Early stage mechanical adaptability and osteogenic differentiation of mouse bone marrow derived mesenchymal stem cell under micro-vibration stimulation environment_Journal of Biomedical Engineering

Authors：

WU Jinjie ¹ , WU Yuehao ² ,  CHEN Xuening ¹ ,  ZHI Wei ²

1. National Engineering Research Center for Biomaterials, Sichuan University, Chengdu 610041, P.R.China;
2. Key Laboratory of Advanced Technologies of Materials (Ministry of Education), School of Materials Science and Engineering, Southwest Jiaotong University, Chengdu 610031, P.R.China;

Corresponding author：

CHEN Xuening, Email: xchen6@scu.edu.cn; ZHI Wei, Email: zhiwei@swjtu.edu.cn

Keywords：

micro-vibration; mesenchymal stem cell; osteogenic differentiation; mechanical adaptability

DOI：

10.7507/1001-5515.201903056

Video：

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This study investigated the early mechanical adaptability and osteogenic differentiation of mouse bone marrow mesenchymal stem cells (M-BMSCs) under micro-vibration stimulation (MVS). M-BMSCs were stimulated by MVS in vitro, cell proliferation, alkaline phosphatase (ALP) activity assay, and cytoskeleton were measured, and cell apoptosis was observed by flow cytometry. Early osteoblast-associated genes, runt-related transcription factor 2 (Runx2), Collagen Ⅰ (Col-Ⅰ) and ALP, were observed by RT-PCR and the activation of extracellular regulated protein kinases 1/2 (ERK1/2) was determined by Western blotting. The results showed that MVS had no significant effect on the proliferation of M-BMSCs. The early apoptosis was induced by mechanical stimulation (for one day), but the apoptosis was decreased after cyclic stimulation for 3 days. At the same time, MVS significantly accelerated the expression of F-actin protein in cytoskeleton, the synthesis of ALP and the ERK1/2 pathway, also up-regulated the expressions of Runx2, Col-Ⅰ and ALP genes. This study indicates that MVS could regulate cellular activity, alter early adaptive structure and finally promote the early osteogenic differentiation of M-BMSCs.

Citation： WU Jinjie, WU Yuehao, CHEN Xuening, ZHI Wei. Early stage mechanical adaptability and osteogenic differentiation of mouse bone marrow derived mesenchymal stem cell under micro-vibration stimulation environment. Journal of Biomedical Engineering, 2020, 37(1): 96-104. doi: 10.7507/1001-5515.201903056 Copy

1.	Mcclarren B, Olabisi R. Strain and vibration in mesenchymal stem cells. Int J Biomater, 2018, 2018(3): 1-13.
2.	Tsimbouri P M, Childs P G, Pemberton G D, et al. Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor. Nat Biomed Eng, 2017, 1(9): 758-770.
3.	Chen Bailing, Lin Tao, Yang Xiaoxi, et al. Low-magnitude, high-frequency vibration promotes the adhesion and the osteogenic differentiation of bone marrow-derived mesenchymal stem cells cultured on a hydroxyapatite-coated surface: The direct role of Wnt/β-catenin signaling pathway activation. Int J Mol Med, 2016, 38(5): 1531-1540.
4.	Oliveira L C, Oliveira R G, Pires-Oliveira D A A. Effects of whole body vibration on bone mineral density in postmenopausal women: a systematic review and meta-analysis. Osteoporos Int, 2016, 27(10): 2913-2933.
5.	Brohawn S G, Su Zhenwei, Mackinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K⁺ channels. Proc Natl Acad Sci U S A, 2014, 111(9): 3614-3619.
6.	Humphrey J D, Dufresne E R, Schwartz M A. Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol, 2014, 15(12): 802-812.
7.	李良, 邓力, 陈孟诗, 等. 力学刺激对 3 月龄骨质疏松大鼠成骨细胞增殖与合成功能的影响. 生物医学工程学杂志, 2004, 21(3): 341-346, 349.
8.	Zhou Yi, Guan Xiaoxu, Liu Tie, et al. Whole body vibration improves osseointegration by up-regulating osteoblastic activity but down-regulating osteoblast-mediated osteoclastogenesis via ERK1/2 pathway. Bone, 2015, 71: 17-24.
9.	Wang L, Hsu H Y, Li X, et al. Effects of frequency and acceleration amplitude on osteoblast mechanical vibration responses: a finite element study. BioMed Res Int, 2016, 2016: 1-16.
10.	Ota T, Chiba M, Hayashi H. Vibrational stimulation induces osteoblast differentiation and the upregulation of osteogenic gene expression in vitro. Cytotechnology, 2016, 68(6): 2287-2299.
11.	Lu Yuezhi, Zhao Qian, Liu Yang, et al. Vibration loading promotes osteogenic differentiation of bone marrow-derived mesenchymal stem cells via p38 MAPK signaling pathway. J Biomech, 2018, 71: 67-75.
12.	孙凌璐, 苏雪莲, 何晓兰, 等. 生物力学信号诱导骨髓间充质干细胞分化的现状. 口腔医学研究, 2018, 34(1): 94-96.
13.	Wehland M, Warnke E, Frett T, et al. The impact of hypergravity and vibration on gene and protein expression of thyroid cells. Microgravity Sci Technol, 2016, 28(3): 261-274.
14.	Zhang Chunxiang, Lu Yanqin, Zhang Linkun, et al. Influence of different intensities of vibration on proliferation and differentiation of human periodontal ligament stem cells. Arch Med Sci, 2015, 11(3): 638-646.
15.	Demiray L, Ozcivici E. Bone marrow stem cells adapt to low-magnitude vibrations by altering their cytoskeleton during quiescence and osteogenesis. Turk J Biol, 2015, 39(1): 88-97.
16.	何万庆, 夏亚一, 王海明, 等. 剪切力诱导细胞骨架重组在力学信号转导机制中的作用. 国际骨科学杂志, 2009, 30(4): 257-260.
17.	李祥, 李涤尘, 王林, 等. 旋转灌注式生物反应器系统构建及在骨组织工程中的应用. 生物医学工程学杂志, 2007, 24(1): 66-70.
18.	林梅. 生物反应器在构建组织工程产品中的应用研究. 医疗卫生装备, 2008, 29(4): 32-34.
19.	You L D, Cowin S C, Schaffler M B, et al. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech, 2001, 34(11): 1375-1386.
20.	查丁胜. 成骨细胞对振动应力作用的早期应答及力学信号转导机制的初步研究. 广州: 南方医科大学, 2008.
21.	Thompson W R, Rubin C T, Rubin J. Mechanical regulation of signaling pathways in bone. Gene, 2012, 503(2): 179-193.
22.	Du Dajiang, Asaoka T, Ushida T, et al. Fabrication and perfusion culture of anatomically shaped artificial bone using stereolithography. Biofabrication, 2014, 6(4): 11.
23.	Bhumiratana S, Bernhard J C, Alfi D M, et al. Tissue-engineered autologous grafts for facial bone Reconstruction. Sci Transl Med, 2016, 8(343): 12.
24.	Li Zhaohui, Cui Zhanfeng. Three-dimensional perfused cell culture. Biotechnol Adv, 2014, 32(2): 243-254.
25.	周腾. 利用仿真建模和有限元分析研究宏观孔隙结构与骨诱导行为的相关性. 成都: 西南交通大学, 2017.
26.	Zhou Yi, Guan Xiaoxu, Zhu Zhuoli, et al. Osteogenic differentiation of bone marrow-derived mesenchymal stromal cells on bone-derived scaffolds: effect of microvibration and role of ERK1/2 activation. Eur Cells Mater, 2011, 22: 12-25.
27.	智伟, 翁杰, 匙峰, 等. 一种细胞培养箱: ZL 201610900515.6. 2018-10-30.
28.	赵丹, 胥春. 力学影响细胞凋亡及其信号转导机制研究进展. 医用生物力学, 2014, 29(2): 188-192.
29.	查丁胜, 陈建庭, 邓轩庚, 等. 不同频率振动应变对成骨细胞增殖及分化能力的影响. 中国骨质疏松杂志, 2008, 14(5): 303-307, 312.
30.	Marycz K, Lewandowski D, Tomaszewski K A, et al. Low-frequency, low-magnitude vibrations (LFLM) enhances chondrogenic differentiation potential of human adipose derived mesenchymal stromal stem cells (hASCs). PeerJ, 2016: e1637.
31.	Wei F Y, Chow S K, Leung K S, et al. Low-magnitude high-frequency vibration enhanced mesenchymal stem cell recruitment in osteoporotic fracture healing through the SDF-1/CXCR4 pathway. Eur Cell Mater, 2016, 31: 341-354.
32.	Weyts F A A, Bosmans B, Niesing R, et al. Mechanical control of human osteoblast apoptosis and proliferation in relation to differentiation. Calcif Tissue Int, 2003, 72(4): 505-512.
33.	Novaleski C K, Kimball E E, Mizuta M, et al. Acute exposure to vibration is an apoptosis-inducing stimulus in the vocal fold epithelium. Tissue Cell, 2016, 48(5): 407-416.
34.	Pavalko F M, Gerard R L, Ponik S M, et al. Fluid shear stress inhibits TNF-alpha-induced apoptosis in osteoblasts: a role for fluid shear stress-induced activation of PI3-kinase and inhibition of caspase-3. J Cell Physiol, 2003, 194(2): 194-205.
35.	王海芳, 梅其炳. 生理性力学刺激对抗骨组织细胞凋亡的研究进展. 细胞生物学杂志, 2009, 31(6): 785-791.
36.	Beltramo E, Berrone E, Giunti S, et al. Effects of mechanical stress and high glucose on pericyte proliferation, apoptosis and contractile phenotype. Exp Eye Res, 2006, 83(4): 989-994.
37.	Zemel A. Active mechanical coupling between the nucleus, cytoskeleton and the extracellular matrix, and the implications for perinuclear actomyosin organization. Soft Matter, 2015, 11(12): 2353-2363.
38.	Akhouayri O, Lafageproust M H, Rattner A, et al. Effects of static or dynamic mechanical stresses on osteoblast phenotype expression in three-dimensional contractile collagen gels. J Cell Biochem, 2015, 76(2): 217-230.
39.	Kim H S, Zheng Mingzhen, Kim D K, et al. Effects of 1,25-dihydroxyvitamin D₃ on the differentiation of MC3T3-E1 osteoblast-like cells. J Periodontal Implant Sci, 2018, 48(1): 34-46.
40.	Zhang Yilin, Hou Weiwei, Liu Yang, et al. Microvibration stimulatesβ-catenin expression and promotes osteogenic differentiation in osteoblasts. Arch Oral Biol, 2016, 70: 47-54.
41.	Sánchez I, Hughes R T, Mayer B J, et al. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature, 1994, 372(6508): 794-798.
42.	Russo C, Lazzaro V, Gazzaruso C, et al. Proinsulin C-peptide modulates the expression of ERK1/2, type I collagen and RANKL in human osteoblast-like cells (Saos-2). Mol Cell Endocrinol, 2017, 442: 134-141.
43.	Sun Yu, Liu Wenzhou, Liu Tao, et al. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. Journal of Receptors and Signal Transduction, 2015, 35(6): 600-604.

1. Mcclarren B, Olabisi R. Strain and vibration in mesenchymal stem cells. Int J Biomater, 2018, 2018(3): 1-13.
2. Tsimbouri P M, Childs P G, Pemberton G D, et al. Stimulation of 3D osteogenesis by mesenchymal stem cells using a nanovibrational bioreactor. Nat Biomed Eng, 2017, 1(9): 758-770.
3. Chen Bailing, Lin Tao, Yang Xiaoxi, et al. Low-magnitude, high-frequency vibration promotes the adhesion and the osteogenic differentiation of bone marrow-derived mesenchymal stem cells cultured on a hydroxyapatite-coated surface: The direct role of Wnt/β-catenin signaling pathway activation. Int J Mol Med, 2016, 38(5): 1531-1540.
4. Oliveira L C, Oliveira R G, Pires-Oliveira D A A. Effects of whole body vibration on bone mineral density in postmenopausal women: a systematic review and meta-analysis. Osteoporos Int, 2016, 27(10): 2913-2933.
5. Brohawn S G, Su Zhenwei, Mackinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K⁺ channels. Proc Natl Acad Sci U S A, 2014, 111(9): 3614-3619.
6. Humphrey J D, Dufresne E R, Schwartz M A. Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol, 2014, 15(12): 802-812.
7. 李良, 邓力, 陈孟诗, 等. 力学刺激对 3 月龄骨质疏松大鼠成骨细胞增殖与合成功能的影响. 生物医学工程学杂志, 2004, 21(3): 341-346, 349.
8. Zhou Yi, Guan Xiaoxu, Liu Tie, et al. Whole body vibration improves osseointegration by up-regulating osteoblastic activity but down-regulating osteoblast-mediated osteoclastogenesis via ERK1/2 pathway. Bone, 2015, 71: 17-24.
9. Wang L, Hsu H Y, Li X, et al. Effects of frequency and acceleration amplitude on osteoblast mechanical vibration responses: a finite element study. BioMed Res Int, 2016, 2016: 1-16.
10. Ota T, Chiba M, Hayashi H. Vibrational stimulation induces osteoblast differentiation and the upregulation of osteogenic gene expression in vitro. Cytotechnology, 2016, 68(6): 2287-2299.
11. Lu Yuezhi, Zhao Qian, Liu Yang, et al. Vibration loading promotes osteogenic differentiation of bone marrow-derived mesenchymal stem cells via p38 MAPK signaling pathway. J Biomech, 2018, 71: 67-75.
12. 孙凌璐, 苏雪莲, 何晓兰, 等. 生物力学信号诱导骨髓间充质干细胞分化的现状. 口腔医学研究, 2018, 34(1): 94-96.
13. Wehland M, Warnke E, Frett T, et al. The impact of hypergravity and vibration on gene and protein expression of thyroid cells. Microgravity Sci Technol, 2016, 28(3): 261-274.
14. Zhang Chunxiang, Lu Yanqin, Zhang Linkun, et al. Influence of different intensities of vibration on proliferation and differentiation of human periodontal ligament stem cells. Arch Med Sci, 2015, 11(3): 638-646.
15. Demiray L, Ozcivici E. Bone marrow stem cells adapt to low-magnitude vibrations by altering their cytoskeleton during quiescence and osteogenesis. Turk J Biol, 2015, 39(1): 88-97.
16. 何万庆, 夏亚一, 王海明, 等. 剪切力诱导细胞骨架重组在力学信号转导机制中的作用. 国际骨科学杂志, 2009, 30(4): 257-260.
17. 李祥, 李涤尘, 王林, 等. 旋转灌注式生物反应器系统构建及在骨组织工程中的应用. 生物医学工程学杂志, 2007, 24(1): 66-70.
18. 林梅. 生物反应器在构建组织工程产品中的应用研究. 医疗卫生装备, 2008, 29(4): 32-34.
19. You L D, Cowin S C, Schaffler M B, et al. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech, 2001, 34(11): 1375-1386.
20. 查丁胜. 成骨细胞对振动应力作用的早期应答及力学信号转导机制的初步研究. 广州: 南方医科大学, 2008.
21. Thompson W R, Rubin C T, Rubin J. Mechanical regulation of signaling pathways in bone. Gene, 2012, 503(2): 179-193.
22. Du Dajiang, Asaoka T, Ushida T, et al. Fabrication and perfusion culture of anatomically shaped artificial bone using stereolithography. Biofabrication, 2014, 6(4): 11.
23. Bhumiratana S, Bernhard J C, Alfi D M, et al. Tissue-engineered autologous grafts for facial bone Reconstruction. Sci Transl Med, 2016, 8(343): 12.
24. Li Zhaohui, Cui Zhanfeng. Three-dimensional perfused cell culture. Biotechnol Adv, 2014, 32(2): 243-254.
25. 周腾. 利用仿真建模和有限元分析研究宏观孔隙结构与骨诱导行为的相关性. 成都: 西南交通大学, 2017.
26. Zhou Yi, Guan Xiaoxu, Zhu Zhuoli, et al. Osteogenic differentiation of bone marrow-derived mesenchymal stromal cells on bone-derived scaffolds: effect of microvibration and role of ERK1/2 activation. Eur Cells Mater, 2011, 22: 12-25.
27. 智伟, 翁杰, 匙峰, 等. 一种细胞培养箱: ZL 201610900515.6. 2018-10-30.
28. 赵丹, 胥春. 力学影响细胞凋亡及其信号转导机制研究进展. 医用生物力学, 2014, 29(2): 188-192.
29. 查丁胜, 陈建庭, 邓轩庚, 等. 不同频率振动应变对成骨细胞增殖及分化能力的影响. 中国骨质疏松杂志, 2008, 14(5): 303-307, 312.
30. Marycz K, Lewandowski D, Tomaszewski K A, et al. Low-frequency, low-magnitude vibrations (LFLM) enhances chondrogenic differentiation potential of human adipose derived mesenchymal stromal stem cells (hASCs). PeerJ, 2016: e1637.
31. Wei F Y, Chow S K, Leung K S, et al. Low-magnitude high-frequency vibration enhanced mesenchymal stem cell recruitment in osteoporotic fracture healing through the SDF-1/CXCR4 pathway. Eur Cell Mater, 2016, 31: 341-354.
32. Weyts F A A, Bosmans B, Niesing R, et al. Mechanical control of human osteoblast apoptosis and proliferation in relation to differentiation. Calcif Tissue Int, 2003, 72(4): 505-512.
33. Novaleski C K, Kimball E E, Mizuta M, et al. Acute exposure to vibration is an apoptosis-inducing stimulus in the vocal fold epithelium. Tissue Cell, 2016, 48(5): 407-416.
34. Pavalko F M, Gerard R L, Ponik S M, et al. Fluid shear stress inhibits TNF-alpha-induced apoptosis in osteoblasts: a role for fluid shear stress-induced activation of PI3-kinase and inhibition of caspase-3. J Cell Physiol, 2003, 194(2): 194-205.
35. 王海芳, 梅其炳. 生理性力学刺激对抗骨组织细胞凋亡的研究进展. 细胞生物学杂志, 2009, 31(6): 785-791.
36. Beltramo E, Berrone E, Giunti S, et al. Effects of mechanical stress and high glucose on pericyte proliferation, apoptosis and contractile phenotype. Exp Eye Res, 2006, 83(4): 989-994.
37. Zemel A. Active mechanical coupling between the nucleus, cytoskeleton and the extracellular matrix, and the implications for perinuclear actomyosin organization. Soft Matter, 2015, 11(12): 2353-2363.
38. Akhouayri O, Lafageproust M H, Rattner A, et al. Effects of static or dynamic mechanical stresses on osteoblast phenotype expression in three-dimensional contractile collagen gels. J Cell Biochem, 2015, 76(2): 217-230.
39. Kim H S, Zheng Mingzhen, Kim D K, et al. Effects of 1,25-dihydroxyvitamin D₃ on the differentiation of MC3T3-E1 osteoblast-like cells. J Periodontal Implant Sci, 2018, 48(1): 34-46.
40. Zhang Yilin, Hou Weiwei, Liu Yang, et al. Microvibration stimulatesβ-catenin expression and promotes osteogenic differentiation in osteoblasts. Arch Oral Biol, 2016, 70: 47-54.
41. Sánchez I, Hughes R T, Mayer B J, et al. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature, 1994, 372(6508): 794-798.
42. Russo C, Lazzaro V, Gazzaruso C, et al. Proinsulin C-peptide modulates the expression of ERK1/2, type I collagen and RANKL in human osteoblast-like cells (Saos-2). Mol Cell Endocrinol, 2017, 442: 134-141.
43. Sun Yu, Liu Wenzhou, Liu Tao, et al. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. Journal of Receptors and Signal Transduction, 2015, 35(6): 600-604.

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Early stage mechanical adaptability and osteogenic differentiation of mouse bone marrow derived mesenchymal stem cell under micro-vibration stimulation environment

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