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Research Article | Open Access

Argonaute (AGO) proteins play an essential role in mediating BMP9-induced osteogenic signaling in mesenchymal stem cells (MSCs)

Yukun Maoa,b,, Na Nib,c, Linjuan Huangb,d, Jiaming Fanb,c, Hao Wangb,c, Fang Heb,c, Qing Liub,e, Deyao Shib,f, Kai Fua,b, Mikhail Pakvasab,g, William Wagstaffb, Andrew Blake Tuckerb,g, Connie Chenb, Russell R. Reidb,g, Rex C. Haydonb, Sherwin H. Hob, Michael J. Leeb, Tong-Chuan Heb,g, Jian Yangh, Le Shenb,g, Lin Caia( ), Hue H. Luub( )
Departments of Spine Surgery and Musculoskeletal Tumor, and Neurosurgery, Zhongnan Hospital of Wuhan University, Wuhan, Hubei Province, 430072, PR China
Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, IL 60637, USA
Ministry of Education Key Laboratory of Diagnostic Medicine, and the School of Laboratory Medicine, Chongqing Medical University, Chongqing, 400016, PR China
Departments of Nephrology, and Obstetrics and Gynecology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, 400016, PR China
Department of Spine Surgery, Second Xiangya Hospital, Central South University, Changsha, Hunan Province, 410011, PR China
Department of Orthopaedic Surgery, Union Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei Province, 430022, PR China
Section of Plastic Surgery and Laboratory of Craniofacial Biology and Development, and Section of Surgical Research, Department of Surgery, The University of Chicago Medical Center, Chicago, IL 60637, USA
Department of Biomedical Engineering, Materials Research Institute, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA

Peer review under responsibility of Chongqing Medical University.

Show Author Information

Abstract

As multipotent progenitor cells, mesenchymal stem cells (MSCs) can renew themselves and give rise to multiple lineages including osteoblastic, chondrogenic and adipogenic lineages. It's previously shown that BMP9 is the most potent BMP and induces osteogenic and adipogenic differentiation of MSCs. However, the molecular mechanism through which BMP9 regulates MSC differentiation remains poorly understood. Emerging evidence indicates that noncoding RNAs, especially microRNAs, may play important roles in regulating MSC differentiation and bone formation. As highly conserved RNA binding proteins, Argonaute (AGO) proteins are essential components of the multi-protein RNA-induced silencing complexes (RISCs), which are critical for small RNA biogenesis. Here, we investigate possible roles of AGO proteins in BMP9-induced lineage-specific differentiation of MSCs. We first found that BMP9 up-regulated the expression of Ago1, Ago2 and Ago3 in MSCs. By engineering multiplex siRNA vectors that express multiple siRNAs targeting individual Ago genes or all four Ago genes, we found that silencing individual Ago expression led to a decrease in BMP9-induced early osteogenic marker alkaline phosphatase (ALP) activity in MSCs. Furthermore, we demonstrated that simultaneously silencing all four Ago genes significantly diminished BMP9-induced osteogenic and adipogenic differentiation of MSCs and matrix mineralization, and ectopic bone formation. Collectively, our findings strongly indicate that AGO proteins and associated small RNA biogenesis pathway play an essential role in mediating BMP9-induced osteogenic differentiation of MSCs.

Keywords

Mesenchymal stem cellsBone formationBMP9Argonaute (AGO) proteinsLineage-specific differentiationmiRNA biogenesisOsteogenic signaling

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Genes & Diseases
Volume 8 Issue 6,
November 2021
Pages 918-930
DOI: 10.1016/j.gendis.2021.04.004
Cite this article:
Mao Y, Ni N, Huang L, et al. Argonaute (AGO) proteins play an essential role in mediating BMP9-induced osteogenic signaling in mesenchymal stem cells (MSCs). Genes & Diseases, 2021, 8(6): 918-930. https://doi.org/10.1016/j.gendis.2021.04.004

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Received: 09 March 2021
Revised: 04 April 2021
Accepted: 16 April 2021
Published: 13 May 2021
© 2021, Chongqing Medical University. Production and hosting by Elsevier B.V.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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