Optimization of the theoretical model for growth rate of mesenchymal stem cells on three-dimensional scaffold under fluid shear stress_Journal of Biomedical Engineering

Authors：

LI Qiang ^1,2 , YANG Li ^1,2 ,  LU Yonggang ^1,2

1. Key Laboratory of Biorheological Science and Technology, Ministry of Education, Chongqing 400044, P.R.China;
2. Bioengineering College, Chongqing University, Chongqing 400044, P.R.China;

Corresponding author：

LU Yonggang, Email: yglv@cqu.edu.cn

Keywords：

mesenchymal stem cells; fluid shear stress; bioreactor; cell growth rate; osteogenic differentiation

DOI：

10.7507/1001-5515.201904025

Video：

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Bone tissue engineering is considered as one of the most promising way to treat large segmental bone defect. When constructing bone tissue engineering graft in vitro, suitable bioreactor is usually used to incubate cell-scaffold complex under perfusion to obtain bone tissue engineering graft with good repair efficiency. However, the theoretical model for growth rate of single cell (especially for stem cell) during this process still has many defects. The difference between stem cells and terminally differentiated cells is always ignored. Based on our previous studies, this study used self-made perfusion apparatus to apply different modes and strengths of fluid shear stress (FSS) to the cells seeded on scaffolds. The effects of FSS on the proliferation and osteogenic differentiation of mesenchymal stem cells (MSCs) were investigated. The regression analysis model of the effect of FSS on the single-cell growth rate of MSCs was further established. The results showed that 0.022 5 Pa oscillatory shear stress had stronger ability to promote proliferation and osteogenic differentiation of MSCs, and the growth rate of a single MSC cell under FSS was modified. This study is expected to provide theoretical guidance for optimizing the perfusion culture condition of bone tissue engineering grafts in vitro.

Citation： LI Qiang, YANG Li, LU Yonggang. Optimization of the theoretical model for growth rate of mesenchymal stem cells on three-dimensional scaffold under fluid shear stress. Journal of Biomedical Engineering, 2019, 36(5): 795-802. doi: 10.7507/1001-5515.201904025 Copy

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2.	Swift J, Ivanovska I L, Buxboim A, et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science, 2013, 341(6149): 1240104.
3.	Ivanovska I L, Shin J W, Swift J, et al. Stem cell mechanobiology: diverse lessons from bone marrow. Trends Cell Biol, 2015, 25(9): 523-532.
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5.	Lambers F M, Kuhn G, Weigt C, et al. Bone adaptation to cyclic loading in murine caudal vertebrae is maintained with age and directly correlated to the local micromechanical environment. J Biomech, 2015, 48(6): 1179-1187.
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7.	Chen G, Xu R, Zhang C, et al. Responses of MSCs to 3D scaffold matrix mechanical properties under oscillatory perfusion culture. ACS Appl Mater Interfaces, 2017, 9(2): 1207-1218.
8.	Li Zhaohui, Cui Zhanfeng. Three-dimensional perfused cell culture. Biotechnol Adv, 2014, 32(2): 243-254.
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10.	Cartmell S H, Porter B D, Garcia A J, et al. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng, 2003, 9(6): 1197-1203.
11.	Kim D H, Heo S J, Kim S H, et al. Shear stress magnitude is critical in regulating the differentiation of mesenchymal stem cells even with endothelial growth medium. Biotechnol Lett, 2011, 33(12): 2351-2359.
12.	Lu Juan, Fan Yijuan, Gong Xiaoyuan, et al. The lineage specification of mesenchymal stem cells is directed by the rate of fluid shear stress. J Cell Physiol, 2016, 231(8): 1752-1760.
13.	Contois D E. Kinetics of bacterial growth - relationship between population density and specific growth rate of continuous cultures. J Gen Microbiol, 1959, 21(1): 40-50.
14.	Galban C J, Locke B R. Analysis of cell growth kinetics and substrate diffusion in a polymer scaffold. Biotechnol Bioeng, 1999, 65(2): 121-132.
15.	Liu Dan, Chua C K, Leong K F. A mathematical model for fluid shear-sensitive 3D tissue construct development. Biomech Model Mechanobiol, 2013, 12(1): 19-31.
16.	Gemmiti C V, Guldberg R E. Fluid flow increases type II collagen deposition and tensile mechanical properties in bioreactor-grown tissue-engineered cartilage. Tissue Eng, 2006, 12(3): 469-479.
17.	Li Deqiang, Tang Tingting, Lu Jianxi, et al. Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor. Tissue Eng Part A, 2009, 15(10): 2773-2783.
18.	McCoy R J, O'Brien F J. Influence of shear stress in perfusion bioreactor cultures for the development of three-dimensional bone tissue constructs: a review. Tissue Eng Part B Rev, 2010, 16(6): 587-601.
19.	Danielyan L, Schaefer R, von Ameln-Mayerhofer A, et al. Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of Parkinson disease. Rejuvenation Res, 2011, 14(1): 3-16.
20.	朱亚召, 王明丽, 俞海洋, 等. 表达重组猪α干扰素的大肠埃希工程菌分批发酵动力学模型的建立. 中国兽药杂志, 2018, 52(09): 9-15.
21.	王龙, 秦鹏, 郭瑞, 等. 甘肃甘南野生羊肚菌液体发酵生长动力学研究. 中国酿造, 2017, 36(6): 99-102.
22.	Riddle R C, Taylor A F, Genetos D C, et al. MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. Am J Physiol Cell Physiol, 2006, 290(3): C776-C784.
23.	Luo Wei, Xiong Wei, Zhou Jun, et al. Laminar shear stress delivers cell cycle arrest and anti-apoptosis to mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai), 2011, 43(3): 210-216.
24.	Du Dajiang, Asaoka T, Ushida T, et al. Fabrication and perfusion culture of anatomically shaped artificial bone using stereolithography. Biofabrication, 2014, 6(4): 045002.
25.	Sikavitsas V I, Bancroft G N, Holtorf H L, et al. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci U S A, 2003, 100(25): 14683-14688.
26.	Xing Min, Wang Xiaoya, Wang Endian, et al. Bone tissue engineering strategy based on the synergistic effects of silicon and strontium ions. Acta Biomater, 2018, 72: 381-395.
27.	Du D, Furukawa K S, Ushida T. 3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering. Biotechnol Bioeng, 2009, 102(6): 1670-1678.

1. Xu Huiyun, Duan Jing, Ren Li, et al. Impact of flow shear stress on morphology of osteoblast-like IDG-SW3 cells. J Bone Miner Metab, 2018, 36(5): 529-536.
2. Swift J, Ivanovska I L, Buxboim A, et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science, 2013, 341(6149): 1240104.
3. Ivanovska I L, Shin J W, Swift J, et al. Stem cell mechanobiology: diverse lessons from bone marrow. Trends Cell Biol, 2015, 25(9): 523-532.
4. Wittkowske C, Reilly G C, Lacroix D, et al. In vitro bone cell models: impact of fluid shear stress on bone formation. Front Bioeng Biotechnol, 2016, 4: 87.
5. Lambers F M, Kuhn G, Weigt C, et al. Bone adaptation to cyclic loading in murine caudal vertebrae is maintained with age and directly correlated to the local micromechanical environment. J Biomech, 2015, 48(6): 1179-1187.
6. Chen Guobao, Dong Chanjuan, Yang Li, et al. 3D scaffolds with different stiffness but the same microstructure for bone tissue engineering. ACS Appl Mater Interfaces, 2015, 7(29): 15790-15802.
7. Chen G, Xu R, Zhang C, et al. Responses of MSCs to 3D scaffold matrix mechanical properties under oscillatory perfusion culture. ACS Appl Mater Interfaces, 2017, 9(2): 1207-1218.
8. Li Zhaohui, Cui Zhanfeng. Three-dimensional perfused cell culture. Biotechnol Adv, 2014, 32(2): 243-254.
9. Raimondi M T, Boschetti F, Falcone L, et al. The effect of media perfusion on three-dimensional cultures of human chondrocytes: integration of experimental and computational approaches. Biorheology, 2004, 41(3-4): 401-410.
10. Cartmell S H, Porter B D, Garcia A J, et al. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng, 2003, 9(6): 1197-1203.
11. Kim D H, Heo S J, Kim S H, et al. Shear stress magnitude is critical in regulating the differentiation of mesenchymal stem cells even with endothelial growth medium. Biotechnol Lett, 2011, 33(12): 2351-2359.
12. Lu Juan, Fan Yijuan, Gong Xiaoyuan, et al. The lineage specification of mesenchymal stem cells is directed by the rate of fluid shear stress. J Cell Physiol, 2016, 231(8): 1752-1760.
13. Contois D E. Kinetics of bacterial growth - relationship between population density and specific growth rate of continuous cultures. J Gen Microbiol, 1959, 21(1): 40-50.
14. Galban C J, Locke B R. Analysis of cell growth kinetics and substrate diffusion in a polymer scaffold. Biotechnol Bioeng, 1999, 65(2): 121-132.
15. Liu Dan, Chua C K, Leong K F. A mathematical model for fluid shear-sensitive 3D tissue construct development. Biomech Model Mechanobiol, 2013, 12(1): 19-31.
16. Gemmiti C V, Guldberg R E. Fluid flow increases type II collagen deposition and tensile mechanical properties in bioreactor-grown tissue-engineered cartilage. Tissue Eng, 2006, 12(3): 469-479.
17. Li Deqiang, Tang Tingting, Lu Jianxi, et al. Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor. Tissue Eng Part A, 2009, 15(10): 2773-2783.
18. McCoy R J, O'Brien F J. Influence of shear stress in perfusion bioreactor cultures for the development of three-dimensional bone tissue constructs: a review. Tissue Eng Part B Rev, 2010, 16(6): 587-601.
19. Danielyan L, Schaefer R, von Ameln-Mayerhofer A, et al. Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of Parkinson disease. Rejuvenation Res, 2011, 14(1): 3-16.
20. 朱亚召, 王明丽, 俞海洋, 等. 表达重组猪α干扰素的大肠埃希工程菌分批发酵动力学模型的建立. 中国兽药杂志, 2018, 52(09): 9-15.
21. 王龙, 秦鹏, 郭瑞, 等. 甘肃甘南野生羊肚菌液体发酵生长动力学研究. 中国酿造, 2017, 36(6): 99-102.
22. Riddle R C, Taylor A F, Genetos D C, et al. MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. Am J Physiol Cell Physiol, 2006, 290(3): C776-C784.
23. Luo Wei, Xiong Wei, Zhou Jun, et al. Laminar shear stress delivers cell cycle arrest and anti-apoptosis to mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai), 2011, 43(3): 210-216.
24. Du Dajiang, Asaoka T, Ushida T, et al. Fabrication and perfusion culture of anatomically shaped artificial bone using stereolithography. Biofabrication, 2014, 6(4): 045002.
25. Sikavitsas V I, Bancroft G N, Holtorf H L, et al. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci U S A, 2003, 100(25): 14683-14688.
26. Xing Min, Wang Xiaoya, Wang Endian, et al. Bone tissue engineering strategy based on the synergistic effects of silicon and strontium ions. Acta Biomater, 2018, 72: 381-395.
27. Du D, Furukawa K S, Ushida T. 3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering. Biotechnol Bioeng, 2009, 102(6): 1670-1678.

Journal of Biomedical Engineering

Optimization of the theoretical model for growth rate of mesenchymal stem cells on three-dimensional scaffold under fluid shear stress

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