SOX9 is dispensable for the initiation of epigenetic remodeling and the activation of marker genes at the onset of chondrogenesis

Liu, Chia-Feng; Angelozzi, Marco; Haseeb, Abdul; Lefebvre, Véronique

doi:10.1242/dev.164459

Cited by 73Osteoarthritis Treatment and MechanismsGenomics and Chromatin DynamicsDevelopmental Biology and Gene Regulation

SOX9 is dispensable for the initiation of epigenetic remodeling and the activation of marker genes at the onset of chondrogenesis

Open access

Liu, Chia-Feng, Angelozzi, Marco, Haseeb, Abdul, Lefebvre, Véronique·2018·Development

DOI 10.1242/dev.164459PMC PMC6078338

Open this paper in CoChat — free account

Abstract

SOX9 controls cell lineage fate and differentiation in major biological processes. It is known as a potent transcriptional activator of differentiation-specific genes, but its earliest targets and its contribution to priming chromatin for gene activation remain unknown. Here, we address this knowledge gap using chondrogenesis as a model system. By profiling the whole transcriptome and the whole epigenome of wild-type and Sox9 -deficient mouse embryo limb buds, we uncover multiple structural and regulatory genes, including Fam101a , Myh14 , Sema3c and Sema3d , as specific markers of precartilaginous condensation, and we provide evidence of their direct transactivation by SOX9. Intriguingly, we find that SOX9 helps remove epigenetic signatures of transcriptional repression and establish active-promoter and active-enhancer marks at precartilage- and cartilage-specific loci, but is not absolutely required to initiate these changes and activate transcription. Altogether, these findings widen our current knowledge of SOX9 targets in early chondrogenesis and call for new studies to identify the pioneer and transactivating factors that act upstream of or along with SOX9 to prompt chromatin remodeling and specific gene activation at the onset of chondrogenesis and other processes.

Integrity signals

Registry

Crossref · 10.1242/dev.164459

Cites

90 of 90 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

In chondrogenic systems, SOX9 can activate enhancers but may not be required for initiation of chromatin changes.
“In chondrogenic systems, SOX9 can activate enhancers (19), but may not be required for the initiation of chromatin changes (20).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [20]
SOX9 may not be crucial for epigenetic changes during chondrogenesis.
“For instance, SOX9 may not be crucial for epigenetic changes during chondrogenesis (20).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [20]

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 · see citing works
The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of <i>Sox5</i> and <i>Sox6</i>
Akiyama, H., Chaboissier, M.-C., Martin, J. F., Schedl, A., & de Crombrugghe, B. (2002) · Genes & Development · doi:10.1101/gad.1017802 · Cited by 1,721 · see citing works
SOX9 directly regulates the type-ll collagen gene
Bell, D. M., Leung, K. K. H., Wheatley, S. C., Ng, L. J., Zhou, S. X., Ling, K., Sham, M. H., Koopman, P. A., Tam, P., & Cheah, K. S. E. (1997) · Nature Genetics · doi:10.1038/ng0697-174 · Cited by 933 · see citing works
Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
Soufi, A., Garcia, M. F., Jaroszewicz, A., Osman, N., Pellegrini, M., & Zaret, K. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.017 · Cited by 780 · cited 1× · see citing works
“Concerted actions have been shown in pluripotent embryonic stem cells for the four master regulators, SOX2, POU5F1 (also known as OCT4), KLF4 and MYC (Soufi et al., 2015), and several transcription factor types have been shown to serve as pioneers in other cells.”
Background
Nosology and classification of genetic skeletal disorders: 2010 revision
Warman, M. L., Cormier‐Daire, V., Hall, C. M., Krakow, D., Lachman, R. S., Merrer, M. F. L., Mortier, G. R., Mundlos, S., Nishimura, G., Rimoin, D. L., et al. (2011) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33909 · Cited by 711 · see citing works
Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development
Ivković, S., Yoon, B. S., Popoff, S. N., Safadi, F. F., Libuda, D. E., Stephenson, R. C., Daluiski, A., & Lyons, K. M. (2003) · Development · doi:10.1242/dev.00505 · Cited by 705 · see citing works
The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration
Hernández‐Hernández, J. M., García-González, E. G., Brun, C. E., & Rudnicki, M. A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.11.010 · Cited by 669 · see citing works
SOX9 Binds DNA, Activates Transcription, and Coexpresses with Type II Collagen during Chondrogenesis in the Mouse
Ng, L. J., Wheatley, S. C., Muscat, G. E. O., Conway-Campbell, J., Bowles, J., Wright, E. M., Bell, D. M., Tam, P., Cheah, K. S. E., & Koopman, P. A. (1997) · Developmental Biology · doi:10.1006/dbio.1996.8487 · Cited by 667 · see citing works
The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos
Wright, E. M., Hargrave, M. R., Christiansen, J. H., Cooper, L. T., Kun, J., Evans, T. M., Gangadharan, U., Greenfield, A., & Koopman, P. A. (1995) · Nature Genetics · doi:10.1038/ng0195-15 · Cited by 661 · see citing works
MicroRNA-140 plays dual roles in both cartilage development and homeostasis
Miyaki, S., Sato, T., Inoue, A., Otsuki, S., Ito, Y., Yokoyama, S., Kato, Y., Takemoto, F., Nakasa, T., Yamashita, S., et al. (2010) · Genes & Development · doi:10.1101/gad.1915510 · Cited by 660 · see citing works
Bone development
Berendsen, A. D., & Olsen, B. R. (2015) · Bone · doi:10.1016/j.bone.2015.04.035 · Cited by 560 · see citing works
A pathway to bone: signaling molecules and transcription factors involved in chondrocyte development and maturation
Kozhemyakina, E. A., Lassar, A. B., & Zelzer, E. (2015) · Development · doi:10.1242/dev.105536 · Cited by 547 · see citing works
Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization
Bi, W., Huang, W., Whitworth, D. J., Deng, J. M., Zhang, Z., Behringer, R. R., & Crombrugghe, B. D. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111092198 · Cited by 541 · see citing works
Therapeutic Strategies for Tendon Healing Based on Novel Biomaterials, Factors and Cells
Groß, G., & Hoffmann, A. (2013) · Pathobiology · doi:10.1159/000347059 · Cited by 469 · see citing works
Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds
Zúñiga, A., Haramis, A.-P. G., McMahon, A. P., & Zeller, R. (1999) · Nature · doi:10.1038/44157 · Cited by 456 · see citing works
Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells
O’Gorman, S., Dagenais, N., Qian, M., & Marchuk, Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14602 · Cited by 436 · see citing works
Recruitment and maintenance of tendon progenitors by TGFβ signaling are essential for tendon formation
Pryce, B. A., Watson, S. S., Murchison, N. D., Staverosky, J. A., Dünker, N., & Schweitzer, R. (2009) · Development · doi:10.1242/dev.027342 · Cited by 421 · see citing works
A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs
Andrey, G., Montavon, T., Mascrez, B., Gonzãlez, F., Noordermeer, D., Leleu, M., Trono, D., Spitz, F., & Duboule, D. (2013) · Science · doi:10.1126/science.1234167 · Cited by 409 · see citing works
Fox transcription factors: from development to disease
Golson, M. L., & Kaestner, K. H. (2016) · Development · doi:10.1242/dev.112672 · Cited by 406 · see citing works
The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus.
Kume, T., Deng, K.-Y., Winfrey, V., Gould, D., Walter, M. A., & Hogan, B. (1998) · Cell · doi:10.1016/s0092-8674(00)81204-0 · Cited by 397 · see citing works
Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice
Adam, R. C., Yang, H., Rockowitz, S., Larsen, S. B., Nikolova, M., Oristian, D., Polak, L., Kadaja, M., Asare, A., Zheng, D., et al. (2015) · Nature · doi:10.1038/nature14289 · Cited by 376 · see citing works
Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro.
Mackie, E. J., Thesleff, I., & Chiquet‐Ehrismann, R. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.6.2569 · Cited by 363 · see citing works
Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis
Oberlender, S. A., & Tuan, R. S. (1994) · Development · doi:10.1242/dev.120.1.177 · Cited by 363 · see citing works
The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage
Ikeda, T., Kamekura, S., Mabuchi, A., Kou, I., Seki, S., Takato, T., Nakamura, K., Kawaguchi, H., Ikegawa, S., & Chung, U. (2004) · Arthritis & Rheumatism · doi:10.1002/art.20611 · Cited by 357 · see citing works
Zp3–cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line
Lewandoski, M. B., Wassarman, K. M., & Martin, G. R. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00059-5 · Cited by 354 · see citing works
SOX9 and the many facets of its regulation in the chondrocyte lineage
Lefebvre, V., & Dvir‐Ginzberg, M. (2016) · Connective Tissue Research · doi:10.1080/03008207.2016.1183667 · Cited by 349 · see citing works
Self-citation
The versatile functions of Sox9 in development, stem cells, and human diseases
Jo, A., Denduluri, S., Zhang, B., Wang, Z., Yin, L., Yan, Z., Kang, R., Shi, L. L., Mok, J., Lee, M. J., et al. (2014) · Genes and Diseases · doi:10.1016/j.gendis.2014.09.004 · Cited by 340 · see citing works
Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption
Feiner, L., Webber, A. L., Brown, C. B., Lu, M. M., Li, J., Feinstein, P. G., Mombaerts, P., Epstein, J. A., & Raper, J. A. (2001) · Development · doi:10.1242/dev.128.16.3061 · Cited by 326 · see citing works
Regulation of Endothelial Cell Differentiation and Specification
Marcelo, K. L., Goldie, L. C., & Hirschi, K. K. (2013) · Circulation Research · doi:10.1161/circresaha.113.300506 · Cited by 308 · see citing works
Sequentially acting Sox transcription factors in neural lineage developmentPreprint
Bergsland, M., Ramsköld, D., Zaouter, C., Klum, S., Sandberg, R., & Muhr, J. (2011) · Genes & Development · doi:10.1101/gad.176008.111 · Cited by 305 · see citing works
Cell fate control by pioneer transcription factors
Iwafuchi-Doi, M., & Zaret, K. S. (2016) · Development · doi:10.1242/dev.133900 · Cited by 304 · see citing works
Bone Ridge Patterning during Musculoskeletal Assembly Is Mediated through SCX Regulation of Bmp4 at the Tendon-Skeleton Junction
Blitz, E., Viukov, S. V., Sharir, A., Shwartz, Y., Galloway, J. L., Pryce, B. A., Johnson, R. L., Tabin, C. J., Schweitzer, R., & Zelzer, E. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.10.010 · Cited by 297 · see citing works
BMPs Are Required at Two Steps of Limb Chondrogenesis: Formation of Prechondrogenic Condensations and Their Differentiation into Chondrocytes
Pizette, S., & Niswander, L. A. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9610 · Cited by 296 · see citing works
The transcription factors SOX9 and SOX5/SOX6 cooperate genome-wide through super-enhancers to drive chondrogenesis
Liu, C.-F., & Lefebvre, V. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv688 · Cited by 287 · see citing works
Self-citation
Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa
Akiyama, H., Chaboissier, M.-C., Behringer, R. R., Rowitch, D. H., Schedl, A., Epstein, J. A., & de Crombrugghe, B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401711101 · Cited by 265 · see citing works
Muscle Contraction Is Necessary to Maintain Joint Progenitor Cell Fate
Kahn, J., Shwartz, Y., Blitz, E., Krief, S., Sharir, A., Breitel, D., Rattenbach, R., Relaix, F., Maire, P., Rountree, R. B., et al. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.04.013 · Cited by 259 · see citing works
Kinetics of tamoxifen‐regulated Cre activity in mice using a cartilage‐specific CreERT to assay temporal activity windows along the proximodistal limb skeleton
Nakamura, E., Nguyen, M., & Mackem, S. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20892 · Cited by 250 · see citing works
Mechanochemical Control of Mesenchymal Condensation and Embryonic Tooth Organ Formation
Mammoto, T., Mammoto, A., Torisawa, Y., Tat, T., Gibbs, A. D., Derda, R., Mannix, R. J., de Bruijn, M., Yung, C. W., Huh, D., et al. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.07.006 · Cited by 229 · see citing works
Transcriptional Co-activators CREB-binding Protein and p300 Regulate Chondrocyte-specific Gene Expression via Association with Sox9
Tsuda, M., Takahashi, S., Takahashi, Y. K., & Asahara, H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303471200 · Cited by 207 · see citing works
Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum
Kawanami, A., Matsushita, T., Chan, Y. Y., & Murakami, S. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.06.059 · Cited by 192 · see citing works
Distinct Transcriptional Programs Underlie Sox9 Regulation of the Mammalian Chondrocyte
Ohba, S., He, X., Hojo, H., & McMahon, A. P. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.06.013 · Cited by 179 · see citing works
Visualization of Cartilage Formation: Insight into Cellular Properties of Skeletal Progenitors and Chondrodysplasia Syndromes
Barna, M., & Niswander, L. A. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.04.016 · Cited by 178 · see citing works
Idiopathic Weight Reduction in Mice Deficient in the High-Mobility-Group Transcription Factor Sox8
Sock, E., Schmidt, K., Hermanns-Borgmeyer, I., Bösl, M. R., & Wegner, M. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.20.6951-6959.2001 · Cited by 176 · see citing works
Transcriptional control of chondrocyte specification and differentiation
Liu, C.-F., Samsa, W. E., Zhou, G. D., & Lefèbvre, V. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.10.004 · Cited by 167 · see citing works
Self-citation
Sox9 and p300 Cooperatively Regulate Chromatin-mediated Transcription
Furumatsu, T., Tsuda, M., Yoshida, K., Taniguchi, N., Ito, T., Hashimoto, M., Ito, T., & Asahara, H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502409200 · Cited by 164 · see citing works
PAVIS: a tool for Peak Annotation and Visualization
Huang, W., Loganantharaj, R., Schroeder, B., Fargo, D. C., & Li, L. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt520 · Cited by 157 · see citing works
SOX E genes: SOX9 and SOX8 in mammalian testis development
Barrionuevo, F. J., & Scherer, G. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.07.015 · Cited by 155 · see citing works
Tendon development and musculoskeletal assembly: emerging roles for the extracellular matrix
Subramanian, A., & Schilling, T. F. (2015) · Development · doi:10.1242/dev.114777 · Cited by 155 · see citing works
Role of Class 3 Semaphorins and Their Receptors in Tumor Growth and Angiogenesis
Gaur, P., Bielenberg, D. R., Samuel, S., Bose, D., Zhou, Y., Gray, M. J., Dallas, N. A., Fan, F., Xia, L., Lu, J., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1810 · Cited by 151 · see citing works
The Expression Pattern of the Chick Homeobox Gene gMHox Suggests a Role in Patterning of the Limbs and Face and in Compartmentalization of Somites
Kuratani, S., Martin, J. F., Wawersik, S., Lilly, B., Gregor Eichele, C., & Olson, E. N. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1037 · Cited by 134 · see citing works
An 18-Base-Pair Sequence in the Mouse Proα1(II) Collagen Gene Is Sufficient for Expression in Cartilage and Binds Nuclear Proteins That Are Selectively Expressed in Chondrocytes
Lefebvre, V., Zhou, G. D., Mukhopadhyay, K., Smith, C. N., Zhang, Z., Eberspaecher, H., Zhou, X., Sinha, S., Maity, S. N., & Crombrugghe, B. D. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4512 · Cited by 131 · see citing works
Self-citation
Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis
Iwamoto, M., Tamamura, Y., Koyama, E., Komori, T., Takeshita, N., Williams, J. A., Nakamura, T., Enomoto‐Iwamoto, M., & Pacifici, M. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.037 · Cited by 118 · see citing works
The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation ofVegf
Eshkar-Oren, I., Viukov, S. V., Salameh, S., Krief, S., Oh, C., Akiyama, H., Gerber, H., Ferrara, N., & Zelzer, E. (2009) · Development · doi:10.1242/dev.034199 · Cited by 115 · see citing works
Molecular basis for the genome engagement by Sox proteins
Hou, L., Srivastava, Y., & Jauch, R. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.08.005 · Cited by 113 · see citing works
Musculoskeletal integration at the wrist underlies modular development of limb tendons
Huang, A. H., Riordan, T. J., Pryce, B. A., Weibel, J. L., Watson, S. S., Long, F., Lefebvre, V., Harfe, B. D., Stadler, H. S., Akiyama, H., et al. (2015) · Development · doi:10.1242/dev.122374 · Cited by 110 · see citing works
Self-citation
Conditional inactivation of Sox9: A mouse model for campomelic dysplasia
Kist, R., Schrewe, H., Balling, R., & Scherer, G. (2002) · genesis · doi:10.1002/gene.10050 · Cited by 109 · see citing works
Arid5b facilitates chondrogenesis by recruiting the histone demethylase Phf2 to Sox9-regulated genes
Hata, K., Takashima, R., Amano, K., Ono, K., Nakanishi, M., Yoshida, M., Wakabayashi, M., Matsuda, A., Maeda, Y., Suzuki, Y., et al. (2013) · Nature Communications · doi:10.1038/ncomms3850 · Cited by 108 · see citing works
The Distribution of the Matricellular Protein Thrombospondin 2 in Tissues of Embryonic and Adult Mice
Kyriakides, T. R., Zhu, Y.-H., Yang, Z., & BORNSTEIN, P. K. (1998) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215549804600904 · Cited by 97 · see citing works
From CNS stem cells to neurons and glia: Sox for everyone
Reiprich, S., & Wegner, M. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1909-6 · Cited by 83 · see citing works
Sema3d controls collective endothelial cell migration by distinct mechanisms via Nrp1 and PlxnD1
Hamm, M. J., Kirchmaier, B. C., & Herzog, W. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201603100 · Cited by 82 · see citing works
Semaphorin 3d signaling defects are associated with anomalous pulmonary venous connections
Degenhardt, K. R., Singh, M. K., Aghajanian, H. K., Massera, D., Wang, Q., Li, J., Li, L., Choi, C., Yzaguirre, A. D., Francey, L. J., et al. (2013) · Nature Medicine · doi:10.1038/nm.3185 · Cited by 81 · see citing works
Central and Peripheral Axon Branches from One Neuron Are Guided Differentially by Semaphorin3D and Transient Axonal Glycoprotein-1
Liu, Y., & Halloran, M. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2710-05.2005 · Cited by 80 · see citing works
RefilinB (FAM101B) targets FilaminA to organize perinuclear actin networks and regulates nuclear shape
Gay, O., Gilquin, B., Nakamura, F., Jenkins, Z. A., McCartney, R., Krakow, D., Deshière, A., Assard, N., Hartwig, J. H., Robertson, S. P., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104211108 · Cited by 75 · see citing works
The SOX9 upstream region prone to chromosomal aberrations causing campomelic dysplasia contains multiple cartilage enhancers
Yao, B., Wang, Q. K., Liu, C.-F., Bhattaram, P., Li, W., Mead, T. J., Crish, J. F., & Lefebvre, V. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv426 · Cited by 73 · see citing works
Self-citation
SOX9: A genomic view of tissue specific expression and action.
Symon, A., & Harley, V. (2017) · International Journal of Biochemistry and Cell Biology · doi:10.1016/j.biocel.2017.03.005 · Cited by 72 · see citing works
Transforming Growth Factor-β-Induced KDM4B Promotes Chondrogenic Differentiation of Human Mesenchymal Stem Cells
Lee, H., Yu, B., Deng, P., Wang, C., & Hong, C. (2015) · Stem Cells · doi:10.1002/stem.2231 · Cited by 70 · see citing works
Foxp1/2/4 regulate endochondral ossification as a suppresser complex
Zhao, H., Zhou, W., Yao, Z., Wan, Y., Cao, J., Zhang, L., Zhao, J., Li, H., Zhou, R., Li, B., et al. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.12.007 · Cited by 69 · see citing works
Chromatin scanning by dynamic binding of pioneer factors
Zaret, K. S., Lerner, J., & Iwafuchi-Doi, M. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.024 · Cited by 68 · see citing works
SOXC proteins amplify canonical WNT signaling to secure nonchondrocytic fates in skeletogenesis
Bhattaram, P., Penzo‐Méndez, A., Kato, K. H., Bandyopadhyay, K., Gadi, A., Taketo, M. M., & Lefebvre, V. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201405098 · Cited by 68 · see citing works
Self-citation
SOX9 modulates the expression of key transcription factors required for heart valve development
Garside, V. C., Cullum, R., Alder, O., Lu, D. Y., Vander Werff, R., Bilenky, M., Zhao, Y., Jones, S. J. M., Marra, M. A., Underhill, T. M., et al. (2015) · Development · doi:10.1242/dev.125252 · Cited by 65 · see citing works
Dhrs3 Protein Attenuates Retinoic Acid Signaling and Is Required for Early Embryonic Patterning
Kam, R. K. T., Shi, W., Chan, S. O., Chen, Y., Xu, G., Lau, C. B., Fung, K., Chan, W. Y., & Zhao, H. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.514984 · Cited by 60 · see citing works
Osteoarthritis
Martel-Pelletier, J., Barr, A., Cicuttini, F., Conaghan, P., Cooper, C., Goldring, M. B., Goldring, S. R., Jones, G., Teichtahl, A., & Pelletier, J. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.72 · Cited by 49 · see citing works
Active gelatinase B is identified by histozymography in the cartilage resorption sites of developing long bones
Lee, E. R., Murphy, G., Elalfy, M., Davoli, M. A., Lamplugh, L., Docherty, A., & Leblond, C. P. (1999) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199907)215:3 · Cited by 47 · see citing works
Semaphorin 3d promotes cell proliferation and neural crest cell development downstream of TCF in the zebrafish hindbrain
Berndt, J. D., & Halloran, M. C. (2006) · Development · doi:10.1242/dev.02583 · Cited by 44 · see citing works
Coordination of limb development by crosstalk among axial patterning pathways
Delgado, I., & Torres, M. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.03.006 · Cited by 44 · see citing works
H3K27me3 demethylases regulate in vitro chondrogenesis and chondrocyte activity in osteoarthritis
Yapp, C., Carr, A. J., Price, A. J., Oppermann, U. C. T., & Snelling, S. J. B. (2016) · Arthritis Research & Therapy · doi:10.1186/s13075-016-1053-7 · Cited by 43 · see citing works
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling
Ray, P., & Chapman, S. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134702 · Cited by 42 · see citing works
The dimerization domain of SOX9 is required for transcription activation of a chondrocyte-specific chromatin DNA template
Coustry, F., Oh, C.-D., Hattori, T., Maity, S. N., de Crombrugghe, B., & Yasuda, H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq417 · Cited by 37 · see citing works
ATX-LPA1 axis contributes to proliferation of chondrocytes by regulating fibronectin assembly leading to proper cartilage formation
Nishioka, T., Arima, N., Kano, K., Hama, K., Itai, E., Yukiura, H., Kise, R., Inoue, A., Kim, S. H., Solnica‐Krezel, L., et al. (2016) · Scientific Reports · doi:10.1038/srep23433 · Cited by 33 · see citing works
Analysis of Chondrogenesis Using Micromass Cultures of Limb Mesenchyme
Underhill, T. M., Dranse, H. J., & Hoffman, L. (2014) · Methods in molecular biology · doi:10.1007/978-1-62703-989-5_19 · Cited by 30 · see citing works
SOX9 Protein Induces a Chondrogenic Phenotype of Mesangial Cells and Contributes to Advanced Diabetic Nephropathy
Kishi, S., Abe, H., Akiyama, H., Tominaga, T., Murakami, T., Mima, A., Nagai, K., Kishi, F., Matsuura, M., Matsubara, T., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.244541 · Cited by 30 · see citing works
abLIM3 is a novel component of adherens junctions with actin-binding activity
Matsuda, M., Yamashita, J. K., Tsukita, S., & Furuse, M. (2010) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2010.07.009 · Cited by 29 · see citing works
Regionalized Twist1 activity in the forelimb bud drives the morphogenesis of the proximal and preaxial skeleton
Loebel, D. A. F., Hor, A. C. C., Bildsoe, H., Jones, V. J., Chen, Y., Behringer, R. R., & Tam, P. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.11.020 · Cited by 25 · see citing works
Filamin-interacting proteins, Cfm1 and Cfm2, are essential for the formation of cartilaginous skeletal elements
Mizuhashi, K., Kanamoto, T., Moriishi, T., Muranishi, Y., Miyazaki, T., Terada, K., Omori, Y., Ito, M., Komori, T., & Furukawa, T. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu007 · Cited by 22 · see citing works
Characterization of Kidney and Skeleton Phenotypes of Mice Double Heterozygous for Foxc1 and Foxc2
Motojima, M., Tanimoto, S., Ohtsuka, M., Matsusaka, T., Kume, T., & Abe, K. (2016) · Cells Tissues Organs · doi:10.1159/000445027 · Cited by 20 · see citing works
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 19 · see citing works
Modelling condensation and the initiation of chondrogenesis in chick wing bud mesenchymal cells levitated in an ultrasound trap
Edwards, G., Coakley, W. T., Ralphs, J. R., & Archer, C. (2010) · European Cells and Materials · doi:10.22203/ecm.v019a01 · Cited by 15 · see citing works
Curcumin inhibits cellular condensation and alters microfilament organization during chondrogenic differentiation of limb bud mesenchymal cells
Kim, D.-K., Kim, S. J., Kang, S.-S., & Jin, E. (2009) · Experimental & Molecular Medicine · doi:10.3858/emm.2009.41.9.072 · Cited by 13 · see citing works
H3K27me3 demethylases regulate in vitro chondrogenesis and chondrocyte activity in osteoarthritis
Yapp, C., Carr, A. J., Price, A. J., Oppermann, U. C. T., & Snelling, S. J. B. (2016) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2016.01.357 · Cited by 11 · see citing works
Biologists abandon Popper at their peril
(2000) · doi:10.1002/(sici)1521-1878(200002)22:2

Flagged first, then by citations

Sorted by citations

SOX9 in cartilage development and disease
Lefebvre, V., Angelozzi, M., & Haseeb, A. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.07.008 · Cited by 226 · see citing works
Self-citation
SOX9 keeps growth plates and articular cartilage healthy by inhibiting chondrocyte dedifferentiation/osteoblastic redifferentiation
Haseeb, A., Kc, R., Angelozzi, M., de Charleroy, C., Rux, D. R., Tower, R. J., Yao, L., da Silva, R. P., Pacifici, M., Qin, L., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019152118 · Cited by 241 · see citing works
Self-citation
Making and shaping endochondral and intramembranous bones
Galea, G. L., Zein, M. R., Allen, S., & Francis‐West, P. H. (2020) · Developmental Dynamics · doi:10.1002/dvdy.278 · Cited by 188 · see citing works
Histone lactylation couples cellular metabolism with developmental gene regulatory networks
Merkuri, F., Rothstein, M., & Simões-Costa, M. (2024) · Nature Communications · doi:10.1038/s41467-023-44121-1 · Cited by 171 · see citing works
Exosomes derived from platelet-rich plasma administration in site mediate cartilage protection in subtalar osteoarthritis
Zhang, Y., Wang, X., Chen, J., Qian, D., Gao, P., Qin, T., Jiang, T., Yi, J., Xu, T., Huang, Y., et al. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01245-8 · Cited by 135 · see citing works
Roles and regulation of SOX transcription factors in skeletogenesis
Lefebvre, V. (2019) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.01.007 · Cited by 101 · see citing works
Self-citation
Cellular and Engineered Organoids for Cardiovascular Models
Thomas, D., Choi, S., Alamana, C., Parker, K. K., & Wu, J. C. (2022) · Circulation Research · doi:10.1161/circresaha.122.320305 · Cited by 95 · see citing works
SOX9 in organogenesis: shared and unique transcriptional functions
Ming, Z., Vining, B., Bagheri-Fam, S., & Harley, V. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04543-4 · Cited by 91 · see citing works
The Roles of the Hippo-YAP signalling pathway in Cartilage and Osteoarthritis.
Sun, K., Guo, J.-C., Guo, Z., Hou, L., Liu, H., Hou, Y., He, J., Guo, F.-J., & Ye, Y.-P. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102015 · Cited by 82 · see citing works
Transcriptional networks controlling stromal cell differentiation
Rauch, A., & Mandrup, S. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00357-7 · Cited by 57 · see citing works
The biological function of BMAL1 in skeleton development and disorders
Chen, G., Tang, Q., Yu, S., Xie, Y., Sun, J., Li, S., & Chen, L. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117636 · Cited by 54 · see citing works
Vascular smooth muscle–specific YAP/TAZ deletion triggers aneurysm development in mouse aorta
Arévalo Martínez, M., Ritsvall, O., Bastrup, J. A., Celik, S., Jakobsson, G., Daoud, F., Winqvist, C., Aspberg, A., Rippe, C., Maegdefessel, L., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.170845 · Cited by 51 · see citing works
Estrogen-related receptors: novel potential regulators of osteoarthritis pathogenesis
Tang, J., Liu, T., Wen, X., Zhou, Z., Yan, J., Gao, J.-P., & Zuo, J. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00270-x · Cited by 50 · see citing works
An Anti‐Inflammatory Composition of Boswellia serrata Resin Extracts Alleviates Pain and Protects Cartilage in Monoiodoacetate‐Induced Osteoarthritis in Rats
Alluri, K. V., Kundimi, S., Sengupta, K., Golakoti, T., & Kilari, E. K. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/7381625 · Cited by 40 · see citing works
Alternate Roles of Sox Transcription Factors beyond Transcription Initiation
Zhang, Y., & Hou, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115949 · Cited by 40 · see citing works
Foxc1 establishes enhancer accessibility for craniofacial cartilage differentiation
Xu, P., Yu, H. V., Tseng, K.-C., Flath, M., Fábián, P., Segil, N., & Crump, J. G. (2021) · eLife · doi:10.7554/elife.63595 · Cited by 39 · see citing works
Evaluation of a Cell-Free Collagen Type I-Based Scaffold for Articular Cartilage Regeneration in an Orthotopic Rat Model
Szychlinska, M. A., Calabrese, G., Ravalli, S., Dolcimascolo, A., Castrogiovanni, P., Fabbi, C., Puglisi, C., Lauretta, G., Rosa, M. D., Castorina, A., et al. (2020) · Materials · doi:10.3390/ma13102369 · Cited by 38 · see citing works
The local and circulating SOX9 as a potential biomarker for the diagnosis of primary bone cancer
Hosseini, A., Mirzaei, A., Salimi, V., Jamshidi, K., Babaheidarian, P., Fallah, S., Rampisheh, Z., Khademian, N., Abdolvahabi, Z., Bahrabadi, M., et al. (2020) · Journal of bone oncology · doi:10.1016/j.jbo.2020.100300 · Cited by 37 · see citing works
Semaphorin 3C as a Therapeutic Target in Prostate and Other Cancers
Hui, D. H. F., Tam, K. J., Jiao, I. Z. F., & Ong, C. J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030774 · Cited by 39 · see citing works
Chondro-inductive hyaluronic acid/chitosan coacervate-based scaffolds for cartilage tissue engineering
Acar, Ö. K., Bedir, S., Kayitmazer, A. B., & Köse, G. T. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.07.176 · Cited by 36 · see citing works
SOX9 reprograms endothelial cells by altering the chromatin landscape
Fuglerud, B. M., Drissler, S., Lotto, J., Stephan, T. L., Thakur, A., Cullum, R., & Hoodless, P. A. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac652 · Cited by 35 · see citing works
“For instance, SOX9 may not be crucial for epigenetic changes during chondrogenesis (20).”
Background
SOX9 and SOX10 control fluid homeostasis in the inner ear for hearing through independent and cooperative mechanisms
Szeto, I. Y. Y., Chu, D. K. H., Chen, P., Chu, K. C., Au, T. Y. K., Leung, K. K. H., Huang, Y., Wynn, S. L., Mak, A. C. Y., Chan, Y., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122121119 · Cited by 34 · see citing works
Pioneer factors in development and cancer
Sunkel, B. D., & Stanton, B. Z. (2021) · iScience · doi:10.1016/j.isci.2021.103132 · Cited by 31 · see citing works
Patterning of cartilaginous condensations in the developing facial skeleton
Paudel, S., Gjorcheska, S., Bump, P. A., & Barske, L. A. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.03.010 · Cited by 29 · see citing works
Comparative analysis demonstrates cell type-specific conservation of SOX9 targets between mouse and chicken
Yamashita, S., Kataoka, K., Yamamoto, H., Kato, T., Hara, S., Yamaguchi, K., Renard-Guillet, C., Katou, Y., Shirahige, K., Ochi, H., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-48979-4 · Cited by 26 · see citing works
USP7 regulates the proliferation and differentiation of ATDC5 cells through the Sox9-PTHrP-PTH1R axis
Dong, X., Xu, X., Yang, C., Luo, Y., Wu, Y., & Wang, J. (2020) · Bone · doi:10.1016/j.bone.2020.115714 · Cited by 24 · see citing works
Histone chip-Seq identifies differential enhancer usage during chondrogenesis as critical for defining cell-type specificity
Cheung, K., Barter, M. J., Falk, J., Proctor, C. J., Reynard, L. N., & Young, D. A. (2020) · The FASEB Journal · doi:10.1096/fj.201902061rr · Cited by 23 · see citing works
Global analysis of histone modifications and long-range chromatin interactions revealed the differential cistrome changes and novel transcriptional players in human dilated cardiomyopathy
Liu, C.-F., Abnousi, A., Bazeley, P., Ni, Y., Morley, M., Moravec, C. S., Hu, M., & Tang, W. H. W. (2020) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2020.06.001 · Cited by 19 · see citing works
Self-citation
Combining segmental bulk- and single-cell RNA-sequencing to define the chondrocyte gene expression signature in the murine knee joint
Sunkara, V., Heinz, G. A., Heinrich, F., Durek, P., Mobasheri, A., Mashreghi, M., & Lang, A. (2021) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2021.03.007 · Cited by 22 · see citing works
The methylation status of the embryonic limb skeletal progenitors determines their cell fate in chicken
Sánchez–Fernández, C., Lorda-Diez, C. I., Hurlé, J. M., & Montero, J. A. (2020) · Communications Biology · doi:10.1038/s42003-020-1012-3 · Cited by 22 · see citing works
Dmrt2 promotes transition of endochondral bone formation by linking Sox9 and Runx2
Ono, K., Hata, K., Nakamura, E., Ishihara, S., Kobayashi, S., Nakanishi, M., Yoshida, M., Takahata, Y., Murakami, T., Takenoshita, S., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01848-1 · Cited by 22 · see citing works
UHRF genes regulate programmed interdigital tissue regression and chondrogenesis in the embryonic limb
Sánchez–Fernández, C., Lorda-Diez, C. I., García‐Porrero, J. A., Montero, J. A., & Hurlé, J. M. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1575-4 · Cited by 20 · see citing works
An Updated View on Temporomandibular Joint Degeneration: Insights from the Cell Subsets of Mandibular Condylar Cartilage
Xu, M., Zhang, X., & He, Y. (2022) · Stem Cells and Development · doi:10.1089/scd.2021.0324 · Cited by 20 · see citing works
TET1 Directs Chondrogenic Differentiation by Regulating SOX9 Dependent Activation of Col2a1 and Acan In Vitro
Smeriglio, P., Grandi, F. C., Taylor, S. E. B., Zalc, A., & Bhutani, N. (2020) · JBMR Plus · doi:10.1002/jbm4.10383 · Cited by 20 · see citing works
Single-Cell Atlas Reveals Fatty Acid Metabolites Regulate the Functional Heterogeneity of Mesenchymal Stem Cells
Xie, J., Lou, Q., Zeng, Y., Liang, Y., Xie, S., Xu, Q., Yuan, L., Wang, J., Jiang, L., Mou, L., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.653308 · Cited by 18 · see citing works
Sox9 Determines Translational Capacity During Early Chondrogenic Differentiation of ATDC5 Cells by Regulating Expression of Ribosome Biogenesis Factors and Ribosomal Proteins
Caron, M. M. J., Eveque, M., Cillero‐Pastor, B., Heeren, R. M. A., Housmans, B., Derks, K., Cremers, A., Peffers, M. J., van Rhijn, L. W., van den Akker, G., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.686096 · Cited by 18 · see citing works
Loss of Foxc1 and Foxc2 function in chondroprogenitor cells disrupts endochondral ossification
Almubarak, A., Lavy, R., Srnic, N., Hu, Y., Maripuri, D. P., Kume, T., & Berry, F. B. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101020 · Cited by 18 · see citing works
Sox9-Increased miR-322-5p Facilitates BMP2-Induced Chondrogenic Differentiation by Targeting Smad7 in Mesenchymal Stem Cells
Zeng, Y., Du, C., Xiao, P., Lei, Y., Zhao, P., Zhu, Z., Gao, S., Chen, B., Cheng, S., Huang, W., et al. (2021) · Stem Cells International · doi:10.1155/2021/9778207 · Cited by 18 · see citing works
Gli1+ Osteogenic Progenitors Contribute to Condylar Development and Fracture Repair
Chen, S., Lin, L., Lei, J., He, Y., & Zhang, Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.819689 · Cited by 18 · see citing works
Chromatin profiling identifies chondrocyte-specific Sox9 enhancers important for skeletal development
Ichiyama-Kobayashi, S., Hata, K., Wakamori, K., Takahata, Y., Murakami, T., Yamanaka, H., Takano, H., Yao, R., Uzawa, N., & Nishimura, R. (2024) · JCI Insight · doi:10.1172/jci.insight.175486 · Cited by 12 · see citing works
Hypomorphic and dominant-negative impact of truncated SOX9 dysregulates Hedgehog–Wnt signaling, causing campomelia
Au, T. Y. K., Yip, R. K. H., Wynn, S. L., Tan, T. Y., Fu, X., Geng, Y., Szeto, I. Y. Y., Niu, B., Yip, K. Y.-L., Cheung, M. C. H., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2208623119 · Cited by 14 · see citing works
Insights into Gene Regulatory Networks in Chondrocytes
Hojo, H., & Ohba, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20246324 · Cited by 12 · see citing works
All-trans-retinoic acid suppresses rat embryo hindlimb bud mesenchymal chondrogenesis by modulating HoxD9 expression
Hong, Q., Li, X., Xie, P., & Du, S. (2021) · Bioengineered · doi:10.1080/21655979.2021.1940613 · Cited by 10 · see citing works
Limb Mesoderm and Head Ectomesenchyme Both Express a Core Transcriptional Program During Chondrocyte Differentiation
Gómez‐Picos, P., Ovens, K. L., & Eames, B. F. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.876825 · Cited by 8 · see citing works
Genome-scale actions of master regulators directing skeletal development
Ohba, S. (2021) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2021.10.001 · Cited by 7 · see citing works
Development, characterization and research of efficacy on in vitro cell culture of glucosamine carrying hyaluronic acid nanoparticles
Şahin, Ş., Bilgiç, E., Salimi, K., Tuncel, A., Karaosmanoğlu, B., Taşkıran, E. Z., Korkusuz, P., & Korkusuz, F. (2019) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2019.05.007 · Cited by 7 · see citing works
A Transcriptome Sequencing Study on Genome‐Wide Gene Expression Differences of 3D Cultured Chondrocytes in Hydrogel Scaffolds with Different Gel Density
Zhang, W., Xia, Y., Yang, L., Yang, W., Dong, Z., Wang, D., & Fan, C. (2020) · Macromolecular Bioscience · doi:10.1002/mabi.202000028 · Cited by 6 · see citing works
Human Adult Fibroblast‐like Synoviocytes and Articular Chondrocytes Exhibit Prominent Overlap in Their Transcriptomic Signatures
Jones, K., Angelozzi, M., Gangishetti, U., Haseeb, A., de Charleroy, C., Lefebvre, V., & Bhattaram, P. (2021) · ACR Open Rheumatology · doi:10.1002/acr2.11255 · Cited by 5 · see citing works
Self-citation
Systems Biology Approach to the Origin of the Tetrapod Limb
Onimaru, K., & Marcon, L. (2021) · Springer eBooks · doi:10.1007/978-3-030-71737-7_5 · Cited by 5 · see citing works
Molecular cloning, characterization, mRNA expression changes and nucleocytoplasmic shuttling during kidney embryonic development of SOX9 in Alligator sinensis
Wang, L., Cai, R., Liu, F., Lv, Y., Zhang, Y., Duan, S., Izaz, A., Zhou, J., Wang, H., Duan, R., et al. (2020) · Gene · doi:10.1016/j.gene.2020.144334 · Cited by 4 · see citing works
Self-assembled porous microgel scaffold with layered drug release for efficient repair of osteochondral microstructure
Chi, M., Zheng, X., Zhang, F., Xuan, Z., Tang, X., Zhang, J., & Lu, L. (2025) · Biomaterials Advances · doi:10.1016/j.bioadv.2025.214402 · Cited by 3 · see citing works
Chromatin accessibility in MSC chondrogenesis, adult hip cartilage chondrocytes and osteoarthritis
Barter, M. J., Soul, J., Cheung, K., Falk, J., Putri, K., Farrier, A. J., Panagiotopoulos, A., Deehan, D. J., Reynard, L. N., & Young, D. A. (2026) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2025.12.015 · Cited by 3 · see citing works
Influence of DNA-methylation at multiple stages of limb chondrogenesis
Pérez-Maldonado, M. A., González-González, X. A., Chimal‐Monroy, J., & Marín‐Llera, J. C. (2024) · Developmental Biology · doi:10.1016/j.ydbio.2024.04.006 · Cited by 3 · see citing works
Effects of Berberine on the Chondrogenic Differentiation of Embryonic Limb Skeletal Progenitors
Duarte‐Olivenza, C., Montero, J. A., & Lorda-Diez, C. I. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s324292 · Cited by 3 · see citing works
SOXs: Master architects of development and versatile emulators of oncogenesis
Saloni, Sachan, M., Rahul, Verma, R. S., & Patel, G. K. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189295 · Cited by 2 · see citing works
Early determination of the dorsal-ventral axis in endochondral ossification in mice
Wu, S., Matsumoto, H., Morita, J., Yamabe, M., Noguchi, A., Ohba, S., Ono, N., & Matsushita, Y. (2025) · Journal of Bone and Mineral Research · doi:10.1093/jbmr/zjaf086 · Cited by 2 · see citing works
Combining segmental bulk- and single-cell RNA-sequencing to define the chondrocyte gene expression signature in the murine knee jointPreprint
Sunkara, V., Heinz, G., Heinrich, F., Durek, P., Mobasheri, A., Mashreghi, M., & Lang, A. (2020) · bioRxiv · doi:10.1101/2020.06.13.148056 · Cited by 17 · see citing works
SOX9 acts as a dynamic pioneer factor inducing stable changes in the chromatin landscape to reprogram endothelial cellsPreprint
Fuglerud, B. M., Drissler, S., Lotto, J., Stephan, T. L., Thakur, A., Cullum, R. L., & Hoodless, P. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.11.293993 · Cited by 2 · see citing works
Runx2 Regulates Chromatin Accessibility to Direct Skeletal Cell ProgramsPreprint
Hojo, H., Saito, T., He, X., Guo, Q., Onodera, S., Azuma, T., Koebis, M., Nakao, K., Aiba, A., Seki, M., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3988393 · Cited by 2 · see citing works
Estrogen-related receptor alpha: A novel perspective on skeletal, muscular, and vascular systems
Wang, L., Wang, Z. X., CAO, N.-P., CHEN, B., HUANG, C.-J., Yang, L., & TIAN, Y. (2024) · Biocell · doi:10.32604/biocell.2023.045349 · Cited by 1 · see citing works
Stage- and cluster-specific regulation of chondrogenic gene programs by Sox9 in mouse embryonic limb buds
Masayasu, S. E. G. A., Uchida, Y., Chiba, T., Matsushima, T., Kita, K., Naoyuki, M., & Asahara, H. (2026) · iScience · doi:10.1016/j.isci.2026.115074 · Cited by 1 · see citing works
4D multimodal wound healing atlas reveals organ-level controls of repair phase transitionsPreprint
Cheong, J. C., Deursen, S. V., Amador, D., Hiner, S., & Woappi, Y. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.15.699736 · Cited by 1 · see citing works
The Role of Collagen Scaffold and Stromal Vascular Fraction on Healing Process in Growth Plate Injury (SOX9 and Histological Examination)
Sananta, P., Imadudin, M. I., Rahaditya, I. G. M. O., Putera, M. A., Andarini, S., Kalsum, U., & Dradjat, R. S. (2020) · Open Access Macedonian Journal of Medical Sciences · doi:10.3889/oamjms.2020.3925
Chondrocytes derived from pluripotent stem cells
Xu, M., O’Brien, A., & Barry, F. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823884-4.00010-9
Deciphering osteoarthritis disease using multimodal mass spectrometry methodologies
Eveque, M. (2021) · doi:10.26481/dis.20210226me
Methylphenidate Promotes Premature Growth Plate Closure: In Vitro Evidence
Pazos‐Pérez, A., Piñeiro-Ramil, M., Franco‐Trepat, E., Guillán‐Fresco, M., López-López, V., Mora, A. J., Alonso‐Pérez, A., & Gómez, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24044175
Foxc1 and Foxc2 function in osteochondral progenitors for the progression through chondrocyte hypertrophy and mineralization of the primary ossification centerPreprint
Almubarak, A., Zhang, Q., Zhang, C., Lassar, A. B., Kume, T., & Berry, F. B. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.26.538325
Influence of global DNA-methylation on chondrogenic fate during digit developmentPreprint
Chimal‐Monroy, J., Pérez-Maldonado, M. A., González-González, X. A., & Marín‐Llera, J. C. (2023) · Research Square · doi:10.21203/rs.3.rs-3425542/v1
Influence of Global Dna-Methylation on Chondrogenic Fate During Digit DevelopmentPreprint
Pérez-Maldonado, M. A., González-González, X. A., Chimal‐Monroy, J., & Marín‐Llera, J. C. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4626591
circNR3C2 promotes chondrogenic differentiation and cartilage repair of human adipose‐derived stem cells via the hsa‐ miR ‐647/ SOX9 pathway
Hou, D., Wang, H., Guo, H., Luo, D., Zheng, X., & Luo, S. (2025) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12561
Adult stem cells in regenerative medicine of skeletal system
Alipour, M., Taboas, J. M., Saeinasab, M., & Sefat, F. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-34152-6.00014-7
Rôle des chondrocytes hypertrophiques dans le remodelage pathologique de la jonction ostéochondrale au cours de l'arthrose : implication du SDF-1 dans l'angiogenèse
Toillon, I. (2021) · theses.fr (ABES) · doi:10.70675/0521c11az1a2bz423az9521zad6dc6c2df87
A spatial and single-cell transcriptomic atlas of the embryonic synovial joint and its explant modelPreprint
Onggo, S. E. S., Yea, J.-H., Young, K. K., Chen, K., Cho, H., Ning, Z., & Cahan, P. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.10.19.760178

SOX9 in cartilage development and disease
Lefebvre, V., Angelozzi, M., & Haseeb, A. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.07.008 · Cited by 226 · see citing works
Self-citation
Unraveling the transcriptional regulatory machinery in chondrogenesis
Akiyama, H., & Lefèbvre, V. (2011) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-011-0273-9 · Cited by 178 · see citing works
Toward understanding S0X9 function in chondrocyte differentiation
Lefrebvre, V., & Crombrugghe, B. D. (1998) · Matrix Biology · doi:10.1016/s0945-053x(98)90065-8 · Cited by 252 · see citing works
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 · see citing works
Histone acetylation influences the activity of Sox9-related transcriptional complex.
Furumatsu, T., & Asahara, H. (2010) · PubMed · doi:10.18926/amo/41320 · Cited by 58 · see citing works

Authors: Liu, C.-F., Angelozzi, M., Haseeb, A., & Lefebvre, V.
Affiliations: Cleveland Clinic (US)
ORCID: Angelozzi, Marco
Haseeb, Abdul
Lefebvre, Véronique
Venue: Development
Publisher: The Company of Biologists
Published: 2018-07-15
Volume: 145
Issue: 14
ISSN: 0950-1991 (ISSN-L)
1477-9129
DOI: 10.1242/dev.164459
PMC: PMC6078338
OpenAlex: W2884620368
Cited by: 73
References: 90
Citations by year: 2026: 4 · 2025: 5 · 2024: 4 · 2023: 6 · 2022: 10 · 2021: 22 · 2020: 15 · 2019: 7
FWCI: 9.39
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.biologists.com/user-licence-1-1/ (vor, 184 d)
Locations: Development (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR46249, AR68308)
Topics: Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: SOX9, chondrogenesis, epigenetic remodeling, chromatin remodeling, transcriptional activation, transcriptional repression, pioneer transcription factors, limb bud, MYH14, SEMA3C, SEMA3D
MeSH terms: Animals, Embryo, Mammalian, Mice, Transgenic, Microfilament Proteins, Nerve Tissue Proteins, Gene Expression Regulation, Developmental, Limb Buds, Myosin Heavy Chains, Chondrogenesis, Myosin Type II, Chromatin Assembly and Disassembly, Epigenesis, Genetic, Mice, SOX9 Transcription Factor

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

SOX9 is dispensable for the initiation of epigenetic remodeling and the activation of marker genes at the onset of chondrogenesis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks