, R. D., Nguyen, K., Kelsh, R. N., Medeiros, D. M., & McCauley, D. W. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.07.022 · Cited by 20
Remodelling of human bone on the chorioallantoic membrane of the chicken egg:De novobone formation and resorption
Moreno-Jiménez, I., Lanham, S., Kanczler, J. M., Hulsart‐Billström, G., Evans, N. D., & Oreffo, R. O. C. (2018) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2711 · Cited by 19
Frontal nasal prominence expression driven by Tcfap2a relies on a conserved binding site for STAT proteins
Donner, A. L., & Williams, T. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20722 · Cited by 19
Two-point rapid palatal expansion: an alternate approach to traditional treatment.
Schneidman, E., Wilson, S., & Erkis, R. (1990) · PubMed · Cited by 19

Authors: Akiyama, H., Chaboissier, M.-C., Martin, J. F., Schedl, A., & de Crombrugghe, B.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
ORCID: Akiyama, Haruhiko
Chaboissier, Marie-Christine
Martin, James F.
Schedl, Andreas
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2002-11-01
Volume: 16
Issue: 21
Pages: 2813-2828
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.1017802
PMC: PMC187468
OpenAlex: W2150134228
Semantic Scholar: e65963187a4e29b254fc91c0e5fb771b639a3d8d
Cited by: 1,721
References: 47
Citations by year: 2026: 52 · 2025: 47 · 2024: 54 · 2023: 73 · 2022: 83 · 2021: 92 · 2020: 98 · 2019: 81 · 2018: 79 · 2017: 82 · 2016: 79 · 2015: 82 · 2014: 89 · 2013: 89 · 2012: 81
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Genes & Development (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
Newcastle University ePrints (Newcastle Univesity)
Funders: March of Dimes Foundation
Volkswagen Foundation
National Institutes of Health (CA-16 672, AR42919)
National Cancer Institute (CA-16672, P30CA016672)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (P01AR042919)
National Institute of Dental and Craniofacial Research (R01DE013509, R29DE012324)
Topics: Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone Tumor Diagnosis and Treatments
Keywords: SOX9, chondrogenic differentiation, chondrogenesis, SOX5, SOX6, Runx2, chondrodysplasia, mesenchymal condensation, apoptosis, Indian hedgehog, Patched1, parathyroid hormone-related protein, chondrocyte hypertrophy, joint formation, limb development, osteogenic differentiation, Cre-loxP conditional knockout
MeSH terms: Animals, Cell Differentiation, Cell Division, DNA-Binding Proteins, High Mobility Group Proteins, Mutation, Nuclear Proteins, Transcription Factors, Signal Transduction, Gene Expression Regulation, Developmental, Chondrocytes, Mice, SOXD Transcription Factors, SOX9 Transcription Factor

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The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6

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