A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2

Zhang, Ying; Xie, Rong-lin; Croce, Carlo M.; Stein, Janet L.; Lian, Jane B.; van Wijnen, Andre J.; Stein, Gary S.

doi:10.1073/pnas.1018493108

Cited by 423Bone Metabolism and DiseasesMicroRNA in disease regulationDevelopmental Biology and Gene Regulation

A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2

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Zhang, Ying, Xie, Rong-lin, Croce, Carlo M., Stein, Janet L., Lian, Jane B., van Wijnen, Andre J., Stein, Gary S.·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1018493108PMC PMC3116419

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Abstract

Lineage progression in osteoblasts and chondrocytes is stringently controlled by the cell-fate–determining transcription factor Runx2. In this study, we directly addressed whether microRNAs (miRNAs) can control the osteogenic activity of Runx2 and affect osteoblast maturation. A panel of 11 Runx2-targeting miRNAs (miR-23a, miR-30c, miR-34c, miR-133a, miR-135a, miR-137, miR-204, miR-205, miR-217, miR-218, and miR-338) is expressed in a lineage-related pattern in mesenchymal cell types. During both osteogenic and chondrogenic differentiation, these miRNAs, in general, are inversely expressed relative to Runx2. Based on 3′UTR luciferase reporter, immunoblot, and mRNA stability assays, each miRNA directly attenuates Runx2 protein accumulation. Runx2-targeting miRNAs differentially inhibit Runx2 protein expression in osteoblasts and chondrocytes and display different efficacies. Thus, cellular context contributes to miRNA-mediated regulation of Runx2. All Runx2-targeting miRNAs (except miR-218) significantly impede osteoblast differentiation, and their effects can be reversed by the corresponding anti-miRNAs. These findings demonstrate that osteoblastogenesis is limited by an elaborate network of functionally tested miRNAs that directly target the osteogenic master regulator Runx2.

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In vitro experiments demonstrated that miR-23a can control the progression of osteoblast and chondrocyte lineages and inhibit osteogenic differentiation by targeting Runx2 and Satb2 in mice.
“The experiments in vitro have demonstrated that it can control the progression of osteoblast and chondrocyte lineages and inhibit osteogenic differentiation by targeting the transcription factors Runx2 and Satb2 in mice.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [109]
The Results (Runx2-Targeting miRNAs Inhibit Osteogenic Differentiation; page unavailable) show that miR-23a inhibits osteogenic differentiation in cultured osteoblasts. They also report that miR-23a reduces Runx2 protein in chondrocytes, but not in osteoblasts. The paper does not demonstrate that miR-23a controls chondrocyte lineage progression or that its inhibition of osteogenic differentiation occurs by targeting both Runx2 and SATB2; SATB2 appears in the title of a cited study. (LLM, conf=0.90)
Experimental — accuracy not yet measured
miR-23a is highly expressed in osteoblasts, chondrocytes, and fibroblast cell lines.
“miR-23a is highly expressed in osteoblasts, chondrocytes, and fibroblast cell lines.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [109]
There existed no notable variance in the number of osteoblasts and osteoclasts between miR-23 transgenic and wild-type mice, along with their activity in bone.
“there existed no notable variance in the number of osteoblasts and osteoclasts between miR-23 transgenic and wild-type mice, along with their activity in the bone.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [109]
The Results section reports miR-23a effects on osteoblast cell cultures, including reduced ALP activity, but does not compare miR-23 transgenic mice with wild-type mice. Searches for that comparison and for osteoclast numbers or activity found no passage addressing the claim. (LLM, conf=0.75)
Experimental — accuracy not yet measured
In connexin43-deficient rats, osteocytes show increased RANKL/OPG ratio.
“In addition, an increase in RANKL/OPG ratio expressed by osteocytes was also observed in connexin43-deficient rats, suggesting that a disruption in cell-to-cell communication between osteocytes may induce the release of local proosteoclastogenic cytokines [33, 196, 197].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [33]
Disruption in cell-to-cell communication between osteocytes may induce release of local proosteoclastogenic cytokines.
“In addition, an increase in RANKL/OPG ratio expressed by osteocytes was also observed in connexin43-deficient rats, suggesting that a disruption in cell-to-cell communication between osteocytes may induce the release of local proosteoclastogenic cytokines [33, 196, 197].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [33]

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Self-citation
MiR-690, a Runx2-targeted miRNA, regulates osteogenic differentiation of C2C12 myogenic progenitor cells by targeting NF-kappaB p65
Yu, S.-H., Geng, Q., Pan, Q., Liu, Z., Ding, S., Xiang, Q., Sun, F., Wang, C., Huang, Y., & Hong, A. (2016) · Cell & Bioscience · doi:10.1186/s13578-016-0073-y · Cited by 35 · see citing works
Computational identification of miRNAs that modulate the differentiation of mesenchymal stem cells to osteoblasts
Seenprachawong, K., Nuchnoi, P., Nantasenamat, C., Prachayasittikul, V., & Supokawej, A. (2016) · PeerJ · doi:10.7717/peerj.1976 · Cited by 15 · see citing works
A Runx2/miR-3960/miR-2861 Regulatory Feedback Loop during Mouse Osteoblast Differentiation
Hu, R., Liu, W., Li, H., Yang, L., Chen, C., Xia, Z., Guo, L., Xie, H., Zhou, H., Wu, X., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.176099 · Cited by 226 · see citing works

Authors: Zhang, Y., Xie, R.-L., Croce, C. M., Stein, J. L., Lian, J. B., van Wijnen, A. J., & Stein, G. S.
Affiliations: University of Massachusetts Chan Medical School (US)
The Ohio State University (US)
Department of Cell Biology and Cancer Center, University of Massachusetts Medical School, Worcester, MA 01655; and
ORCID: Zhang, Ying
Croce, Carlo M.
Stein, Janet L.
Lian, Jane B.
Stein, Gary S.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-05-31
Volume: 108
Issue: 24
Pages: 9863-9868
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1018493108
PMC: PMC3116419
OpenAlex: W2028928108
Cited by: 423
References: 48
Citations by year: 2026: 7 · 2025: 10 · 2024: 19 · 2023: 20 · 2022: 15 · 2021: 27 · 2020: 36 · 2019: 42 · 2018: 32 · 2017: 36 · 2016: 35 · 2015: 46 · 2014: 24 · 2013: 42 · 2012: 27
FWCI: 12.71
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
Funders: National Institutes of Health
National Cancer Institute (P01CA129242, P01CA082834)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR049069, R01AR039588)
National Institute of Dental and Craniofacial Research (R37DE012528)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: microRNA, Runx2, osteogenic differentiation, osteoblasts, chondrogenic differentiation, mesenchymal lineage, microRNA target regulation, miR-218, transcription factor regulation
MeSH terms: Animals, Base Sequence, Cell Differentiation, Cell Line, Gene Expression Regulation, Luciferases, Osteoblasts, Osteogenesis, RNA, Messenger, Blotting, Western, Cell Lineage, Chondrocytes, 3' Untranslated Regions, Gene Expression Profiling, RNA Stability, MicroRNAs, NIH 3T3 Cells, Core Binding Factor Alpha 1 Subunit, Mice

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A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2

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