Research progress of different mechanical stimulation regulating chondrocytes metabolism_Journal of Biomedical Engineering

Authors：

YANG Guanglu ^1,2 , GUO Yang ^1,2 , TU Pengcheng ^1,2 , WU Chengjie ^1,2 , PAN Yalan ⁴ ,  MA Yong ^1,2,3

1. Department of Traumatology & Orthopedics, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing 210029, P.R.China;
2. Laboratory of New Techniques of Restoration & Reconstruction of Orthopedics and Traumatology, Nanjing University of Chinese Medicine, Nanjing 210023, P.R.China;
3. School of Chinese Medicine, School of Integrated Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210023, P.R.China;
4. Nursing Institute of Integrated Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210023, P.R.China;

Corresponding author：

Keywords：

chondrocyte; mechanical stimulation; metabolism

DOI：

10.7507/1001-5515.202001044

Video：

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Abstract Full text Figures/Tables Video References Cited by

As a kind of mechanical effector cells, chondrocytes can produce a variety of physical and chemical signals under the stimulation of multiaxial load in vivo, which affect their own growth, development and apoptosis. Therefore, simulating the mechanical environment in vivo has become a research hotspot in the culture of chondrocytes in vitro. Although a large number of reports have fully proved that different mechanical stimulation can regulate the metabolism of chondrocytes, the loading scheme has not been agreed. Starting from different mechanical forms, this review will explore the differences in the regulation of chondrocyte metabolism by different mechanical stimuli, so as to find an advantage scheme to promote the growth and proliferation of chondrocytes and to develop a more stable, effective and reliable experimental strategy.

Citation： YANG Guanglu, GUO Yang, TU Pengcheng, WU Chengjie, PAN Yalan, MA Yong. Research progress of different mechanical stimulation regulating chondrocytes metabolism. Journal of Biomedical Engineering, 2020, 37(6): 1101-1108. doi: 10.7507/1001-5515.202001044 Copy

1.	Ramage L, Nuki G, Salter D M. Signalling cascades in mechanotransduction: cell-matrix interactions and mechanical loading. Scand J Med Sci Sports, 2009, 19(4): 457-469.
2.	Li Ke, Zhang Chunqiu, Qiu Lulu, et al. Advances in application of mechanical stimuli in bioreactors for cartilage tissue engineering. Tissue Eng Part B Rev, 2017, 23(4): 399-411.
3.	Bleuel J, Zaucke F, Brüggemann G P, et al. Effects of cyclic tensile strain on chondrocyte metabolism: a systematic review. PLoS ONE, 2015, 10(3): e0119816.
4.	杨自权, 门亚勋. 等轴牵张应变对骨间充质干细胞成软骨分化早期的影响. 中国骨伤, 2018, 31(9): 846-852.
5.	Ohtsuki T, Shinaoka A, Kumagishi-Shinaoka K, et al. Mechanical strain attenuates cytokine-induced ADAMTS9 expression via transient receptor potential vanilloid type 1. Exp Cell Res, 2019, 383(2): 111556.
6.	Zhu G Z, Qian Y P, Wu W T, et al. Negative effects of high mechanical tensile strain stimulation on chondrocyte injury in vitro. Biochem Biophys Res Commun, 2019, 510(1): 48-52.
7.	Liu Q, Yang H X, Duan J, et al. Bilateral anterior elevation prosthesis boosts chondrocytes proliferation in mice mandibular condyle. Oral Dis, 2019, 25(6): 1589-1599.
8.	Yang Y, Wang Y, Kong Y W, et al. Mechanical stress protects against osteoarthritis via regulation of the AMPK/NF-κB signaling pathway. J Cell Physiol, 2019, 234(6): 9156-9167.
9.	Zhong D Y, Chen X I, Zhang W, et al. Excessive tensile strain induced the change in chondrocyte phenotype. Acta Bioeng Biomech, 2018, 20(2): 3-10.
10.	Yanoshita M, Hirose N, Okamoto Y, et al. Cyclic tensile strain upregulates pro-inflammatory cytokine expression Via FAK-MAPK signaling in chondrocytes. Inflammation, 2018, 41(5): 1621-1630.
11.	Liu Q, Hu X Q, Zhang X, et al. Effects of mechanical stress on chondrocyte phenotype and chondrocyte extracellular matrix expression. Sci Rep, 2016, 6: 37268.
12.	Machida T, Nishida K, Nasu Y, et al. Inhibitory effect of JAK inhibitor on mechanical stress-induced protease expression by human articular chondrocytes. Inflamm res, 2017, 66(11): 999-1009.
13.	Lohberger B, Kaltenegger H, Weigl L, et al. Mechanical exposure and diacerein treatment modulates integrin-FAK-MAPKs mechanotransduction in human osteoarthritis chondrocytes. Cell Signal, 2019, 56: 23-30.
14.	Ma D D, Kou X X, Jin J, et al. Hydrostatic compress force enhances the viability and decreases the apoptosis of condylar chondrocytes through integrin-FAK-ERK/PI3K pathway. Int J Mol Sci, 2016, 17(11): 1847.
15.	姚旺祥, 戴晗豪, 桂鉴超. 机械应力促进炎性环境中软骨修复的机制研究. 浙江大学学报: 医学版, 2019, 48(5): 517-525.
16.	Montagne K, Onuma Y, Ito Y, et al. High hydrostatic pressure induces pro-osteoarthritic changes in cartilage precursor cells: A transcriptome analysis. PLoS One, 2017, 12(8): e0183226.
17.	Nazempour A, Quisenberry C R, Abu-Lail Ne I, et al. Combined effects of oscillating hydrostatic pressure, perfusion and encapsulation in a novel bioreactor for enhancing extracellular matrix synthesis by bovine chondrocytes. Cell Tissue Res, 2017, 370(1): 179-193.
18.	Mellor L F, Steward A J, Nordberg R C, et al. Comparison of simulated microgravity and hydrostatic pressure for chondrogenesis of hASC. Aerosp Med Hum Perform, 2017, 88(4): 377-384.
19.	Ogura T, Minas T, Tsuchiya A, et al. Effects of hydrostatic pressure and deviatoric stress on human articular chondrocytes for designing neo-cartilage construct. J Tissue Eng Regen Med, 2019, 13(7): 1143-1152.
20.	Saha A, Rolfe R, Carroll S, et al. Chondrogenesis of embryonic limb bud cells in micromass culture progresses rapidly to hypertrophy and is modulated by hydrostatic pressure. Cell Tissue Res, 2017, 368(1): 47-59.
21.	Ogura T, Tsuchiya A, Minas T, et al. Optimization of extracellular matrix synthesis and accumulation by human articular chondrocytes in 3-dimensional construct with repetitive hydrostatic pressure. Cartilage, 2018, 9(2): 192-201.
22.	Chang S F, Huang K C, Chang H I, et al. 2 dyn/cm² shear force upregulates kruppel-like factor 4 expression in human chondrocytes to inhibit the interleukin-1β-activated nuclear factor-κB. J Cell Physiol, 2018, 234(1): 958-968.
23.	Zhang M, Yang H, Lu L, et al. Matrix replenishing by BMSCs is beneficial for osteoarthritic temporomandibular joint cartilage. Osteoarthr Cartil, 2017, 25(9): 1551-1562.
24.	Su Y P, Chen C N, Chang H I, et al. Low shear stress attenuates COX-2 expression induced by resistin in human osteoarthritic chondrocytes. J Cell Physiol, 2017, 232(6): 1448-1457.
25.	Adeniran-Catlett A E, Beguin E, Bozal F K, et al. Suspension-based differentiation of adult mesenchymal stem cells toward chondrogenic lineage. Connect Tissue Res, 2016, 57(6): 466-475.
26.	Kuang B, Zeng Z B, Qin Q. Biomechanically stimulated chondrocytes promote osteoclastic bone resorption in the mandibular condyle. , 2018: 248-257.
27.	Guo T, Yu L, Lim C G, et al. Effect of dynamic culture and periodic compression on human mesenchymal stem cell proliferation and chondrogenesis. Ann Biomed Eng, 2016, 44(7): 2103-2113.
28.	Park I S, Choi W H, Park D Y, et al. Effect of joint mimicking loading system on zonal organization into tissue-engineered cartilage. PLoS ONE, 2018, 13(9): e0202834.
29.	DiFederico E, Shelton J C, Bader D L. Complex mechanical conditioning of cell-seeded agarose constructs can influence chondrocyte biosynthetic activity. Biotechnol Bioeng, 2017, 114(7): 1614-1625.
30.	Wang L, Shen H, Nie J C, et al. Functional testing on engineered cartilage to identify the role played by shearing. Med Eng Phys, 2018, 51: 17-23.
31.	Young I C, Chuang S T, Gefen A, et al. A novel compressive stress-based osteoarthritis-like chondrocyte system. Exp Biol Med, 2017, 242(10): 1062-1071.
32.	Diao H J, Fung H S, Yeung P, et al. Dynamic cyclic compression modulates the chondrogenic phenotype in human chondrocytes from late stage osteoarthritis. Biochem Biophys Res Commun, 2017, 486(1): 14-21.
33.	Horner C B, Hirota K, Liu J Z, et al. Magnitude-dependent and inversely-related osteogenic/chondrogenic differentiation of human mesenchymal stem cells under dynamic compressive strain. J Tissue Eng Regen Med, 2018, 12(2): e637-e647.
34.	Kowsari-Esfahan R, Jahanbakhsh A, Saidi M S, et al. A microfabricated platform for the study of chondrogenesis under different compressive loads. J Mech Behav Biomed Mater, 2018, 78: 404-413.
35.	Chen C H, Kuo C Y, Chen J P. Effect of cyclic dynamic compressive loading on chondrocytes and adipose-derived stem cells co-cultured in highly elastic cryogel scaffolds. Int J Mol Sci, 2018, 19(2): 370.
36.	Scholtes S, Krämer E, Weisser M, et al. Global chondrocyte gene expression after a single anabolic loading period: Time evolution and re-inducibility of mechano-responses. J Cell Physiol, 2018, 233(1): 699-711.
37.	Remya N S, Nair P D. Mechanoresponsiveness of human umbilical cord mesenchymal stem cells in in vitro chondrogenesis-A comparative study with growth factor induction. J Biomed Mater Res A, 2016, 104(10): 2554-2566.
38.	Iseki T, Rothrauff B B, Kihara S, et al. Dynamic compressive loading improves cartilage repair in an in vitro model of microfracture: Comparison of 2 mechanical loading regimens on simulated microfracture based on fibrin gel scaffolds encapsulating connective tissue progenitor cells. Am J Sports Med, 2019, 47(9): 2188-2199.
39.	Kanaguchi A A, Yonemitsu I, Ikeda Y, et al. Low-intensity pulsed ultrasound stimulation for mandibular condyle osteoarthritis lesions in rats. Oral Dis, 2018, 24(4): 600-610.
40.	Zhou H Y, Li Q, Wang J X, et al. Low-intensity pulsed ultrasound repair in mandibular condylar cartilage injury rabbit model. Arch Oral Biol, 2019, 104: 60-66.
41.	Hsieh Y L, Chen H Y, Yang C C. Early intervention with therapeutic low-intensity pulsed ultrasound in halting the progression of post-traumatic osteoarthritis in a rat model. Ultrasound Med Biol, 2018, 44(12): 2637-2645.
42.	Rothenberg J B, Jayaram P, Naqvi U, et al. The role of low-intensity pulsed ultrasound on cartilage healing in knee osteoarthritis: A review. PM R, 2017, 9(12): 1268-1277.
43.	Li Xiaofei, Sun Yueli, Zhou Zhilun, et al. Mitigation of articular cartilage degeneration and subchondral bone sclerosis in osteoarthritis progression using low-intensity ultrasound stimulation. Ultrasound Med Biol, 2019, 45(1): 148-159.
44.	Tang Z F, Li H Y. Effects of fibroblast growth factors 2 and low intensity pulsed ultrasound on the repair of knee articular cartilage in rabbits. Eur Rev Med Pharmacol Sci, 2018, 22(8): 2447-2453.
45.	Ito A, Aoyama T, Yamaguchi S, et al. Low-intensity pulsed ultrasound inhibits messenger RNA expression of matrix metalloproteinase-13 induced by interleukin-1β in chondrocytes in an intensity-dependent manner. Ultrasound Med Biol, 2012, 38(10): 1726-1733.
46.	Uddin S M Z, Richbourgh B, Ding Y, et al. Chondro-protective effects of low intensity pulsed ultrasound. Osteoarthr Cartil, 2016, 24(11): 1989-1998.
47.	Nishida T, Kubota S, Aoyama E, et al. Low-intensity pulsed ultrasound (LIPUS) treatment of cultured chondrocytes stimulates production of CCN family protein 2(CCN2), a protein involved in the regeneration of articular cartilage: mechanism underlying this stimulation. Osteoarthr Cartil, 2017, 25(5): 759-769.
48.	杜登悝, 陈世荣, 易刚, 等. 低强度脉冲超声促进人骨性关节炎软骨细胞合成细胞外基质. 细胞与分子免疫学杂志, 2016, 32(11): 1536-1540.
49.	Sekino J, Nagao M, Kato S, et al. Low-intensity pulsed ultrasound induces cartilage matrix synthesis and reduced MMP13 expression in chondrocytes. Biochem Biophys Res Commun, 2018, 506(1): 290-297.
50.	Xia P, Wang X J, Qu Y P, et al. TGF-β1-induced chondrogenesis of bone marrow mesenchymal stem cells is promoted by low-intensity pulsed ultrasound through the integrin-mTOR signaling pathway. Stem Cell Res Ther, 2017, 8(1): 281.
51.	Grimm D, Egli M, Krüger M, et al. Tissue engineering under microgravity conditions–use of stem cells and specialized cells. Stem Cells Dev, 2018, 27(12): 787-804.
52.	Wuest S L, Caliò M, Wernas T, et al. Influence of mechanical unloading on articular chondrocyte dedifferentiation. Int J Mol Sci, 2018, 19(5): 1289.
53.	Chen L Y, Liu G J, Li W J, et al. Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells following transfection with Indian hedgehog and sonic hedgehog using a rotary cell culture system. Cell Mol Biol Lett, 2019, 24: 16.
54.	Yin H Y, Wang Y, Sun Z, et al. Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater, 2016, 33: 96-109.
55.	Fitzgerald J, Endicott J, Hansen U, et al. Articular cartilage and sternal fibrocartilage respond differently to extended microgravity. NPJ Microgravity, 2019, 5: 3.
56.	Wang T T, Xie W, Ye W W, et al. Effects of electromagnetic fields on osteoarthritis. Biomed Pharmacother, 2019, 118: 109282.
57.	Anbarasan S, Baraneedharan U, Paul S F, et al. Low dose short duration pulsed electromagnetic field effects on cultured human chondrocytes: An experimental study. Indian J Orthop, 2016, 50(1): 87-93.
58.	Parate D, Franco-Obregón A, Fröhlich J, et al. Enhancement of mesenchymal stem cell chondrogenesis with short-term low intensity pulsed electromagnetic fields. Sci Rep, 2017, 7(1): 9421.
59.	Escobar J F, Vaca-González J J, Guevara J M, et al. In vitro evaluation of the effect of stimulation with magnetic fields on chondrocytes. Bioelectromagnetics, 2020, 41(1): 41-51.
60.	Redeker J I, Schmitt B, Grigull N P, et al. Effect of electromagnetic fields on human osteoarthritic and non-osteoarthritic chondrocytes. BMC Complement Altern Med, 2017, 17(1): 402.
61.	Zhou J, Liao Y, Xie H T, et al. Pulsed electromagnetic field ameliorates cartilage degeneration by inhibiting mitogen-activated protein kinases in a rat model of osteoarthritis. Phys Ther Sport, 2017, 24: 32-38.

1. Ramage L, Nuki G, Salter D M. Signalling cascades in mechanotransduction: cell-matrix interactions and mechanical loading. Scand J Med Sci Sports, 2009, 19(4): 457-469.
2. Li Ke, Zhang Chunqiu, Qiu Lulu, et al. Advances in application of mechanical stimuli in bioreactors for cartilage tissue engineering. Tissue Eng Part B Rev, 2017, 23(4): 399-411.
3. Bleuel J, Zaucke F, Brüggemann G P, et al. Effects of cyclic tensile strain on chondrocyte metabolism: a systematic review. PLoS ONE, 2015, 10(3): e0119816.
4. 杨自权, 门亚勋. 等轴牵张应变对骨间充质干细胞成软骨分化早期的影响. 中国骨伤, 2018, 31(9): 846-852.
5. Ohtsuki T, Shinaoka A, Kumagishi-Shinaoka K, et al. Mechanical strain attenuates cytokine-induced ADAMTS9 expression via transient receptor potential vanilloid type 1. Exp Cell Res, 2019, 383(2): 111556.
6. Zhu G Z, Qian Y P, Wu W T, et al. Negative effects of high mechanical tensile strain stimulation on chondrocyte injury in vitro. Biochem Biophys Res Commun, 2019, 510(1): 48-52.
7. Liu Q, Yang H X, Duan J, et al. Bilateral anterior elevation prosthesis boosts chondrocytes proliferation in mice mandibular condyle. Oral Dis, 2019, 25(6): 1589-1599.
8. Yang Y, Wang Y, Kong Y W, et al. Mechanical stress protects against osteoarthritis via regulation of the AMPK/NF-κB signaling pathway. J Cell Physiol, 2019, 234(6): 9156-9167.
9. Zhong D Y, Chen X I, Zhang W, et al. Excessive tensile strain induced the change in chondrocyte phenotype. Acta Bioeng Biomech, 2018, 20(2): 3-10.
10. Yanoshita M, Hirose N, Okamoto Y, et al. Cyclic tensile strain upregulates pro-inflammatory cytokine expression Via FAK-MAPK signaling in chondrocytes. Inflammation, 2018, 41(5): 1621-1630.
11. Liu Q, Hu X Q, Zhang X, et al. Effects of mechanical stress on chondrocyte phenotype and chondrocyte extracellular matrix expression. Sci Rep, 2016, 6: 37268.
12. Machida T, Nishida K, Nasu Y, et al. Inhibitory effect of JAK inhibitor on mechanical stress-induced protease expression by human articular chondrocytes. Inflamm res, 2017, 66(11): 999-1009.
13. Lohberger B, Kaltenegger H, Weigl L, et al. Mechanical exposure and diacerein treatment modulates integrin-FAK-MAPKs mechanotransduction in human osteoarthritis chondrocytes. Cell Signal, 2019, 56: 23-30.
14. Ma D D, Kou X X, Jin J, et al. Hydrostatic compress force enhances the viability and decreases the apoptosis of condylar chondrocytes through integrin-FAK-ERK/PI3K pathway. Int J Mol Sci, 2016, 17(11): 1847.
15. 姚旺祥, 戴晗豪, 桂鉴超. 机械应力促进炎性环境中软骨修复的机制研究. 浙江大学学报: 医学版, 2019, 48(5): 517-525.
16. Montagne K, Onuma Y, Ito Y, et al. High hydrostatic pressure induces pro-osteoarthritic changes in cartilage precursor cells: A transcriptome analysis. PLoS One, 2017, 12(8): e0183226.
17. Nazempour A, Quisenberry C R, Abu-Lail Ne I, et al. Combined effects of oscillating hydrostatic pressure, perfusion and encapsulation in a novel bioreactor for enhancing extracellular matrix synthesis by bovine chondrocytes. Cell Tissue Res, 2017, 370(1): 179-193.
18. Mellor L F, Steward A J, Nordberg R C, et al. Comparison of simulated microgravity and hydrostatic pressure for chondrogenesis of hASC. Aerosp Med Hum Perform, 2017, 88(4): 377-384.
19. Ogura T, Minas T, Tsuchiya A, et al. Effects of hydrostatic pressure and deviatoric stress on human articular chondrocytes for designing neo-cartilage construct. J Tissue Eng Regen Med, 2019, 13(7): 1143-1152.
20. Saha A, Rolfe R, Carroll S, et al. Chondrogenesis of embryonic limb bud cells in micromass culture progresses rapidly to hypertrophy and is modulated by hydrostatic pressure. Cell Tissue Res, 2017, 368(1): 47-59.
21. Ogura T, Tsuchiya A, Minas T, et al. Optimization of extracellular matrix synthesis and accumulation by human articular chondrocytes in 3-dimensional construct with repetitive hydrostatic pressure. Cartilage, 2018, 9(2): 192-201.
22. Chang S F, Huang K C, Chang H I, et al. 2 dyn/cm² shear force upregulates kruppel-like factor 4 expression in human chondrocytes to inhibit the interleukin-1β-activated nuclear factor-κB. J Cell Physiol, 2018, 234(1): 958-968.
23. Zhang M, Yang H, Lu L, et al. Matrix replenishing by BMSCs is beneficial for osteoarthritic temporomandibular joint cartilage. Osteoarthr Cartil, 2017, 25(9): 1551-1562.
24. Su Y P, Chen C N, Chang H I, et al. Low shear stress attenuates COX-2 expression induced by resistin in human osteoarthritic chondrocytes. J Cell Physiol, 2017, 232(6): 1448-1457.
25. Adeniran-Catlett A E, Beguin E, Bozal F K, et al. Suspension-based differentiation of adult mesenchymal stem cells toward chondrogenic lineage. Connect Tissue Res, 2016, 57(6): 466-475.
26. Kuang B, Zeng Z B, Qin Q. Biomechanically stimulated chondrocytes promote osteoclastic bone resorption in the mandibular condyle. , 2018: 248-257.
27. Guo T, Yu L, Lim C G, et al. Effect of dynamic culture and periodic compression on human mesenchymal stem cell proliferation and chondrogenesis. Ann Biomed Eng, 2016, 44(7): 2103-2113.
28. Park I S, Choi W H, Park D Y, et al. Effect of joint mimicking loading system on zonal organization into tissue-engineered cartilage. PLoS ONE, 2018, 13(9): e0202834.
29. DiFederico E, Shelton J C, Bader D L. Complex mechanical conditioning of cell-seeded agarose constructs can influence chondrocyte biosynthetic activity. Biotechnol Bioeng, 2017, 114(7): 1614-1625.
30. Wang L, Shen H, Nie J C, et al. Functional testing on engineered cartilage to identify the role played by shearing. Med Eng Phys, 2018, 51: 17-23.
31. Young I C, Chuang S T, Gefen A, et al. A novel compressive stress-based osteoarthritis-like chondrocyte system. Exp Biol Med, 2017, 242(10): 1062-1071.
32. Diao H J, Fung H S, Yeung P, et al. Dynamic cyclic compression modulates the chondrogenic phenotype in human chondrocytes from late stage osteoarthritis. Biochem Biophys Res Commun, 2017, 486(1): 14-21.
33. Horner C B, Hirota K, Liu J Z, et al. Magnitude-dependent and inversely-related osteogenic/chondrogenic differentiation of human mesenchymal stem cells under dynamic compressive strain. J Tissue Eng Regen Med, 2018, 12(2): e637-e647.
34. Kowsari-Esfahan R, Jahanbakhsh A, Saidi M S, et al. A microfabricated platform for the study of chondrogenesis under different compressive loads. J Mech Behav Biomed Mater, 2018, 78: 404-413.
35. Chen C H, Kuo C Y, Chen J P. Effect of cyclic dynamic compressive loading on chondrocytes and adipose-derived stem cells co-cultured in highly elastic cryogel scaffolds. Int J Mol Sci, 2018, 19(2): 370.
36. Scholtes S, Krämer E, Weisser M, et al. Global chondrocyte gene expression after a single anabolic loading period: Time evolution and re-inducibility of mechano-responses. J Cell Physiol, 2018, 233(1): 699-711.
37. Remya N S, Nair P D. Mechanoresponsiveness of human umbilical cord mesenchymal stem cells in in vitro chondrogenesis-A comparative study with growth factor induction. J Biomed Mater Res A, 2016, 104(10): 2554-2566.
38. Iseki T, Rothrauff B B, Kihara S, et al. Dynamic compressive loading improves cartilage repair in an in vitro model of microfracture: Comparison of 2 mechanical loading regimens on simulated microfracture based on fibrin gel scaffolds encapsulating connective tissue progenitor cells. Am J Sports Med, 2019, 47(9): 2188-2199.
39. Kanaguchi A A, Yonemitsu I, Ikeda Y, et al. Low-intensity pulsed ultrasound stimulation for mandibular condyle osteoarthritis lesions in rats. Oral Dis, 2018, 24(4): 600-610.
40. Zhou H Y, Li Q, Wang J X, et al. Low-intensity pulsed ultrasound repair in mandibular condylar cartilage injury rabbit model. Arch Oral Biol, 2019, 104: 60-66.
41. Hsieh Y L, Chen H Y, Yang C C. Early intervention with therapeutic low-intensity pulsed ultrasound in halting the progression of post-traumatic osteoarthritis in a rat model. Ultrasound Med Biol, 2018, 44(12): 2637-2645.
42. Rothenberg J B, Jayaram P, Naqvi U, et al. The role of low-intensity pulsed ultrasound on cartilage healing in knee osteoarthritis: A review. PM R, 2017, 9(12): 1268-1277.
43. Li Xiaofei, Sun Yueli, Zhou Zhilun, et al. Mitigation of articular cartilage degeneration and subchondral bone sclerosis in osteoarthritis progression using low-intensity ultrasound stimulation. Ultrasound Med Biol, 2019, 45(1): 148-159.
44. Tang Z F, Li H Y. Effects of fibroblast growth factors 2 and low intensity pulsed ultrasound on the repair of knee articular cartilage in rabbits. Eur Rev Med Pharmacol Sci, 2018, 22(8): 2447-2453.
45. Ito A, Aoyama T, Yamaguchi S, et al. Low-intensity pulsed ultrasound inhibits messenger RNA expression of matrix metalloproteinase-13 induced by interleukin-1β in chondrocytes in an intensity-dependent manner. Ultrasound Med Biol, 2012, 38(10): 1726-1733.
46. Uddin S M Z, Richbourgh B, Ding Y, et al. Chondro-protective effects of low intensity pulsed ultrasound. Osteoarthr Cartil, 2016, 24(11): 1989-1998.
47. Nishida T, Kubota S, Aoyama E, et al. Low-intensity pulsed ultrasound (LIPUS) treatment of cultured chondrocytes stimulates production of CCN family protein 2(CCN2), a protein involved in the regeneration of articular cartilage: mechanism underlying this stimulation. Osteoarthr Cartil, 2017, 25(5): 759-769.
48. 杜登悝, 陈世荣, 易刚, 等. 低强度脉冲超声促进人骨性关节炎软骨细胞合成细胞外基质. 细胞与分子免疫学杂志, 2016, 32(11): 1536-1540.
49. Sekino J, Nagao M, Kato S, et al. Low-intensity pulsed ultrasound induces cartilage matrix synthesis and reduced MMP13 expression in chondrocytes. Biochem Biophys Res Commun, 2018, 506(1): 290-297.
50. Xia P, Wang X J, Qu Y P, et al. TGF-β1-induced chondrogenesis of bone marrow mesenchymal stem cells is promoted by low-intensity pulsed ultrasound through the integrin-mTOR signaling pathway. Stem Cell Res Ther, 2017, 8(1): 281.
51. Grimm D, Egli M, Krüger M, et al. Tissue engineering under microgravity conditions–use of stem cells and specialized cells. Stem Cells Dev, 2018, 27(12): 787-804.
52. Wuest S L, Caliò M, Wernas T, et al. Influence of mechanical unloading on articular chondrocyte dedifferentiation. Int J Mol Sci, 2018, 19(5): 1289.
53. Chen L Y, Liu G J, Li W J, et al. Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells following transfection with Indian hedgehog and sonic hedgehog using a rotary cell culture system. Cell Mol Biol Lett, 2019, 24: 16.
54. Yin H Y, Wang Y, Sun Z, et al. Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater, 2016, 33: 96-109.
55. Fitzgerald J, Endicott J, Hansen U, et al. Articular cartilage and sternal fibrocartilage respond differently to extended microgravity. NPJ Microgravity, 2019, 5: 3.
56. Wang T T, Xie W, Ye W W, et al. Effects of electromagnetic fields on osteoarthritis. Biomed Pharmacother, 2019, 118: 109282.
57. Anbarasan S, Baraneedharan U, Paul S F, et al. Low dose short duration pulsed electromagnetic field effects on cultured human chondrocytes: An experimental study. Indian J Orthop, 2016, 50(1): 87-93.
58. Parate D, Franco-Obregón A, Fröhlich J, et al. Enhancement of mesenchymal stem cell chondrogenesis with short-term low intensity pulsed electromagnetic fields. Sci Rep, 2017, 7(1): 9421.
59. Escobar J F, Vaca-González J J, Guevara J M, et al. In vitro evaluation of the effect of stimulation with magnetic fields on chondrocytes. Bioelectromagnetics, 2020, 41(1): 41-51.
60. Redeker J I, Schmitt B, Grigull N P, et al. Effect of electromagnetic fields on human osteoarthritic and non-osteoarthritic chondrocytes. BMC Complement Altern Med, 2017, 17(1): 402.
61. Zhou J, Liao Y, Xie H T, et al. Pulsed electromagnetic field ameliorates cartilage degeneration by inhibiting mitogen-activated protein kinases in a rat model of osteoarthritis. Phys Ther Sport, 2017, 24: 32-38.

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