Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues

The long noncoding RNA (lncR) ANRIL in the human genome is an established genetic risk factor for atherosclerosis, periodontitis, diabetes, and cancer. However, the regulatory role of lncR-ANRIL in bone and adipose tissue metabolism remains unclear. To elucidate the function of lncRNA ANRIL in a mou...

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Main Authors: Yao Liu, Zoe Xiaofang Zhu, Elissa K. Zboinski, Wei Qiu, Junxiang Lian, Shibo Liu, Thomas E. Van Dyke, Hans E. Johansson, Qisheng Tu, En Luo, Jake Jinkun Chen
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:RNA Biology
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Online Access:https://www.tandfonline.com/doi/10.1080/15476286.2023.2268489
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author Yao Liu
Zoe Xiaofang Zhu
Elissa K. Zboinski
Wei Qiu
Junxiang Lian
Shibo Liu
Thomas E. Van Dyke
Hans E. Johansson
Qisheng Tu
En Luo
Jake Jinkun Chen
author_facet Yao Liu
Zoe Xiaofang Zhu
Elissa K. Zboinski
Wei Qiu
Junxiang Lian
Shibo Liu
Thomas E. Van Dyke
Hans E. Johansson
Qisheng Tu
En Luo
Jake Jinkun Chen
author_sort Yao Liu
collection DOAJ
description The long noncoding RNA (lncR) ANRIL in the human genome is an established genetic risk factor for atherosclerosis, periodontitis, diabetes, and cancer. However, the regulatory role of lncR-ANRIL in bone and adipose tissue metabolism remains unclear. To elucidate the function of lncRNA ANRIL in a mouse model, we investigated its ortholog, AK148321 (referred to as lncR-APDC), located on chr4 of the mouse genome, which is hypothesized to have similar biological functions to ANRIL. We initially revealed that lncR-APDC in mouse bone marrow cells (BMSCs) and lncR-ANRIL in human osteoblasts (hFOBs) are both increased during early osteogenesis. Subsequently, we examined the osteogenesis, adipogenesis, osteoclastogenesis function with lncR-APDC deletion/overexpression cell models. In vivo, we compared the phenotypic differences in bone and adipose tissue between APDC-KO and wild-type mice. Our findings demonstrated that lncR-APDC deficiency impaired osteogenesis while promoting adipogenesis and osteoclastogenesis. Conversely, the overexpression of lncR-APDC stimulated osteogenesis, but impaired adipogenesis and osteoclastogenesis. Furthermore, KDM6B was downregulated with lncR-APDC deficiency and upregulated with overexpression. Through binding-site analysis, we identified miR-99a as a potential target of lncR-APDC. The results suggest that lncR-APDC exerts its osteogenic function via miR-99a/KDM6B/Hox pathways. Additionally, osteoclasto-osteogenic imbalance was mediated by lncR-APDC through MAPK/p38 and TLR4/MyD88 activation. These findings highlight the pivotal role of lncR-APDC as a key regulator in bone and fat tissue metabolism. It shows potential therapeutic for addressing imbalances in osteogenesis, adipogenesis, and osteoclastogenesis.
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spelling doaj-art-322a8458f00b4c4aa6e3e80bddbaab092025-08-20T03:12:47ZengTaylor & Francis GroupRNA Biology1547-62861555-85842023-12-0120183684610.1080/15476286.2023.2268489Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissuesYao Liu0Zoe Xiaofang Zhu1Elissa K. Zboinski2Wei Qiu3Junxiang Lian4Shibo Liu5Thomas E. Van Dyke6Hans E. Johansson7Qisheng Tu8En Luo9Jake Jinkun Chen10State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, ChinaDivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USADivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USADivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USADivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USAState Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, ChinaCenter for Clinical and Translational Research, The Forsyth Institute, Cambridge, MA, USAResearch and Development, LGC Biosearch Technologies, Petaluma, CA, USADivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USAState Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, ChinaDivision of Oral Biology, Tufts University School of Dental Medicine, Boston, MA, USAThe long noncoding RNA (lncR) ANRIL in the human genome is an established genetic risk factor for atherosclerosis, periodontitis, diabetes, and cancer. However, the regulatory role of lncR-ANRIL in bone and adipose tissue metabolism remains unclear. To elucidate the function of lncRNA ANRIL in a mouse model, we investigated its ortholog, AK148321 (referred to as lncR-APDC), located on chr4 of the mouse genome, which is hypothesized to have similar biological functions to ANRIL. We initially revealed that lncR-APDC in mouse bone marrow cells (BMSCs) and lncR-ANRIL in human osteoblasts (hFOBs) are both increased during early osteogenesis. Subsequently, we examined the osteogenesis, adipogenesis, osteoclastogenesis function with lncR-APDC deletion/overexpression cell models. In vivo, we compared the phenotypic differences in bone and adipose tissue between APDC-KO and wild-type mice. Our findings demonstrated that lncR-APDC deficiency impaired osteogenesis while promoting adipogenesis and osteoclastogenesis. Conversely, the overexpression of lncR-APDC stimulated osteogenesis, but impaired adipogenesis and osteoclastogenesis. Furthermore, KDM6B was downregulated with lncR-APDC deficiency and upregulated with overexpression. Through binding-site analysis, we identified miR-99a as a potential target of lncR-APDC. The results suggest that lncR-APDC exerts its osteogenic function via miR-99a/KDM6B/Hox pathways. Additionally, osteoclasto-osteogenic imbalance was mediated by lncR-APDC through MAPK/p38 and TLR4/MyD88 activation. These findings highlight the pivotal role of lncR-APDC as a key regulator in bone and fat tissue metabolism. It shows potential therapeutic for addressing imbalances in osteogenesis, adipogenesis, and osteoclastogenesis.https://www.tandfonline.com/doi/10.1080/15476286.2023.2268489Long non-coding RNAgenetic animal modelsepigeneticsbone metabolismmolecular pathways-remodellingcells of bones-osteoblasts & osteoclasts & BMSCs
spellingShingle Yao Liu
Zoe Xiaofang Zhu
Elissa K. Zboinski
Wei Qiu
Junxiang Lian
Shibo Liu
Thomas E. Van Dyke
Hans E. Johansson
Qisheng Tu
En Luo
Jake Jinkun Chen
Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
RNA Biology
Long non-coding RNA
genetic animal models
epigenetics
bone metabolism
molecular pathways-remodelling
cells of bones-osteoblasts & osteoclasts & BMSCs
title Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
title_full Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
title_fullStr Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
title_full_unstemmed Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
title_short Long non-coding RNA APDC plays important regulatory roles in metabolism of bone and adipose tissues
title_sort long non coding rna apdc plays important regulatory roles in metabolism of bone and adipose tissues
topic Long non-coding RNA
genetic animal models
epigenetics
bone metabolism
molecular pathways-remodelling
cells of bones-osteoblasts & osteoclasts & BMSCs
url https://www.tandfonline.com/doi/10.1080/15476286.2023.2268489
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