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

Chen,Bailing; Lin,Tao; Yang,Xiaoxi; Li,Yiqiang; Xie,Denghui; Zheng,Wenhui; Cui,Haowen; Deng,Weimin; Tan,Xin

doi:10.3892/ijmm.2016.2757

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

Authors:
- Bailing Chen
- Tao Lin
- Xiaoxi Yang
- Yiqiang Li
- Denghui Xie
- Wenhui Zheng
- Haowen Cui
- Weimin Deng
- Xin Tan
View Affiliations

Affiliations: Department of Spine Surgery, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong 510080, P.R. China, Department of Spine Surgery, Chinese PLA General Hospital (301 Hospital), Beijing 100853, P.R. China, Department of Orthopedics, Guangzhou Women and Children's Medical Center, Guangzhou, Guangdong 510623, P.R. China, Department of Spine Surgery, The Third Affiliated Hospital of Southern Medical University (Academy of Orthopedics), Guangzhou, Guangdong 510630, P.R. China, Department of Physiology, Zhongshan School of Medicine of Sun Yat-sen University, Guangzhou, Guangdong 510080, P.R. China, Department of Rehabilitation, General Hospital of Guangzhou Military Command of PLA, Guangzhou, Guangdong 510000, P.R. China
Published online on: September 28, 2016 https://doi.org/10.3892/ijmm.2016.2757
Pages: 1531-1540

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The positive effect of low-magnitude, high‑frequency (LMHF) vibration on implant osseointegration has been demonstrated; however, the underlying cellular and molecular mechanisms remain unknown. The aim of this study was to explore the effect of LMHF vibration on the adhesion and the osteogenic differentiation of bone marrow-derived mesenchymal stem cells (BMSCs) cultured on hydroxyapatite (HA)-coated surfaces in an in vitro model as well as to elucidate the molecular mechanism responsible for the effects of LMHF vibration on osteogenesis. LMHF vibration resulted in the increased expression of fibronectin, which was measured by immunostaining and RT-qPCR. Stimulation of BMSCs by LMHF vibration resulted in the rearrangement of the actin cytoskeleton with more prominent F-actin. Moreover, the expression of β1 integrin, vinculin and paxillin was notably increased following LMHF stimulation. Scanning electron microscope observations revealed that there were higher cell numbers and more extracellular matrix attached to the HA-coated surface in the LMHF group. Alkaline phosphatase activity as well as the expression of osteogenic-specific genes, namely Runx2, osterix, collagen I and osteocalcin, were significantly elevated in the LMHF group. In addition, the protein expression of Wnt10B, β-catenin, Runx2 and osterix was increased following exposure to LMHF vibration. Taken together, the findings of this study indicate that LMHF vibration promotes the adhesion and the osteogenic differentiation of BMSCs on HA-coated surfaces in vitro, and LMHF vibration may directly induce osteogenesis by activating the Wnt/β‑catenin signaling pathway. These data suggest that LMHF vibration enhances the osseointegration of bone to a HA-coated implant, and provide a scientific foundation for improving bone-implant osseointegration through the application of LMHF vibration.

View Figures

View References

1	Meirelles L, Arvidsson A, Andersson M, Kjellin P, Albrektsson T and Wennerberg A: Nano hydroxyapatite structures influence early bone formation. J Biomed Mater Res A. 87:299–307. 2008. View Article : Google Scholar : PubMed/NCBI
2	Kujala S, Ryhänen J, Danilov A and Tuukkanen J: Effect of porosity on the osteointegration and bone ingrowth of a weight-bearing nickel-titanium bone graft substitute. Biomaterials. 24:4691–4697. 2003. View Article : Google Scholar : PubMed/NCBI
3	Chen BL, Xie DH, Zheng ZM, Lu W, Ning CY, Li YQ, Li FB and Liao WM: Comparison of the effects of alendronate sodium and calcitonin on bone-prosthesis osseointegration in osteoporotic rats. Osteoporos Int. 22:265–270. 2011. View Article : Google Scholar
4	Ohkawa Y, Tokunaga K and Endo N: Intermittent administration of human parathyroid hormone (1–34) increases new bone formation on the interface of hydroxyapatitecoated titanium rods implanted into ovariectomized rat femora. J Orthop Sci. 13:533–542. 2008. View Article : Google Scholar : PubMed/NCBI
5	Boden SD, Kang J, Sandhu H and Heller JG: Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies. Spine. 27:2662–2673. 2002. View Article : Google Scholar : PubMed/NCBI
6	Hokugo A, Saito T, Li A, Sato K, Tabata Y and Jarrahy R: Stimulation of bone regeneration following the controlled release of water-insoluble oxysterol from biodegradable hydrogel. Biomaterials. 35:5565–5571. 2014. View Article : Google Scholar : PubMed/NCBI
7	Rizzoli R, Reginster JY, Boonen S, Bréart G, Diez-Perez A, Felsenberg D, Kaufman JM, Kanis JA and Cooper C: Adverse reactions and drug-drug interactions in the management of women with postmenopausal osteoporosis. Calcif Tissue Int. 89:91–104. 2011. View Article : Google Scholar : PubMed/NCBI
8	Frost HMA: A 2003 update of bone physiology and Wolff's Law for clinicians. Angle Orthod. 74:3–15. 2004.PubMed/NCBI
9	Burr DB, Robling AG and Turner CH: Effects of biomechanical stress on bones in animals. Bone. 30:781–786. 2002. View Article : Google Scholar : PubMed/NCBI
10	Rubin C, Recker R, Cullen D, Ryaby J, McCabe J and McLeod K: Prevention of postmenopausal bone loss by a low-magnitude, high-frequency mechanical stimuli: a clinical trial assessing compliance, efficacy, and safety. J Bone Miner Res. 19:343–351. 2004. View Article : Google Scholar : PubMed/NCBI
11	Rubin C, Turner AS, Bain S, Mallinckrodt C and McLeod K: Anabolism. Low mechanical signals strengthen long bones. Nature. 412:603–604. 2001. View Article : Google Scholar : PubMed/NCBI
12	Xie L, Jacobson JM, Choi ES, Busa B, Donahue LR, Miller LM, Rubin CT and Judex S: Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone. 39:1059–1066. 2006. View Article : Google Scholar : PubMed/NCBI
13	Rubin C, Turner AS, Müller R, Mittra E, McLeod K, Lin W and Qin YX: Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res. 17:349–357. 2002. View Article : Google Scholar : PubMed/NCBI
14	Garman R, Gaudette G, Donahue LR, Rubin C and Judex S: Low-level accelerations applied in the absence of weight bearing can enhance trabecular bone formation. J Orthop Res. 25:732–740. 2007. View Article : Google Scholar : PubMed/NCBI
15	Judex S, Lei X, Han D and Rubin C: Low-magnitude mechanical signals that stimulate bone formation in the ovariectomized rat are dependent on the applied frequency but not on the strain magnitude. J Biomech. 40:1333–1339. 2007. View Article : Google Scholar
16	De Smet E, Jaecques SV, Wevers M, Jansen JA, Jacobs R, Sloten JV and Naert IE: Effect of controlled early implant loading on bone healing and bone mass in guinea pigs, as assessed by micro-CT and histology. Eur J Oral Sci. 114:232–242. 2006. View Article : Google Scholar : PubMed/NCBI
17	Ogawa T, Possemiers T, Zhang X, Naert I, Chaudhari A, Sasaki K and Duyck J: Influence of whole-body vibration time on peri-implant bone healing: a histomorphometrical animal study. J Clin Periodontol. 38:180–185. 2011. View Article : Google Scholar
18	Ogawa T, Zhang X, Naert I, Vermaelen P, Deroose CM, Sasaki K and Duyck J: The effect of whole-body vibration on peri-implant bone healing in rats. Clin Oral Implants Res. 22:302–307. 2011. View Article : Google Scholar
19	Chen B, Li Y, Xie D and Yang X: Low-magnitude high-frequency loading via whole body vibration enhances bone-implant osseointegration in ovariectomized rats. J Orthop Res. 30:733–739. 2012. View Article : Google Scholar
20	Liu X, Bao C, Hu J, Yin G and Luo E: Effects of clodronate combined with hydroxyapatite on multi-directional differentiation of mesenchymal stromal cells. Arch Med Sci. 6:670–677. 2010. View Article : Google Scholar : PubMed/NCBI
21	Fassina L, Saino E, Sbarra MS, Visai L, De Angelis MG, Magenes G and Benazzo F: In vitro electromagnetically stimulated SAOS-2 osteoblasts inside porous hydroxyapatite. J Biomed Mater Res A. 93:1272–1279. 2010.
22	Gong SH, Lee H, Pae A, Noh K, Shin YM, Lee JH and Woo YH: Gene expression of MC3T3-E1 osteoblastic cells on titanium and zirconia surface. J Adv Prosthodont. 5:416–422. 2013. View Article : Google Scholar : PubMed/NCBI
23	Di Palma F, Chamson A, Lafage-Proust MH, Jouffray P, Sabido O, Peyroche S, Vico L and Rattner A: Physiological strains remodel extracellular matrix and cell-cell adhesion in osteoblastic cells cultured on alumina-coated titanium alloy. Biomaterials. 25:2565–2575. 2004. View Article : Google Scholar : PubMed/NCBI
24	Lacouture ME, Schaffer JL and Klickstein LB: A comparison of type I collagen, fibronectin, and vitronectin in supporting adhesion of mechanically strained osteoblasts. J Bone Miner Res. 17:481–492. 2002. View Article : Google Scholar : PubMed/NCBI
25	Patel MJ, Chang KH, Sykes MC, Talish R, Rubin C and Jo H: Low magnitude and high frequency mechanical loading prevents decreased bone formation responses of 2T3 preosteoblasts. J Cell Biochem. 106:306–316. 2009. View Article : Google Scholar : PubMed/NCBI
26	Zhou Y, Guan X, Zhu Z, Gao S, Zhang C, Li C, Zhou K, Hou W and Yu H: Osteogenic differentiation of bone marrow-derived mesenchymal stromal cells on bone-derived scaffolds: effect of microvibration and role of ERK1/2 activation. Eur Cell Mater. 22:12–25. 2011.PubMed/NCBI
27	Prè D, Ceccarelli G, Visai L, Benedetti L, Imbriani M, Cusella De Angelis MG and Magenes G: High-frequency vibration treatment of human bone marrow stromal cells increases differentiation toward bone tissue. Bone Marrow Res. 2013:8034502013. View Article : Google Scholar : PubMed/NCBI
28	Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, Cullen DM, Zhao W, Li C, Kharode Y, Sauter L, Babij P, Brown EL, et al: Wnt/beta-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem. 281:31720–31728. 2006. View Article : Google Scholar : PubMed/NCBI
29	Premaraj S, Souza I and Premaraj T: Mechanical loading activates β-catenin signaling in periodontal ligament cells. Angle Orthod. 81:592–599. 2011. View Article : Google Scholar : PubMed/NCBI
30	Hou WW, Zhu ZL, Zhou Y, Zhang CX and Yu HY: Involvement of Wnt activation in the micromechanical vibration-enhanced osteogenic response of osteoblasts. J Orthop Sci. 16:598–605. 2011. View Article : Google Scholar : PubMed/NCBI
31	Kubota T, Michigami T and Ozono K: Wnt signaling in bone metabolism. J Bone Miner Metab. 27:265–271. 2009. View Article : Google Scholar : PubMed/NCBI
32	Zhang C, Li J, Zhang L, Zhou Y, Hou W, Quan H, Li X, Chen Y and Yu H: Effects of mechanical vibration on proliferation and osteogenic differentiation of human periodontal ligament stem cells. Arch Oral Biol. 57:1395–1407. 2012. View Article : Google Scholar : PubMed/NCBI
33	Kim IS, Song YM, Lee B and Hwang SJ: Human mesenchymal stromal cells are mechanosensitive to vibration stimuli. J Dent Res. 91:1135–1140. 2012. View Article : Google Scholar : PubMed/NCBI
34	Lau E, Lee WD, Li J, Xiao A, Davies JE, Wu Q, Wang L and You L: Effect of low-magnitude, high-frequency vibration on osteogenic differentiation of rat mesenchymal stromal cells. J Orthop Res. 29:1075–1080. 2011. View Article : Google Scholar : PubMed/NCBI
35	Roy M, Fielding GA, Beyenal H, Bandyopadhyay A and Bose S: Mechanical, in vitro antimicrobial, and biological properties of plasma-sprayed silver-doped hydroxyapatite coating. ACS Appl Mater Interfaces. 4:1341–1349. 2012. View Article : Google Scholar : PubMed/NCBI
36	Su B, Peng X, Jiang D, Wu J, Qiao B, Li W and Qi X: In vitro and in vivo evaluations of nano-hydroxyapatite/polyamide 66/glass fibre (n-HA/PA66/GF) as a novel bioactive bone screw. PLoS One. 8:e683422013. View Article : Google Scholar : PubMed/NCBI
37	Duan Y, Zhu S, Guo F, Zhu J, Li M, Ma J and Zhu Q: The effect of adhesive strength of hydroxyapatite coating on the stability of hydroxyapatite-coated prostheses in vivo at the early stage of implantation. Arch Med Sci. 8:199–208. 2012. View Article : Google Scholar : PubMed/NCBI
38	Olivares-Navarrete R, Hyzy SL, Hutton DL, Erdman CP, Wieland M, Boyan BD and Schwartz Z: Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials. 31:2728–2735. 2010. View Article : Google Scholar : PubMed/NCBI
39	Puleo DA and Nanci A: Understanding and controlling the bone-implant interface. Biomaterials. 20:2311–2321. 1999. View Article : Google Scholar : PubMed/NCBI
40	Dumas V, Ducharne B, Perrier A, Fournier C, Guignandon A, Thomas M, Peyroche S, Guyomar D, Vico L and Rattner A: Extracellular matrix produced by osteoblasts cultured under low-magnitude, high-frequency stimulation is favourable to osteogenic differentiation of mesenchymal stem cells. Calcif Tissue Int. 87:351–364. 2010. View Article : Google Scholar : PubMed/NCBI
41	Sato K, Adachi T, Matsuo M and Tomita Y: Quantitative evaluation of threshold fiber strain that induces reorganization of cytoskeletal actin fiber structure in osteoblastic cells. J Biomech. 38:1895–1901. 2005. View Article : Google Scholar : PubMed/NCBI
42	Zheng L, Song J, Li Z, Fan Y, Zhao Z, Chen Y, Deng F and Hu Y: The mechanism of myoblast deformation in response to cyclic strain - A cytomechanical study. Cell Biol Int. 32:754–760. 2008. View Article : Google Scholar : PubMed/NCBI
43	Wixler V, Geerts D, Laplantine E, Westhoff D, Smyth N, Aumailley M, Sonnenberg A and Paulsson M: The LIM-only protein DRAL/FHL2 binds to the cytoplasmic domain of several alpha and beta integrin chains and is recruited to adhesion complexes. J Biol Chem. 275:33669–33678. 2000. View Article : Google Scholar : PubMed/NCBI
44	Mierke CT: The role of vinculin in the regulation of the mechanical properties of cells. Cell Biochem Biophys. 53:115–126. 2009. View Article : Google Scholar : PubMed/NCBI
45	Mierke CT: The role of focal adhesion kinase in the regulation of cellular mechanical properties. Phys Biol. 10:0650052013. View Article : Google Scholar : PubMed/NCBI
46	Carvalho RS, Scott JE and Yen EH: The effects of mechanical stimulation on the distribution of beta 1 integrin and expression of beta 1-integrin mRNA in TE-85 human osteosarcoma cells. Arch Oral Biol. 40:257–264. 1995. View Article : Google Scholar : PubMed/NCBI
47	Marie PJ: Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 473:98–105. 2008. View Article : Google Scholar : PubMed/NCBI
48	Nakashima K and de Crombrugghe B: Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet. 19:458–466. 2003. View Article : Google Scholar : PubMed/NCBI
49	Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB and Stein GS: Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol. 143:420–430. 1990. View Article : Google Scholar : PubMed/NCBI
50	Mantila Roosa SM, Liu Y and Turner CH: Gene expression patterns in bone following mechanical loading. J Bone Miner Res. 26:100–112. 2011. View Article : Google Scholar
51	Winkler DG, Sutherland MK, Geoghegan JC, Yu C, Hayes T, Skonier JE, Shpektor D, Jonas M, Kovacevich BR, Staehling-Hampton K, et al: Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J. 22:6267–6276. 2003. View Article : Google Scholar : PubMed/NCBI