Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells

Background. Hedgehog (Hh) signaling is essential for osteoblast differentiation of mesenchymal progenitors during endochondral bone formation. However, the critical role of Hh signaling during adult bone remodeling remains to be elucidated. Methods. A Smoothened (SMO) antagonist/Hedgehog inhibitor,...

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Main Authors: Nihal AlMuraikhi, Nuha Almasoud, Sarah Binhamdan, Ghaydaa Younis, Dalia Ali, Muthurangan Manikandan, Radhakrishnan Vishnubalaji, Muhammad Atteya, Abdulaziz Siyal, Musaad Alfayez, Abdullah Aldahmash, Moustapha Kassem, Nehad M. Alajez
Format: Article
Language:English
Published: Wiley 2019-01-01
Series:Stem Cells International
Online Access:http://dx.doi.org/10.1155/2019/3435901
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author Nihal AlMuraikhi
Nuha Almasoud
Sarah Binhamdan
Ghaydaa Younis
Dalia Ali
Muthurangan Manikandan
Radhakrishnan Vishnubalaji
Muhammad Atteya
Abdulaziz Siyal
Musaad Alfayez
Abdullah Aldahmash
Moustapha Kassem
Nehad M. Alajez
author_facet Nihal AlMuraikhi
Nuha Almasoud
Sarah Binhamdan
Ghaydaa Younis
Dalia Ali
Muthurangan Manikandan
Radhakrishnan Vishnubalaji
Muhammad Atteya
Abdulaziz Siyal
Musaad Alfayez
Abdullah Aldahmash
Moustapha Kassem
Nehad M. Alajez
author_sort Nihal AlMuraikhi
collection DOAJ
description Background. Hedgehog (Hh) signaling is essential for osteoblast differentiation of mesenchymal progenitors during endochondral bone formation. However, the critical role of Hh signaling during adult bone remodeling remains to be elucidated. Methods. A Smoothened (SMO) antagonist/Hedgehog inhibitor, BMS-833923, identified during a functional screening of a stem cell signaling small molecule library, was investigated for its effects on the osteoblast differentiation of human skeletal (mesenchymal) stem cells (hMSC). Alkaline phosphatase (ALP) activity and Alizarin red staining were employed as markers for osteoblast differentiation and in vitro mineralization capacity, respectively. Global gene expression profiling was performed using the Agilent® microarray platform. Effects on in vivo ectopic bone formation were assessed by implanting hMSC mixed with hydroxyapatite-tricalcium phosphate granules subcutaneously in 8-week-old female nude mice, and the amount of bone formed was assessed using quantitative histology. Results. BMS-833923, a SMO antagonist/Hedgehog inhibitor, exhibited significant inhibitory effects on osteoblast differentiation of hMSCs reflected by decreased ALP activity, in vitro mineralization, and downregulation of osteoblast-related gene expression. Similarly, we observed decreased in vivo ectopic bone formation. Global gene expression profiling of BMS-833923-treated compared to vehicle-treated control cells, identified 348 upregulated and 540 downregulated genes with significant effects on multiple signaling pathways, including GPCR, endochondral ossification, RANK-RANKL, insulin, TNF alpha, IL6, and inflammatory response. Further bioinformatic analysis employing Ingenuity Pathway Analysis revealed significant enrichment in BMS-833923-treated cells for a number of functional categories and networks involved in connective and skeletal tissue development and disorders, e.g., NFκB and STAT signaling. Conclusions. We identified SMO/Hedgehog antagonist (BMS-833923) as a powerful inhibitor of osteoblastic differentiation of hMSC that may be useful as a therapeutic option for treating conditions associated with high heterotopic bone formation and mineralization.
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spelling doaj-art-1f652ce2bc424c3288a264907e42aba62025-08-20T03:54:42ZengWileyStem Cells International1687-966X1687-96782019-01-01201910.1155/2019/34359013435901Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem CellsNihal AlMuraikhi0Nuha Almasoud1Sarah Binhamdan2Ghaydaa Younis3Dalia Ali4Muthurangan Manikandan5Radhakrishnan Vishnubalaji6Muhammad Atteya7Abdulaziz Siyal8Musaad Alfayez9Abdullah Aldahmash10Moustapha Kassem11Nehad M. Alajez12Stem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaMolecular Endocrinology Unit (KMEB), Department of Endocrinology, University Hospital of Odense and University of Southern Denmark, Odense, DenmarkStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaCancer Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Qatar Foundation (QF), PO Box 34110, Doha, QatarStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaStem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, Riyadh 11461, Saudi ArabiaCancer Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Qatar Foundation (QF), PO Box 34110, Doha, QatarBackground. Hedgehog (Hh) signaling is essential for osteoblast differentiation of mesenchymal progenitors during endochondral bone formation. However, the critical role of Hh signaling during adult bone remodeling remains to be elucidated. Methods. A Smoothened (SMO) antagonist/Hedgehog inhibitor, BMS-833923, identified during a functional screening of a stem cell signaling small molecule library, was investigated for its effects on the osteoblast differentiation of human skeletal (mesenchymal) stem cells (hMSC). Alkaline phosphatase (ALP) activity and Alizarin red staining were employed as markers for osteoblast differentiation and in vitro mineralization capacity, respectively. Global gene expression profiling was performed using the Agilent® microarray platform. Effects on in vivo ectopic bone formation were assessed by implanting hMSC mixed with hydroxyapatite-tricalcium phosphate granules subcutaneously in 8-week-old female nude mice, and the amount of bone formed was assessed using quantitative histology. Results. BMS-833923, a SMO antagonist/Hedgehog inhibitor, exhibited significant inhibitory effects on osteoblast differentiation of hMSCs reflected by decreased ALP activity, in vitro mineralization, and downregulation of osteoblast-related gene expression. Similarly, we observed decreased in vivo ectopic bone formation. Global gene expression profiling of BMS-833923-treated compared to vehicle-treated control cells, identified 348 upregulated and 540 downregulated genes with significant effects on multiple signaling pathways, including GPCR, endochondral ossification, RANK-RANKL, insulin, TNF alpha, IL6, and inflammatory response. Further bioinformatic analysis employing Ingenuity Pathway Analysis revealed significant enrichment in BMS-833923-treated cells for a number of functional categories and networks involved in connective and skeletal tissue development and disorders, e.g., NFκB and STAT signaling. Conclusions. We identified SMO/Hedgehog antagonist (BMS-833923) as a powerful inhibitor of osteoblastic differentiation of hMSC that may be useful as a therapeutic option for treating conditions associated with high heterotopic bone formation and mineralization.http://dx.doi.org/10.1155/2019/3435901
spellingShingle Nihal AlMuraikhi
Nuha Almasoud
Sarah Binhamdan
Ghaydaa Younis
Dalia Ali
Muthurangan Manikandan
Radhakrishnan Vishnubalaji
Muhammad Atteya
Abdulaziz Siyal
Musaad Alfayez
Abdullah Aldahmash
Moustapha Kassem
Nehad M. Alajez
Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
Stem Cells International
title Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
title_full Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
title_fullStr Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
title_full_unstemmed Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
title_short Hedgehog Signaling Inhibition by Smoothened Antagonist BMS-833923 Reduces Osteoblast Differentiation and Ectopic Bone Formation of Human Skeletal (Mesenchymal) Stem Cells
title_sort hedgehog signaling inhibition by smoothened antagonist bms 833923 reduces osteoblast differentiation and ectopic bone formation of human skeletal mesenchymal stem cells
url http://dx.doi.org/10.1155/2019/3435901
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