Int J Stomatol ›› 2020, Vol. 47 ›› Issue (6): 652-660.doi: 10.7518/gjkq.2020111

• Reviews • Previous Articles     Next Articles

Advances in mechanisms for osteogenic differentiation of human periodontal ligament cells induced by cyclic tensile stress

Li Jingya1(),Shui Yusen1,Guo Yongwen2()   

  1. 1. State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases, West China School of Stomatology, Sichuan University, Chengdu 610041, China
    2. State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Dept. of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China
  • Received:2020-03-29 Revised:2020-06-23 Online:2020-11-01 Published:2020-11-06
  • Contact: Yongwen Guo E-mail:BeiBei980524@163.com;orthoguo@126.com
  • Supported by:
    Youth Program of National Natural Science Foundation of China(81600896);Research and Develop Program of West China Hospital of Stomatology, Sichuan University(LCYJ2019-14)

Abstract:

Orthodontic tooth movement (OTM) is a complex mechanical-biological mechanism, which is biologically based on mechanical-mediated periodontal tissue remodelling. Bone resorption on the pressure side and bone deposition on the tension side of the periodontal ligament could be observed. Human periodontal ligament cells (hPDLCs) were found to support osteogenic differentiation and periodontal tissue regeneration and maintain homeostasis. At present, many studies have used cyclic tension stress (CTS) for mechanical stimulation during orthodontic treatment to understand the osteogenic differentiation of tension-side hPDLCs. In this review, we will probe into how hPDLCs, as mechanosensitive cells, create initial induction to mechanical signals and then convert primary signals into downstream signals via different mechanotransduction signal pathways. After mechanosensitive cells are regulated, gene expression and protein synthesis are performed. Finally, the paradentium implements bone remodelling. Therefore, this review focuses on the molecular signals and pathways involved in this mechanical signal transduction to discuss how hPDLCs biologically respond to CTS stimulation. This review can provide theoretical evidence for shortening orthodontic treatment time and possible insights into the mechanisms of OTM for further studies.

Key words: cyclic tension stress, human periodontal ligament cells, mechanosensing, mechanotransduction, osteogenic differentiation

CLC Number: 

  • R783.5

TrendMD: 
[1] Lekic P, Mcculloch C. Periodontal ligament cell populations: the central role of fibroblasts in creating a unique tissue[J]. Anat Rec, 1996,245(2):327-341.
pmid: 8769671
[2] Weston CR, Davis RJ. The JNK signal transduction pathway[J]. Curr Opin Cell Biol, 2007,19(2):142-149.
doi: 10.1016/j.ceb.2007.02.001 pmid: 17303404
[3] Humphrey JD, Dufresne ER, Schwartz MA. Me-chanotransduction and extracellular matrix homeostasis[J]. Nat Rev Mol Cell Biol, 2014,15(12):802-812.
doi: 10.1038/nrm3896 pmid: 25355505
[4] Zeng Q, Guo Y, Liu Y, et al. Integrin-β1, not integrin- β5, mediates osteoblastic differentiation and ECM formation promoted by mechanical tensile strain[J]. Biol Res, 2015,48(1):25.
doi: 10.1186/s40659-015-0014-y
[5] Li S, Hua ZC. FAK expression: regulation and the-rapeutic potential[J]. Adv Cancer Res, 2008,101:45-61.
doi: 10.1016/S0065-230X(08)00403-X pmid: 19055942
[6] Sawada Y, Tamada M, Dubin-Thaler BJ, et al. Force sensing by mechanical extension of the Src family kinase substrate p130Cas[J]. Cell, 2006,127(5):1015-1026.
pmid: 17129785
[7] Wang Y, Zuo Z, Luo P, et al. The effect of cyclic tensile force on the actin cytoskeleton organization and morphology of human periodontal ligament cells[J]. Biochem Biophys Res Commun, 2018,506(4):950-955.
pmid: 30401563
[8] Gp N, Ej E, Gg G. FAK, talin and PIPKIγ regulate endocytosed integrin activation to polarize focal adhesion assembly[J]. Nat Cell Biol, 2016,18(5):491-503.
doi: 10.1038/ncb3333 pmid: 27043085
[9] Nam HY, Balaji Raghavendran HR, Pingguan-Mur-phy B, et al. Fate of tenogenic differentiation poten-tial of human bone marrow stromal cells by uniaxial stretching affected by stretch-activated calcium channel agonist gadolinium[J]. PLoS One, 2017,12(6):e0178117.
pmid: 28654695
[10] Boutahar N, Guignandon A, Vico L, et al. Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation[J]. J Biol Chem, 2004,279(29):30588-30599.
doi: 10.1074/jbc.M313244200 pmid: 15096502
[11] Leonardi R, Talic N F, Loreto C. MMP-13 (collagenase 3) immunolocalisation during initial orthodontic tooth movement in rats[J]. Acta Histochem, 2007,109(3):215-220.
doi: 10.1016/j.acthis.2007.01.002 pmid: 17350083
[12] Apajalahti S, Sorsa T, Railavo S, et al. The in vivo levels of matrix metalloproteinase-1 and-8 in gingival crevicular fluid during initial orthodontic tooth movement[J]. J Dent Res, 2003,82(12):1018-1022.
doi: 10.1177/154405910308201216 pmid: 14630906
[13] Kasper G, Glaeser JD, Geissler S, et al. Matrix metalloprotease activity is an essential link between mechanical stimulus and mesenchymal stem cell behavior[J]. Stem Cells, 2007,25(8):1985-1994.
doi: 10.1634/stemcells.2006-0676 pmid: 17495113
[14] Tantilertanant Y, Niyompanich J, Everts V, et al. Cyclic tensile force-upregulated IL6 increases MMP3 expression by human periodontal ligament cells[J]. Arch Oral Biol, 2019,107:104495.
pmid: 31377584
[15] Jiang L, Tang Z. Expression and regulation of the ERK1/2 and p38 MAPK signaling pathways in periodontal tissue remodeling of orthodontic tooth movement[J]. Mol Med Rep, 2018,17(1):1499-1506.
doi: 10.3892/mmr.2017.8021 pmid: 29138812
[16] Katz S, Boland R, Santillan G. Modulation of ERK 1/2 and p38 MAPK signaling pathways by ATP in osteoblasts: involvement of mechanical stress-ac-tivated calcium influx, PKC and Src activation[J]. Int J Biochem Cell Biol, 2006,38(12):2082-2091.
pmid: 16893669
[17] Ren D, Wei F, Hu L, et al. Phosphorylation of Runx2, induced by cyclic mechanical tension via ERK1/2 pathway, contributes to osteodifferentiation of human periodontal ligament fibroblasts[J]. J Cell Physiol, 2015,230(10):2426-2436.
pmid: 25740112
[18] Papadopoulou A, Iliadi A, Eliades T, et al. Early res-ponses of human periodontal ligament fibroblasts to cyclic and static mechanical stretching[J]. Eur J Or-thod, 2017,39(3):258-263.
[19] Li L, Han M, Li S, et al. Cyclic tensile stress during physiological occlusal force enhances osteogenic differentiation of human periodontal ligament cells via ERK1/2-Elk1 MAPK pathway[J]. DNA Cell Biol, 2013,32(9):488-497.
pmid: 23781879
[20] Liu D, Wang Z, Zhan J, et al. Hydrogen sulfide pro-motes proliferation and neuronal differentiation of neural stem cells and protects hypoxia-induced de-crease in hippocampal neurogenesis[J]. Pharmacol Biochem Behav, 2014,116:55-63.
doi: 10.1016/j.pbb.2013.11.009 pmid: 24246910
[21] Song ZC, Li S, Dong JC, et al. Enamel matrix pro-teins regulate hypoxia-induced cellular biobehavior and osteogenic differentiation in human periodontal ligament cells[J]. Biotech Histochem, 2017,92(8):606-618.
pmid: 29205072
[22] Li L, Han MX, Li S, et al. Hypoxia regulates the proliferation and osteogenic differentiation of human periodontal ligament cells under cyclic tensile stress via mitogen-activated protein kinase pathways[J]. J Periodontol, 2014,85(3):498-508.
doi: 10.1902/jop.2013.130048 pmid: 23805815
[23] Wang Y, Hu B, Hu R, et al. TAZ contributes to osteo-genic differentiation of periodontal ligament cells under tensile stress[J]. J Periodontal Res, 2020,55(1):152-160.
doi: 10.1111/jre.12698 pmid: 31539181
[24] Kletsas D, Basdra EK, Papavassiliou AG. Effect of protein kinase inhibitors on the stretch-elicited c-Fos and c-Jun up-regulation in human PDL osteoblast-like cells[J]. J Cell Physiol, 2002,190(3):313-321.
doi: 10.1002/jcp.10052 pmid: 11857447
[25] Konstantonis D, Papadopoulou A, Makou M, et al. The role of cellular senescence on the cyclic stre-tching-mediated activation of MAPK and ALP expression and activity in human periodontal liga-ment fibroblasts[J]. Exp Gerontol, 2014,57:175-180.
doi: 10.1016/j.exger.2014.05.010 pmid: 24858180
[26] Yamashiro K, Myokai F, Hiratsuka K, et al. Oligonu-cleotide array analysis of cyclic tension-responsive genes in human periodontal ligament fibroblasts[J]. Int J Biochem Cell Biol, 2007,39(5):910-921.
pmid: 17409011
[27] Papadopoulou A, Iliadi A, Eliades T, et al. Early responses of human periodontal ligament fibroblasts to cyclic and static mechanical stretching[J]. Eur J Orthod, 2017,39(3):258-263.
pmid: 27932408
[28] Kook SH, Hwang JM, Park JS, et al. Mechanical force induces typeⅠ collagen expression in human periodontal ligament fibroblasts through activation of ERK/JNK and AP-1[J]. J Cell Biochem, 2009,106(6):1060-1067.
doi: 10.1002/jcb.22085 pmid: 19206162
[29] Franceschi RT, Xiao G, Jiang D, et al. Multiple signaling pathways converge on the Cbfa1/Runx2 transcription factor to regulate osteoblast differentia-tion[J]. Connect Tissue Res, 2003,44(1):109-116.
[30] Yamaguchi N, Chiba M, Mitani H. The induction of c-fos mRNA expression by mechanical stress in human periodontal ligament cells[J]. Arch Oral Biol, 2002,47(6):465-471.
pmid: 12102763
[31] Carnes DL, Maeder CL, Graves DT. Cells with os-teoblastic phenotypes can be explanted from human gingiva and periodontal ligament[J]. J Periodontol, 1997,68(7):701-707.
pmid: 9249643
[32] Li S, Li F, Zou S, et al. PTH1R signalling regulates the mechanotransduction process of cementoblasts under cyclic tensile stress[J]. Eur J Orthod, 2018,40(5):537-543.
doi: 10.1093/ejo/cjx099 pmid: 29394342
[33] Ono W, Sakagami N, Nishimori S, et al. Parathyroid hormone receptor signalling in osterix-expressing mesenchymal progenitors is essential for tooth root formation[J]. Nat Commun, 2016,7:11277.
pmid: 27068606
[34] Xu Q, Yuan X, Zhang X, et al. Mechanoadaptive responses in the pPeriodontium are coordinated by Wnt[J]. J Dent Res, 2019,98(6):689-697.
doi: 10.1177/0022034519839438 pmid: 30971171
[35] Clevers H, Nusse R. Wnt/β-catenin signaling and disease[J]. Cell, 2012,149(6):1192-1205.
pmid: 22682243
[36] He Y, Liu Z, Qiao C, et al. Expression and signi-ficance of Wnt signaling components and their target genes in breast carcinoma[J]. Mol Med Rep, 2014,9(1):137-143.
pmid: 24190141
[37] Chang M, Lin H, Fu H, et al. MicroRNA-195-5p regulates osteogenic differentiation of periodontal ligament cells under mechanical loading[J]. J Cell Physiol, 2017,232(12):3762-3774.
pmid: 28181691
[38] Yu W, Hu B, Shi X, et al. Nicotine inhibits osteo-genic differentiation of human periodontal ligament cells under cyclic tensile stress through canonical Wnt pathway and α7 nicotinic acetylcholine receptor[J]. J Periodontal Res, 2018,53(4):555-564.
doi: 10.1111/jre.12545 pmid: 29603740
[39] De Boer J, Wang HJ, Van Blitterswijk C. Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells[J]. Tissue Eng, 2004,10(3/4):393-401.
[40] Mihara N, Chiba T, Yamaguchi K, et al. Minimal essential region for krüppel-like factor 5 expression and the regulation by specificity protein 3-GC box binding[J]. Gene, 2017,601:36-43.
doi: 10.1016/j.gene.2016.12.002 pmid: 27940107
[41] Chen Z, Zhang Q, Wang H, et al. Klf5 mediates odontoblastic differentiation through regulating dentin-specific extracellular matrix gene expression during mouse tooth development[J]. Sci Rep, 2017,7:46746.
doi: 10.1038/srep46746 pmid: 28440310
[42] Han N, Chen Z, Zhang Q. Expression of KLF5 in odontoblastic differentiation of dental pulp cells during in vitro odontoblastic induction and in vivo dental repair[J]. Int Endod J, 2017,50(7):676-684.
doi: 10.1111/iej.12672 pmid: 27334851
[43] Guo L, He P, No YR, et al. Krüppel-like factor 5 incorporates into the β-catenin/TCF complex in response to LPA in colon cancer cells[J]. Cell Signal, 2015,27(5):961-968.
doi: 10.1016/j.cellsig.2015.02.005 pmid: 25683913
[44] Fei Y, Xiao L, Doetschman T, et al. Fibroblast growth factor 2 stimulation of osteoblast differentiation and bone formation is mediated by modulation of the Wnt signaling pathway[J]. J Biol Chem, 2011,286(47):40575-40583.
pmid: 21987573
[45] De Crescenzo G, Pham PL, Durocher Y, et al. Trans-forming growth factor-beta (TGF-β) binding to the extracellular domain of the type Ⅱ TGF-β receptor: receptor capture on a biosensor surface using a new coiled-coil capture system demonstrates that avidity contributes significantly to high affinity binding[J]. J Mol Biol, 2003,328(5):1173-1183.
doi: 10.1016/s0022-2836(03)00360-7 pmid: 12729750
[46] Liu M, Sun F, Feng Y, et al. MicroRNA-132-3p re-presses Smad5 in MC3T3-E1 osteoblastic cells under cyclic tensile stress[J]. Mol Cell Biochem, 2019,458(1/2):143-157.
[47] Li W, Li H, Lu R, et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing[J]. Proc Natl Acad Sci U S A, 2004,101(5):1350-1355.
doi: 10.1073/pnas.0308308100 pmid: 14745017
[48] Elbediwy A, Vincent Mistiaen ZI, Thompson BJ. YAP and TAZ in epithelial stem cells: a sensor for cell polarity, mechanical forces and tissue damage[J]. Bioessays, 2016,38(7):644-653.
doi: 10.1002/bies.201600037 pmid: 27173018
[49] Yang Y, Wang BK, Chang ML, et al. Cyclic stretch enhances osteogenic differentiation of human perio-dontal ligament cells via YAP activation[J]. Biomed Res Int, 2018,2018:2174824.
doi: 10.1155/2018/2174824 pmid: 30519570
[50] Wang Y, Hu B, Hu R, et al. TAZ contributes to osteo-genic differentiation of periodontal ligament cells under tensile stress[J]. J Periodontal Res, 2020,55(1):152-160.
doi: 10.1111/jre.12698 pmid: 31539181
[51] Sun B, Wen Y, Wu X, et al. Expression pattern of YAP and TAZ during orthodontic tooth movement in rats[J]. J Mol Histol, 2018,49(2):123-131.
pmid: 29356923
[52] Steinert AF, Weissenberger M, Kunz M, et al. Indian hedgehog gene transfer is a chondrogenic inducer of human mesenchymal stem cells[J]. Arthritis Res Ther, 2012,14(4):R168.
pmid: 22817660
[53] Taipale J, Cooper MK, Maiti T, et al. Patched acts catalytically to suppress the activity of Smoothened[J]. Nature, 2002,418(6900):892.
doi: 10.1038/nature00989 pmid: 12192414
[54] Yang X, Matsuda K, Bialek P, et al. ATF4 is a subs-trate of RSK2 and an essential regulator of osteoblast biology: implication for Coffin-Lowry syndrome[J]. Cell, 2004,117(3):387-398.
pmid: 15109498
[55] Yang S, Wei F, Hu L, et al. PERK-eIF2α-ATF4 path-way mediated by endoplasmic reticulum stress re-sponse is involved in osteodifferentiation of human periodontal ligament cells under cyclic mechanical force[J]. Cell Signal, 2016,28(8):880-886.
pmid: 27079961
[56] Lafoya B, Munroe JA, Mia MM, et al. Notch: a multi-functional integrating system of microenvironmental signals[J]. Dev Biol, 2016,418(2):227-241.
pmid: 27565024
[1] Abulaiti Guliqihere,Qin Xu,Zhu Guangxun. Research progress of mitophagy in the onset and development of periodontal disease [J]. Int J Stomatol, 2024, 51(1): 68-73.
[2] Liu Tiqian,Liang Xing,Liu Weiqing,Li Xiaohong,Zhu Rui.. Research progress on the role and mechanism of occlusal trauma in the development of periodontitis [J]. Int J Stomatol, 2023, 50(1): 19-24.
[3] Zhang Jingyi,Li Danwei,Sun Yu,Lei Yayan,Liu Tao,Gong Yu. In vitro cytotoxicity of composite resin and compomer and effect on osteogenic differentiation of osteoblasts [J]. Int J Stomatol, 2022, 49(4): 412-419.
[4] Hong Yaya,Chen Xuepeng,Si Misi. Advances in research on noncoding RNA during the osteogenic differentiation of dental follicle stem cells [J]. Int J Stomatol, 2022, 49(3): 263-271.
[5] Guo Yuting,Lü Xuechao. Research progress on drugs regulating the osteogenic differentiation of dental pulp stem cells [J]. Int J Stomatol, 2021, 48(6): 737-744.
[6] Liu Juan,Chen Bin,Yan Fuhua. Effects of platelet-rich plasma and concentrated growth factor on the proliferation and osteogenic differentiation of human periodontal cells [J]. Int J Stomatol, 2021, 48(5): 520-527.
[7] Yang Yeqing,Chen Ming,Wu Buling. Research progress on circular RNA in the osteogenic differentiation of mesenchymal stem cells [J]. Int J Stomatol, 2020, 47(3): 257-262.
[8] Liu Junqi,Chen Yiyin,Yang Wenbin. Research progress on N6-methyladenosine for regulating the osteogenic differentiation of bone marrow mesenchymal stem cells [J]. Int J Stomatol, 2020, 47(3): 263-269.
[9] Wang Runting,Fang Fuchun. Progress in research of non-coding RNAs in osteogenic differentiation of human periodontal ligament stem cells [J]. Int J Stomatol, 2020, 47(2): 138-145.
[10] Yu Xiaohong,Liu Yu,Zeng Lian,Yang Yanling,Wang Zhou,Li Wei. Effects of enamel matrix derivative on proliferation and osteogenic differentiation of human periodontal ligament stem cells [J]. Int J Stomatol, 2020, 47(1): 24-31.
[11] Zhou Tingru,Li Yongsheng. Advances of dental pulp stem cells in osteogenic microenvironment [J]. Int J Stomatol, 2019, 46(6): 675-679.
[12] Wei Hu,Yifan Wang,Yifang Yuan,Ying Li,Bin Guo. Research progress on regulatory mechanism of the circadian clock genes on osteogenesis and bone resorption [J]. Int J Stomatol, 2019, 46(3): 302-307.
[13] Tingting Li,Yufeng Zhang,Ruoxi Wang,Zhiqing Huang,Lü Xie,Yifan Xue,Yulan Wang. Mechanism and application of osteogenesis induced by graphene and its derivatives modified composite materials [J]. Inter J Stomatol, 2018, 45(6): 673-677.
[14] Hao Yilin, Fang Fuchun, Wu Buling. Functions of microRNA on the osteogenic differentiation of human periodontal ligament-derived cells [J]. Inter J Stomatol, 2018, 45(1): 46-49.
[15] Wu Caijuan, Yang Lan, Guo Lühua. Role and mechanism of the calcitonin gene related peptide in bone tissue regeneration [J]. Inter J Stomatol, 2017, 44(4): 488-492.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Foreign Med Sci: Stomatol, 1999, 26(06): .
[2] . [J]. Foreign Med Sci: Stomatol, 1999, 26(06): .
[3] . [J]. Foreign Med Sci: Stomatol, 1999, 26(06): .
[4] . [J]. Foreign Med Sci: Stomatol, 1999, 26(06): .
[5] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[6] . [J]. Foreign Med Sci: Stomatol, 1999, 26(05): .
[7] . [J]. Foreign Med Sci: Stomatol, 1999, 26(04): .
[8] . [J]. Foreign Med Sci: Stomatol, 1999, 26(04): .
[9] . [J]. Foreign Med Sci: Stomatol, 2004, 31(02): 126 -128 .
[10] . [J]. Inter J Stomatol, 2008, 35(S1): .